Fig 9 - uploaded by Pavel Balaban
Content may be subject to copyright.
Schematic representation of electrophysiological results of GABA applications and known interconnections of feeding and withdrawal circuits. Filled circles, inhibitory action; empty circles, excitatory action; arrows, direction of activation flow
Source publication
GABA-immunoreactive fibers were observed in the neuropile of each ganglion of Helix lucorum, while GABA-immunoreactive neural somata were found only in the buccal, cerebral, and pedal ganglia. Bath application of 10(-5) M GABA to the preparation "buccal mass-buccal ganglia" elicited a sequence of radula movements characteristic of feeding behavior....
Citations
... Collectively, GABA appeared capable of coordinating multiple motor systems required to achieve the highly complex feeding behavior of Clione (Arsharvsky et al., 1993). GABA produced similar organizational effects in the land snail Helix lucorum, where it promoted feeding movements and inhibited the neural circuit controlling an incompatible behavior: defensive withdrawal (Bravarenko et al., 2001). (A) GABAli neurons in the visceral ganglion (V g.) and right parietal ganglion (R Pa g.). ...
... The subsequent identification of GABAergic commissural neurons with predominant contralateral synaptic actions substantiated this proposal (Norekian, 1999;Jing and Weiss, 2003;Díaz-Ríos and Miller, 2005). The presence of GABAli fibers in the connectives between ganglia also suggested its involvement in the control and integration of motor systems, another premise that was confirmed by behavioral studies (Arshavsky et al., 1993;Bravarenko et al., 2001) and with the identification of GABAergic CBIs and BCIs in the Aplysia and Clione feeding systems Wu et al., 2003;Norekian and Malyshev, 2005). ...
The neurotransmitter gamma-aminobutyric acid (GABA) is widely distributed in the mammalian central nervous system, where it acts as a major mediator of synaptic inhibition. GABA also serves as a neurotransmitter in a range of invertebrate phyla, including arthropods, echinoderms, an-nelids, nematodes, and platyhelminthes. This article reviews evidence supporting the neurotransmitter role of GABA in gastropod molluscs, with an emphasis on its presence in identified neurons and well-characterized neural circuits. The collective findings indicate that GABAergic signaling participates in the selection and specification of motor programs, as well as the bilateral coordination of motor circuits. While relatively few in number, GABAergic neurons can influence neural circuits via inhibitory, excitatory, and modulatory synaptic actions. GABA’s colocalization with peptidergic and classical neurotransmitters can broaden its integrative capacity. The functional properties of GABAergic neurons in simpler gastropod systems may provide insight into the role of this neurotransmitter phenotype in more complex brains.
... Finally, alternate splicing of gene transcripts and the production of multiple neuropeptides from single precursor proteins means that complex cocktails of neuropeptides can be released from single neurons (Sossin et al. 1990, Santama et al. 1996, Santama and Benjamin 2000, cummins et al. 2011. hus, even synaptic connections between individual neurons can involve numerous transmitters and receptors, and in the control of feeding (Arshavsky et al. 1993, diaz-Rios et al. 1999, Bravarenko et al. 2001) and the processing of sensory information (Alkon et al. 1993, Jin et al. 2009, Kobayashi et al. 2012. ...
For many biologists the nervous system is a particularly fascinating organ system. The nervous system is involved in or is even responsible for many features that are regarded as being characteristic of animals in general. Since the last comprehensive work was published about 50 years ago, the time has probably come to provide a new review on recent, newly gathered knowledge on the structure of invertebrate nervous systems, especially since new methods have come into use. These advances now enable us to demonstrate neuronal architecture down to the level of the genes and the cell types involved, allowing a new view on nervous systems and comparisons among different taxa. These new findings may help in development of new hypotheses, or support of existing hypotheses on phylogenetic relationships and evolutionary pathways in the nervous system. In spite of many open questions we already have a good knowledge of how nervous systems work, how they are constructed, and how they may have evolved. There is certain evidence that the first nervous systems are represented by rather simple sensory–motor circuits, followed by nerve nets (plexus) located within the epithelia, and finally neuronal circuits composed of sensory cells, interneurons, and brains. Therefore, this book concentrates on invertebrates and structure and these new evolutionary aspects, here discussed as ‘research highlights’ or ‘perspectives’. Sensory structures are only touched on peripherally. Whereas some taxa have been studied extensively and well-written reviews may already exist, in other taxa our knowledge on the nervous system is still scant and scarce.
... GABA is known to be a neurotransmitter in the buccal ganglia of several gastropod species: Aplysia californica (Diaz- Rios et al., 1999), Clione limacina (Arshavsky et al., 1993), Helisoma trivolvis ( Richmond et al., 1991), Lymnaea stagnalis (Hatakeyama and Ito, 2000), Helix pomatia (Hernadi, 1994), Helix lucorum ( Bravarenko et al., 2001), Helix aspersa ) and Limax maximus (Cooke and Gelperin, 1988). Furthermore, GABA transmission and modulation in the buccal ganglion has been implicated in the control of feeding behaviors in Aplysia ( Jing et al., 2003), Clione (Arshavsky et al., 1993), Helisoma ( Richmond et al., 1986;Murphy, 1993;Richmond et al., 1994), Helix (Bravarenko et al., 2001) and Limax (Cooke and Gelperin, 1988). ...
... In fact, the number and distribution of GABA-ir neurons in panpulmonates and nudibranchs are very similar to each other. Most of the GABA-ir buccal neurons in Helisoma trivolis ( Richmond et al., 1991) , Lymnaea stagnalis (Hatakeyama andIto, 2000), Helix pomatia (Hernadi, 1994), Helix lucorum ( Bravarenko et al., 2001) and Limax maximus (Cooke and Gelperin, 1988) It is unclear as to why Pleurobranchaea has more buccal GABA-ir neurons than all other gastropods examined to date. As mentioned earlier, GABA and the buccal ganglia have been heavily implicated in the control of feeding behavior in gastropods. ...
Phylogenetic comparisons of neurotransmitter distribution are important for understanding the ground plan organization of nervous systems. This study describes the GABA-immunoreactive (GABA-ir) neurons in the buccal ganglia of six sea slug species (Mollusca, Gastropoda, Euthyneura, Nudipleura). In the nudibranch species, Hermissenda crassicornis, Tritonia diomedea, Tochuina tetraquetra, and Dendronotus iris, the number of GABA-ir neurons was highly consistent. Another nudibranch, Melibe leonina, however, contained approximately half the number of GABA-ir neurons. This may relate to its loss of a radula and its unique feeding behavior. The GABA immunoreactivity in a sister group to the nudibranchs, Pleurobranchaea californica, differed drastically from that of the nudibranchs. Not only did it have significantly more GABA-ir neurons but it also had a unique GABA distribution pattern. Furthermore, unlike the nudibranchs, the Pleurobranchaea GABA distribution was also different from that of other, more distantly related, euopisthobranch and panpulmonate snails and slugs. This suggests that the Pleurobranchaea GABA distribution may be a derived feature, unique to this lineage. The majority of GABA-ir axons and neuropil in the Nudipleura were restricted to the buccal ganglia, commissures and connectives. However, in Tritonia and Pleurobranchaea we detected a few GABA-ir fibers in buccal nerves that innervate feeding muscles. Although the specific functions of the GABA-ir neurons in the species in this study are not known, the innervation pattern suggests these neurons may play an integrative or regulatory role in bilaterally coordinated behaviors in the Nudipleura. This article is protected by copyright. All rights reserved.
... Finally, alternate splicing of gene transcripts and the production of multiple neuropeptides from single precursor proteins means that complex cocktails of neuropeptides can be released from single neurons (Sossin et al. 1990, Santama et al. 1996, Santama and Benjamin 2000, cummins et al. 2011). Thus, even synaptic connections between individual neurons can involve numerous transmitters and receptors, and in the control of feeding (Arshavsky et al. 1993, diaz-Rios et al. 1999, Bravarenko et al. 2001) and the processing of sensory information (Alkon et al. 1993, Jin et al. 2009, Kobayashi et al. 2012. ...
Gastropods comprise the second largest class in the Animal Kingdom with 60,000 to 80,000 living species occupying ecological niches covering the globe. Anatomy, behaviour and development vary significantly between the five clades of Patellogastropoda, Vetigastropoda,Neritimorpha, Caenogastropoda and Heterobranchia. Generally, the central nervous system consists of paired cerebral, buccal, pleural and pedal ganglia and five ganglia of thevisceral loop, but the ganglia demonstrate vary degrees of asymmetry (chiastoneury, euthyneury) and fusion due to the combined processes of centralizationand torsion, which is a 180o rotation of the posterior portion of the body that occurs early in larval development. Giant, identifiable neurons with characteristic locations, axonal morphology and physiological properties have led to the adoption of some heterobranchs as ‘model organisms’ for investigation of motor and centralpattern generation activity, molecular basis of learning and memory, and single cell transcriptomes. Gastropods also possess extensive peripheral nervous systems containing axons efferent and afferentto the central ganglia and also large numbers of peripheral neurons located within different organs of the body. Most of the classical, small molecule neurotransmitters identified in vertebrates are also found in the central and peripheral neuronsof gastropods together with numerous neuropeptides. The first neural elements (cells of the apical organ, posterior pioneerneurons, peripheralsensory neurons)and also many central neurons appear during trochophore-veliger larval stages, although many more neurons are added during metamorphosis and postlarval development.Gastropods thus provide a unique diversity of form, function and development of the nervous systems offering the opportunity to investigate adaptive evolution of the nervous system at levels of analysis ranging from behaviour to its molecular underpinnings.
... Gamma aminobutyric acid (GABA), synthesized from the amino acid glutamate by glutamate decarboxylase (Fig. 8A), is a ubiquitous neurotransmitter that generally mediates inhibitory synaptic transmission. In several species of gastropod molluscs, GABAergic neurotransmission has been implicated in behaviors such respiration [56], olfaction [57,58], feeding [59][60][61][62] and reproduction [63], however its role specifically in Nudibranchs remains poorly understood [64]. Comparative immuno-localization of GABA in the CNS of several Nudibranch species, including Tritonia, revealed clusters of conserved GABAergic neurons in the cerebral and pedal ganglia [64]. ...
Background: The sea slug Tritonia diomedea (Mollusca, Gastropoda, Nudibranchia), has a simple and highly accessible nervous system, making it useful for studying neuronal and synaptic mechanisms underlying behavior. Although many important contributions have been made using Tritonia, until now, a lack of genetic information has impeded exploration at the molecular level.
Results: We performed Illumina sequencing of central nervous system mRNAs from Tritonia, generating 133.1 million 100 base pair, paired-end reads. De novo reconstruction of the RNA-Seq data yielded a total of 185,546 contigs, which partitioned into 123,154 non-redundant gene clusters (unigenes). BLAST comparison with RefSeq and Swiss-Prot protein databases, as well as mRNA data from other invertebrates (gastropod molluscs: Aplysia californica, Lymnaea stagnalis and Biomphalaria glabrata; cnidarian: Nematostella vectensis) revealed that up to 76,292 unigenes in the Tritonia transcriptome have putative homologues in other databases, 18,246 of which are below a more stringent E-value cut-off of 1x10-6. In silico prediction of secreted proteins from the Tritonia transcriptome shotgun assembly (TSA) produced a database of 579 unique sequences of secreted proteins, which also exhibited markedly higher expression levels compared to other genes in the TSA.
Conclusions: Our efforts greatly expand the availability of gene sequences available for Tritonia diomedea. We were able to extract full length protein sequences for most queried genes, including those involved in electrical excitability, synaptic vesicle release and neurotransmission, thus confirming that the transcriptome will serve as a useful tool for probing the molecular correlates of behavior in this species. We also generated a neurosecretome database that will serve as a useful tool for probing peptidergic signalling systems in the Tritonia brain.
... Recording of multiple-cell activity with fluorescent or absorption VSD is performed using contact (LK ×25 0.4 NA, W.D. < 0.025, LOMO [3,46,48]) or water immersion (Olympus UMPlanF1 20×, 0.5 NA, W.D. 3.3 or similar ×10-20 [13,16,47] objectives, which can be combined with intracellular recording and stimulation at a suitable working distance [5,48]. For recording using a contactless objective, stained specimens are sometimes embedded in 1-1.5% agarose [6] prepared in normal physiological saline. ...
Studies of the electrical activity and plasticity of neural networks, individual nerve cells, and their subcellular compartments are now impractical without using optical methods to visualize functional signals which allow electrical events to be recorded both in many neurons simultaneously and in individual dendrites and axons and provide for linking these data to precise morphological images. Use of voltage-sensitive dyes (VSD) is the only of the small number of currently available methods which combines high spatial resolution with the ability to record ultrafast signals (
... GABA-mediated neurotransmission and neuromodulation have been shown to be significant for a range of behaviors in gastropods including: feeding (Bravarenko et al., 2001;Jing et al., 2003;Norekian and Malyshev, 2005;Diaz-Rios and Miller, 2005), respiration (Moccia et al., 2009), olfaction (Ito et al., 2004;Kobayashi et al., 2008), graviception (Jin et al., 2009), reproduction (Romanova et al., 1996), and developmental metamorphosis (Morse et al., 1979(Morse et al., , 1980. The pattern of GABA distribution in other gastropods has led to the speculation that GABA is involved in coordinating bilateral systems such as those regulating locomotion and feeding (Diaz-Rios et al., 1999;Bravarenko et al., 2001;Ierusalimsky and Balaban, 2001). ...
... GABA-mediated neurotransmission and neuromodulation have been shown to be significant for a range of behaviors in gastropods including: feeding (Bravarenko et al., 2001;Jing et al., 2003;Norekian and Malyshev, 2005;Diaz-Rios and Miller, 2005), respiration (Moccia et al., 2009), olfaction (Ito et al., 2004;Kobayashi et al., 2008), graviception (Jin et al., 2009), reproduction (Romanova et al., 1996), and developmental metamorphosis (Morse et al., 1979(Morse et al., , 1980. The pattern of GABA distribution in other gastropods has led to the speculation that GABA is involved in coordinating bilateral systems such as those regulating locomotion and feeding (Diaz-Rios et al., 1999;Bravarenko et al., 2001;Ierusalimsky and Balaban, 2001). Swimming in the nudibranchs is such a bilateral system that involves inhibitory connectivity. ...
... Within Gastropoda, GABA-ir has been described to varying degrees in pulmonate snails and slugs (Mollusca, Gastropoda, Pulmonata). This includes the species Helisoma trivolvis (Richmond et al., 1991), Planorbis corneus (Turner and Cottrell, 1978), Lymnnaea stagnalis (Hatakeyama and Ito, 2000), Helix pomatia (Hernadi, 1994), Helix aspersa , Helix lucorum (Bravarenko et al., 2001), Cepaea nemoralis (Dyakonova et al., 1995), and Limax maximus (Cooke and Gelperin, 1988). GABA-ir neurons are located primarily in the cerebral, pedal, and buccal ganglia in the above species, although a single pair of neurons was found in the pleural ganglia of Lymnaea. ...
The relative simplicity of certain invertebrate nervous systems, such as those of gastropod molluscs, allows behaviors to be dissected at the level of small neural circuits composed of individually identifiable neurons. Elucidating the neurotransmitter phenotype of neurons in neural circuits is important for understanding how those neural circuits function. In this study, we examined the distribution of γ-aminobutyric-acid;-immunoreactive (GABA-ir) neurons in four species of sea slugs (Mollusca, Gastropoda, Opisthobranchia, Nudibranchia): Tritonia diomedea, Melibe leonina, Dendronotus iris, and Hermissenda crassicornis. We found consistent patterns of GABA immunoreactivity in the pedal and cerebral-pleural ganglia across species. In particular, there were bilateral clusters in the lateral and medial regions of the dorsal surface of the cerebral ganglia as well as a cluster on the ventral surface of the pedal ganglia. There were also individual GABA-ir neurons that were recognizable across species. The invariant presence of these individual neurons and clusters suggests that they are homologous, although there were interspecies differences in the numbers of neurons in the clusters. The GABAergic system was largely restricted to the central nervous system, with the majority of axons confined to ganglionic connectives and commissures, suggesting a central, integrative role for GABA. GABA was a candidate inhibitory neurotransmitter for neurons in central pattern generator (CPG) circuits underlying swimming behaviors in these species, however none of the known swim CPG neurons were GABA-ir. Although the functions of these GABA-ir neurons are not known, it is clear that their presence has been strongly conserved across nudibranchs. J. Comp. Neurol. 522:794-810, 2014. © 2013 Wiley Periodicals, Inc.
... До полнительные требования также накладыва ет тип применяемого красителя, требующий определенных условий получения удовлетво рительного сигнала. Для регистрации с флуо ресцентными или абсорбционными ПЗК множественной клеточной активности ис пользуются контактные (ЛК ×25 0.4 NA, W.D. <0.025, ЛОМО; [3,46,48]), а также водно им мерсионные объективы (Olympus UMPlanFl 20×, 0.5 NA, W.D. 3.3 или аналоги 10-20×, [13,16,47]), которые можно сочетать с внутрикле точным отведением и стимуляцией при доста точном рабочем расстоянии [5,48] после окрашивания иногда заливают в 1-1.5% ную агарозу [6], приготовленную на нормаль ном физиологическом растворе. Воздушные объективы практически непригодны для реги страции с абсорбционными красителями из за колеблющейся водной поверхности, изменяю щей интенсивность проходящего света гораздо сильнее, чем полезный сигнал. ...
Currently, the studies of electrical activity and plasticity of neuronal networks are impossible without employing of imaging techniques to visualize functional signals that allowing revealing electrical events in multiple neurons, as well as in their tiny dendrites and axons placed on their morphological picture. Imaging with voltage-sensitive dyes (VSD) is one of unique available methods that providing both high spatial resolution and ultrafast sampling (< 0.1 ms) in realtime with perfect S-to-N ratio. During the last decade a significant progress in VSD application has been achieved due to major method improvements and new probe synthesis especially in the field of research of initiation and propagation of action potentials. There was evidence of the method efficiency and usability while the method was added to the toolbox of modern neuroscience for research in hottest topics.
... such as in the respiratory neural network of the pond snail Lymnaea stagnalis (Cheung et al. 2006) and in the feeding system of the terrestrial snail Helix lucorum (Bravarenko et al. 2001), and excitatory GABAergic synaptic responses emerged after pairing of exogenous GABA with postsynaptic depolarization in the photoreceptor of the marine snail Hermissenda crassicornis (Alkon et al. 1992). ...
Classical neurotransmitters, such as glutamate and γ-aminobutyric acid (GABA), often have different actions on invertebrate neurons from those reported for vertebrate neurons. In the terrestrial mollusk Limax, glutamate was found to function as an inhibitory transmitter in the procerebrum (PC), but it has not yet been clarified how GABA acts in the PC. We thus examined what effects GABA exerts on PC neurons in the present study. For this purpose, we first applied GABA to isolated PC preparations and recorded postsynaptic currents and potentials in PC neurons. The GABA application reduced the amplitude of inhibitory postsynaptic currents and depolarization-induced outward currents recorded in nonbursting neurons and increased the number of spontaneous spikes of nonbursting neurons. However, direct GABA-induced currents were not observed in either bursting or nonbursting neurons. These results suggest a potential direct effect of GABA on outward currents resulting in enhanced excitability of PC neurons. Next, we measured the change in [Ca(2+)](i) in cultured PC neurons by application of GABA. The GABA application increased spontaneous Ca(2+) events in cultured neurons. These Ca(2+) events were ascribable to the influx of extracellular Ca(2+). We then confirmed the presence of GABA and GABA receptors in the PC. The GABA-like immunoreactivity was observed in the neuropil layers of the PC, and the mRNAs for both GABA(A) and GABA(B) receptors were expressed in the PC. In particular, GABA(B) receptor mRNA, rather than GABA(A), was found to be more abundantly expressed in the PC. These results suggest that GABA functions as an excitatory modulator for PC neurons via mainly GABA(B) receptors.
... GABA also plays a role in modulating and coordinating systems related to feeding of Asterias rubens (Newman and Thorndyke,'94), and it controls foraging and regulates defecation in Caenorhabditis elegans (White et al.,'86). Excitatory GABAergic signaling contributes to the generation of feeding motor programs in pulmonate and pteropod mollusks (Arshavsky et al., '91, '93;Richmond et al., '91, '94;Norekian, '99;Bravarenko et al., 2001). In Clione, administration of exogenous GABA produced activation not only of the neural network involved in buccal feeding, but also of the neural network that controls the prey capture response of the buccal cones (Arshavsky et al., '93; Norekian and Satterlie,'93). ...
Here, we report the presence of the γ-aminobutyric acid (GABA)-ergic system in the calcisponge Leucandra aspera and examine the cellular localization of the components of this system, including GABA-like receptors using immunofluorescence and confocal microscopy. Furthermore, we demonstrate for the first time that GABA plays a functional role as a messenger in regulating sponge-feeding behavior. We found that both GABA(B) R1 and R2 subunits are present in the choanocytes of sponges as well as in the eso- and endopinacocytes. The functional role of GABA in the feeding behavior of this sponge was tested. The involvement of GABA receptors in the endocytic processes in L. aspera was demonstrated with dextran conjugated to Texas Red as a marker for material ingestion and by treating isolated sponge cells with a GABA(B) receptor agonist and an antagonist. The amount of dextran that was ingested increased in dissociated sponge cells when the GABA(B) receptor agonist baclofen was used, and this stimulatory effect was prevented by treatment with the GABA(B) receptor antagonist phaclofen. The baclofen effect on uptake was blocked by treatment with pertussis toxin, thus indicating a role for G proteins in modulating feeding behavior in L. aspera. Moreover, we found evidence that GABA receptors are involved in the consumption of dissolved organic matter by sponge cells. These findings suggest that GABA receptors and their functional role are highly conservative traits in the animal kingdom prenervous system evolution.
