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Homologues of serotonergic central pattern generator neurons in related nudibranch molluscs with divergent behaviors

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Abstract

Homologues of a neuron that contributes to a species-specific behavior were identified and characterized in species lacking that behavior. The nudibranch Tritonia diomedea swims by flexing its body dorsally and ventrally. The dorsal swim interneurons (DSIs) are components of the central pattern generator (CPG) underlying this rhythmic motor pattern and also activate crawling. Homologues of the DSIs were identified in six nudibranchs that do not exhibit dorsal–ventral swimming: Tochuina tetraquetra, Melibe leonina, Dendronotus iris, D. frondosus, Armina californica, and Triopha catalinae. Homology was based upon shared features that distinguish the DSIs from all other neurons: (1) serotonin immunoreactivity, (2) location in the Cerebral serotonergic posterior (CeSP) cluster, and (3) axon projection to the contralateral pedal ganglion. The DSI homologues, named CeSP-A neurons, share additional features with the DSIs: irregular basal firing, synchronous inputs, electrical coupling, and reciprocal inhibition. Unlike the DSIs, the CeSP-A neurons were not rhythmically active in response to nerve stimulation. The CeSP-A neurons in Tochuina and Triopha also excited homologues of the Tritonia Pd5 neuron, a crawling efferent. Thus, the CeSP-A neurons and the DSIs may be part of a conserved network related to crawling that may have been co-opted into a rhythmic swim CPG in Tritonia.

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Abbreviations

ASD:

Antiserum diluent

CeSP:

Cerebral serotonergic posterior

CPG:

Central pattern generator

DSI:

Dorsal swim interneuron

PBS:

Phosphate buffered saline

Pd5:

Pedal 5

PdN2:

Pedal nerve 2

PP:

Pedal–pedal connective

Tpep:

Tritonia pedal peptide

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Acknowledgments

The authors thank Michael Baltzley for assistance in identifying Pd5 homologues, Evan Hill and Akira Sakurai for providing dye fills of Tritonia DSIs, Birgit Neuhaus and Priyal Shah for acquiring the confocal images, and Akira Sakurai for assistance with the spike shape analysis. We also thank Michael Baltzley, Shaun Cain, David Duggins, Erica Iyengar, James Murray, Thomas Pirtle, and Winsor Watson for collecting animals. Ronald Calabrese, Robert Calin-Jageman, Charles Derby, Joshua Lillvis, Dorothy Paul, Akira Sakurai, and two anonymous reviewers provided valuable comments on earlier versions of this manuscript. These experiments complied with the “Principles of animal care”, publication No. 86-23, revised 1985 of the National Institute of Health, and also with the current laws of the USA.

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  1. James M. Newcomb

    Present address: Department of Biology, NEC Box # 29, New England College, 24 Bridge St, Henniker, NH 03242-3296, USA

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  1. Department of Biology, Georgia State University, P.O. Box 4010, Atlanta, GA, 30302-4010, USA

    James M. Newcomb & Paul S. Katz

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This material is based upon work supported by the National Science Foundation, under Grant No. 0445768, and a GSU Research Program Enhancement grant to PSK.

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Newcomb, J.M., Katz, P.S. Homologues of serotonergic central pattern generator neurons in related nudibranch molluscs with divergent behaviors. J Comp Physiol A 193, 425–443 (2007). https://doi.org/10.1007/s00359-006-0196-4

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