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The Physiology of Low-Frequency Electrosensory Systems
... The tube of the ampullary receptors is filled with a mucous substance of very low electrical resistivity while the wall of the ampulla is highly resistive, being composed of flattened cells that interconnect by means of tight junctions and desmosomes ( Jørgensen, 2005). Ampullary electroreceptors respond to stimuli of direct or near direct current (<0.1 Hz) or alternating current of low frequencies (usually <10 Hz), but can reach up to 50 Hz depending on the species (Bodznick and Montgomery, 2005;Zakon, 1986). From an embryological point of view, these low-frequency electroreceptors are believed to have derived from the neural plaques that will form the ciliated cells of the lateral line and other mechanoreceptors in vertebrates (Northcutt et al., 1995;Ronan and Bodznick, 1986). ...
... From an embryological point of view, these low-frequency electroreceptors are believed to have derived from the neural plaques that will form the ciliated cells of the lateral line and other mechanoreceptors in vertebrates (Northcutt et al., 1995;Ronan and Bodznick, 1986). All known ampullary electroreceptors are enervated by nerve fibers from the lateral line system, which reinforces this hypothesis (Bodznick and Montgomery, 2005;Northcutt, 1997Northcutt, , 2005Zakon, 1986). ...
... For instance, all nonteleost ampullary receptors are excited by cathodic stimuli (when the lumen of the ampulla becomes negative relative to the base of the sensory cells) and inhibited by anodic stimuli (when the lumen of the ampoule becomes positive). The teleost electroreceptors (in this chapter represented by catfish and gymnotiforms), on the other hand, function inversely and are stimulated by anodic stimuli (Bodznick and Montgomery, 2005). This difference appears to reflect quite clearly the nonhomology between the ampullary receptors of teleosts and nonteleosts. ...
... Ampullary electroreceptors detect DC and low-frequency sinusoidal (alternating current, AC) electrostatic fields from < 0.1 Hz to up to 10-50 Hz (usually < 30 Hz), depending on species (see §2.4). These low-frequency fields can elicit responses in ampullary electroreceptors at field strengths as low as c. 1 μV cm −1 in freshwater electroreceptive taxa (fishes and amphibia) and less than a remarkable 1 nV cm −1 in marine taxa (Bodznick & Montgomery, 2005;Bullock & Heiligenberg, 1986;Kajiura & Holland, 2002;Kalmijn, 1974;Peters et al., 2007;Zakon, 1986). Although natural electric fields in fresh water are up to 10 times stronger than in seawater (due to the lower shunt conductance of fresh water), the ampullary electroreceptors of freshwater fishes and amphibia are generally one to two orders of magnitude less sensitive than those of marine taxa; the disparity probably arises from the higher electrical ambient noise level in fresh water, which sets limits to the useful sensitivity of electroreceptors (Bodznick & Montgomery, 2005). ...
... These low-frequency fields can elicit responses in ampullary electroreceptors at field strengths as low as c. 1 μV cm −1 in freshwater electroreceptive taxa (fishes and amphibia) and less than a remarkable 1 nV cm −1 in marine taxa (Bodznick & Montgomery, 2005;Bullock & Heiligenberg, 1986;Kajiura & Holland, 2002;Kalmijn, 1974;Peters et al., 2007;Zakon, 1986). Although natural electric fields in fresh water are up to 10 times stronger than in seawater (due to the lower shunt conductance of fresh water), the ampullary electroreceptors of freshwater fishes and amphibia are generally one to two orders of magnitude less sensitive than those of marine taxa; the disparity probably arises from the higher electrical ambient noise level in fresh water, which sets limits to the useful sensitivity of electroreceptors (Bodznick & Montgomery, 2005). 2.2 | Ampullary electroreceptor functions 2.2.1 | Detection of non-electrogenic prey animals ...
... Electroreceptors comprise a layer of electroreceptor hair cells (each of which bears an apical primary kinocilium, but few or no microvilli) and supporting cells located at the base of a jelly-filled duct that leads to a cutaneous pore (Jørgensen, 2005;Baker et al., 2013; Figure 3). The duct wall comprises a layer of flattened basement membrane cells of high electrical resistance (Bodznick & Montgomery, 2005). Ampullary receptors detect electrostatic fields via the potential difference between the cutaneous pore and the base of the organ (Zakon, 1986(Zakon, , 1988. ...
Electroreception, the capacity to detect external underwater electric fields with specialised receptors, is a phylogenetically widespread sensory modality in fishes and amphibians. In passive electroreception, a capacity possessed by c. 16% of fish species, an animal uses low‐frequency‐tuned ampullary electroreceptors to detect microvolt‐range bioelectric fields from prey, without the need to generate its own electric field. In active electroreception (electrolocation), which occurs only in the teleost lineages Mormyroidea and Gymnotiformes, an animal senses its surroundings by generating a weak (< 1 V) electric‐organ discharge (EOD) and detecting distortions in the EOD‐associated field using high‐frequency‐tuned tuberous electroreceptors. Tuberous electroreceptors also detect the EODs of neighbouring fishes, facilitating electrocommunication. Several other groups of elasmobranchs and teleosts generate weak (< 10 V) or strong (> 50 V) EODs that facilitate communication or predation, but not electrolocation. Approximately 1.5% of fish species possess electric organs. This review has two aims. First, to synthesise our knowledge of the functional biology and phylogenetic distribution of electroreception and electrogenesis in fishes, with a focus on freshwater taxa and with emphasis on the proximate (morphological, physiological and genetic) bases of EOD and electroreceptor diversity. Second, to describe the diversity, biogeography, ecology and electric signal diversity of the mormyroids and gymnotiforms and to explore the ultimate (evolutionary) bases of signal and receptor diversity in their convergent electrogenic–electrosensory systems. Four sets of potential drivers or moderators of signal diversity are discussed. First, selective forces of an abiotic (environmental) nature for optimal electrolocation and communication performance of the EOD. Second, selective forces of a biotic nature targeting the communication function of the EOD, including sexual selection, reproductive interference from syntopic heterospecifics and selection from eavesdropping predators. Third, non‐adaptive drift and, finally, phylogenetic inertia, which may arise from stabilising selection for optimal signal‐receptor matching.
... The electrosensory division of the lateral line system was lost independently in the lineages leading to extant neopterygian fishes (gars, bowfin and teleosts) and to anuran amphibians (neither of the major anamniote lab models, i.e., the teleost zebrafish and the frog Xenopus, has electroreceptors). However, electrosensory lateral line organs evolved independently at least twice within the teleosts, most likely from neuromast hair cells (Bullock et al., 1983;Northcutt, 1986;Bodznick, 1989;Alves-Gomes, 2001;Bodznick and Montgomery, 2005;Kawasaki, 2009;Baker et al., 2013). The entire lateral line system was lost in amniotes, with the transition to life on land. ...
... Similarly, our only detailed understanding of non-teleost ampullary organ physiology until very recently had come from current-and voltage-clamp approaches to study epithelial currents in dissected single ampullary organ preparations from skates (Bennett and Obara, 1986;Lu and Fishman, 1995;Bodznick and Montgomery, 2005). These revealed that L-type voltage-gated calcium channels are required both for voltage-sensing in the apical (lumenal, i.e., exterior-facing) electroreceptor membrane, and for neurotransmitter release basally. ...
... These revealed that L-type voltage-gated calcium channels are required both for voltage-sensing in the apical (lumenal, i.e., exterior-facing) electroreceptor membrane, and for neurotransmitter release basally. The basal membrane is repolarized by voltage-gated potassium channels and calcium-dependent chloride channels, while the apical membrane is repolarized by the calcium-gated potassium channel BK (Bennett and Obara, 1986;Lu and Fishman, 1995;Bodznick and Montgomery, 2005;King et al., 2016). BK was recently cloned directly from skate ampullary organs (King et al., 2016), a little over 40 years after its properties were initially discovered using the same preparation (Clusin et al., 1975;Clusin and Bennett, 1977a;Clusin and Bennett, 1977b). ...
The anamniote lateral line system, comprising mechanosensory neuromasts and electrosensory ampullary organs, is a useful model for investigating the developmental and evolutionary diversification of different organs and cell types. Zebrafish neuromast development is increasingly well understood, but neither zebrafish nor Xenopus is electroreceptive and our molecular understanding of ampullary organ development is rudimentary. We have used RNA-seq to generate a lateral line-enriched gene-set from late-larval paddlefish (Polyodon spathula). Validation of a subset reveals expression in developing ampullary organs of transcription factor genes critical for hair cell development, and genes essential for glutamate release at hair cell ribbon synapses, suggesting close developmental, physiological and evolutionary links between non-teleost electroreceptors and hair cells. We identify an ampullary organ-specific proneural transcription factor, and candidates for the voltage-sensing L-type Cav channel and rectifying Kv channel predicted from skate (cartilaginous fish) ampullary organ electrophysiology. Overall, our results illuminate ampullary organ development, physiology and evolution.
... Algae, aquatic invertebrates and vertebrates in freshwater generate electric fields of several millivolts in direct current (DC) mode and up to 10 Hz in frequency of alternating current (AC), particularly during body and respiratory movements (Peters & Bretschneider, 1972). On the other hand, voltages in the sea tend to be between 1 and 200 μV (Bodznick & Montgomery, 2005). Stem vertebrates evolved ampullary electroreceptors that sense these fields (Kalmijn, 1988;Zakon, 1988;Zupanc & Bullock, 2005). ...
... There are major differences in signal amplitude and consequently, receptor sensitivity between electric fishes in ocean and freshwater vary significantly (Bodznick & Montgomery, 2005;Kalmijn, 1988). ...
... Signals from marine animals will be <1 μV at a distance of 10-20 cm, and behavioural detection thresholds can be <10 nV/cm in marine elasmobranchs (Kalmijn, 1988). Freshwater fishes are one or two orders of magnitude less sensitive than marine species (Bodznick & Montgomery, 2005) in line with their stronger signals. The active space for mormyrid and gymnotiforme signalling is estimated to be an ellipsoid of 10-20 cm (Hopkins, 1999). ...
Fishes utilize electric signals for passive and active electrolocation and communication at night in murky water. To our knowledge, the mechanism of transmission of fish electric signals through water has not been addressed. In such a medium, the transmission of electrical signals can occur by movement of ions (ion conduction) under the influence of a generated electric field, or through its perturbation by nearby objects that have electric permittivity different than water. This latter property refers to the ability of a medium to resist the formation of electric fields with no involvement of ion transport. In this study, we discuss the relevance of each mechanism in the context of previous reports on transmission of signals by electric fishes in water environments.
... The lower three traces for AFF and AEN represent the spike activity in response to a 1 Hz, 2 µV extrinsic electrosensory stimulus, the representation of the stimulus itself, and the record of ventilation. Reprinted from Bodznick & Montgomery [2005], with permission from Springer. ...
... The elasmobranch electrosensory system provides a simple model to examine the mechanisms underlying causal inference in the vertebrate brain. The electric sense belongs to the octavolateral system and hence shows similarities to the vestibular, lateral line and auditory systems [Bodznick & Montgomery, 2005]. Transduction in elasmobranch electroreceptors is mediated by sensory hair cells, thus comparative analysis may provide insight into hair cell mechanisms elsewhere. ...
... While here we focussed on the electrosensory system, ampullary electroreceptors are octavolateralis senses. Thus, they share developmental and anatomical similarities with the other senses derived from hair cells such as vestibular, lateral line and auditory systems [Bodznick & Montgomery, 2005]. These similarities extend to the central projections and central processing of information in cerebellar-like circuitry [Bodznick & Montgomery, 2005]. ...
We develop a theory of how the functional design of the electrosensory system in sharks reflects the inevitability of noise in high-precision measurements, and how the Central Nervous System may have developed an efficient solution to the problem of inferring parameters of stimulus sources, such as their location, via Bayesian neural computation.
We use Finite Element Method to examine how the electrical properties of shark tissues and the geometrical configuration of both the shark body and the electrosensory array, act to focus weak electric fields in the aquatic environment, so that the majority of the voltage drop is signalled across the electrosensory cells. We analyse snapshots of two ethologically relevant stimuli: localized prey-like dipole electric sources, and uniform electric fields resembling motion-induced and other fields encountered in the ocean. We demonstrated that self movement (or self state) not only affects the measured field, by perturbing the self field, but also affects the external field.
Electrosensory cells provide input to central brain regions via primary afferent nerves. Inspection of elasmobranch electrosensory afferent spike trains and inter-spike interval distributions indicates that they typically have fairly regular spontaneous inter-spike intervals with skewed Gaussian-like variability.
However, because electrosensory afferent neurons converge onto secondary neurons, we consider the convergent input a "super afferent" with the pulse train received by a target neuron approaching a Poisson process with shorter mean intervals as the number of independent convergent spike trains increases.
We implement a spiking neural particle filter which takes simulated electrosensory "super afferent" spike trains and can successfully infer the fixed Poisson parameter, or the equivalent real world state, distance to a source. The circuit obtained by converting the mathematical model to a network structure bears a striking resemblance to the cerebellar-like hindbrain circuits of the dorsal octavolateral nucleus.
The elasmobranchs’ ability to sense electric fields down to a limit imposed by thermodynamics seems extraordinary. However we predict that the theories presented here generalize to other sensory systems, particularly the other octavolateralis senses which share cerebellar-like circuitry, suggesting that the cerebellum itself also plays a role in dynamic state estimation.
... The electrosensory division of the lateral line system was lost independently in the lineages leading to extant neopterygian fishes (gars, bowfin and teleosts) and to anuran amphibians (neither of the major anamniote lab models, i.e., the teleost zebrafish and the frog Xenopus, has electroreceptors). However, electrosensory lateral line organs evolved independently at least twice within the teleosts, most likely from neuromast hair cells (Bullock et al., 1983;Northcutt, 1986;Bodznick, 1989;Alves-Gomes, 2001;Bodznick and Montgomery, 2005;Kawasaki, 2009;Baker et al., 2013). The entire lateral line system was lost in amniotes, with the transition to life on land. ...
... Similarly, our only detailed understanding of non-teleost ampullary organ physiology until very recently had come from current-and voltage-clamp approaches to study epithelial currents in dissected single ampullary organ preparations from skates (Bennett and Obara, 1986;Lu and Fishman, 1995;Bodznick and Montgomery, 2005). These revealed that L-type voltage-gated calcium channels are required both for voltage-sensing in the apical (lumenal, i.e., exterior-facing) electroreceptor membrane, and for neurotransmitter release basally. ...
... These revealed that L-type voltage-gated calcium channels are required both for voltage-sensing in the apical (lumenal, i.e., exterior-facing) electroreceptor membrane, and for neurotransmitter release basally. The basal membrane is repolarized by voltage-gated potassium channels and calcium-dependent chloride channels, while the apical membrane is repolarized by the calcium-gated potassium channel BK (Bennett and Obara, 1986;Lu and Fishman, 1995;Bodznick and Montgomery, 2005;King et al., 2016). BK was recently cloned directly from skate ampullary organs (King et al., 2016), a little over 40 years after its properties were initially discovered using the same preparation (Clusin et al., 1975;Clusin and Bennett, 1977a;Clusin and Bennett, 1977b). ...
The anamniote lateral line system, comprising mechanosensory neuromasts and electrosensory ampullary organs, is a useful model for investigating the developmental and evolutionary diversification of different organs and cell types. Zebrafish neuromast development is increasingly well understood, but neither zebrafish nor $\textit{Xenopus}$ is electroreceptive and our molecular understanding of ampullary organ development is rudimentary. We have used RNA-seq to generate a lateral line-enriched gene-set from late-larval paddlefish ($\textit{Polyodon spathula}$). Validation of a subset reveals expression in developing ampullary organs of transcription factor genes critical for hair cell development, and genes essential for glutamate release at hair cell ribbon synapses, suggesting close developmental, physiological and evolutionary links between non-teleost electroreceptors and hair cells. We identify an ampullary organ-specific proneural transcription factor, and candidates for the voltage-sensing L-type Ca$_v$ channel and rectifying K$_v$ channel predicted from skate (cartilaginous fish) ampullary organ electrophysiology. Overall, our results illuminate ampullary organ development, physiology and evolution.
... Detecting electrical signals emitted from the environment and estimating the position of their source is called passive electrolocation [ 3,11,12 ] . In the aquatic environment, weak electric fi elds of both abiotic and biotic origin can be found. ...
... In contrast, weakly electric fi sh actively produce and detect high-frequency electric signals for the purpose of active electrolocation and for electrocommunication. low amplitudes. These receptor organs are used for passive electrolocation [ 11 ] . Ampullary electroreceptors were fi rst found in elasmobranch fi sh, i.e., in sharks and rays, where they are called ampullae of Lorenzini. ...
... Individual receptor cells are less sensitive; e.g., in skates their fi ring frequency can be changed by a stimulus no smaller than 2 m V cm −1 . The much higher behavioral sensitivity of the animal might be explained by averaging over many receptor cells situated in several ampullae and by central nervous processes [ 11,14 ] . ...
Electroreception by animals living in aquatic environments is a widespread phenomenon found in many vertebrates. With ampullary electroreceptor organs or trigeminal electroreceptor structures, these animals can detect even extremely weak electric sources in their surroundings, a process called passive electrolocation.
... Two distinct types of electroreceptor organs mediate electroreception in both groups of weakly electric teleosts (Fig.1A) (Gibbs, 2004;Jørgensen, 2005). 'Ampullary' organs detect lowfrequency environmental electric fields (passive electroreception); they comprise relatively few electroreceptor cells (generally with short, sparse apical microvilli) in epithelia at the base of mucousfilled ducts, which open to the surface via pores (Gibbs, 2004;Bodznick and Montgomery, 2005;Jørgensen, 2005). 'Tuberous' organs of varying morphology detect high-frequency electric fields from electric organ discharges (self-generated and/or from other fish) for active electroreception; they lack ducts and are 'plugged' by loosely packed epidermal cells, with the electroreceptor cells (which generally have numerous apical microvilli) surrounded by an intraepidermal cavity (Gibbs, 2004;Bodznick and Montgomery, 2005;Jørgensen, 2005;Kawasaki, 2005). ...
... 'Ampullary' organs detect lowfrequency environmental electric fields (passive electroreception); they comprise relatively few electroreceptor cells (generally with short, sparse apical microvilli) in epithelia at the base of mucousfilled ducts, which open to the surface via pores (Gibbs, 2004;Bodznick and Montgomery, 2005;Jørgensen, 2005). 'Tuberous' organs of varying morphology detect high-frequency electric fields from electric organ discharges (self-generated and/or from other fish) for active electroreception; they lack ducts and are 'plugged' by loosely packed epidermal cells, with the electroreceptor cells (which generally have numerous apical microvilli) surrounded by an intraepidermal cavity (Gibbs, 2004;Bodznick and Montgomery, 2005;Jørgensen, 2005;Kawasaki, 2005). Teleost electroreceptors are distributed on both the head and trunk, and are part of the lateral line system; depending on their position, they are innervated by anterior (pre-otic) or posterior (post-otic) lateral line nerves, which project centrally to a special 'electrosensory lateral line lobe' in the medulla (Bullock et al., 1983;Gibbs, 2004;Bell and Maler, 2005;Bodznick and Montgomery, 2005). ...
... 'Tuberous' organs of varying morphology detect high-frequency electric fields from electric organ discharges (self-generated and/or from other fish) for active electroreception; they lack ducts and are 'plugged' by loosely packed epidermal cells, with the electroreceptor cells (which generally have numerous apical microvilli) surrounded by an intraepidermal cavity (Gibbs, 2004;Bodznick and Montgomery, 2005;Jørgensen, 2005;Kawasaki, 2005). Teleost electroreceptors are distributed on both the head and trunk, and are part of the lateral line system; depending on their position, they are innervated by anterior (pre-otic) or posterior (post-otic) lateral line nerves, which project centrally to a special 'electrosensory lateral line lobe' in the medulla (Bullock et al., 1983;Gibbs, 2004;Bell and Maler, 2005;Bodznick and Montgomery, 2005). The anterior and posterior lateral line nerves also innervate the mechanosensory hair cells of lateral line neuromasts (Fig.1B), which are distributed in characteristic lines over the head and trunk and detect local water movement (Bleckmann and Zelick, 2009). ...
Electroreception is an ancient vertebrate sense with a fascinating evolutionary history involving multiple losses as well as independent evolution at least twice within teleosts. We review the phylogenetic distribution of electroreception and the morphology and innervation of electroreceptors in different vertebrate groups. We summarise recent work from our laboratory that has confirmed the homology of ampullary electroreceptors in non-teleost jawed vertebrates by showing, in conjunction with previously published work, that these are derived embryonically from lateral line placodes. Finally, we review hypotheses to explain the distribution of electroreception within teleosts, including the hypothesis that teleost ampullary and tuberous electroreceptors evolved via the modification of mechanosensory hair cells in lateral line neuromasts. We conclude that further experimental work on teleost electroreceptor development is needed to test such hypotheses.
... Within jawed vertebrates, electroreception has been lost independently at least three times (in the lineages leading to anuran amphibians, amniotes and neopterygian fishes, i.e. gars, bowfins and teleosts) (Bullock et al., 1983;New, 1997;Northcutt, 1997;Schlosser, 2002a), and has also evolved at least twice independently within the teleosts (in siluriforms and gymnotiforms, and in mormyriforms) (Alves-Gomes, 2001;Bullock et al., 1983;New, 1997;Northcutt, 1997) and convergently as a specialization of trigeminal nerve endings in monotremes (Pettigrew, 1999) and dolphins (Czech-Damal et al., 2012). Teleost electroreceptors are innervated by lateral line nerves projecting to a special 'electrosensory lateral line lobe' in the hindbrain (Bodznick and Montgomery, 2005), but in contrast to non-teleost electroreceptors (Lu and Fishman, 1995), teleost electroreceptors are excited by anodal stimuli, and the basal membrane is the voltage sensor (Bodznick and Montgomery, 2005). As neurotransmitter release is triggered in mechanosensory hair cells by opening voltage-gated channels in the basal membrane, electroreceptors may have evolved in some teleosts via genetic modification of the mechanisms underlying neuromast hair cell differentiation (Bodznick and Montgomery, 2005), but this hypothesis remains untested. ...
... Within jawed vertebrates, electroreception has been lost independently at least three times (in the lineages leading to anuran amphibians, amniotes and neopterygian fishes, i.e. gars, bowfins and teleosts) (Bullock et al., 1983;New, 1997;Northcutt, 1997;Schlosser, 2002a), and has also evolved at least twice independently within the teleosts (in siluriforms and gymnotiforms, and in mormyriforms) (Alves-Gomes, 2001;Bullock et al., 1983;New, 1997;Northcutt, 1997) and convergently as a specialization of trigeminal nerve endings in monotremes (Pettigrew, 1999) and dolphins (Czech-Damal et al., 2012). Teleost electroreceptors are innervated by lateral line nerves projecting to a special 'electrosensory lateral line lobe' in the hindbrain (Bodznick and Montgomery, 2005), but in contrast to non-teleost electroreceptors (Lu and Fishman, 1995), teleost electroreceptors are excited by anodal stimuli, and the basal membrane is the voltage sensor (Bodznick and Montgomery, 2005). As neurotransmitter release is triggered in mechanosensory hair cells by opening voltage-gated channels in the basal membrane, electroreceptors may have evolved in some teleosts via genetic modification of the mechanisms underlying neuromast hair cell differentiation (Bodznick and Montgomery, 2005), but this hypothesis remains untested. ...
... Teleost electroreceptors are innervated by lateral line nerves projecting to a special 'electrosensory lateral line lobe' in the hindbrain (Bodznick and Montgomery, 2005), but in contrast to non-teleost electroreceptors (Lu and Fishman, 1995), teleost electroreceptors are excited by anodal stimuli, and the basal membrane is the voltage sensor (Bodznick and Montgomery, 2005). As neurotransmitter release is triggered in mechanosensory hair cells by opening voltage-gated channels in the basal membrane, electroreceptors may have evolved in some teleosts via genetic modification of the mechanisms underlying neuromast hair cell differentiation (Bodznick and Montgomery, 2005), but this hypothesis remains untested. Although the molecular mechanisms underlying mechanosensory hair cell formation have been intensively studied (Driver and Kelley, 2009;Puligilla and Kelley, 2009), few papers have reported gene expression during ampullary organ development (Freitas et al., 2006;Metscher et al., 1997;Modrell and Baker, 2012;Modrell et al., 2011a;Modrell et al., 2011b;O'Neill et al., 2007). ...
Ampullary organ electroreceptors excited by weak cathodal electric fields are used for hunting by both cartilaginous and non-teleost bony fishes. Despite similarities of neurophysiology and innervation, their embryonic origins remain controversial: bony fish ampullary organs are derived from lateral line placodes, whereas a neural crest origin has been proposed for cartilaginous fish electroreceptors. This calls into question the homology of electroreceptors and ampullary organs in the two lineages of jawed vertebrates. Here, we test the hypothesis that lateral line placodes form electroreceptors in cartilaginous fishes by undertaking the first long-term in vivo fate-mapping study in any cartilaginous fish. Using DiI tracing for up to 70 days in the little skate, Leucoraja erinacea, we show that lateral line placodes form both ampullary electroreceptors and mechanosensory neuromasts. These data confirm the homology of electroreceptors and ampullary organs in cartilaginous and non-teleost bony fishes, and indicate that jawed vertebrates primitively possessed a lateral line placode-derived system of electrosensory ampullary organs and mechanosensory neuromasts.
... As a result, electric fields propagate with nearly infinite speed, and are present throughout their full extent almost instantaneously [13], [14]. The biologically important characteristics encoded in electric stimuli are the local intensity, orientation and the polarity of a field [14]. Electric flux lines describe a curved path along the direction of the current and do not point straight to their source. ...
... Electric flux lines describe a curved path along the direction of the current and do not point straight to their source. Behavioural experiments indicate that the stimulus frequency ranging from DC up to 8 Hz has little, if any significance for behaviour, as electroreceptive predators attack artificial dipoles provided as long as their frequencies are within the detectable range [14], [15]. ...
... Physiologically, the ampullae of Lorenzini, which are the electroreceptors of elasmobranchs, are not true DC receptors, and this characteristic is important for their normal mode of operation within the animal’s own DC background field [1], [14], [15]. In order to sense the DC field produced by prey, elasmobranchs must move with respect to their prey [1], [14], [15]. ...
In the aquatic environment, living organisms emit weak dipole electric fields, which spread in the surrounding water. Elasmobranchs detect these dipole electric fields with their highly sensitive electroreceptors, the ampullae of Lorenzini. Freshwater sawfish, Pristis microdon, and two species of shovelnose rays, Glaucostegus typus and Aptychotrema rostrata were tested for their reactions towards weak artificial electric dipole fields. The comparison of sawfishes and shovelnose rays sheds light on the evolution and function of the elongated rostrum ('saw') of sawfish, as both groups evolved from a shovelnose ray-like ancestor. Electric stimuli were presented both on the substrate (to mimic benthic prey) and suspended in the water column (to mimic free-swimming prey). Analysis of around 480 behavioural sequences shows that all three species are highly sensitive towards weak electric dipole fields, and initiate behavioural responses at median field strengths between 5.15 and 79.6 nV cm(-1). The response behaviours used by sawfish and shovelnose rays depended on the location of the dipoles. The elongation of the sawfish's rostrum clearly expanded their electroreceptive search area into the water column and enables them to target free-swimming prey.
... The sensory hair cells of the chondrichthyan ampullary organs function as passive electroreceptors that are stimulated by weak cathodal currents, or electrical stimuli that induce a negative charge at the pore, lumen and apical end of the receptor cell (Bodznick & Montgomery, 2005;Murray, 1962Murray, , 1965. The glycoprotein hydrogel inside the ampullary canals conducts protons (Josberger et al., 2016) that allow charges that accumulate at the skin surface to be detected by the sensory receptors located several cm away within a subdermal ampulla. ...
... Electroreceptors, like other sensory hair cells, constantly release neurotransmitter and the associated afferent nerve fibres exhibit a resting discharge of action potentials (Bodznick & Montgomery, 2005). When the sensory cell detects a net positive charge, the discharge rate of the afferent nerve decreases, whereas a negative charge increases the discharge rate (Murray, 1962(Murray, , 1965. ...
Electroreception in marine fishes occurs across a variety of taxa and is best understood in the chondrichthyans (sharks, skates, rays, and chimaeras). Here, we present an up‐to‐date review of what is known about the biology of passive electroreception and we consider how electroreceptive fishes might respond to electric and magnetic stimuli in a changing marine environment. We briefly describe the history and discovery of electroreception in marine Chondrichthyes, the current understanding of the passive mode, the morphological adaptations of receptors across phylogeny and habitat, the physiological function of the peripheral and central nervous system components, and the behaviours mediated by electroreception. Additionally, whole genome sequencing, genetic screening and molecular studies promise to yield new insights into the evolution, distribution, and function of electroreceptors across different environments. This review complements that of electroreception in freshwater fishes in this special issue, which provides a comprehensive state of knowledge regarding the evolution of electroreception. We conclude that despite our improved understanding of passive electroreception, several outstanding gaps remain which limits our full comprehension of this sensory modality. Of particular concern is how electroreceptive fishes will respond and adapt to a marine environment that is being increasingly altered by anthropogenic electric and magnetic fields.
... Mormyrid fish, as well as a number of non-electrogenic fish, use a passive electrosensory system to detect small, low-frequency electric fields generated by invertebrate prey (Bodznick and Montgomery, 2005). However, detecting these signals is more complex for mormyrids because, at the same time, they employ an electromotor system for both navigation and communication that involves the repeated generation of large pulsed electric fields known as electric organ discharges (EODs). ...
... Large firing rate modulations were sometimes observed, presumably due to spontaneous movements of the worm, which brought it very near to the pore of the electroreceptor innervated by the recorded afferent. Given the steep falloff of electrical dipole fields with distance (Bodznick and Montgomery, 2005), a strong dependence of neural response magnitude on the exact location of the prey relative to the electroreceptor is expected. A comparison of the magnitude of firing rate variations in the presence of worms to those induced by artificial prey-like stimuli indicate that actual prey are capable of inducing firing rate modulations as large or larger than those used in the present study. ...
Studies of cerebellum-like circuits in fish have demonstrated that synaptic plasticity shapes the motor corollary discharge responses of granule cells into highly-specific predictions of self-generated sensory input. However, the functional significance of such predictions, known as negative images, has not been directly tested. Here we provide evidence for improvements in neural coding and behavioral detection of prey-like stimuli due to negative images. In addition, we find that manipulating synaptic plasticity leads to specific changes in circuit output that disrupt neural coding and detection of prey-like stimuli. These results link synaptic plasticity, neural coding, and behavior and also provide a circuit-level account of how combining external sensory input with internally generated predictions enhances sensory processing.
... Because the peak sensitivity of ampullary electroreceptors is thought to be in the approximate range of 0-60 Hz, an assessment of low-frequency energy serves as an indicator of the contribution of the localized emf-EOD to ampullary stimulation (Bodznick and Montgomery, 2005). Here we quantified 'low-frequency energy' (LFE) as the signal power (in decibels) in the PSD at 30 Hz, following Crampton et al. (2013). ...
... These voltages range from tens to hundreds of millivolts (see vertical scale bars in Figs. 3-10) and in all cases greatly exceed the known threshold sensitivity of gymnotiform ampullary electroreceptors -reported as less than one tenth of a millivolt (Bodznick and Montgomery, 2005). ...
Descriptions of the head-to-tail electric organ discharge (ht-EOD) waveform – typically recorded with electrodes at a distance of approximately 1–2 body lengths from the center of the subject – have traditionally been used to characterize species diversity in gymnotiform electric fish. However, even taxa with relatively simple ht-EODs show spatiotemporally complex fields near the body surface that are determined by site-specific electrogenic properties of the electric organ and electric filtering properties of adjacent tissues and skin. In Brachyhypopomus, a pulse-discharging genus in the family Hypopomidae, the regional characteristics of the electric organ and the role that the complex ‘near field’ plays in communication and/or electrolocation are not well known. Here we describe, compare, and discuss the functional significance of diversity in the ht-EOD waveforms and near-field spatiotemporal patterns of the electromotive force (emf-EODs) among a species-rich sympatric community of Brachyhypopomus from the upper Amazon.
... Neuromasts function as displacement detectors of local water flow, used for prey/predator detection, obstacle avoidance and behaviours such as schooling. Electrosensory hair cells are collected in ampullary organs 3,4 , either at the surface or recessed in pores filled with mucous jelly of low electrical resistance, distributed in fields flanking the lines of mechanosensory neuromasts 5,6 . Transduction is direct: cathodal stimuli open voltage-gated calcium channels in the apical membrane 3 ; the information is used for prey/predator detection, orientation and migration. ...
... Electrosensory hair cells are collected in ampullary organs 3,4 , either at the surface or recessed in pores filled with mucous jelly of low electrical resistance, distributed in fields flanking the lines of mechanosensory neuromasts 5,6 . Transduction is direct: cathodal stimuli open voltage-gated calcium channels in the apical membrane 3 ; the information is used for prey/predator detection, orientation and migration. Afferent innervation for mechanosensory hair cells in a given neuromast line, and for electrosensory hair cells in the ampullary organ fields flanking that line, is provided by neurons within a specific lateral line ganglion 7 . ...
Electroreception is an ancient subdivision of the lateral line sensory system, found in all major vertebrate groups (though lost in frogs, amniotes and most ray-finned fishes). Electroreception is mediated by 'hair cells' in ampullary organs, distributed in fields flanking lines of mechanosensory hair cell-containing neuromasts that detect local water movement. Neuromasts, and afferent neurons for both neuromasts and ampullary organs, develop from lateral line placodes. Although ampullary organs in the axolotl (a representative of the lobe-finned clade of bony fishes) are lateral line placode-derived, non-placodal origins have been proposed for electroreceptors in other taxa. Here we show morphological and molecular data describing lateral line system development in the basal ray-finned fish Polyodon spathula, and present fate-mapping data that conclusively demonstrate a lateral line placode origin for ampullary organs and neuromasts. Together with the axolotl data, this confirms that ampullary organs are ancestrally lateral line placode-derived in bony fishes.
... Furthermore, conditions of marine habitats impose different physical constraints than those encountered in freshwater. For example, compared to freshwater teleosts, both marine elasmobranchs and siluriforms (catfishes) show similar differences in the spatial organization of ampullary receptors relative to the skin surface, presumably to account for the conductance of saltwater and relative skin resistances (Bodznick & Montgomery, 2005). Here, we provide a first look at the quantity, distribution, and density of both electroreceptor types (ampullary and tuberous) on the heads of gymnotiforms, representing multiple genera and families, collected from two broad habitat categories (river channels and floodplain lakes). ...
Sensory organs are generally fine-tuned to an organism's environment and ecological niche. Many examples of this environmentally influenced fine-tuning exist for sensory modalities, such as vision and audition, but this link is poorly understood for electroreception. This study investigates the distribution of electroreceptor pores on the heads of select members of the Gymnotiformes, Neotropical weakly electric knifefishes that use electric signals for orientation, communication, and prey localization. We evaluated the distribution and density of electroreceptors among select gymnotiform genera and discuss whether apparent differences could be consistent with ecological factors, such as habitat type and feeding behavior. Evidence for such patterns has been found in elasmobranchs; however, differences in the functional roles of the electrosensory system in gymnotiforms (e. g. electrocommu-nication) may alter these patterns within this diverse clade of freshwater fishes. Scanning electron microscopy was used to image the heads of specimens collected from diverse habitats. Pores associated with ampullary and tuberous electroreceptor organs were enumerated using digital image processing software and mean pore counts were compared across six different regions of the head. Previously unknown pore types and distribution patterns are described. Additionally, unique electroreceptor distributions were found in some species with specialized feeding modes. This study provides the first quantitative comparative analysis of electroreceptor distributions across multiple gymnotiform families and genera, providing an important step toward understanding the factors that have shaped the evolution of electroreception in this diverse group of Neotropical fishes.
... Rays (Raja clavata) only showed good detection capabilities for AC fields of 16 and 32 Hz after increasing the electric field strength by factors of 8 and 32, respectively (Kalmijn, 1974), whereas two shark species (Scyliorhinus canicula and Triakis semifasciata) no longer responded to AC stimuli with frequencies >16 Hz (Kalmijn, 1973(Kalmijn, , 1974. Although the ampullary electroreceptors of the elasmobranchs are not DC sensitive, the movement of the animal relative to the stimulus source causes the standing DC electric field signals to be automatically converted into low-frequency AC signals, which represent an adequate stimulus (Bodznick and Montgomery, 2005;Kalmijn, 1974). Taking these relationships into account for the electroreception of toothed whales, tests in which the animals can perceive weak electric fields while moving would be an interesting extension of the present experimental approach. ...
For the two dolphin species Sotalia guianensis (Guiana dolphin) and Tursiops truncatus (bottlenose dolphin), previous research has shown that the vibrissal crypts located on the rostrum represent highly innervated, ampullary electroreceptors and that both species are correspondingly sensitive to weak electric fields. In the present study, for a comparative assessment of the sensitivity of the bottlenose dolphin's electroreceptive system, we determined detection thresholds for DC and AC electric fields with two bottlenose dolphins. In a psychophysical experiment, the animals were trained to respond to electric field stimuli using the go/no-go paradigm. We show that the two bottlenose dolphins are able to detect DC electric fields as low as 2.4 and 5.5 µV cm−1 , respectively, a detection threshold in the same order of magnitude as those in the platypus and the Guiana dolphin. Detection thresholds for AC fields (1, 5 and 25 Hz) were generally higher than those for DC fields, and the sensitivity for AC fields decreased with increasing frequency. Although the electroreceptive sensitivity of dolphins is lower than that of elasmobranchs, it is suggested that it allows for both micro-and macro-scale orientation. In dolphins pursuing benthic foraging strategies, electroreception may facilitate short-range prey detection and target-oriented snapping of their prey. Furthermore, the ability to detect weak electric fields may enable dolphins to perceive the Earth's magnetic field through induction-based magnetoreception, thus allowing large-scale orientation.
... The ancestors of weakly electric fishes had a category of electroreceptors known as ampullary receptors, which detect low-frequency electric signals in the water. Ampullary receptors can detect, for example, the currents released by muscles that move the operculum (Bodznick and Montgomery, 2005;Grewe et al., 2011), or by the movements of prey items (MacIver et al., 2001). ...
The adaptive-shift hypothesis for the evolution of cave-dwelling species posits that ancestor species in surface habitats had exaptations for subterranean life that were exploited when individuals invaded caves. Weakly electric Gymnotiform fishes, nocturnal South American teleost fishes, have features that appear to be likely exaptations for troglobitic life. These fishes have active electrosensory systems in which fish generate weak electric fields that are detected by specialized electroreceptors. Gymnotiform fishes use their electric fields for navigation, prey capture (scene analysis), and social communication. Although active electrosensory systems appear to be exaptations for troglobitic life, as fish use these systems to “see in the dark”, producing electric fields is energetically costly. Cave habitats, which often are low in resources, may not be able to support such high energetic demands. Eigenmannia vicentespelaea, a species of weakly electric fish that is endemic to the São Vicente II cave in central Brazil, surprisingly generates stronger electric fields than their surface relatives. The increase in strength of electric fields may result simply from differences in size between cave and surface populations, but may also be due to lack of predation pressure in the cave or increases in “sensory volumes” and acuity that improve prey localization and capture. Eigenmannia vicentespelaea exhibits the classical phenotypes of any troglobitic fish: these fish have small to nonexistent eyes and loss of pigmentation. The closest living surface relative, Eigenmannia trilineata, inhabits streams nearby and has eyes and pigmentation. The electrosensory and locomotor behavior of both species of fish were measured in their natural habitats using a grid recording system. Surface Eigenmannia exhibited dramatic circadian changes in social behavior, such as hiding under rocks during the day and foraging in groups at night, while cave Eigenmannia displayed territorial behavior with no apparent circadian modulations. The territorial behavior involved electrical and movement-based interactions that may be a form of boundary patrolling. Electrosocial behavior and scene analysis are mechanistically interlinked because both stem from active sensing tactics.
... In other groups, notably frogs and teleost fishes, ampullary receptors have been completely lost. However, at least two groups of teleost fishes have independently evolved a different type of electroreceptors responding to anodal stimuli (positive on the outside of the animal) rather than cathodal stimuli as in other vertebrates (Bullock, Bodznick, and Northcutt 1983;Bodznick and Montgomery 2005;Baker et al. 2013). These are found either in ampullary organs resembling those of other vertebrates ( Fig. 1.6C) or in tuberous organs, in which a plug of epidermal cells separates the receptor cells from the surface. ...
... Thus, electroreception, via ampullary receptors, is an important sensory system, which has been conserved over hundreds of millions of years. The ampullary electroreceptors decribed so far are excited by weak cathodal stimuli, which probably open voltage-gated Ca + channels in the apical membrane (Teeter et al. 1980, Münz et al. 1984, Lu and Fishman 1995, Bodznick and Montgomery 2005. The neuromasts, the sensory organs of the mechanosensory lateral line system (Fig. 35E), have some anatomical similarities to the ampullary organs and possess a kinocilium and a number of microvilli of variable length (see Mechanosensory Lateral Line section). ...
... The electrosensory division of the lateral line system Electroreception, i.e., the ability to detect weak electric fields in water, was only discovered in the midtwentieth century, in conjunction with the finding that "weakly electric" teleost fishes generate electric fields (Lissmann 1951(Lissmann , 1958Lissmann and Machin 1958) by discharging "electric organs" composed of modified muscle cells (Markham 2013;Gallant et al. 2014). Weakly electric fishes have diverse "tuberous" electrosensory organs stimulated by the highfrequency electric fields generated by electric organ discharges, and morphologically distinct "ampullary" organs stimulated by the low-frequency electric fields around other animals (Bodznick and Montgomery 2005;Jørgensen 2005). (Tiny direct-current standing electric fields develop around animals in water owing to the leakage of ions across mucous membranes, with a low-frequency component imparted by, for example, rhythmic limb or ventilation movements; Wilkens and Hofmann 2005;Bedore and Kajiura 2013.) ...
Synopsis:
The vertebrate lateral line system comprises a mechanosensory division, with neuromasts containing hair cells that detect local water movement ("distant touch"); and an electrosensory division, with electrosensory organs that detect the weak, low-frequency electric fields surrounding other animals in water (primarily used for hunting). The entire lateral line system was lost in the amniote lineage with the transition to fully terrestrial life; the electrosensory division was lost independently in several lineages, including the ancestors of frogs and of teleost fishes. (Electroreception with different characteristics subsequently evolved independently within two teleost lineages.) Recent gene expression studies in a non-teleost actinopterygian fish suggest that electroreceptor ribbon synapses employ the same transmission mechanisms as hair cell ribbon synapses, and show that developing electrosensory organs express transcription factors essential for hair cell development, including Atoh1 and Pou4f3. Previous hypotheses for electroreceptor evolution suggest either that electroreceptors and hair cells evolved independently in the vertebrate ancestor from a common ciliated secondary cell, or that electroreceptors evolved from hair cells. The close developmental and putative physiological similarities implied by the gene expression data support the latter hypothesis, i.e., that electroreceptors evolved in the vertebrate ancestor as a "sister cell-type" to lateral line hair cells.
... They are broadly tuned and behave as low-pass filters ($30-40 Hz to virtually DC). This low-frequency tuning allows ampullary receptors to integrate inputs over time, which makes them exquisitely sensitive to very weak electrical fields (approximately 10-20 mV cm À1 in freshwater fish, and <1 mV cm À1 in marine fish), but largely unable to detect the high-frequency components present in most EODs (Bodznick and Montgomery, 2005). Ampullary receptors function primarily in passive electrolocationi.e., in the ability of fish to passively detect the bioelectric fields generated even by animals that do not have electric organs. ...
Electric fish generate electric organ discharges (EODs) from an electric organ and sense these discharges via sensory cells termed eletroreceptors. Amazingly, electrocommunication evolved independently in two groups of fishes. EODs are used in the same ways as signals in other modalities and are similarly influenced by natural and sexual selection. The EOD waveform conveys information on the species, age, sex, and individual identity of the signaler, and brief modulations of the EOD emission rate transmit information about breeding status, dominance/subordinance, and motivation. As with many sexually dimorphic communication signals, EOD waveform is regulated by gonadal steroids by long-term actions on the morphology and physiology of the neurons and electric organ while short-term modulations of EOD rate signaling motivational states are driven by peptides and amines at the brain stem pacemaker nucleus.
EOD waveforms are similar in juveniles and females in many species, reminiscent of the plumage similarities of juvenile and female birds. In species in which males compete for reproductive access to females, male signals are more conspicuous and/or ornate than those of females and carry costs, such as increased risk of predation and/or energetic costs. Similarly, the electrical signals produced by males are more conspicuous both to conspecific females and to potential predators.
A striking feature of electrocommunication is the wealth of species diversity including variation in the magnitude and direction of sex differences in body size, EOD properties, and other electrical behaviors; diversity in habitat preferences, sociality, and associated diversity in physiology and patterning of the EOD; and variation in courtship and parental behavior. This diversity is coupled with numerous striking examples of convergence in the behavior and physiology between the two different orders of fish that independently evolved electrocommunication. These features lend themselves to comparative studies of the hormonal control of reproductive and communication behavior and make electric fish excellent model animals for studying how evolutionary lability of neuroendocrine mechanisms that regulate sex differences can lead to species diversity in sexually dimorphic behavior.
... The fact that electroreception is still present in most fish taxa, with the notable exception of many teleosts, shows that the perception of electric signals offers an advantage in the aquatic habitat. The majority of electroreceptive animals use passive electrolocation, during which they can detect and analyze electric signals from the environment (Bodznick and Montgomery 2005;Wilkens and Hofmann 2005). ...
African weakly electric fish live nocturnally in tropical freshwater streams. To sense their surroundings, they have developed a highly specialized system of two senses, which allows them to perceive nearby objects at high precision with an active electric sense and to detect large, fast-moving objects with their visual sense at greater distances. Both senses are highly specialized and are equipped with matched filters for efficient detection and analysis of relevant object features and for neglecting unimportant items. Active electrolocation in the near field involves the production of an electric signal, which serves as a carrier for sensory information. This signal and the resulting electric field around the fish are shaped by the fish’s body and its internal structure. The electric skin properties and the accessory structures of the electroreceptor organs further filter
the signal and form two electroreceptive foveae. In contrast, the visual system is adapted for detecting large objects at longer distances. A grouped retina forms a visual matched filter, which filters out small, nearby objects but efficiently detects fast-moving distant objects even under noisy and dim light conditions.
... The resultant transcutaneous potential is the source of electrosensory self-stimulation or ventilatory reafference (Montgomery, 1984b), by which a change in the internal potential of the animal (and basal regions of the ampullary receptor cells) proportionately modulates the regular discharge of all primary afferent neurons. Thus, electrosensory receptors and primary afferents exhibit common mode noise and also a central adaptive filter in the hindbrain circuit, which has important implications for noise rejection and central processing of electrosensory information (see Bodznick and Montgomery, 2005). ...
... With only three pairs of electrosensory tubules, the coelacanth electric sense is a low-resolution electro-detector. These fish therefore have limited sensitivity to the directional properties of electric fields, and are probably not capable of extracting complex spatial information for localizing bioelectric field sources at different orientations relative to their head 1,8 . This makes them unique among extant electrosensitive fishes in having limited ability to discriminate the relative movements of prey, with their electric sense having little, or perhaps no, involvement in tracking prey. ...
The cartilaginous and non-neopterygian bony fishes have an electric sense typically comprised of hundreds or thousands of sensory canals distributed in broad clusters over the head. This morphology facilitates neural encoding of local electric field intensity, orientation, and polarity, used for determining the position of nearby prey. The coelacanth rostral organ electric sense, however, is unique in having only three paired sensory canals with distribution restricted to the dorsal snout, raising questions about its function. To address this, we employed magnetic resonance imaging methods to map electrosensory canal morphology in the extant coelacanth, Latimeria chalumnae, and a simple dipole 'rabbit ears' antennae model with toroidal gain function to approximate their directional sensitivity. This identified a unique focal region of electrosensitivity directly in front of the mouth, and is the first evidence of a low-resolution electro-detector that solely facilitates prey ingestion.
... Mormyriforms and gymnotiforms also independently evolved electric organsmodified muscle cells that generate weak, high-frequency electric fieldsand "tuberous" electroreceptors that perceive electric organ discharges (self-generated and/or from other fish) for electrolocation and communication. Teleost electroreceptors cannot be homologous to non-teleost electroreceptors, as their electrophysiology is different and they respond to anodal stimuli rather than cathodal stimuli as in all non-teleost electroreceptors (Bodznick and Montgomery, 2005). However, they are innervated by lateral line nerves and the most plausible hypothesis, which remains to be tested, is that they evolved convergently via the genetic modification of neuromast hair cells (reviewed in Baker et al., 2013). ...
The lateral line system of anamniote vertebrates enables the detection of local water movement and weak bioelectric fields. Ancestrally, it comprises neuromasts – small sense organs containing mechanosensory hair cells - distributed in characteristic lines over the head and trunk, flanked on the head by fields of electroreceptive ampullary organs, innervated by afferent neurons projecting respectively to the medial and dorsal octavolateral nuclei in the hindbrain. Given the independent loss of the electrosensory system in multiple lineages, the development and evolution of the mechanosensory and electrosensory components of the lateral line must be dissociable. Nevertheless, the entire system arises from a series of cranial lateral line placodes, which exhibit two modes of sensory organ formation: elongation to form sensory ridges that fragment (with neuromasts differentiating in the center of the ridge, and ampullary organs on the flanks), or migration as collectives of cells, depositing sense organs in their wake. Intensive study of the migrating posterior lateral line placode in zebrafish has yielded a wealth of information concerning the molecular control of migration and neuromast formation in this migrating placode, in this cypriniform teleost species. However, our mechanistic understanding of neuromast and ampullary organ formation by elongating lateral line placodes, and even of other zebrafish lateral line placodes, is sparse or non-existent. Here, we attempt to highlight the diversity of lateral line development and the limits of the current research focus on the zebrafish posterior lateral line placode. We hope this will stimulate a broader approach to this fascinating sensory system.
... Many aquatic animals have the ability to detect naturally occurring electrical stimuli with specialized electroreceptors in their skin [1,2]. However, most of these electroreceptive animals can only detect weak electric fields originating in the environment by the help of their ampullary electroreceptors, a process that is called passive electrolocation [3,4]. In contrast, animals using active electrolocation actively emit electric signals into their environment and perceive these signals. ...
Weakly electric fish use a process called 'active electrolocation' to
orientate in their environment and to localize objects based on their
electrical properties. To do so, the fish discharge an electric organ
which emits brief electrical current pulses (electric organ discharge,
EOD) and in return sense the generated electric field which builds up
surrounding the animal. Caused by the electrical properties of nearby
objects, fish measure characteristic signal modulations with an array of
electroreceptors in their skin. The fish are able to gain important
information about the geometrical properties of an object as well as its
complex impedance and its distance. Thus, active electrolocation is an
interesting feature to be used in biomimetic approaches. We used this
sensory principle to identify different insertions in the walls of
Plexiglas tubes. The insertions tested were composed of aluminum, brass
and graphite in sizes between 3 and 20 mm. A carrier signal was emitted
and perceived with the poles of a commercial catheter for medical
diagnostics. Measurements were performed with the poles separated by 6.3
to 55.3 mm. Depending on the length of the insertion in relation to the
sender-receiver distance, we observed up to three peaks in the measured
electric images. The first peak was affected by the material of the
insertion, while the distance between the second and third peak strongly
correlated with the length of the insertion. In a second experiment we
tested whether various materials could be detected by using signals of
different frequency compositions. Based on their electric images we were
able to discriminate between objects having different resistive
properties, but not between objects of complex impedances.
... Further, derived electroreceptor primordia develop at the lateral edges of neuromast lines from a distinct cell lineage, similar to primitive electroreceptors (Northcutt, 2005;Vischer, 1989aVischer, , 1989b. Finally, like the primitive electrosensory system, it is clear that derived electrosensory systems are ontogenetically and phylogenetically related to the mechanosensory lateral line system (Bell & Maler, 2005;Bodznick & Montgomery, 2005), which does arise from placodes in teleosts (Ghysen & Dambly-Chaudi é re, 2004). These many similarities suggest at least some overlap in developmental gene regulatory networks for primitive and derived electroreceptors. ...
Mormyrid fishes communicate using pulses of electricity, conveying information about their identity, behavioral state, and location. They have long been used as neuroethological model systems because they are uniquely suited to identifying cellular mechanisms for behavior. They are also remarkably diverse, and they have recently emerged as a model system for studying how communication systems may influence the process of speciation. These two lines of inquiry have now converged, generating insights into the neural basis of evolutionary change in behavior, as well as the influence of sensory and motor systems on behavioral diversification and speciation. Here, we review the mechanisms of electric signal generation, reception, and analysis and relate these to our current understanding of the evolution and development of electromotor and electrosensory systems. We highlight the enormous potential of mormyrids for studying evolutionary developmental mechanisms of behavioral diversification, and make the case for developing genomic and transcriptomic resources. A complete mormyrid genome sequence would enable studies that extend our understanding of mormyrid behavior to the molecular level by linking morphological and physiological mechanisms to their genetic basis. Applied in a comparative framework, genomic resources would facilitate analysis of evolutionary processes underlying mormyrid diversification, reveal the genetic basis of species differences in behavior, and illuminate the origins of a novel vertebrate sensory and motor system. Genomic approaches to studying the evo-devo-neuroethology of mormyrid communication represent a deeply integrative approach to understanding the evolution, function, development, and mechanisms of behavior.
... Detection of electrical signals coming from the environment and estimating the position of their source is called passive electrolocation [4,5]. In the aquatic environment, weak electric fields of both abiotic and biotic origin can be found. ...
Building autonomous underwater robots is a challenging problem. Different sensory modalities have been employed successfully, some inspired by human and animal senses. The European ANGELS project uses an electric sense inspired by weakly electric fish. These fish have the unique ability to navigate and orient in complete darkness by using self-produced electrical fields. They emit electric signals into the environment, which in turn they perceive with an array of electroreceptor organs in their skin. The fish's whole body serves as an antenna, which shapes the emitted electrical field. As a result, the animals are able to detect, localize and analyze objects in their vicinity and to perceive a 3-dimensional electrical picture of their surroundings. Here, we review biological experimental results highlighting the animal's perceptual abilities, which allow them to navigate in extreme environments where vision can not be used. In addition, electric fishes use electric signals for communication. Behavioral communication strategies such as synchronization of electric signals and fixed-order-signaling can play a role in group coherence. Because of their unique sensory abilities, electric fish can serve as a model system for roboticists building underwater vehicles that can communicate and navigate in extreme environments where vision is not possible. In ANGELS, the electric sense is used to navigate a robot without knowledge of the surroundings, keep multi robots in formation, reconstruct an image of the environment and communicate between different robots - all inspired by our biological investigations.
... D. The same data plotted as a function of the increase in image contrast showing that all points are fitted by the same line systems must have sensory adaptation mechanisms allowing measurement of these changes in waveform and amplitude of the image due to a varying environment. Evidences from in vivo electrophysiological recordings confirm this hypothesis (Bell et al., 1993; Bodznick and Montgomery, 1994; Bastian, 1995; Bell et al., 1997; Mohr et al., 2003; Bastian et al., 2004; Pereira et al., 2005; Caputi et al., 2008). 6 What " merkwelt " can be constructed with electroreception? ...
https://www.researchgate.net/publication/237082166_pereira_y_caputi/file/3deec51b6864462661.pdf
... The reduction of canal length in free ampullae may move the ampullary bulb out of an ampullary capsule, which may increase background noise (Kalmijn 1974). The decrease in sensitivity may not matter because the electrical signals detected in fresh water are much stronger than those detected in the marine environment (Bodznick and Montgomery 2005). Himantura dalyensis, like D. sabina (Puzdrowski and Leonard 1993), D. zugei, H. gerrardi and H. uarnak (Chu and Wen 1979), possesses three groups of ampullary clusters. ...
Mechanoreceptive and electroreceptive anatomical specialisations in freshwater elasmobranch fishes are largely unknown. The freshwater whipray, Himantura dalyensis, is one of a few Australian elasmobranch species that occur in low salinity (oligohaline) environments. The distribution and morphology of the mechanoreceptive lateral line and the electroreceptive ampullae of Lorenzini were investigated by dissection and compared with previous studies on related species. The distribution of the pit organs resembles that of a marine ray, Dasyatis sabina, although their orientation differs. The lateral line canals of H. dalyensis are distributed similarly compared with two marine relatives, H. gerrardi and D. sabina. However, convolutions of the ventral canals and proliferations of the infraorbital canal are more extensive in H. dalyensis than H. gerrardi. The intricate nature of the ventral, non-pored canals suggests a mechanotactile function, as previously demonstrated in D. sabina. The ampullary system of H. dalyensis is not typical of an obligate freshwater elasmobranch (i.e. H. signifer), and its morphology and pore distribution resembles those of marine dasyatids. These results suggest that H. dalyensis is euryhaline, with sensory systems adapted similarly to those described in marine and estuarine species.
... The ampullae are tonic receptors that adapt to dc fields within seconds [Kalmijn, 1974 [Kalmijn, , 1978 Aadland, 1992]. The adaptation to dc fields has two consequences: first, the animal has to move with respect to the dc field in order to detect it, and second, it enables elasmobranchs to detect weak, modulated voltage gradients in the presence of their own bioelectric field [Kalmijn, 1974 [Kalmijn, , 1978; Bodznick and Montgomery, 2005] . However, the ampullae of Lorenzini are low-frequency electroreceptors that detect electric fields of frequencies near dc to at least 15 Hz [Bodznick and Boord, 1986]. ...
The ampullae of Lorenzini are the electroreceptors of elasmobranchs. Ampullary pores located in the elasmobranch skin are each connected to a gel-filled canal that ends in an ampullary bulb, in which the sensory epithelium is located. Each ampulla functions as an independent receptor that measures the potential difference between the ampullary pore opening and the body interior. In the elasmobranch head, the ampullary bulbs of different ampullae are aggregated in 3-6 bilaterally symmetric clusters, which can be surrounded by a connective tissue capsule. Each cluster is innervated by one branch of the anterior lateral line nerve (ALLN). Only the dorsal root of the ALLN carries electrosensory fibers, which terminate in the dorsal octavo-lateral nucleus (DON) of the medulla. Each ampullary cluster projects into a distinctive area in the central zone of the DON, where projection areas are somatotopically arranged. Sharks and rays can possess thousands of ampullae. Amongst other functions, the use of electroreception during prey localization is well documented. The distribution of ampullary pores in the skin of elasmobranchs is influenced by both the phylogeny and ecology of a species. Pores are grouped in distinct pore fields, which remain recognizable amongst related taxa. However, the density of pores within a pore field, which determines the electroreceptive resolution, is influenced by the ecology of a species. Here, I compare the pore counts per pore field between rhinobatids (shovelnose rays) and pristids (sawfish). In both groups, the number of ampullary pores on the ventral side of the rostrum is similar, even though the pristid rostrum can comprise about 20% of the total length. Ampullary pore numbers in pristids are increased on the upper side of the rostrum, which can be related to a feeding strategy that targets free-swimming prey in the water column. Shovelnose rays pin their prey onto the substrate with their disk, while repositioning their mouth for ingestion and thus possess large numbers of pores ventrally around the mouth and in the area between the gills.
... Three different types of electroreceptors are used for electroreception. The ampullary organs provide information about low-frequency external electrical fields (Bennett, 1971;Szabo, 1974;Bodznick & Montgomery, 2005) and are used in passive electrolocation. Secondly 'Knollenorgans' are responsive to the high frequencies contained in the EODs of conspecifics and are used in intra-specific electrocommunication (Bennett, 1965;Xu-Friedman & Hopkins, 1999). ...
Gnathonemus petersii and other African weakly electric fish (Mormyridae) produce electric signals in order to sense their environment, a process called active electrolocation. During active electrolocation electrical images of objects in the environment are cast onto a mosaic of electroreceptors, which are embedded in the animal's skin. In Gn. petersii and four other species of mormyrid fish, the densities of electroreceptor organs (mormyromasts and ampullary organs) were determined at various skin regions, including the chin, the nasal region and the back. In all species investigated, the highest mormyromast densities were found at the chin, followed by the nasal region. In addition to this comparative approach, we investigated the electroreceptive epidermis of Gn. petersii in more detail. At the moveable chin appendix, the Schnauzenorgan, scanning electron microscopy analysis helped to elucidate the mosaic-like distribution and the morphology of the electroreceptor organs and their embedding in the epidermis. Because the number of mormyromasts increased very little when fish got bigger, receptor organ densities decreased with standard length. Mormyromast density at the Schnauzenorgan, especially at its tip, highly exceeded that at all other skin regions. Along the Schnauzenorgan, receptor densities decreased exponentially from the tip towards the base. At the nasal region, mormyromast densities were more than three times higher compared to the rest of the fish's head and trunk. A similar distribution to that of the mormyromasts was found for the ampullary electroreceptor organs, which are used for passive electroreception. Our findings support the hypothesis that at least in Gn. petersii the Schnauzenorgan and the nasal region are electroreceptive foveae.
... An external mass of granule cells, the dorsal granular ridge, gives rise to the parallel fibres, which run in a rostro-caudal direction and comprise the molecular layer of the DON (Bodznick & Boord, 1986;Bell & Maler, 2005). Based on anatomical (Bodznick & Boord, 1986;Schmidt & Bodznick, 1987) and physiological (Conley & Bodznick, 1994;Hjelmstad et al., 1996;New, 2001;Bodznick & Montgomery, 2005) evidence, the dorsal granular ridge receives a variety of inputs, including higher order electrosensory input, proprioceptive information and motor corollary discharge signals (Montgomery et al., 1995;Bell, 2002). ...
... These objects therefore excite the tuberous class of electroreceptors (receptors tuned to the fish's own EOD; Kawasaki, 2005). Animals emit weak electric fields (e.g., during respiration), and these are detected by the ampullary class of electroreceptors (Fortune and Rose, 1997;Bodznick and Montgomery, 2005;Wilkens and Hofman, 2005;Eeuwes et al., 2008). Prey and predators (not plants) will therefore excite both ampullary and tuberous electroreceptors within the same localized patch of skin. ...
The present article reports on the telencephalic connections of regions of the dorsal telencephalon of the weakly electric fish Apteronotus leptorhynchus and Gymnotus sp. that are involved in learning and memory: the lateral (DL), central (DC), and dorsal (DD) regions of the pallium and the intermediate region between DL and DC (Dx). We find that the main route of transmission consists of diencephalic (preglomerular complex; PG) glutamatergic input to DL; glutamatergic projections from DL to DC and Dx; and glutamatergic output from DC/Dx to di-, mes-, and rhombencephalic nuclei. Although PG efferents to DL are spatially organized, the projection from DL to DC appears to be diffuse. The connections of DD are entirely intrinsic to the pallium: DL projects to DD (glutamatergic) and DD feeds back to DL (glutamatergic); DD also projects to DC and has strong contralateral connections. In addition, DL and DD receive input from subpallial regions; we suggest that these are associated with the previously identified γ-aminobutyric acid (GABA)-ergic, dopaminergic, and somatostatin-positive input to these regions. The DL/DD connections are very complex, because DL projects to and receives input from different subdivisions of DD. These subdivisions are linked by circuitry intrinsic to DD itself. DL and DD both contain recurrent putatively excitatory (glutamatergic) connections as well as local putatively inhibitory (GABAergic) interneurons. In contrast, recurrent excitatory connections appears to be absent in DC, and local inhibition is also barely present. Finally, we speculate on the implications of this pattern of connectivity for theories of short-term memory and long-term associative memory.
Electricity, the interaction between electrically charged objects, is widely known to be fundamental to the functioning of living systems. However, this appreciation has largely been restricted to the scale of atoms, molecules, and cells. By contrast , the role of electricity at the ecological scale has historically been largely neglected, characterised by punctuated islands of research infrequently connected to one another. Recently, however, an understanding of the ubiquity of electrical forces within the natural environment has begun to grow, along with a realisation of the multitude of ecological interactions that these forces may influence. Herein, we provide the first comprehensive collation and synthesis of research in this emerging field of electric ecology. This includes assessments of the role electricity plays in the natural ecology of predator-prey interactions, pollination, and animal dispersal, among many others, as well as the impact of anthropogenic activity on these systems. A detailed introduction to the ecology and physiology of electroreception-the biological detection of ecologically relevant electric fields-is also provided. Further to this, we suggest avenues for future research that show particular promise, most notably those investigating the recently discovered sense of aerial electroreception.
Zwischen zwei ungleich geladenen Teilchen entsteht ein elektrisches Feld, in dem eine Ladung auf die andere eine Kraft ausübt. Der Betrag dieser elektrostatischen Kraft ist proportional zum Produkt der beiden Ladungsmengen und umgekehrt proportional zum Quadrat des Abstands der Ladungsmittelpunkte (Coulomb-Gesetz). Die elektrostatische Kraft wirkt je nach Vorzeichen der Ladungen anziehend oder abstoßend. Elektrische Felder werden durch das Vektorfeld der elektrischen Feldstärke beschrieben. Das Vektorfeld ordnet jedem Punkt im Raum einen Vektor für die Richtung und einen Betrag für die elektrische Feldstärke zu (Einheit: Volt pro Meter, V m–1). Elektrische Feldlinien laufen definitionsgemäß von Plus nach Minus. Konstanter Gleichstrom (DC-Strom; Strom ist gleich Ladung pro Zeit; Einheit: Ampere = Coulomb s–1) ist ein elektrischer Strom, dessen Stärke und Richtung sich über die Zeit nicht ändern. Wechselstrom (AC-Strom) ist ein Strom, der seine Richtung (Polung) regelmäßig wechselt und über die Zeit gemittelt null ist. Eine entsprechende Definition gilt für die Begriffe Gleichspannung und Wechselspannung. Die elektrische Leitfähigkeit (Einheit: Siemens pro Meter, S m–1) gibt die Fähigkeit eines Stoffs an, elektrischen Strom zu leiten. Den Kehrwert der elektrischen Leitfähigkeit nennt man elektrische Widerstand (Einheit: Ohm, Ω). Ein Ohm’scher Widerstand ist ein elektrischer Widerstand, der im Gleichstromkreis genau so groß ist wie im Wechselstromkreis. Kondensatoren haben einen kapazitiven Widerstand (jeder Kondensator setzt einem Stromfluss einen frequenzabhängigen Widerstand entgegen, bei Gleichstrom ist dieser Widerstand unendlich groß). Der elektrische Widerstand eines Kondensators (Xc) hängt von der Kapazität des Kondensators und der Frequenz der anliegenden Wechselspannung ab (Xc = 1/2 π F C, mit F = Frequenz und C = Kapazität des Kondensators). Komplexe Widerstände (z. B. Widerstände der Pflanzen- und Tiergewebe) setzen sich sowohl aus einem Ohm’schen als auch aus einem kapazitiven Widerstand zusammen.
Synopsis
We review the lateral line and electroreceptor systems among craniates and highlight unique gains and losses. Distinctive features permit grouping of derived animals with respect to similarities (stereocilia and kinocilia length) and share with a single afferent versus two afferents among electroreceptors and lateral line, respectively. Transformations of the dorsal and intermediate nuclei exceeds both in loss and gain among vertebrates, in particular derived bony fishes. We are providing an integrated perspective of various craniates, taking both evolution and development into a unique perspective of neurons, hair cells, as well as dorsal and intermediate nuclei into consideration.
Synopsis
The ability to actively generate an electric field and use it's distortions for navigation, object detection and communication requires a specialized sensory organ, the tuberous electroreceptors. This chapter reviews the basic physiological properties, discusses similarities and differences across species and then focuses on the active electrosensory system of South American Gymnotiform fish. The primary electroreceptor afferents have served as a model system for general questions of neural coding reaching far beyond the electrosensory system. Addressed topics arch from stimulus encoding in single neurons and neuronal populations to coding with bursts and synchrony combined and supplemented with modeling approaches.
Synopsis
Many fishes and amphibians use their passive electrosensory system to detect prey or to avoid predators. In this chapter we review how the paddlefish (Polyodon spathula), a fish that has up to 70, 000 electroreceptors, has contributed to our understanding of the passive electric sense.
The first relays of the vertebrate electrosensory system arise from epidermal specializations with voltage-sensitive receptor cells that are tuned to the relevant frequencies of bioelectric fields. Despite diverse phylogenetic origins and adaptations to varying habitats, electroreceptor organs share a number of morphological and functional characteristics to facilitate the detection of low-intensity electric fields. Much of the current knowledge of physiological mechanisms underlying electrosensory transduction has been gleaned from in vivo electrophysiological recordings from primary electrosensory afferents or recordings of electrical impulses from the organs themselves. Recent advances in genetic and patch-clamp electrophysiological techniques have made detailed comparisons of the molecular mechanisms of transduction possible. These comparisons have the potential to shed light on convergent mechanisms of stimulus transduction and filtering among diverse species as well as broad themes of signal transduction relevant to other hair cell-based sensory systems.
In the jawless lampreys, most nonteleost jawed fishes, and aquatic-stage amphibians, the lateral line system has a mechanosensory division responding to local water movement (“distant touch”) and an electrosensory division responding to low-frequency cathodal (exterior-negative) electric stimuli, such as the weak electric fields surrounding other animals. The electrosensory division was lost in the ancestors of teleost fishes and their closest relatives and in the ancestors of frogs and toads. However, anodally sensitive lateral line electroreception evolved independently at least twice within teleosts, most likely via modification of the mechanosensory division. This chapter briefly reviews this sensory system and describes our current understanding of the development of nonteleost lateral line electroreceptors, both in terms of their embryonic origin from lateral line placodes and at the molecular level. Gene expression analysis, using candidate genes and more recent unbiased transcriptomic (differential RNA sequencing) approaches, suggests a high degree of conservation between nonteleost electroreceptors and mechanosensory hair cells both in their development and in aspects of their physiology, including transmission mechanisms at the ribbon synapse. Taken together, these support the hypothesis that electroreceptors evolved in the vertebrate ancestor via the diversification of lateral line hair cells.
This chapter provides an overview of the three aspects: passive electrolocation; the generation of electric fields; and active electrolocation. There are two basic types of fish electroreceptors, tuberous and ampullary. The tuberous receptors are concerned with active electrolocation, while the ampullary receptors are the ones that detect the 'unintentional' electrical emissions of other animals. Although the weak electric organ discharge (EOD) almost certainly evolved before the strong, the chapter deals with the latter first. The electric eel, Electrophoros electricus, is a big freshwater fish. It is an apex predator that stuns its prey by electric shock using the large and complex electric organ. The organ has three compartments; a main organ, which is responsible for generating most of the high voltage EOD, a more caudal organ of Sachs and a ventrally located Hunter's organ. The latter two compartments generate weaker electric fields that are used in active electrolocation.
The mechanosensory lateral line system is one component of a multisensory array derived from the embryonic dorsolateral placode series. This chapter describes the evolutionary history of the lateral line system, including the associated electroreceptive systems. The major morphological and physiological characteristics and the behavioral significance are described for each system. The arrangement of both systems in each group of vertebrates is described systematically. Neuromasts, the sensory unit of the lateral line system, arose with the origin of vertebrates, and multiple types are found in all gnathostome lineages. Electroreceptors arose at the same time or slightly later, but have been lost and reevolved multiple times. Several descendent taxa also evolved electrogenic organs and an active electrosensory system.
With a special electric organ, weakly electric fish emit electric signals, each of which builds up an electric field around them in the water. To sense locally occurring voltages caused by their own signals, the fish use thousands of electroreceptor organs distributed over their skin. Nearby objects are detected because they distort the self-produced electric field and thus project electric images onto the array of electroreceptors. By analysing these electric images, the fish can detect and localize objects in the water and recognize their electrical and spatial properties. Inspired by these remarkable capabilities of weakly electric fish, we designed technical sensor systems that can solve similar sensing problems. We applied the principles of active electrolocation by building devices that produce electrical current pulses and simultaneously sense local current densities. Depending on the specific task, sensors can be designed which (i) detect an object, (ii) localize it in space, (iii) determine its distance and (iv) measure its electrical properties. Our biomimetic sensor systems proved to be insensitive to environmental disturbances such as heat, pressure or turbidity. They can be used in a wide range of applications, such as material identification, remote distance measurements and medical diagnostics.
This chapter describes the central neuroanatomy of the mechanosensory and electrosensory lateral line system in each craniate group (hagfishes, lampreys, cartilaginous and ray-finned fishes, lobe-finned fishes). It may be concluded that the mechanosensory lateral line system is ancestral for craniates (including hagfishes and vertebrates), and that electroreception is ancestral for vertebrates (including lampreys and gnathostomes). Many peripheral (cranial nerves) and central nervous commonalities are noted for the two sensory systems. The main focus is on ascending (lateral lemniscal) multisynaptic pathways from primary rhombencephalic via midbrain and diencephalic centers into dorsal telencephalic (pallial) centers. There is a parallel pattern of ascending connectivity of the two modalities up to the midbrain in lampreys, cartilaginous and ray-finned fishes as well as in amphibians. Basal ray-finned fishes resemble cartilaginous fishes in many details, whereas teleosts (derived ray-finned fishes) lose the electrosensory system, only to have it re-evolve various times. In the diencephalon, depending on the taxon, three general areas may be involved in lateral line processing: dorsal thalamus, posterior tuberculum and hypothalamus. The question of whether parallel processing of lateral line electrosense and mechanosense is maintained in the diencephalon and telencephalon is discussed in the different taxa. Within the telencephalon, the medial pallium (hippocampus homologue) in gnathostomes, and maybe lampreys, may represent the ancestral recipient of diencephalic lateral line input. However, tetrapods (amphibians) show input from lateral line related diencephalic centers to the subpallial striatum and not the pallium.
Many groups of fishes perceive naturally occurring electric stimuli. They possess ampullary electroreceptor organs that respond to low‐frequency electric fields. Two nocturnally active teleost groups produce weak electric signals (electric organ discharges, EOD), which they perceive with tuberous electroreceptor organs. In addition to “passive electrolocation,” these weakly electric fish perform “active electrolocation,” during which they detect alterations of their EOD caused by nearby objects. This enables them to perceive the complex impedance of objects and thus to identify animated objects. In addition, they can measure distance, size, shape, and other 3D object properties. When inspecting an object, the weakly electric fish Gnathonemus petersii employs two “electrical foveae" that are located on their moveable chin appendage and in the nasal region. The former is used for object inspection, while the latter is used for object detection during foraging. The brain of weakly electric fishes extracts information about objects by analyzing the input from the electroreceptor organs. The study of electroreceptive brain areas has revealed many general principals of neural processing of sensory and motor information.
The lateral line system of fishes and amphibians comprises two ancient sensory systems: mechanoreception and electroreception. Electroreception is found in all major vertebrate groups (i.e. jawless fishes, cartilaginous fishes, and bony fishes); however, it was lost in several groups including anuran amphibians (frogs) and amniotes (reptiles, birds, and mammals), as well as in the lineage leading to the neopterygian clade of bony fishes (bowfins, gars, and teleosts). Electroreception is mediated by modified "hair cells," which are collected in ampullary organs that flank lines of mechanosensory hair cell containing neuromasts. In the axolotl (a urodele amphibian), grafting and ablation studies have shown a lateral line placode origin for both mechanosensory neuromasts and electrosensory ampullary organs (and the neurons that innervate them). However, little is known at the molecular level about the development of the amphibian lateral line system in general and electrosensory ampullary organs in particular. Previously, we identified Eya4 as a marker for lateral line (and otic) placodes, neuromasts, and ampullary organs in a shark (a cartilaginous fish) and a paddlefish (a basal ray-finned fish). Here, we show that Eya4 is similarly expressed during otic and lateral line placode development in the axolotl (a representative of the lobe-finned fish clade). Furthermore, Eya4 expression is specifically restricted to hair cells in both neuromasts and ampullary organs, as identified by coexpression with the calcium-buffering protein Parvalbumin3. As well as identifying new molecular markers for amphibian mechanosensory and electrosensory hair cells, these data demonstrate that Eya4 is a conserved marker for lateral line placodes and their derivatives in all jawed vertebrates.
The suppression of self-generated electrosensory noise (reafference) and other predictable signals in the elasmobranch medulla is accomplished in part by an adaptive filter mechanism, which now appears to represent a more universal form of the modifiable efference copy mechanism discovered by Bell, It also exists in the gymnotid electrosensory lateral lobe and mechanosensory lateral line nucleus in other teleosts, In the skate dorsal nucleus, motor corollary discharge, proprioceptive and descending electrosensory signals all contribute in an independent and additive fashion to a cancellation input to the projection neurons that suppresses their response to reafference, The form of the cancellation signal is quite stable and apparently well-preserved between bouts of a particular behavior, but it can also be modified within minutes to match changes in the form of the reafference associated with that behavior. Motor corollary discharge, proprioceptive and electrosensory inputs are each relayed to the dorsal nucleus from granule cells of the vestibulolateral cerebellum. Direct evidence from intracellular studies and direct electrical stimulation of the parallel fiber projection support an adaptive filter model that places a principal site of the filter's plasticity at the synapses between parallel fibers and projection neurons.
Elasmobranch fish have an electrosensory system which they use for prey detection and for orientation. Sensory inputs to this system are corrupted by a form of reafference generated by the animal's own ventilation, but this noise is reduced by sensory processing within the medullary nucleus of the electrosensory system. This noise cancellation is achieved, at least in part, by a common mode rejection mechanism. In this study we have examined characteristics of neurones within the medullary nucleus in an attempt to understand the neural circuitry responsible for common mode suppression. Our results are in accord with previous indications that ascending efferent neurones of the medullary nucleus are monosynaptically activated from the ipsilateral electrosensory nerves and project to the midbrain. We demonstrate that in Raja erinacea, as has been previously shown in one other species (Cephaloscyllium isabella), ascending efferent neurones typically have a discrete focal excitatory receptive field and an inhibitory receptive field which may be discrete or diffuse and which often includes a contralateral component. We identify a group of interneurones within the medullary nucleus which are driven monosynaptically from the electrosensory nerves, have simple discrete excitatory receptive fields and respond vigorously to imposed common mode signals. The simplest model of the circuitry underlying common mode rejection that is consistent with the evidence is that direct afferent input impinges onto the basal dendrites of the ascending efferent neurones and onto interneurones within the nucleus, and the interneurones in turn inhibit the ascending efferents. The pattern of this projection, including commissural inputs, determines the nature and extent of ascending efferents' inhibitory surrounds and mediates the suppression of common mode signals.
Elasmobranchs have an electric sense that is sensitive enough to detect electric fields as weak as those induced through their bodies as they swim through the earth’s magnetic field. Because the intensity and direction of these fields are related to the speed and direction of the movements that cause them, elasmobranchs could use their electric sense in navigation. There is evidence that they do. According to a current theory, elasmobranchs can determine their direction of motion in an Earth-fixed frame using a computation involving electroreceptor voltages, swimming speed and the local geomagnetic field vector. However, this theory is inconsistent with physical and biological constraints, notably that elasmobranch electroreceptors can not measure d.c. voltages, and that a voltage due to water flow in the ocean is not uniquely interpretable in terms of the speed and direction of flow at the point where the electrical measurement is made. This paper presents a new theory that explains how an elasmobranch could use its electric sense to determine a compass bearing as it swims. According to this theory, the direction cue is the directional asymmetry of the change in induced electroreceptor voltage during turns. A neural network could use this cue to determine swimming direction by comparing vestibular and electrosensory signals.
Elasmobranch fishes have an electroreceptive system which they use for prey detection and orientation. Sensory inputs in this system are corrupted by a form of reafference generated by the animal's own ventilation. However, we show here that in the carpet shark, Cephaloscylium isabella, as in two previously studied batoid species, this ventilatory ‘noise’ is reduced by sensory processing within the medullary nucleus of the electrosensory system. It has been proposed that the noise cancellation is achieved by a common mode rejection mechanism. One prediction of this hypothesis is that secondary neurons within the medullary nucleus should have both excitatory and inhibitory components to their receptive fields. This prediction is experimentally verified here. Projection neurons of the medullary nucleus in the carpet shark typically have a focal excitatory, and a diffuse inhibitory, receptive field organization including a component of contralateral inhibition. This result provides strong support for the hypothesis that ventilatory suppression in the elasmobranch electrosensory system is achieved by a common mode mechanism.
Note: Department of Biology, Wesleyan University, Middletown, CT 06457, USA.
Present address: Department of Zoology, University of Auckland, Auckland, New Zealand.
The electroreceptors of elasmobranchs are strongly modulated by the fish's own ventilation but this source of potential interference is suppressed within the medulla. The mechanism for the suppression is thought to be based on the common mode nature of the ventilatory noise, i.e. it is of the same amplitude and phase for all of the electroreceptors, compared with environmental electric fields which affect the receptors differentially. Evidence for the common mode suppression hypothesis is provided here in skates by the observation that the response to an artificial common mode stimulus that is independent of ventilation and delivered through an electrode inserted into the animal's gut is also suppressed by the medullary neurons; the extent to which a particular neuron suppresses the responses to the gut stimulus and to ventilation is similar. In addition, a potential modulation of 5–150μV is measured between the skate's interior and the sea water during ventilation and this appears to be responsible for the self-stimulation. By passing d.c. or sinusoidal currents through the gut electrode it is demonstrated that this ventilatory potential is due to the variable shunting of a standing d.c. potential across the fish's skin by the opening and closing of the mouth and gill slits during ventilation. Osmoregulatory ion-pumping appears to contribute to the production of the d.c. potential.
Note: Present address: Department of Biology, Wesleyan University, Middletown, CT 06457, USA.
Present address: Department of Zoology, University of Auckland, Auckland, New Zealand.
The electrosensory lateral line lobe (ELL) of mormyrid electric fish is a cerebellum-like structure that receives primary afferent input from electroreceptors in the skin. Purkinje-like cells in ELL store and retrieve a temporally precise negative image of prior sensory input. The stored image is derived from the association of centrally originating predictive signals with peripherally originating sensory input. The predictive signals are probably conveyed by parallel fibers. Recent in vitro experiments have demonstrated that pairing parallel fiber-evoked excitatory postsynaptic potentials (epsps) with postsynaptic spikes in Purkinje-like cells depresses the strength of these synapses. The depression has a tight dependence on the temporal order of pre- and postsynaptic events. The postsynaptic spike must follow the onset of the epsp within a window of about 60 msec for the depression to occur and pairings at other delays yield a nonassociative enhancement of the epsp. Mathematical analyses and computer simulations are used here to test the hypothesis that synaptic plasticity of the type established in vitro could be responsible for the storage of temporal patterns that is observed in vivo. This hypothesis is confirmed. The temporally asymmetric learning rule established in vitro results in the storage of activity patterns as observed in vivo and does so with significantly greater fidelity than other types of learning rules. The results demonstrate the importance of precise timing in pre- and postsynaptic activity for accurate storage of temporal information.
When physiological conditions are simulated, skate electroreceptors produce small maintained oscillatory currents. Larger damped oscillations of similar time-course are observed in voltage clamp. Subtraction of leakage in voltage clamp data shows that the oscillations involve no net outward current across the lumenal surface of the epithelium. The oscillations are much faster than the late outward current generated by the lumenal membranes of the receptor cells. Treatment of the basal surface of the epithelium with tetraethyl ammonium (TEA), high K, Co, or EGTA reversibly blocks the oscillations in voltage clamp, but has little or no effect on the epithelial action potential in current clamp or on the current-voltage relation. The TEA sensitivity of the oscillations indicates that they involve a potassium conductance in the basal membranes of the receptor cells. Treatment of the basal membranes with TEA and high calcium, with strontium, or with barium causes these membranes to produce large regenerative responses. Direct stimulation of the basal membranes then elicits a lumen-positive action potential whereas stimulation of the lumenal membranes elicits a diphasic action potential. Excitability of the basal membranes is abolished by extracellular Co, Mn, or La. Modulation of the lumenal membrane calcium conductance by the basal membrane conductances probably gives rise to the oscillatory receptor currents evoked by small voltage stimuli. The slower calcium-activated late conductance in the lumenal membranes may be involved in sensory accommodation.
In the isolated sensory epithelium of the Plotosus electroreceptor, the receptor current has been dissected into inward Ca current, ICa, and superimposed outward transient of Ca-gated K current, IK(Ca). In control saline (170 mM/liter Na), with IK(Ca) abolished by K blockers, ICa declined in two successive exponential phases with voltage-dependent time constants. Double-pulse experiments revealed that the test ICa was partially depressed by prepulses, maximally near voltage levels for the control ICa maximum, which suggests current-dependent inactivation. In low Na saline (80 mM/liter), ICa declined in a single phase with time constants similar to those of the slower phase in control saline. The test ICa was then unaffected by prepulses. The implied presence of two Ca current components, the fast and slow ICa's, were further examined. In control saline, the PSP externally recorded from the afferent nerve showed a fast peak and a slow tonic phase. The double-pulse experiments revealed that IK(Ca) and the peak PSP were similarly depressed, i.e., secondarily to inactivation of the peak current. The steady inward current, however, was unaffected by prolonged prepulses that were stepped to 0 mV, the in situ DC level. Therefore, the fast ICa seems to initiate IK(Ca) and phasic release of transmitter, which serves for phasic receptor responses. The slow ICa may provide persistent active current, which has been shown to maintain tonic receptor operation.
The tonic electroreceptors of the marine catfish Plotosus consist of a cluster of ampullae of sensory epithelia, each of which is an isolated receptor unit that is attached to the distant skin with only a long duct. The single-cell layered sensory epithelium has pear-shaped receptor cells interspersed with thin processes of supporting cells. The apical border of the receptor cells is joined to the supporting cells with junctional complexes. Single ampullae were excised and electrically isolated by an air gap. Receptor responses were recorded as epithelial current under voltage clamp, and postsynaptic potentials (PSP) were recorded externally from the afferent nerve in the presence of tetrodotoxin. The ampulla showed a DC potential of -19.2 +/- 6.5 mV (mean +/- SD, n = 18), and an input resistance of 697 +/- 263 K omega (n = 21). Positive voltage steps evoked inward currents with two peaks and a positive dip, associated with PSPs. The apical membrane proved to be inactive. The inward current was ascribed to Ca current, and the positive dip to Ca-gated transient K current, bot in the basal membrane of receptor cells. The Ca channels proved to have ionic selectivity in the order of Sr2+ greater than Ca2+ greater than Ba2+, and presumably they also passed outward current nonselectively. Double-pulse experiments further revealed a current-dependent inactivation for a part of the Ca current.
African electric fish of a pulse species, Brienomyrus brachyistius (Mormyridae), housed singly in a large, circular arena, were presented with electrical stimuli which mimicked a conspecific intruder. Stimuli were produced with either dipolar or bipolar electrodes in three different geometries. We tracked the unconditioned approach response paths taken by the fish and compared tracks for each of the geometries. The results suggest that B. brachyistius can determine neither the distance nor the direction of an electric dipole from afar, but that they do manage to find the source by maintaining a precise alignment of their body axis parallel to the direction of the local electric field vector (parallel to current lines) while swimming. This behaviour ultimately leads to the current source. We propose that this behaviour may be a simple mechanism mediating the approach response of one electric fish to another.
Ampullae of Lorenzini are sensitive electroreceptors. Applied potentials affect receptor cells which transmit synaptically to afferent fibers. Cathodal stimuli in the ampullary lumen sometimes evoke all-or-none "receptor spikes," which are negative-going recorded in the lumen, but more frequently they evoke graded damped oscillations. Cathodal stimuli evoke nerve discharge, usually at stimulus strengths subthreshold for obvious receptor oscillations or spikes. Anodal stimuli decrease any ongoing spontaneous nerve activity. Cathodal stimuli evoke long-lasting depolarizations (generator or postsynaptic potentials) in afferent fibers. Superimposed antidromic spikes are reduced in amplitude, suggesting that the postsynaptic potentials are generated similarly to other excitatory postsynaptic potentials. Anodal stimuli evoke hyperpolarizations of nerves in preparations with tonic activity and in occasional silent preparations; presumably tonic release of excitatory transmitter is decreased. These data are explicable as follows: lumenal faces of receptor cells are tonically (but asynchronously) active generating depolarizing responses. Cathodal stimuli increase this activity, thereby leading to increased depolarization of and increased release of transmitter from serosal faces, which are inexcitable. Anodal stimuli act oppositely. Receptor spikes result from synchronized receptor cell activity. Since cathodal stimuli act directly to hyperpolarize serosal faces, strong cathodal stimuli overcome depolarizing effects of lumenal face activity and are inhibitory. Conversely, strong anodal stimuli depolarize serosal faces, thereby causing release of transmitter, and are excitatory. These properties explain several anomalous features of responses of ampullae of Lorenzini.
Synaptic plasticity occurs in several regions of the vertebrate brain and is believed to mediate the storage of behaviorally significant information during learning. Synaptic plasticity is well demonstrated in most cases, but the behavioral meaning of the relevant neural signals and the behavioral role of the plasticity are uncertain. In this paper we describe a case of synaptic plasticity which involves identifiable sensory and motor signals and which appears to mediate the storage of an image of past sensory input. Corollary discharge signals associated with the motor command that drives the electric organ are prominent in the electrosensory lobe of mormyrid electric fish. Some of these corollary discharge signals elicit a negative image or representation of the electrosensory input pattern that has followed recent motor commands. When the temporal and spatial pattern of sensory input changes, the corollary discharge effect also changes in a corresponding manner. The cellular mechanisms by which the corollary discharge-evoked representation is stored were investigated by intracellular recording from cells of the electrosensory lobe and pairing intracellular current pulses with the corollary discharge signal. The results indicate that the representation of recent sensory input is stored by means of anti-Hebbian plasticity at the synapses between corollary discharge-conveying fibers and cells of the electrosensory lobe. The results also suggest that dendritic spikes and plasticity at inhibitory synapses are involved in the phenomenon.
The electrosensory system of elasmobranchs is extremely sensitive to weak electric fields, with behavioral thresholds having been reported at voltage gradients as low as 5 nV/cm. To achieve this amazing sensitivity, the electrosensory system must extract weak extrinsic signals from a relatively large reafferent background signal associated with the animal's own movements. Ventilatory movements, in particular, strongly modulate the firing rates of primary electrosensory afferent nerve fibers, but this modulation is greatly suppressed in the medullary electrosensory processing nucleus, the dorsal octavolateral nucleus. Experimental evidence suggests that the neural basis of reafference suppression involves a common-mode rejection mechanism supplemented by an adaptive filter that fine tunes the cancellation. We present a neural model and computer simulation results that support the hypothesis that the adaptive component may involve an anti-Hebbian form of synaptic plasticity at molecular layer synapses onto ascending efferent neurons, the principal output neurons of the nucleus. Parallel fibers in the molecular layer carry a wealth of proprioceptive, efference copy, and sensory signals related to the animal's own movements. The proposed adaptive mechanism acts by canceling out components of the electrosensory input signal that are consistently correlated with these internal reference signals.
Cerebellum-like structures in fish appear to act as adaptive sensory processors, in which learned predictions about sensory input are generated and subtracted from actual sensory input, allowing unpredicted inputs to stand out. Pairing sensory input with centrally originating predictive signals, such as corollary discharge signals linked to motor commands, results in neural responses to the predictive signals alone that are 'negative images' of the previously paired sensory responses. Adding these 'negative images' to actual sensory inputs minimizes the neural response to predictable sensory features. At the cellular level, sensory input is relayed to the basal region of Purkinje-like cells, whereas predictive signals are relayed by parallel fibres to the apical dendrites of the same cells. The generation of negative images could be explained by plasticity at parallel fibre synapses. We show here that such plasticity exists in the electrosensory lobe of mormyrid electric fish and that it has the necessary properties for such a model: it is reversible, anti-hebbian (excitatory postsynaptic potentials (EPSPs) are depressed after pairing with a postsynaptic spike) and tightly dependent on the sequence of pre- and postsynaptic events, with depression occurring only if the postsynaptic spike follows EPSP onset within 60 ms.
The generation of expectations about sensory input and the subtraction of such expectations from actual input appear to be important features of sensory processing. This paper describes the generation of sensory expectations within cerebellum-like structures of four distinct groups of fishes: Mormyridae; Rajidae; Scorpaenidae; and Apteronotidae. These structures consist of a sheet-like array of principal cells. Apical dendrites of the principal cells extend out into a molecular layer where they are contacted by parallel fibers. The basilar regions of the arrays receive primary afferent input from octavolateral endorgans, i.e., electroreceptors, mechanical lateral line neuromasts, or eighth nerve endorgans. The parallel fibers in the molecular layer convey various types of information, including corollary discharge signals associated with motor commands, sensory information from other modalities such as proprioception, and descending input from higher stages of the sensory modality that is processed by the structure. Associations between the signals conveyed by the parallel fibers and particular patterns of sensory input to the basal layers lead to the generation of a negative image of expected sensory input within the principal cell array. Addition of this negative image to actual sensory input results in the subtraction of expected from actual input, allowing the unexpected or novel input to stand out more clearly. Intracellular recording indicates that the negative image is probably generated by means of anti-Hebbian synaptic plasticity at the parallel fiber to principal cell synapse. The results are remarkably similar in the different fishes and may generalize to cerebellum-like structures in other sensory systems and taxa.
I will briefly review the history of the bill sense of the platypus, a sophisticated combination of electroreception and mechanoreception that coordinates information about aquatic prey provided from the bill skin mechanoreceptors and electroreceptors, and provide an evolutionary account of electroreception in the three extant species of monotreme (and what can be inferred of their ancestors). Electroreception in monotremes is compared and contrasted with the extensive body of work on electric fish, and an account of the central processing of mechanoreceptive and electroreceptive input in the somatosensory neocortex of the platypus, where sophisticated calculations seem to enable a complete three-dimensional fix on prey, is given.
The suppression of self-generated electrosensory noise (reafference) and other predictable signals in the elasmobranch medulla is accomplished in part by an adaptive filter mechanism, which now appears to represent a more universal form of the modifiable efference copy mechanism discovered by Bell. It also exists in the gymnotid electrosensory lateral lobe and mechanosensory lateral line nucleus in other teleosts. In the skate dorsal nucleus, motor corollary discharge, proprioceptive and descending electrosensory signals all contribute in an independent and additive fashion to a cancellation input to the projection neurons that suppresses their response to reafference. The form of the cancellation signal is quite stable and apparently well-preserved between bouts of a particular behavior, but it can also be modified within minutes to match changes in the form of the reafference associated with that behavior. Motor corollary discharge, proprioceptive and electrosensory inputs are each relayed to the dorsal nucleus from granule cells of the vestibulolateral cerebellum. Direct evidence from intracellular studies and direct electrical stimulation of the parallel fiber projection support an adaptive filter model that places a principal site of the filter's plasticity at the synapses between parallel fibers and projection neurons.
The mormyrid electrosensory lateral line lobe (ELL) is one of several different sensory structures in fish that behave as adaptive sensory processors. These structures generate negative images of predictable features in the sensory inflow which are added to the actual inflow to minimize the effects of predictable sensory features. The negative images are generated through a process of association between centrally originating predictive signals and sensory inputs from the periphery. In vitro studies in the mormyrid ELL show that pairing of parallel fiber input with Na+ spikes in postsynaptic cells results in synaptic depression at the parallel fiber synapses. The synaptic plasticity observed at the cellular level and the associative process of generating negative images of predicted sensory input at the systems level share a number of properties. Both are rapidly established, anti-Hebbian, reversible, input-specific and tightly restricted in time. These common properties argue strongly that associative depression at the parallel fiber synapse contributes to the adaptive generation of negative images in the mormyrid ELL.
Male stingrays use their ampullary electroreceptors to locate mates, but the effect of gonadal androgens on electrosensory encoding during the reproductive season is unknown. We tested the hypothesis that gonadal androgens induce neurophysiological changes in the electrosense of male Atlantic stingrays. During the primary androgen increase in wild males, the electrosensory primary afferent neurons show an increase in discharge regularity, a downshift in best frequency (BF) and bandpass, and a greater sensitivity to low-frequency stimuli from 0.01 to 4 Hz. Experimental implants of dihydrotestosterone in male stingrays induced a similar lowered BF and bandpass and increased average neural sensitivity to low-frequency stimuli (0.5-2 Hz) by a factor of 1.5. Primary afferents from long ampullary canals (>3 cm) were more sensitive and had a lower bandpass and BF than did afferents from short canals (<2 cm). We propose that these androgen-induced changes in the frequency response properties of electrosensory afferents enhance mate detection by male stingrays and may ultimately increase the number of male reproductive encounters with females. Furthermore, differences in primary afferent sensitivity among short and long canals may facilitate detection, orientation, and localization of conspecifics during social interactions.
Our computational analyses and experiments demonstrate that ampullary electroreceptors in paddlefish (Polyodon spathula) contain 2 distinct types of continuously active noisy oscillators. The spontaneous firing of afferents reflects both rhythms, and as a result is stochastically biperiodic (quasiperiodic). The first type of oscillator resides in the sensory epithelia, is recorded as approximately 26 Hz and +/-70 microV voltage fluctuations at the canal skin pores, and gives rise to a noisy peak at f(e) approximately 26 Hz in power spectra of spontaneous afferent firing. The second type of oscillator resides in afferent terminals, is seen as a noisy peak at f(a) approximately 30-70 Hz that dominates the power spectra of spontaneous afferent firing, and corresponds to the mean spontaneous firing rate. Sideband peaks at frequencies of f(a) +/- f(e) are consistent with epithelia-to-afferent unidirectional synaptic coupling or, alternatively, nonlinear mixing of the 2 oscillatory processes. External stimulation affects the frequency of only the afferent oscillator, not the epithelial oscillators. Application of temperature gradients localized the f(e) and f(a) oscillators to different depths below the skin. Having 2 distinct types of internal oscillators is a novel form of organization for peripheral sensory receptors, of relevance for other hair cell sensory receptors.
Electric fields in natural waters present a wealth of sensory information. Bioelectric fields direct electrosensitive fishes to their prey, environmental fields provide important orientational cues, and the fields induced by the animals’ motion through the earth’s magnetic field offer oceanic species complete compass data. Particularly sensitive to electric fields are the marine sharks, skates, and rays, but the weakly electric fishes, the common catfishes, and several of the more primitive fishes are also known for their keen electric sense.
The acute electrical sensitivity of marine sharks and rays is the greatest known in the Animal Kingdom. I investigate the possibility that the underlying biophysical principles are the very same as those encountered in the central nervous system of animal and man. The elasmobranch ampullae of Lorenzini detect the weak electric fields originating from the oceanic environment, whereas the nerve cells of the brain detect the electric fields arising, well, from the central nervous system. In responding to electrical signals, the cell membranes of excitable cells behave in different regions of the cell as negative or positive conductors. The negative and positive conductances in series, loaded by the cell's electrolytic environment, constitute a positive feedback circuit. The result may be of an all-or-none nature, as in peripheral nerve conduction, or of a graded nature, as in central processing. In this respect, the operation of the elasmobranch ampullae of Lorenzini is more akin to the graded, integrative processes of higher brain centers than to the conduction of nerve action potentials. Hence, the positive-feedback ampullary circuit promises to help elucidate the functioning of the central nervous system as profoundly as the squid giant axon has served to reveal the process of nervous conduction.
Electroreceptors are sense organs by which animals obtain biologically relevant information from natural electric fields (Machin, 1962; Kalmijn, 1971; cf. Bennett’s reviews, 1971b and c, and Bullock’s Introduction to the present Volume, Chapter 1). Therefore, however suggestive the electrical characteristics of a sense organ may be, the final justification for using the term electroreceptor depends upon the role that the sense organ in question plays in the animal’s life. To establish and analyze this role, a basic knowledge of the natural electric fields and the information they provide is an essential prerequisite. Whether the information is of biological significance to electrosensitive animals must be determined by appropriate behavioral experiments.
This is the second paper in a series that describes the morphology, immunohistochemistry, and synaptology of the mormyrid electrosensory lateral line lobe (ELL). The ELL is a highly laminated cerebellum-like structure in the rhombencephalon that subserves an active electric sense: Objects in the nearby environment of the fish are detected on the basis of changes in the reafferent electrosensory signals that are generated by the animal's own electric organ discharge. The present paper describes interneurons in the superficial (molecular, ganglionic, and plexiform) layers of the ELL cortex that were analyzed in the light and electron microscopes after Golgi impregnation, intracellular labeling, neuroanatomical tracing, and γ-aminobutyric acid (GABA) immunohistochemistry.
1.
The response properties of 322 single units in the electroreceptive midbrain (lateral mesencephalic nucleus, LMN) of the thornback ray,Platyrhinoidis triseriata, were studied using uniform and local electric fields. Tactile, visual, or auditory stimuli were also presented to test for multimodality.
2.
Most LMN electrosensory units (81%) are silent in the absence of stimulation. Those with spontaneous activity fired irregularly at 0.5 to 5 impulses/s, the lower values being more common. Two units had firing rates greater than 10/s.
3.
Midbrain electrosensory units are largely phasic, responding with one or a few spikes per stimulus onset or offset or both, but the adaptation characteristics of some neurons are complex. The same neuron can exhibit phasic or phasic-tonic responses, depending upon orientation of the electric field. Tonic units without any initial phasic overshoot were not recorded. Even the phasic-tonic units adapt to a step stimulus within several seconds.
4.
Unit thresholds are generally lower than 0.3 V/cm, the weakest stimulus delivered, although thresholds as high as 5V/cm were recorded. Neuronal responses reach a maximum, with few exceptions, at 100 V/cm and decrease rapidly at higher intensities.
5.
LMN neurons are highly sensitive to stimulus repetition rates: most responded to frequencies of 5 pulses/s or less: none responded to rates greater than 10/s. Three distinct response patterns are recognized.
6.
Best frequencies in response to sinusoidal stimuli range from 0.2 Hz (the lowest frequency delivered) to 4 Hz. Responses decrease rapidly at 8 Hz or greater, and no units responded to frequencies greater than 32 Hz.
7.
Most LMN neurons have small, well defined excitatory electroreceptive fields (RFs) exhibiting no surround inhibition, at least as detectable by methods employed here. Seventy-eight percent of units recorded had RFs restricted to the ventral surface: of these, 98% were contralateral. The remaining 22% of units had disjunct dorsal and ventral receptive fields.
8.
Electrosensory RFs on the ventral surface are somatotopically organized. Anterior, middle, and posterior body surfaces are mapped at the rostral, middle, and caudal levels, respectively, of the contralateral LMN. The lateral, middle, and medial body are mapped at medial, middle, and lateral levels of the nucleus. Moreover, the RFs of all units isolated in a given dorsoventral electrode track are nearly superimposable. About 40% of LMN, measured from the dorsal surface, is devoted to input from ventral electroreceptors located in a small region rostral and lateral to the mouth.
9.
The rostrocaudal extent of the somatotopic map includes regions of the neuraxis previously divided into 2 nuclei of the lateral mesencephalic complex, the anterior nucleus (AN) anteriorly and lateral nucleus (LMN) caudally. The single, unfractured somatotopic map reported here is continuous across the boundary of these two regions. This suggests that AN may not be a distinct nucleus but rather a rostral extension of LMN.
10.
LMN neurons are sensitive to the orientation of a uniform electric field. Maximum and minimum responses can be recorded at orientations separated by just 30. Single unit best orientations are largely a function of the orientation of ampullary canals from which a unit receives input.
11.
The majority of LMN electrosensory units are bimodal, responding vigorously to a camel-hair brush applied gently to the skin. This midbrain mechanosensitivity apparently is not mediated by the ampullae of Lorenzini since tactile stimuli adequate in the midbrain do not excite medullary electrosensory neurons. Mechanosensory minimum RFs are generally larger than but invariably overlap with electrosensory RFs. The somatotopic maps of the 2 modalities are congruent. Cross-modality interactions in bimodal units were observed and will be discussed.
The biotic and abiotic electric phenomena in the habitat of the electrosensitive catfish,Ictalurus nebulosus LeS were investigated. Fish, insect larvae, tadpoles and snails proved to possess electric fields that can be described as stationary fields of the dipole type, upon which fluctuations, due to respiration or other movements, are superimposed. The frequency components of these fields fall within the DC to 10 Hz range, whereas the potential gradients are in the order of magnitude of 10 mV/m. The maximal potential differences found were several millivolts. These measurements were carried out in tap water with a specific resistance = 20 m. Further, hydroelectric fields were measured in some find-localities ofIctalurus. Potential gradients up to 15 mV/m have been recorded in water with a specific resistance = 110 m. These fields proved to be stationary, fairly constant in direction and strength, and strongly dependent on the structure of the bottom of the pool and the depth of the water. The possible significance of these biotic and abiotic fields toIctalurus is discussed.
1.
The electrogenic Na-K pump activity was studied in thePlotosus electroreceptor. Single ampullae (sensory epithelium) were dissected free, and mounted over an air gap at the ampullary duct, to electrically isolate the receptor activity for current- and voltage-clamp experiments.
2.
After equilibration in K-free saline, the bathing medium around the ampulla was exchanged to test saline. Under current-clamp, 4 mM K saline induced reversible hyperpolarization of about 13 mV. Under voltage-clamp, the 4 mM saline induced an outward current of about 10 nA.
3.
Both responses were suppressed by ouabain, with a half suppression at 1.510–7
M for current, which suggested involvement of ionic pumps. In the K-free saline, ouabain alone induced no response.
4.
The current response to high K saline was always outward, and was dependent on K concentration. In the presence of ouabain, high K saline as high as 40 mM, ten times the standard K, induced no inward current, which suggested little contribution of K conductance to the responses.
5.
The outward current responses were induced, also dose-dependently, by various alkali metal cations. The apparent dissociation constants were 6.8, 1.2, 21.7, and 85.1 mM for K, Rb, Cs, and Li, suggesting their potency in the order of Rb>K> Cs>Li.
6.
Thus, the hyperpolarization and outward current responses were due to an electrogenic NaK pump in the basal face of the sensory epithelium. The Na-K pump seems to be responsible, to a certain extent, for maintenance of the negative DC potential in the standard 4 mM K saline, which supplies an outward current to bias the sensory epithelium in situ.
1.
The use of electroreception in feeding depends on the detection of the weak fields of the prey above the interference produced by the predator's own bioelectric fields.
2.
In this study, the ray's ventilatory movements are shown to produce powerful modulation of electroreceptive afferent input.
3.
The afferent discharge pattern results mainly from changes of the electric fields within the animal, since it is similar in afferents which innervate ampullary canals of opposite orientation.
4.
If inputs from canals of opposite orientation are subtracted by the CNS, the sensitivity to external fields is enhanced, and the ventilatory interference removed by common mode rejection.
5.
Recordings from secondary electrosensory neurons provide evidence that the appropriate inputs exist for common mode rejection, and that ventilation related activity is greatly reduced in these cells and virtually absent in recordings from a mesencephalic electrosensory area.
1. This is the first detailed description of the projection to the cerebral cortex of afferent information coming from electroreceptors in the bill of the platypus, Ornithorhynchus anatinus. 2. In animals anaesthetized with chloralose, with the bill immersed in tap water, applying a potential difference between plate electrodes on either side of the bill produced large amplitude potentials from the surface of a postero-lateral region of cerebral cortex. Response threshold was 300 microV cm-1, somewhat lower than threshold measured for single identified electroreceptors. Electroreceptor threshold was at least three orders of magnitude lower than threshold of mechanoreceptors to electrical stimuli (Gregory, Iggo, McIntyre & Proske, 1989a). 3. Monopolar stimulation of the bill revealed a crossed projection. The map on the cortical surface had the bill oriented dorso-laterally, its base towards the mid-line, the tip on the lateral edge, pointing slightly forwards. The edge of the bill faced backwards. Electrosensory information coming from the edge of the bill appeared to be much more strongly represented than input from the dorsal surface. 4. Weak electrical and mechanical stimuli applied to the bill both evoked large amplitude potentials from the same region of cortex indicating that there was complete overlap between the regions receiving tactile and electrosensory inputs. 5. Inserting microelectrodes into the deeper layers of cortex revealed burst discharges in single cells and groups of cells in response to weak electrical stimulation of the bill. Activity could be recorded over a range of depths from 0.3 to 4 mm, with the majority of responses coming from cells 1-3 mm deep. Histological examination of lesion sites made at 1.1 mm and at 3 mm suggested that cells in the pyramidal and ganglion layers were involved in generating the activity. 6. Some evidence was obtained for interactions at the level of the cerebral cortex between activity generated by tactile and electrosensory inputs. When electrical and mechanical stimuli were both applied to the bill with an interstimulus interval of less than 25 ms, cortical neuronal responses generated by one stimulus were completely suppressed by the other. However no evidence was obtained of a direct convergence at the level of the cortex between the two modalities. 7. Cortical activity could be evoked in response to rapidly changing voltage fields. This observation, together with our earlier finding of a high rate sensitivity of the receptors, emphasizes the high dynamic sensitivity of the system. 8. It is concluded that the electrosensory system of the platypus is closely associated with the sense of touch.(ABSTRACT TRUNCATED AT 400 WORDS)
Multimodal sensory areas that include vision have been identified physiologically in two separate pallial areas in the telencephalon and in the tectum of the mesencephalon. Multi-sensory integration occurs in the medial pallium of the little skate, Raja erinacea, and a primitive squalomorph shark, Squalus acanthias, whereas in the advanced galeomorph shark, Ginglymostoma cirratum, a major multimodal area is in the dorsal pallium pars centralis. Pars centralis has undergone extensive hypertrophy in the evolution of advanced batoids and galeomorph sharks. More complete studies are required on individual species to assess the possibility that there has been an evolutionary shift in major sensory processing areas from medial to dorsal pallium among the elasmobranchs.
Most retinofugal fibers in elasmobranchs project spatiotopically to the tectum, the central zone of which is an area of multimodal integration. The spatiotopic tectal map of the electrosense in the little skate includes only that part of the electrosensory field that is within the visual field, and individual points on the tectum represent the same spatial location in each sense. In both maps the region of space near the horizon is greatly overrepresented. For vision this corresponds to a band of increased retinal ganglion cell density, and for both senses the overrepresentation may be related to the importance of this region of space in the skate's natural orienting. Spatial congruence of visual and electrosensory maps should ensure that individual tectal cells integrate multimodal information in a space-specific fashion.
1. This is a report of further observations on the response characteristics of electroreceptors in the bill of the platypus, Ornithorhynchus anatinus, first described by Gregory, Iggo, McIntyre & Proske (1987). 2. The main finding is that, with the bill immersed in water, applying a potential difference between large plate electrodes on either side of the bill, produced detectable responses in a population of electroreceptors to field strengths as low as 4 mV cm-1. Threshold for individual receptors lay between 4 and 25 mV cm-1. 3. An electric dipole placed in the water close to the receptive field could also elicit responses, threshold being lowest when the cathode was near the centre of the field. On several occasions the most sensitive spot was seen, under the microscope, to correspond to the mouth of a mucous sensory gland (Andres & Von Düring, 1984). Response intensity fell when the dipole was moved further away, the drop being less steep in a direction over the top of the bill towards the mid-line. 4. For individual receptors the latency of the first impulse initiated by supramaximal voltage pulses was 1.1-1.8 ms. Latencies tended to be shorter when the site of the receptor lay closer to the recording electrodes. Plotting each latency against conduction path length for eleven receptors gave an approximately linear relation from which was calculated an average axonal conduction velocity of 56 m s-1. The plot yielded an estimate of impulse initiation time of 0.8 ms. It is argued that this is too short to include a synaptic delay. A peripheral synapse is found in all non-mammalian electroreceptors. 5. Electroreceptors responded to both steady and rapidly changing potential gradients. For ramp-shaped gradients of 1-50 V s-1 peak firing rate was approximately proportional to log stimulus velocity. In response to sinusoidal potential changes a 1:1 relation between each afferent impulse and the peak of the stimulating waveform could be obtained over the range 12-300 Hz. Threshold was at its lowest at 50-100 Hz. Tuning curves measured with the bill immersed in water were little different from those obtained by focal stimulation with the bill in air. 6. It is concluded that platypus electroreceptors, supplied by the trigeminal nerve, and which are therefore not part of the acoustico-lateralis system as in non-mammalian electroreceptors, are also unique in not having a peripheral synapse. Furthermore, they are able to respond to both steady and rapidly changing voltage gradients.(ABSTRACT TRUNCATED AT 400 WORDS)
1. Afferent responses were recorded from filaments of the trigeminal nerve in each of two platypuses (Ornithorhynchus anatinus) anaesthetized with alpha-chloralose. All receptive fields were located along the lateral border of the upper bill. Discrete receptive fields could be identified as belonging to two distinct classes of sensory receptor. 2. The most prominent response was an irregular resting discharge which could be increased or decreased by weak electric pulses. These receptors were insensitive to moderately strong mechanical stimulation, and it was concluded that they were electroreceptors. 3. Each electroreceptor had a single spot of maximum sensitivity on the bill surface. When the stimulating electrode over this spot was the cathode it excited the receptor for the duration of the stimulating pulse, using stimulus strengths as low as 20 mV. When it was the anode, it inhibited the discharge. Cathodal excitation was followed by rebound inhibition and anodal inhibition by rebound excitation. 4. Receptors responded to cathodal steps with an initial high-frequency burst of impulses, followed by a lower maintained rate of discharge. Rapidly changing pulses were similarly effective in exciting receptors, adding support to the claim that platypuses are able to detect moving prey by the electrical activity associated with muscle contraction. 5. The centres of the receptive fields of two electroreceptors were marked by the insertion of fine entomological pins. Histological examination established the presence of a large mucus-secreting gland at the marked spot. The epidermal duct of the gland contained an elaborate myelinated innervation, with morphologically distinct axon terminals that we identify as the electroreceptors. 6. As well as electroreceptors, the skin of the bill contained three kinds of mechanoreceptors: slow-adapting receptors, rapidly adapting, vibration-sensitive receptors and receptors with an intermediate adaptation rate. The slowly adapting receptors were characterized by their low threshold to mechanical stimuli, irregular discharge and significant dynamic sensitivity. Vibration receptors showed maintained responses to sinusoidal vibration of the skin up to 600 Hz. 7. These experiments confirm an earlier report that the platypus bill is an electrodetector organ. The presence of electroreceptors of a unique structure and supplied by the trigeminal nerve indicates that electroreception has evolved independently in monotremes. This in turn emphasizes that monotremes are a highly evolved group which split off from the main mammalian stem a long time ago.
The response properties of 322 single units in the electroreceptive midbrain (lateral mesencephalic nucleus, LMN) of the thornback ray, Platyrhinoidis triseriata, were studied using uniform and local electric fields. Tactile, visual, or auditory stimuli were also presented to test for multimodality. Most LMN electrosensory units (81%) are silent in the absence of stimulation. Those with spontaneous activity fired irregularly at 0.5 to 5 impulses/s, the lower values being more common. Two units had firing rates greater than 10/s. Midbrain electrosensory units are largely phasic, responding with one or a few spikes per stimulus onset or offset or both, but the adaptation characteristics of some neurons are complex. The same neuron can exhibit phasic or phasic-tonic responses, depending upon orientation of the electric field. Tonic units without any initial phasic over-shoot were not recorded. Even the phasic-tonic units adapt to a step stimulus within several seconds. Unit thresholds are generally lower than 0.3 microV/cm, the weakest stimulus delivered, although thresholds as high as 5 microV/cm were recorded, Neuronal responses reach a maximum, with few exceptions, at 100 microV/cm and decrease rapidly at higher intensities. LMN neurons are highly sensitive to stimulus repetition rates: most responded to frequencies of 5 pulses/s or less; none responded to rates greater than 10/s. Three distinct response patterns are recognized. Best frequencies in response to sinusoidal stimuli range from 0.2 Hz (the lowest frequency delivered) to 4 Hz. Responses decrease rapidly at 8 Hz or greater, and no units responded to frequencies greater than 32 Hz. Most LMN neurons have small, well defined excitatory electroreceptive fields (RFs) exhibiting no surround inhibition, at least as detectable by methods employed here. Seventy-eight percent of units recorded had RFs restricted to the ventral surface: of these, 98% were contralateral. The remaining 22% of units had disjunct dorsal and ventral receptive fields. Electrosensory RFs on the ventral surface are somatotopically organized. Anterior, middle, and posterior body surfaces are mapped at the rostral, middle, and caudal levels, respectively, of the contralateral LMN. The lateral, middle, and medial body are mapped at medial, middle, and lateral levels of the nucleus. Moreover, the RFs of all units isolated in a given dorsoventral electrode track are nearly superimposable. About 40% of LMN, measured from the dorsal surface, is devoted to input from ventral electroreceptors located in a small region rostral and lateral to the mouth.(ABSTRACT TRUNCATED AT 400 WORDS)
Specializations for electroreception in sense organs and brain centers are found in a wide variety of fishes and amphibians, though probably in a small minority of teleost taxa. No other group of vertebrates or invertebrates is presently suspected to have adaptations for electroreception in the definition given here. The distribution among fishes is unlike any other sense modality in that it has apparently been invented, lost completely and reinvented several times independently, using distinct receptors and central nuclei in the medulla. There are so far no clearly borderline or transitional fishes, either physiologically or anatomically. We rather expect a few new electroreceptive taxa to be found. The evoked potential method and the newly validated central anatomical criteria provide two useful tools for searching.
The dorsal octavolateral nucleus is the primary electrosensory nucleus in the elasmobranch medulla. We have studied the topographic organization of electrosensory afferent projections within the dorsal nucleus of the little skate, Raja erinacea , by anatomical (HRP) and physiological experiments.
The electrosensory organs (ampullae of Lorenzini) in skates are located in four groups on each side of the body, and each group is innervated by a separate ramus of the anterior lateral line nerve (ALLN). Transganglionic transport of HRP in individual rami demonstrated that electroreceptor afferents in each ramus project to a separate, nonoverlapping division of the central zone of the ipsilateral dorsal nucleus. These divisions, which are distinct areas separated by compact cell plates, are somatopically arranged. The volume of each division of the dorsal nucleus that is related to a single ramus is proportional to the number of ampullae innervated by the ramus, but not to the body surface area on which the receptors are distributed. Nearly one‐half of the nucleus is devoted to electrosensory inputs from the buccal and superficial ophthalmic ampullae concentrated in a small area on the ventral surface of the head rostral to the mouth. Multiple and single unit recordings demonstrated that adjacent cells in the nucleus have similar receptive fields on the body surface and revealed a detailed point‐to‐point somatotopy within the nucleus. With threshold stimuli most single units have ipsilateral receptive fields made up by excitatory inputs from 2–5 ampullary organs.
The somatotopy within the mechanosensory medial nucleus, also revealed by the HRP fills of individual ALLN rami, appears less rigid than that in the dorsal nucleus, as extensive overlap is present in the terminal fields of separate ALLN rami.
Single neurons that respond to activation of the ampullary (tonic) type of electroreceptors were recorded in the posterior lateral line lobe of electric fish of the family Mormyridae. The cells are not only affected by primary afferent activity but also by an efference copy associated with the motor command to discharge the electric organ. A curarized preparation was used in which the electric organ discharge (EOD) is silenced but the command signal, which would normally elicit an EOD, can be recorded. Cells are of two types; 'outside positive' cells, in which the discharge rates are accelerated by long-duration outside positive electrical stimuli in the water; and 'outside negative' cells, in which discharge rates are accelerated by outside negative stimuli. Both types are also affected by brief electrical pulses that mimic the effect of the EOD. Both cell types usually have receptive fields of 1-2 cm2. In both cell types, the effect of the command-associated efference copy is always opposite to the effect of electrical stimuli given at short, consistent delays after the command. The normal function of the efference copy is probably to reduce the effects of EOD-induced afferent activity and thus to minimize interference with the sensing of external electrical sources. The efference copy is not fixed but changes over a period of minutes to match a change in the pattern of afferent activity. Changes in polarity (acceleration or deceleration), amplitude, time course, and spatial distribution of the afferent pattern result in corresponding changes in the efference copy. The synchronized motoneuronal volley that drives the electric organ, i.e., the actual EOD motor command, does not vary. Changes in the efference copy depend only on changes in the afferent activity that follows the command. The principle of an efference copy that depends on the afferent feedback elicited by a motor output, rather than on the pattern of the motor output, may be applicable elsewhere.
The exquisite sensitivity of elasmobranch fishes to electric fields is thought to reside in electroreceptive organs called ampullae of Lorenzini. We measured the stimulus-response behavior of ampullary organs excised from skates. Under open-circuit conditions, the ampullary organ showed three distinct response states: spontaneous repetitive spikes, evoked spikes, and small, damped oscillatory responses. Under short-circuit conditions, the amplitude range for a linear current response to a sinusoidal (0.5 Hz) voltage clamp of an organ (assessed by spectral analysis of the harmonics generated) was 7-200 microV rms. Changes in the spike firing rate of the afferent nerve innervating the organ were evident for voltage clamps of the ampullary epithelium of 3 microV and the spike rate saturated for clamp steps exceeding 100 microV. Thus, the linear response range of the ampullary epithelium exceeded the range in spike firing rate of the afferent nerve. The steady-state transorgan electrical properties under voltage clamp conditions were obtained by analysis of complex admittance determinations in the frequency range 0.05-20 Hz for perturbations (< 100 microV rms) in the linear range. Admittance functions were distinctly related to the preparation states observed under open-circuit conditions. A negative real part in the organ admittance (i.e., a steady-state negative conductance generated by the preparation) was a common characteristic of the two (open-circuit) excitable states. The negative conductance was also confirmed by the direction of current flow through the ampullary epithelium in response to step voltage clamps. We conclude that the steady state-negative conductance is an essential property of the ampullary epithelium,and we suggest that the interplay of negative and positive conductances generated by ion channels in apical and basal membranes of receptor cells results in signal amplification that may contribute significantly to the electric field sensitivity of ampullary organs.
The present investigation was designed to determine the number and internal organization of somatosensory fields in monotremes. Microelectrode mapping methods were used in conjunction with cytochrome oxidase and myelin staining to reveal subdivisions and topography of somatosensory cortex in the platypus and the short-billed echidna. The neocortices of both monotremes were found to contain four representations of the body surface. A large area that contained neurons predominantly responsive to cutaneous stimulation of the contralateral body surface was identified as the primary somatosensory area (SI). Although the overall organization of SI was similar in both mammals, the platypus had a relatively larger representation of the bill. Furthermore, some of the neurons in the bill representation of SI were also responsive to low amplitude electrical stimulation. These neurons were spatially segregated from neurons responsive to pure mechanosensory stimulation. Another somatosensory field (R) was identified immediately rostral to SI. The topographic organization of R was similar to that found in SI; however, neurons in R responded most often to light pressure and taps to peripheral body parts. Neurons in cortex rostral to R were responsive to manipulation of joints and hard taps to the body. We termed this field the manipulation field (M). The mediolateral sequence of representation in M was similar to that of both SI and R, but was topographically less precise. Another somatosensory field, caudal to SI, was adjacent to SI laterally at the representation of the face, but medially was separated from SI by auditory cortex. Its position relative to SI and auditory cortex, and its topographic organization led us to hypothesize that this caudal field may be homologous to the parietal ventral area (PV) as described in other mammals. The evidence for the existence of four separate representations in somatosensory cortex in the two species of monotremes indicates that cortical organization is more complex in these mammals than was previously thought. Because the two monotreme families have been separate for at least 55 million years (Richardson, B.J. [1987] Aust. Mammal. 11:71-73), the present results suggest either that the original differentiation of fields occurred very early in mammalian evolution or that the potential for differentiation of somatosensory cortex into multiple fields is highly constrained in evolution, so that both species arrived at the same solution independently.
In lateral line and electrosensory systems of fish, the animal's own movements create unwanted stimulation that could interfere with the detection of biologically important signals. Here we report that an adaptive filter in the medullary nuclei of both senses suppresses self-stimulation. Second-order electrosensory neurons in an elasmobranch fish and mechanosensory neurons in a teleost fish learn to cancel the effects of stimuli that are presented coupled to the fish's movements. A model is proposed for how the adaptive filter is realized by the cerebellar-like circuits of the hindbrain nuclei in these senses.
Two ampullary epithelial properties necessary for electroreception were used to identify the types of ion channels and transporters found in apical and basal membranes of ampullary receptor cells of skates and to assess their individual role under voltage-clamp conditions. The two essential properties are (1) a steady-state negative conductance generated in apical membranes and (2) a small, spontaneous current oscillation originating in basal membranes (Lu and Fishman, 1995). The effects of pharmacological agents and ion substitutions on these properties were evaluated from transorgan or transepithelial complex admittance determinations in the frequency range 0.125 to 50 Hz measured in individual, isolated ampullary organs. In apical membranes, L-type Ca channels were found to be responsible for generation of the steady-state negative conductance. In basal membranes, K and Ca-dependent Cl (Cl(Ca)) channels were demonstrated to contribute to a net positive membrane conductance. L-type Ca channels were also evident in basal membranes and are thought to function in synaptic transmission from the electroreceptive epithelium to the primary afferent nerve. In addition to ion channels in basal membranes, two transporters (Na+/K+ pump and Na(+)-Ca+ exchanger) were apparent. Rapid (minutes) cessation of the current oscillation after blockage of any of the basal ion channels (Ca, Cl(Ca), K) suggests critical involvement of each of these channel types in the generation of the oscillation. Suppression of either Na+/K+ transport or Na(+)-Ca2+ exchange also eliminated the oscillation but at a slower rate, indicating an indirect effect.
The addition of noise to a system can sometimes improve its ability to transfer information reliably. This phenomenon--known as stochastic resonance--was originally proposed to account for periodicity in the Earth's ice ages, but has now been shown to occur in many systems in physics and biology. Recent experimental and theoretical work has shown that the simplest system exhibiting 'stochastic resonance' consists of nothing more than signal and noise with a threshold-triggered device (when the signal plus noise exceeds the threshold, the system responds momentarily, then relaxes to equilibrium to await the next triggering event). Here we introduce a class of non-dynamical and threshold-free systems that also exhibit stochastic resonance. We present and analyse a general mathematical model for such systems, in which a sequence of pulses is generated randomly with a probability (per unit time) that depends exponentially on an input. When this input is a sine-wave masked by additive noise, we observe an increase in the output signal-to-noise ratio as the level of noise increases. This result shows that stochastic resonance can occur in a broad class of thermally driven physico-chemical systems, such as semiconductor p-n junctions, mesoscopic electronic devices and voltage-dependent ion channels, in which reaction rates are controlled by activation barriers.
Stochastic resonance is the phenomenon whereby the addition of an optimal level of noise to a weak information-carrying input to certain nonlinear systems can enhance the information content at their outputs. Computer analysis of spike trains has been needed to reveal stochastic resonance in the responses of sensory receptors except for one study on human psychophysics. But is an animal aware of, and can it make use of, the enhanced sensory information from stochastic resonance? Here, we show that stochastic resonance enhances the normal feeding behaviour of paddlefish (Polyodon spathula), which use passive electroreceptors to detect electrical signals from planktonic prey. We demonstrate significant broadening of the spatial range for the detection of plankton when a noisy electric field of optimal amplitude is applied in the water. We also show that swarms of Daphnia plankton are a natural source of electrical noise. Our demonstration of stochastic resonance at the level of a vital animal behaviour, feeding, which has probably evolved for functional success, provides evidence that stochastic resonance in sensory nervous systems is an evolutionary adaptation.
The functioning of electroreceptor organs of Ictalurus sp. was investigated by inhibiting synaptic transmission by the administration of tetanus toxin in vitro. A piece of Ictalurus skin of about 20 mm diameter was mounted in an Ussing-type chamber. After establishing the normal functioning of the organ, tetanus toxin (TeTx) was applied basolaterally for 150 min in 66.7 pM and 400 pM concentrations, while the single unit nerve activity was recorded extracellularly. Spontaneous spike activity and the sensitivity of the electroreceptor organs were measured. The results show that TeTx reduces sensitivity to less then 20% of its original value, whereas the spontaneous activity is unaffected by the treatment. This indicates that the afferent nerve is capable of generating impulses independent of receptor cell neurotransmitter release. In the discussion we suggest two alternative mechanisms for the emergence of the spontaneous spike activity.
The central connections of the electrosensory system were studied in the paddlefish Polyodon spathula by injecting biotinylated dextran amines into the dorsal octavolateral nucleus (DON), the cerebellum, and the mesencephalic tectum. The sole target of primary electrosensory fibers is the ipsilateral dorsal octavolateral nucleus. The principal neurons ascending from this nucleus project to the torus semicircularis, the lateral mesencephalic nucleus, and the mesencephalic tectum. The mesencephalic tectum projects back to the nucleus preeminentialis, which, in turn, projects to the cerebellar auricles and to the DON. The auricles are the main source of parallel fibers in the cerebellar crest ventral to the DON. The DON also receives input from the contralateral DON. These descending feedback loops are very similar to those of other electrosensory fishes. However, the paddlefish is unique in having three mesencephalic targets of electrosensory information. It is the only bony fish known to have extensive projections directly to the mesencephalic tectum and to a lateral mesencephalic nucleus in addition to the torus semicircularis.
The electric sense of elasmobranch fishes (sharks and rays) is an important sensory modality known to mediate the detection of bioelectric stimuli. Although the best known function for the use of the elasmobranch electric sense is prey detection, relatively few studies have investigated other possible biological functions. Here, we review recent studies that demonstrate the elasmobranch electrosensory system functions in a wide number of behavioral contexts including social, reproductive and anti-predator behaviors. Recent work on non-electrogenic stingrays demonstrates that the electric sense is used during reproduction and courtship for conspecific detection and localization. Electrogenic skates may use their electrosensory encoding capabilities and electric organ discharges for communication during social and reproductive interactions. The electric sense may also be used to detect and avoid predators during early life history stages in many elasmobranch species. Embryonic clearnose skates demonstrate a ventilatory freeze response when a weak low-frequency electric field is imposed upon the egg capsule. Peak frequency sensitivity of the peripheral electrosensory system in embryonic skates matches the low frequencies of phasic electric stimuli produced by natural fish egg-predators. Neurophysiology experiments reveal that electrosensory tuning changes across the life history of a species and also seasonally due to steroid hormone changes during the reproductive season. We argue that the ontogenetic and seasonal variation in electrosensory tuning represent an adaptive electrosensory plasticity that may be common to many elasmobranchs to enhance an individual's fitness throughout its life history.