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Anatomical characteristics of lamina amacrine cells, revealed by Golgi staining and electron microscopy. ~ A ! Golgi impregnation showing a top–down view of the superficial plexus of amacrine tangential processes with regularly spaced nodes comprising varicose specializations ~ one node shown boxed ! . ~ B ! Golgi impregnation showing converging processes from several amacrines providing apposed varicose specializations at one node ~ boxed ! . ~ C–E ! Low-power electron micrographs showing amacrine tangential process ~ arrowed am in C ! , amacrine swellings distal in the lamina ~ am in D ! , and convergence of amacrine processes, as in boxed areas, denoted by boutons equipped with synaptic specializations ~ arrowed in D & E ! . Receptor profiles are labeled R. ~ F ! Lamina amacrines can have various sizes, spreading through between 6 and 12 optic cartridges. In this schematic, the minimal spacing necessary to provide one optic cartridge with its six amacrine processes ~ indicated by arrowed bracket 2– 6 ! is reconstructed by overlapping five identical amacrine cells ~ 2– 6 ! , the shapes of which correspond to the single element ~ 1 ! shown to the left, which supplies one or two a processes to each of five optic cartridges ~ under bracket 1 ! . ~ G ! Golgi-impregnated amacrine including cell body and cell body fiber. Scale for A ϭ 10 μ m; scale for B ϭ 5 μ m; 1 μ m scale in C also applies to D, E. Scales for F,G ϭ 10 μ m.
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Amacrine cells in the external plexiform layer of the fly's lamina have been intracellulary recorded and dye-filled for the first time. The recordings demonstrate that like the lamina's short photoreceptors R1-R6, type 1 lamina amacrine neurons exhibit nonspiking, "sign-conserving" sustained depolarizations in response to illumination. This contras...
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... anatomical features of lamina amacrine cells are illustrated in Fig. 1. The large, ellipsoid-shaped cell bodies of type 1 lamina amacrines ~Fig. 1G! lie 10-20 µm proximal to the lamina among axons forming the outer part of the first optic chiasma, and are the only neurons originating from this level. Cell bodies of lamina monopolar cells lie distal to the plexiform layer. The cell bodies of T1 efferent ...
Citations
... In P. camtschaticus, the TH-positive tangential cells exhibited few similarities with catecholaminergic tangential neurons previously identified in Pacifastacus leniusculus (Elofsson et al., 1977). Remarkably, the amacrine and tangential neurons form local circuits within the lamina in crustaceans (Nässel, 1977;Stowe et al., 1977;Strausfeld and Nässel, 1981;Sztarker et al., 2005Sztarker et al., , 2009Thoen et al., 2017) and insects (Strausfeld, 1976;Douglass and Strausfeld, 2005). ...
Identifying the neurotransmitters secreted by specific neurons in crustacean eyestalks is crucial to understanding their physiological roles. Here, we combined immunocytochemistry with confocal microscopy and identified the neurotransmitters dopamine (DA), serotonin (5-HT), and acetylcholine (ACh) in the optic neuropils and X-organ sinus gland (XO-SG) complex of the eyestalks of Paralithodes camtschaticus (red king crab). The distribution of Ach neurons was studied by choline acetyltransferase (ChAT) immunohistochemistry and compared with that of DA neurons examined in the same or adjacent sections by tyrosine hydroxylase (TH) immunohistochemistry. We detected 5-HT, TH, and ChAT in columnar, amacrine, and tangential neurons in the optic neuropils and established the presence of immunoreactive fibers and neurons in the terminal medulla in the XO region of the lateral protocerebrum. Additionally, we detected ChAT and 5-HT in the endogenous cells of the SG of P. camtschaticus for the first time. Furthermore, localization of 5-HT- and ChAT-positive cells in the SG indicated that these neurotransmitters locally modulate the secretion of neurohormones that are synthesized in the XO. These findings establish the presence of several neurotransmitters in the XO-SG complex of P. camtschaticus.
... While targeting the lamina ganglionaris, we found three cells showing distinct responses to only R-CPL (Fig. 4). A brief pulse of white light elicited a graded depolarization plateau (Fig. 4A,D) closely resembling the response of the sign-conserving amacrine neurons of a blowfly (Douglass and Strausfeld, 2005). Under the dynamic polarization stimulus, when the polarizer moved to R-CPL, the membrane potential re-polarized as if the stimulus was fading out for a short while (Fig. 4B,C). ...
Stomatopods, or so-called mantis shrimps, are the only animal group known to possess circular polarization vision along with linear polarization vision. By using the rhabdomere of a distally located photoreceptor as a wave retarder, the eyes of mantis shrimps are able to convert circularly polarized light into linearly polarized light. As a result, their circular polarization vision is based on the linearly polarized light-sensitive photoreceptors commonly found in many arthropods. To investigate how linearly and circularly polarized light signals might be processed, we presented a dynamic polarized light stimulus while recording from photoreceptors or lamina neurons in intact mantis shrimps Haptosquilla pulchella . The results indicate that all the circularly polarized light-sensitive photoreceptors also showed differential responses to the changing e-vector angle of linearly polarized light. When stimulated with linearly polarized light of varying e-vector angle, most photoreceptors produced a concordant sinusoidal response. In contrast, some lamina neurons doubled the response frequency in reacting to linearly polarized light. These responses resembled a rectified sum of two-channel linear polarization-sensitive photoreceptors indicating that polarization visual signals are processed at or before the first optic lobe. Noticeably, within the lamina, there was one type of neuron that showed a steady depolarization response to all stimuli except right-handed circularly polarized light. Together, our findings suggest that, between the photoreceptors and lamina neurons, linearly and circularly polarized light may be processed in parallel and different from one another.
... Whether such amacrine arrangements would provide discrete local circuits for receptor pooling is an open question. However, observations of lamina amacrine cells in insects describe highly restricted fields of processes (Douglass and Strausfeld, 2005), as have descriptions of amacrines in decapod and stomatopod crustaceans (Sztarker et al., 2005;Thoen et al., 2017). ...
Animals that have true color vision possess several spectral classes of photoreceptors. Pancrustaceans (Hexapoda + Crustacea) that integrate spectral information about their reconstructed visual world do so from photoreceptor terminals supplying their second optic neuropils, with subsequent participation of the third (lobula) and deeper centers (optic foci). Here we describe experiments and correlative neural arrangements underlying convergent visual pathways in two species of branchiopod crustaceans that have to cope with a broad range of spectral ambience and illuminance in ephemeral pools, yet possess just two optic neuropils, the lamina and optic tectum. Electroretinographic recordings and multimodel inference based on modeled spectral absorptance were used to identify the most likely number of spectral photoreceptor classes in their compound eyes. Recordings from the retina provide support for four color channels. Neuroanatomical observations resolve arrangements in their laminas that suggest signal summation at low light intensities, incorporating chromatic channels. Neuroanatomical observations demonstrate that spatial summation in the lamina of the two species are mediated by quite different mechanisms, both of which allow signals from several ommatidia to be pooled at single lamina monopolar cells. We propose that such summation provides sufficient signal for vision at intensities equivalent to those experienced by insects in terrestrial habitats under dim starlight. Our findings suggest that despite the absence of optic lobe neuropils necessary for spectral discrimination utilized by true color vision, four spectral photoreceptor classes have been maintained in Branchiopoda for vision at very low light intensities at variable ambient wavelengths that typify conditions in ephemeral fresh water habitats.
... By a similar line of reasoning, the "weighted sum" temporal evolution rule common to decades of neural networks-a variation of which is described below for our model-may be justified as an approximate model of neuronal interactions. Direct input from presynaptic graded potential cells in insects leads to similarly shaped postsynaptic potentials (Douglass and Strausfeld 2005), with both excitation and inhibition relative to the presynaptic resting potential being passed through some synaptic weight to postsynaptic neurons. The response of a graded potential neuron with multiple presynaptic connections may be modeled as a sum of the presynaptic inputs relative to resting, with each input weighted by the strength of the corresponding synapse. ...
Visual binding is the process of associating the responses of visual interneurons in different visual submodalities all of which are responding to the same object in the visual field. Recently identified neuropils in the insect brain termed optic glomeruli reside just downstream of the optic lobes and have an internal organization that could support visual binding. Working from anatomical similarities between optic and olfactory glomeruli, we have developed a model of visual binding based on common temporal fluctuations among signals of independent visual submodalities. Here we describe and demonstrate a neural network model capable both of refining selectivity of visual information in a given visual submodality, and of associating visual signals produced by different objects in the visual field by developing inhibitory neural synaptic weights representing the visual scene. We also show that this model is consistent with initial physiological data from optic glomeruli. Further, we discuss how this neural network model may be implemented in optic glomeruli at a neuronal level.
... These dendrites contact up to six neighboring cartridges and have been shown to be postsynaptic to lamina amacrine cells (Strausfeld and Campos-Ortega, 1973). Lamina amacrine cells encompass several lamina cartridges in flies (Douglass and Strausfeld, 2005) and might thus provide an alternative candidate cell type for spatial summation. However, physiological evidence from these neurons in flies suggests otherwise (Douglass and Strausfeld, 2005). ...
... Lamina amacrine cells encompass several lamina cartridges in flies (Douglass and Strausfeld, 2005) and might thus provide an alternative candidate cell type for spatial summation. However, physiological evidence from these neurons in flies suggests otherwise (Douglass and Strausfeld, 2005). Descriptions of lamina amacrine cells from insects other than flies are very rare because, as Strausfeld and Blest (1970) explain, they only infrequently label with the Golgi technique. ...
Animals use vision over a wide range of light intensities, from dim starlight to bright sunshine. For animals active in very dim light the visual system is challenged by several sources of visual noise. Adaptations in the eyes, as well as in the neural circuitry, have evolved to suppress the noise and enhance the visual signal, thereby improving vision in dim light. Among neural adaptations, spatial summation of visual signals from neighboring processing units is suggested to increase the reliability of signal detection and thus visual sensitivity. In insects, the likely neural candidates for carrying out spatial summation are the lamina monopolar cells (LMCs) of the first visual processing area of the insect brain (the lamina). We have classified LMCs in three species of hawkmoths having considerably different activity periods but very similar ecology - the diurnal Macroglossum stellatarum, the nocturnal Deilephila elpenor and the crepuscular-nocturnal Manduca sexta. Using this classification, we investigated the anatomical adaptations of hawkmoth LMCs suited for spatial summation. We found that specific types of LMCs have dendrites extending to significantly more neighboring cartridges in the two nocturnal and crepuscular species than in the diurnal species, making these LMC types strong candidates for spatial summation. Moreover, while the absolute number of cartridges visited by the LMCs differed between the two dim-light species, their dendritic extents were very similar in terms of visual angle, possibly indicating a limiting spatial acuity. Interestingly, the overall size of the lamina neuropil did not correlate with the size of its LMCs. This article is protected by copyright. All rights reserved.
© 2015 Wiley Periodicals, Inc.
... Due to the small cell size and the internal location, so far only few lamina large monopolar cells have been recorded from electrophysiological experiments (Zheng et al., 2006;Pantazis et al., 2008). The electrophysiological properties of lamina interneurons are mostly proposed based on recordings from larger fly species (Douglass and Strausfeld, 2005). However, some neurotransmitters used by lamina neurons have been revealed by immunocytochemistry studies. ...
High temporal resolution of vision relies on the rapid kinetics of the photoresponse in the light-sensing photoreceptor neurons. It is well known that the rapid recovery of photoreceptor membrane potential at the end of light stimulation depends on timely deactivation of the visual transduction cascade within photoreceptors. Whether any extrinsic factor contributes to the termination speed of the photoresponse is unknown.
In this thesis, using Drosophila as a model system, I show that a feedback circuit mediated by both neurons and glia in the visual neuropile lamina is required for rapid repolarization of the photoreceptor at the end of the light response.
In the first part of my thesis work, I provide evidence that lamina epithelial glia, the major glia in the visual neuropile, is involved in a retrograde regulation that is critical for rapid repolarization of the photoreceptor at the end of light stimulation. I identified the gene affected in a slrp (slow receptor potential) mutant that is defective in photoreceptor response termination, and found it needs to be expressed in both neurons and epithelial glia to rescue the mutant phenotype. The gene product SLRP, an ADAM (a disintegrin and metalloprotease) protein, is localized in a special structure of epithelial glia, gnarl, and is required for gnarl formation. This glial function of SLRP is independent of the metalloprotease activity.
In the second part of my thesis work, I demonstrate that glutamatergic transmission from lamina intrinsic interneurons, the amacrine cells, to the epithelial glia is required for the rapid repolarization of photoreceptors at the end of the light response. From an RNAi-based screen, I identified a vesicular glutamate transporter (vGluT) in amacrine cells as an indispensable factor for the rapid repolarization of the photoreceptor, suggesting a critical role of glutamatergic transmission from amacrine cells in this retrograde regulation. Further, I found that loss of a glutamate-gated chloride channel GluCl phenocopies vGluT downregulation. Cell specific knockdown indicates that GluCl functions in both neurons and glia. In the lamina, a FLAG-tagged GluCl colocalized with the SLRP protein in the gnarl-like structures, and this localization pattern of GluCl depends on SLRP, suggesting that lamina epithelial glia receive glutamatergic input from amacrine cells through GluCl at the site of gnarl. Since the amacrine cell itself is innervated by photoreceptors, these observations suggest that a photoreceptor — amacrine cell — epithelial glia — photoreceptor feedback loop facilitates rapid repolarization of photoreceptors at the end of the light response.
In summary, my thesis research has revealed a feedback regulation mechanism that helps to achieve rapid kinetics of photoreceptor response. This visual regulation contributes to the temporal resolution of the visual system, and may be important for vision during movement and for motion detection. In addition, this work may also advance our understanding of glial function, and change our concept about the effect of glutamatergic transmission.
... The fact that lamina amacrine neurons connect different cartridges of lamina neurons and spines along laminar monopolar neurons suggests that there is communication across color channels within lamina cartridges (Fischbach and Dittrich, 1989;Douglass and Strausfeld, 2005;Souza et al., 1987). This suggests that initial steps of color processing occur in the lamina and are communicated to the medulla (Menzel, 1974;, although the axons of short-wavelength photoreceptors (blue to ultraviolet; R7 -R9 in bees) proceed through the lamina, apparently without contacting laminar neurons, and terminate in the medulla. ...
... In particular, layers 4 and 5a correlated well with serotonin staining and with complex layering of GABAergic fibers (Fig. 1) suggesting that neuronal processes in these layers are subject to spatially restricted inhibition and neuromodulatory control. Most of the tangential neurons we recorded from had their major branches in layers 4 and 5a [ Fig. 2E-G; the "serpentine layer" (Ehmer and Gronenberg, 2002;Strausfeld, 1976) that separated the outer from the inner medulla (Strausfeld, 2005)]. Nearly all of the large field medulla neurons had processes in the serpentine layer, which means that the computational operations occurring in the serpentine layer could be pivotal to understanding how the medulla directly interfaces with the protocerebrum. ...
The mechanisms of processing a visual scene involve segregating features (such as color) into separate information channels at different stages within the brain, processing these features, and then integrating this information at higher levels in the brain. To examine how this process takes place in the insect brain, we focused on the medulla, an area within the optic lobe through which all of the visual information from the retina must pass before it proceeds to central brain areas. We used histological and immunocytochemical techniques to examine the bumblebee medulla and found that the medulla is divided into eight layers. We then recorded and morphologically identified 27 neurons with processes in the medulla. During our recordings we presented color cues to determine whether response types correlated with locations of the neural branching patterns of the filled neurons among the medulla layers. Neurons in the outer medulla layers had less complex color responses compared to neurons in the inner medulla layers and there were differences in the temporal dynamics of the responses among the layers. Progressing from the outer to the inner medulla, neurons in the different layers appear to process increasingly complex aspects of the natural visual scene. J. Comp. Neurol. 513:441-456, 2009. (c) 2009 Wiley-Liss, Inc.
... In parallel with the structural analyses of the lamina's synaptic circuits, which are most complete for Drosophila, the electrophysiological properties of lamina neurons are reported but mostly from larger fly species (e.g. [22,23] [24,25,26,27,28,29,30]). Together, these reveal visual phenomena such as spatial summation and amplification of visual signals, lateral inhibition, light adaptation, and even peripheral substrates for movement detection and colour coding (reviewed in [31]). ...
... Compatible with this suggestion, Sinakevitch and Strausfeld [47] reported NMDA1 receptor-like immunoreactivity on T1 neurons in P. sericata. Glutamate may thus be used as a transmitter in amacrine neurons for wide-field interconnections (see also [29,30]). We also entertain the possibility that lamina monopolar neuron L2 may use glutamate for signaling within the lamina at some of its many minority classes of synapses, but that neither L1 nor L2 shows clear evidence of doing so at their chief output terminals in the medulla. ...
Synaptic connections of neurons in the Drosophila lamina, the most peripheral synaptic region of the visual system, have been comprehensively described. Although the lamina has been used extensively as a model for the development and plasticity of synaptic connections, the neurotransmitters in these circuits are still poorly known. Thus, to unravel possible neurotransmitter circuits in the lamina of Drosophila we combined Gal4 driven green fluorescent protein in specific lamina neurons with antisera to gamma-aminobutyric acid (GABA), glutamic acid decarboxylase, a GABA(B) type of receptor, L-glutamate, a vesicular glutamate transporter (vGluT), ionotropic and metabotropic glutamate receptors, choline acetyltransferase and a vesicular acetylcholine transporter. We suggest that acetylcholine may be used as a neurotransmitter in both L4 monopolar neurons and a previously unreported type of wide-field tangential neuron (Cha-Tan). GABA is the likely transmitter of centrifugal neurons C2 and C3 and GABA(B) receptor immunoreactivity is seen on these neurons as well as the Cha-Tan neurons. Based on an rdl-Gal4 line, the ionotropic GABA(A) receptor subunit RDL may be expressed by L4 neurons and a type of tangential neuron (rdl-Tan). Strong vGluT immunoreactivity was detected in alpha-processes of amacrine neurons and possibly in the large monopolar neurons L1 and L2. These neurons also express glutamate-like immunoreactivity. However, antisera to ionotropic and metabotropic glutamate receptors did not produce distinct immunosignals in the lamina. In summary, this paper describes novel features of two distinct types of tangential neurons in the Drosophila lamina and assigns putative neurotransmitters and some receptors to a few identified neuron types.
... However, a recent publication by Douglass and Strausfeld (2005) apparently challenges this view. They report obtaining intracellular recordings from three amacrine cells in Phaenicia and show partially dye-filled processes of these neurons as evidence. ...
At the layer of first visual synapses, information from photoreceptors is processed and transmitted towards the brain. In fly compound eye, output from photoreceptors (R1-R6) that share the same visual field is pooled and transmitted via histaminergic synapses to two classes of interneuron, large monopolar cells (LMCs) and amacrine cells (ACs). The interneurons also feed back to photoreceptor terminals via numerous ligand-gated synapses, yet the significance of these connections has remained a mystery. We investigated the role of feedback synapses by comparing intracellular responses of photoreceptors and LMCs in wild-type Drosophila and in synaptic mutants, to light and current pulses and to naturalistic light stimuli. The recordings were further subjected to rigorous statistical and information-theoretical analysis. We show that the feedback synapses form a negative feedback loop that controls the speed and amplitude of photoreceptor responses and hence the quality of the transmitted signals. These results highlight the benefits of feedback synapses for neural information processing, and suggest that similar coding strategies could be used in other nervous systems.
... It is conceivable that amacrine cells form an isomorphic network of functionally connected elements (see Discussion) supporting input from photoreceptor terminals at many optic cartridges. One definitive recording has been obtained from an amacrine cell of the green bottle fly Phaenicia sericata, identified as such by dye injection (Douglass & Strausfeld, 2004). The cell showed a steady depolarizing response to both transient and sustained illumination over stimulation periods as long as 500 ms, and a noninverting response to light intensity. ...
... Since recent recordings from amacrine cells (Douglass & Strausfeld, 2004) show strong responses across a wide range of frequencies, an amacrine cell in the model responds identically to the photoreceptor in the same optic cartridge. However, since amacrine cells form an input to T1, which exhibits a small response to sustained illumination and an inverted response to light intensity Fig. 4. Integration of neuronally based EMD model outputs into a generic tangential cell by spatial summation, addition of a constant~f spon , the spontaneous firing rate), and finally half-wave rectification (POS). ...
... Panel G shows a directionally selective T5 unit which combines the Tm1 and Tm9 units shown with neighboring Tm units to compute the direction of stimulus motion. (Douglass & Strausfeld, 2004), it is necessary for the amacrine outputs to be high-pass filtered and sign-inverted on the way to T1. These operations are proposed to occur at the amacrine-T1 synapse. ...
Based on comparative anatomical studies and electrophysiological experiments, we have identified a conserved subset of neurons in the lamina, medulla, and lobula of dipterous insects that are involved in retinotopic visual motion direction selectivity. Working from the photoreceptors inward, this neuronal subset includes lamina amacrine (alpha) cells, lamina monopolar (L2) cells, the basket T-cell (T1 or beta), the transmedullary cell Tm1, and the T5 bushy T-cell. Two GABA-immunoreactive neurons, the transmedullary cell Tm9 and a local interneuron at the level of T5 dendrites, are also implicated in the motion computation. We suggest that these neurons comprise the small-field elementary motion detector circuits the outputs of which are integrated by wide-field lobula plate tangential cells. We show that a computational model based on the available data about these neurons is consistent with existing models of biological elementary motion detection, and present a comparable version of the Hassenstein-Reichardt (HR) correlation model. Further, by using the model to synthesize a generic tangential cell, we show that it can account for the responses of lobula plate tangential cells to a wide range of transient stimuli, including responses which cannot be predicted using the HR model. This computational model of elementary motion detection is the first which derives specifically from the functional organization of a subset of retinotopic neurons supplying the lobula plate. A key prediction of this model is that elementary motion detector circuits respond quite differently to small-field transient stimulation than do spatially integrated motion processing neurons as observed in the lobula plate. In addition, this model suggests that the retinotopic motion information provided to wide-field motion-sensitive cells in the lobula is derived from a less refined stage of processing than motion inputs to the lobula plate.
