Comparative Mapping of GABA‐Immunoreactive Neurons in the Buccal Ganglia of Nudipleura Molluscs

Abstract

Phylogenetic comparisons of neurotransmitter distribution are important for understanding the ground plan organization of nervous systems. This study describes the γ-aminobutyric acid (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.

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

“…The presence of major GABAergic tracts in the commissures of the cerebral, pedal, and buccal ganglia is consistent with observations in other panpulmonate species as well as in euopisthobranchs and nudibranchs (Cooke & Gelperin, 1988;Díaz-Ríos et al, 1999;Gunaratne et al, 2014;Gunaratne & Katz, 2016;Richmond et al, 1991). These paired ganglia control motor behaviors such as feeding and locomotion that require bilateral coordination.…”

“…Molecular clock analysis estimates that this divergence occurred approximately 237 Mya near the Permian/Triassic transition. The recent localization of GABAli in the buccal ganglia of Nudipleura (Gunaratne & Katz, ) sets the stage for exploring whether GABA‐DA colocalization predated divergence of the Tectipleura and Nudipleura groups. This avenue of investigation should provide opportunities to explore the functional consequences of classical neurotransmitter colocalization in identified neurons and tractable motor networks (Miller, ).…”

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.…”

Histamine and histidine decarboxylase in the olfactory system and brain of the common cuttlefish Sepia officinalis (Linnaeus, 1758)

“…For example, Arendt, Tosches, and Marlow (2016) compared the neurodevelopment of cnidarians through bilatarians and reported several "distinct integration centers" which may be conserved regions common across the animal kingdom and foundational to the bilaterian nerve chord and brain (Arendt, 2003;Tessmar-Raible et al, 2007). Another standard method is to compare the expression of neurotransmitters in cell populations (Arendt, 2003;Croll, 2006;Gunaratne & Katz, 2016;Northcutt & Muske, 1994;Wollesen, Cummins, Degnan, & Wanninger, 2010a;Wollesen, Degnan, & Wanninger, 2010b). As in vertebrates, multiple neurotransmitters have long been known to exist in cephalopods (reviewed in Packard, 1972;Tansey, 1979;Messenger, 1996;De Lisa, Salzano, Moccia, Scaloni, & Di Cosmo, 2013).…”