Comparative mapping of GABA‐immunoreactive neurons in the central nervous systems of nudibranch molluscs

Abstract

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.

Deep mRNA Sequencing of the Tritonia diomedea Brain Transcriptome Provides Access to Gene Homologues for Neuronal Excitability, Synaptic Transmission and Peptidergic Signalling

“…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 [59–62] 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].…”

“…In several species of gastropod molluscs, GABAergic neurotransmission has been implicated in behaviors such respiration [56], olfaction [57,58], feeding [59–62] 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]. Indeed, knowing the sequences of genes involved in different modes of synaptic transmission, including GABA, dopamine, glutamate, acetylcholine, and neuropeptides, provides avenues for exploring the CNS at the molecular level, such as localization of defined protein epitopes, or mRNA in situ hybridization.…”

Relaxing effect of eugenol and essential oils in Pomacea canaliculata

“…The EO of H. ringens promoted deep anesthesia (111 to 554µL L -1 ) without mortality in silver catfish (SILVA et al, 2013), and its effect was attributed to the presence of pulegone (96.66%), an allosteric modulator of GABA (TONG & COATS, 2010). As GABA immunoreactive neurons are reported in the central nervous system of gastropods (HATAKEYAMA & ITO, 2000;GUNARATNE et al, 2014;, this result was unexpected. Pomacea canaliculata can cause losses in agriculture (COWI, 2002) and public health problems because it is an intermediate host of the nematode Angiostrongylus cantonensis, responsible for causing meningitis in humans (SONG et al, 2016).…”

Range extension for the region of sympatry between the nudibranchsHermissenda opalescensandHermissenda crassicornisin the northeastern Pacific

“…Depending on how long this range overlap has existed, earlier studies purportedly of H. crassicornis may have in fact been studying H. opalescens or a mixture of the two species. In particular, interpretations of the extensive history of neurobiological research with animals collected from various locations in California should now consider the potential effects of species-specific differences in neural circuits or behaviour (e.g., Alkon 1973Alkon , 1980Cavallo et al 2014;Gunaratne et al 2014;Gunaratne and Katz 2016;Webber et al 2017). In the future, careful species identification is required for all studies of Hermissenda along the northeast Pacific coast of North America, and further sampling is needed to verify both the northern range boundary for H. opalescens and the southern range boundary for H. crassicornis.…”

“…This division has resurrected the three species names originally described in the genus that had previously been unified into a single trans-Pacific species, H. crassicornis (sensu lato) (O'Donoghue 1922). Beyond the biogeographic and evolutionary implications of recognizing the three species anew, the discovery that H. crassicornis (sensu lato) was a species complex may have important ramifications for interpreting more than 40 years of neurobiological study of the animals (e.g., Alkon 1973Alkon , 1980Crow 2004;Blackwell 2006;Cavallo et al 2014;Gunaratne et al 2014;Gunaratne and Katz 2016;Webber et al 2017). It is possible that phenotypic heterogeneity amongst the species includes both neural and behavioural characters, and thus, care may be needed in integrating conclusions made in studies with animals from different locations.…”