GABA as a Neurotransmitter in Gastropod Molluscs

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, annelids, 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.

• Publication year

  2019

• Venue

  The Biological Bulletin

• Publication date

  2019-01-16

• Fields of study

  Biology, Medicine

• Identifiers
  DOI 10.1086/701377PMID 30933636PMCID PMC7710352
• External record

  Open on Semantic Scholar

• Source metadata

  Semantic Scholar, PubMed

• No claims are published for this paper.

• No concepts are published for this paper.

• GABA‐like immunoreactivity in Biomphalaria: Colocalization with tyrosine hydroxylase‐like immunoreactivity in the feeding motor systems of panpulmonate snails

  2018influential reference
• Whole genome analysis of a schistosomiasis-transmitting freshwater snail

  2017cited by this paper
• Central nervous system transcriptome of Biomphalaria alexandrina, an intermediate host for schistosomiasis

  2017cited by this paper
• GABA‐, histamine‐, and FMRFamide‐immunoreactivity in the visual, vestibular and central nervous systems of Hermissenda crassicornis

  2017cited by this paper
• Comparative Mapping of GABA‐Immunoreactive Neurons in the Buccal Ganglia of Nudipleura Molluscs

  2016cited by this paper
• Mechanisms and functions of GABA co-release

  2016cited by this paper
• Deep mRNA Sequencing of the Tritonia diomedea Brain Transcriptome Provides Access to Gene Homologues for Neuronal Excitability, Synaptic Transmission and Peptidergic Signalling

  2015cited by this paper
• Complementary Interactions between Command-Like Interneurons that Function to Activate and Specify Motor Programs

  2014cited by this paper
• Comparative mapping of GABA‐immunoreactive neurons in the central nervous systems of nudibranch molluscs

  2014cited by this paper
• Midbrain dopamine neurons sustain inhibitory transmission using plasma membrane uptake of GABA, not synthesis

  2014cited by this paper
• PKC-mediated GABAergic enhancement of dopaminergic responses: implication for short-term potentiation at a dual-transmitter synapse.

  2014cited by this paper
• Release of a single neurotransmitter from an identified interneuron coherently affects motor output on multiple time scales.

  2013cited by this paper
• The Nicotinic Acetylcholine Receptor: The Founding Father of the Pentameric Ligand-gated Ion Channel Superfamily*

  2012cited by this paper
• Corelease of Dopamine and GABA by a Retinal Dopaminergic Neuron

  2012cited by this paper
• Faculty Opinions recommendation of Dopaminergic neurons inhibit striatal output through non-canonical release of GABA.

  2012cited by this paper
• De Novo Sequencing and Transcriptome Analysis of the Central Nervous System of Mollusc Lymnaea stagnalis by Deep RNA Sequencing

  2012cited by this paper
• Dopaminergic neurons inhibit striatal output via non-canonical release of GABA

  2012cited by this paper
• Evidence for glutamate, GABA and NO in coordinating behaviour in the sponge, Ephydatia muelleri (Demospongiae, Spongillidae)

  2010cited by this paper
• GABAB receptors: physiological functions and mechanisms of diversity.

  2010cited by this paper
• Evolutionary emergence of synaptic nervous systems: what can we learn from the non‐synaptic, nerveless Porifera?

  2010cited by this paper
• GABAA- and AMPA-like receptors modulate the activity of an identified neuron within the central pattern generator of the pond snail Lymnaea stagnalis

  2009cited by this paper
• Distinct Inhibitory Neurons Exert Temporally Specific Control over Activity of a Motoneuron ReceivingConcurrent Excitation and Inhibition

  2009cited by this paper
• 5-HT and GABA modulate intrinsic excitability of type I interneurons in Hermissenda.

  2009cited by this paper
• Comparative Neurobiology of Feeding in the Opisthobranch Sea Slug, Aplysia, and the Pulmonate Snail, Helisoma: Evolutionary Considerations

  2009cited by this paper
• Transcriptome analysis of the central nervous system of the mollusc Lymnaea stagnalis

  2009cited by this paper
• Non-synaptic neuronal mechanisms of learning and memory in gastropod molluscs.

  2008cited by this paper
• Co-transmission of dopamine and GABA in periglomerular cells.

  2008cited by this paper
• Target-Specific Regulation of Synaptic Efficacy in the Feeding Central Pattern Generator of Aplysia: Potential Substrates for Behavioral Plasticity?

  2006cited by this paper
• Neuronal transcriptome of Aplysia: neuronal compartments and circuitry.

  2006cited by this paper
• GABA and glutamate specifically induce contractions in the sponge Tethya wilhelma

  2006cited by this paper
• Rapid dopaminergic signaling by interneurons that contain markers for catecholamines and GABA in the feeding circuitry of Aplysia.

  2005cited by this paper
• Responses of cerebral GABA-containing CBM neuron to taste stimulation with seaweed extracts in Aplysia kurodai.

  2005cited by this paper
• Coordinated excitatory effect of GABAergic interneurons on three feeding motor programs in the mollusk Clione limacina.

  2005influential reference
• Dynamical basis of intentions and expectations in a simple neuronal network.

  2004cited by this paper
• GAMMA-AMINOBUTYRIC ACID AND OTHER BLOCKING COMPOUNDS IN CRUSTACEA

  2004cited by this paper
• Dopaminergic contributions to modulatory functions of a dual-transmitter interneuron in Aplysia.

  2004cited by this paper
• Anatomy of the giant dopamine-containing neurone in the left pedal ganglion of Planorbis corneus

  2004cited by this paper
• Fast synaptic connections from CBIs to pattern-generating neurons in Aplysia: initiation and modification of motor programs.

  2003influential reference
• Identification of a GABA-containing cerebral-buccal interneuron-11 in Aplysia californica.

  2003influential reference
• Concerted GABAergic Actions of Aplysia Feeding Interneurons in Motor Program Specification

  2003influential reference
• EXP-1 is an excitatory GABA-gated cation channel

  2003cited by this paper
• Colocalization of gamma-aminobutyric acid-like immunoreactivity and catecholamines in the feeding network of Aplysia californica.

  2002influential reference
• Interneuronal Basis of the Generation of Related but Distinct Motor Programs in Aplysia: Implications for Current Neuronal Models of Vertebrate Intralimb Coordination

  2002cited by this paper
• Behavior and Its Neural Control in Gastropod Molluscs

  2002cited by this paper
• Interneuronal and peptidergic control of motor pattern switching in Aplysia.

  2002cited by this paper
• GABA RECEPTORS

  2002cited by this paper
• Participation of GABA in establishing behavioral hierarchies in the terrestrial snail

  2001influential reference
• The Molecular Biology of Memory Storage: A Dialogue Between Genes and Synapses

  2001cited by this paper
• The neuronal basis of feeding in the snail, Helisoma, with comparisons to selected gastropods.

  2001cited by this paper
• Ontogenesis of the snail, Helix aspersa: Embryogenesis timetable and ontogenesis of GABA-like immunoreactive neurons in the central nervous system

  2001cited by this paper
• Neural Mechanisms of Motor Program Switching inAplysia

  2001cited by this paper
• Pharmacology of GABA and Glycine Neurotransmission

  2001cited by this paper
• GABA Enhances Transmission at an Excitatory Glutamatergic Synapse

  2001cited by this paper
• GABA and responses to GABA in the stomatogastric ganglion of the crab Cancer borealis.

  2000cited by this paper
• Distribution and developmental changes in GABA‐like immunoreactive neurons in the central nervous system of pond snail, Lymnaea stagnalis

  2000influential reference
• Localization of GABA‐like immunoreactivity in the central nervous system of Aplysia californica

  1999cited by this paper
• GABAergic Excitatory Synapses and Electrical Coupling Sustain Prolonged Discharges in the Prey Capture Neural Network of Clione limacina

  1999cited by this paper
• Crustacean studies and the early history of GABA.

  1999cited by this paper
• Identification and characterization of catecholaminergic neuron B65, which initiates and modifies patterned activity in the buccal ganglia of Aplysia.

  1998influential reference
• Different roles of neurons B63 and B34 that are active during the protraction phase of buccal motor programs in Aplysia californica.

  1997cited by this paper
• Evolution and overview of classical transmitter molecules and their receptors

  1996cited by this paper
• Intrinsic and extrinsic neuromodulation of motor circuits.

  1995cited by this paper
• Localisation of gamma aminobutyric acid (GABA)-like immunoreactivity in the echinoderm Asterias rubens

  1994cited by this paper
• Gamma‐aminobutyric acid in the nervous system of a planarian

  1994cited by this paper
• GABA regulates the buccal motor output of Helisoma by two pharmacologically distinct actions

  1994influential reference
• Distribution and anatomy of GABA-like immunoreactive neurons in the central and peripheral nervous system of the snail Helix pomatia

  1994influential reference
• Cerebral neurons underlying prey capture movements in the pteropod mollusc, Clione limacina

  1993cited by this paper
• Dopaminergic neuron B20 generates rhythmic neuronal activity in the feeding motor circuitry of Aplysia.

  1993cited by this paper
• FMRFamide and GABA Produce Functionally Opposite Effects on Prey-Capture Reactions in the Pteropod Mollusk Clione limacina.

  1993cited by this paper
• GABA‐Mediated Synaptic Interaction Between the Visual and Vestibular Pathways of Hermissenda

  1993cited by this paper
• The GABAergic nervous system of Caenorhabditis elegans

  1993cited by this paper
• Pharmacologically induced elements of the hunting and feeding behavior in the pteropod mollusk Clione limacina. I. Effects of GABA.

  1993cited by this paper
• The VD1/RPD2 neuronal system in the central nervous system of the pond snail Lymnaea stagnalis studied by in situ hybridization and immunocytochemistry

  1992influential reference
• Identification and characterization of cerebral-to-buccal interneurons implicated in the control of motor programs associated with feeding in Aplysia

  1991influential reference
• Sequence of a functional invertebrate GABAA receptor subunit which can form a chimeric receptor with a vertebrate alpha subunit.

  1991cited by this paper
• Expression of diverse neuropeptide cotransmitters by identified motor neurons in Aplysia

  1991cited by this paper
• The role of pacemaker properties and synaptic input in generation and modulation of spiking activity in a pair of electrically coupled peptidergic neurons.

  1991influential reference
• Evidence for the presence, synthesis, immunoreactivity, and uptake of GABA in the nervous system of the snail Helisoma trivolvis

  1991influential reference
• Gamma-aminobutyric acid induces feeding behaviour in the marine mollusc, Clione limacina.

  1991cited by this paper
• Immunohistochemistry of Diverging and Converging Neurotransmitter Systems in Mollusks.

  1991cited by this paper
• GABA receptors in insects.

  1990cited by this paper
• The neurobiology of disease

  1990cited by this paper
• Cloning of genomic and cDNA sequences encoding an invertebrate gamma-aminobutyric acidA receptor subunit.

  1990cited by this paper
• Voltage-clamp characterization of Cl- conductance gated by GABA and L-glutamate in single neurons of Aplysia.

  1989cited by this paper
• The bag cell neurons of Aplysia. A model for the study of the molecular mechanisms involved in the control of prolonged animal behaviors.

  1989cited by this paper
• The Sharpey-Schafer Lecture. Ionic channels: evolutionary origins and modern roles.

  1989cited by this paper
• Pharmacological profile of gamma-aminobutyric acid (GABA) receptors of identified central neurones from Helix Aspersa

  1989cited by this paper
• Distribution of GABA-like immunoreactive neurons in the slug Limax maximus

  1988influential reference
• Distinct GABA and glutamate receptors may share a common channel in Aplysia neurons.

  1987cited by this paper
• GABA-immunoreactivity in inhibitory motor neurons of the nematode Ascaris

  1987cited by this paper
• What do GABA neurons really do? They make possible variability generation in relation to demand.

  1986cited by this paper
• Evidence for GABA as a neurotransmitter in the leech

  1986cited by this paper
• Mechanisms of pattern generation underlying swimming in Tritonia. IV. Gating of central pattern generator.

  1985cited by this paper
• Immunocytochemical localization and direct assays of serotonin-containing neurons in Aplysia.

  1984cited by this paper
• Mechanisms of pattern generation underlying swimming in Tritonia. III. Intrinsic and synaptic mechanisms for delayed excitation.

  1983cited by this paper
• 3H‐GABA uptake selectively labels identifiable neurons in the leech central nervous system

  1983cited by this paper
• Identification of additional histaminergic neurons in Aplysia: improvement of single cell isolation techniques for in tandem physiological and chemical studies.

  1980cited by this paper
• Morphology of two electrotonically-coupled giant neurosecretory neurons in the snail, Lymnaea stagnalis

  1980influential reference
• Associative Behavioral Modification in Hermissenda: Cellular Correlates

  1980cited by this paper
• Behavioral biology of Aplysia : a contribution to the comparative study of opisthobranch molluscs

  1979cited by this paper

• Insomnia treatment based on the regulation of the GABAergic system: traditional Chinese medicine perspectives and therapeutic approaches

  2026cites this paper
• Understanding Target-Specific Effects of Antidepressant Drug Pollution on Molluscs: A Systematic Review Report

  2025cites this paper
• Neurochemically-evoked activity in slice preparations of the octopus arm nerve cord

  2025cites this paper
• Oxidative Stress-Mediated Neuroinflammation in the Pathophysiology of Schizophrenia

  2025cites this paper
• The role of dopamine, acetylcholine, GABA, beta endorphin, and agmatine in the pathophysiology of delirium in children.

  2025cites this paper
• How the diffuse neuroendocrine system shapes health, homeostasis, and cancer.

  2025cites this paper
• Phagocytic Function Analyses of GABBR-Related Microglia in Immature Developing Epileptic Brain Based on 10× Single-Nucleus RNA Sequencing Technology

  2025cites this paper
• First evidence of an anxiety-like behavior and its pharmacological modulation in a molluscan model organism, Lymnaea stagnalis

  2025cites this paper
• Allatotropin (AT) related peptides L-ATRP and D2-ATRP diastereomers activate an endogenous receptor and suppress heart rate in the Pacific abalone Haliotis discus hannai.

  2024cites this paper
• The effects of functional biscuits on intestinal mucosal microbiota composition, brain function, and antioxidant activity

  2024cites this paper
• Insights and progress on the biosynthesis, metabolism, and physiological functions of gamma-aminobutyric acid (GABA): a review

  2024cites this paper
• Three-dimensional molecular atlas highlights spatial and neurochemical complexity in the axial nerve cord of octopus arms.

  2024cites this paper
• An Enzyme Assay Kit for GABA Quantification in Plant Tissues.

  2024cites this paper
• Understanding the function of the GABAergic system and its potential role in rheumatoid arthritis

  2023cites this paper
• Molecular characterization of nervous system organization in the hemichordate acorn worm Saccoglossus kowalevskii

  2023cites this paper
• Gamma-aminobutyric acid (GABA) suppresses hemocyte phagocytosis by binding to GABA receptors and modulating corresponding downstream pathways in blood clam, Tegillarca granosa.

  2023cites this paper
• Design, Dft and Molecular Doping Studies of Metal Complexes as a Neurotransmitter Modulator of Autism Spectrum Disease in Preschool Children

  2023cites this paper
• GABRP is a Promising Prognostic Biomarker and Associated with Immune Cell Infiltration in Lung Squamous Cell Carcinoma

  2023cites this paper
• α-Aminobutyric Acid Constrains Macrophage-Associated Inflammatory Diseases through Metabolic Reprogramming and Epigenetic Modification

  2023cites this paper
• Molecular characterization of nervous system organization in the hemichordate Saccoglossus kowalevskii

  2023cites this paper
• From reproductive behaviour to responses to predators: Ocean acidification does not impact the behaviour of an herbivorous marine gastropod.

  2023cites this paper
• A whole-cell recording database of neuromodulatory action in the adult neocortex

  2022cites this paper
• Histamine and gamma-aminobutyric acid in the nervous system of Pygospio elegans (Annelida: Spionidae): structure and recovery during reparative regeneration

  2022cites this paper
• Responses of early life stages of European abalone (Haliotis tuberculata) to ocean acidification after parental conditioning: Insights from a transgenerational experiment.

  2022cites this paper
• Anxiolytic effect of YangshenDingzhi granules: Integrated network pharmacology and hippocampal metabolomics

  2022cites this paper
• The Role of Vesicle Release and Synaptic Transmission in Depression.

  2022cites this paper
• Competitive Cyclists’ Freely Chosen Cadence Is History Dependent

  2022cites this paper
• A 5-Minute Rest Period Weakens the Phenomenon of History Dependence of Freely Chosen Pedalling Cadence and Entails a Borderland Observation

  2022cites this paper
• History Dependence of Freely Chosen Index Finger Tapping Rhythmicity

  2022cites this paper
• Physiological roles and metabolism of γ-aminobutyric acid (GABA) in parasitic protozoa.

  2022cites this paper
• Freely chosen cadence during ergometer cycling is dependent on pedalling history

  2021cites this paper
• Alterations in neurotransmitter levels and transcription factor expression following intranasal buprenorphine administration.

  2021cites this paper
• United States Pharmacopeia (USP) Safety Review of Gamma-Aminobutyric Acid (GABA)

  2021cites this paper
• Tetrabromobisphenol A acts a neurodevelopmental disruptor in early larval stages of Mytilus galloprovincialis.

  2021cites this paper
• The role of ligand-gated chloride channels in behavioural alterations at elevated CO2 in a cephalopod.

  2021cites this paper
• Identification and localization of a gonadotropin‐releasing hormone‐related neuropeptide in Biomphalaria, an intermediate host for schistosomiasis

  2020cites this paper
• Genomic signatures of host‐associated divergence and adaptation in a coral‐eating snail, Coralliophila violacea (Kiener, 1836)

  2020cites this paper
• Proteome changes in muscles, ganglia, and gills in Corbicula fluminea clams exposed to crude oil: Relationship with behavioural disturbances.

  2020cites this paper
• Low concentrations of oxazepam induce feeding and molecular changes in Radix balthica juveniles.

  2020cites this paper