A role for dopamine in the peripheral sensory processing of a gastropod mollusc

Jeffrey William Brown, Brittany M. Schaub, Bennett L. Klusas, Andrew X. Tran, Alexander J. Duman, Samantha J. Haney, Abigail C. Boris, Megan P. Flanagan, Nadia Delgado, Grace Torres, Solymar Rolón-Martínez, Lee O. Vaasjo, Mark W. Miller, Rhanor Gillette

Research output: Contribution to journalArticle

Abstract

Histological evidence points to the presence of dopamine (DA) in the cephalic sensory organs of multiple gastropod molluscs, suggesting a possible sensory role for the neurotransmitter. We investigated the sensory function of DA in the nudipleuran Pleurobranchaea californica, in which the central neural correlates of sensation and foraging behavior have been well characterized. Tyrosine hydroxylase-like immunoreactivity (THli), a signature of the dopamine synthetic pathway, was similar to that found in two other opisthobranchs and two pulmonates previously studied: 1) relatively few (<100) THli neuronal somata were observed in the central ganglia, with those observed found in locations similar to those documented in the other snails but varying in number, and 2) the vast majority of THli somata were located in the peripheral nervous system, were associated with ciliated, putative primary sensory cells, and were highly concentrated in chemotactile sensory organs, giving rise to afferent axons projecting to the central nervous system. We extended these findings by observing that applying a selective D2/D3 receptor antagonist to the chemo- and mechanosensory oral veil-tentacle complex of behaving animals significantly delayed feeding behavior in response to an appetitive stimulus. A D1 blocker had no effect. Recordings of the two major cephalic sensory nerves, the tentacle and large oral veil nerves, in a deganglionated head preparation revealed a decrease of stimulus-evoked activity in the former nerve following application of the same D2/D3 antagonist. Broadly, our results implicate DA in sensation and engender speculation regarding the foraging-based decisions the neurotransmitter may serve in the nervous system of Pleurobranchaea and, by extension, other gastropods.

Original languageEnglish (US)
Article numbere0208891
JournalPloS one
Volume13
Issue number12
DOIs
StatePublished - Dec 1 2018

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Molluscs
tyrosine 3-monooxygenase
Gastropoda
Mollusca
dopamine
molluscs
Pleurobranchaea
Dopamine
Tyrosine 3-Monooxygenase
Neurology
nerve tissue
sense organs
Head
Carisoprodol
Processing
neurotransmitters
Neurotransmitter Agents
antagonists
mouth
foraging

ASJC Scopus subject areas

  • Biochemistry, Genetics and Molecular Biology(all)
  • Agricultural and Biological Sciences(all)

Cite this

Brown, J. W., Schaub, B. M., Klusas, B. L., Tran, A. X., Duman, A. J., Haney, S. J., ... Gillette, R. (2018). A role for dopamine in the peripheral sensory processing of a gastropod mollusc. PloS one, 13(12), [e0208891]. https://doi.org/10.1371/journal.pone.0208891

A role for dopamine in the peripheral sensory processing of a gastropod mollusc. / Brown, Jeffrey William; Schaub, Brittany M.; Klusas, Bennett L.; Tran, Andrew X.; Duman, Alexander J.; Haney, Samantha J.; Boris, Abigail C.; Flanagan, Megan P.; Delgado, Nadia; Torres, Grace; Rolón-Martínez, Solymar; Vaasjo, Lee O.; Miller, Mark W.; Gillette, Rhanor.

In: PloS one, Vol. 13, No. 12, e0208891, 01.12.2018.

Research output: Contribution to journalArticle

Brown, JW, Schaub, BM, Klusas, BL, Tran, AX, Duman, AJ, Haney, SJ, Boris, AC, Flanagan, MP, Delgado, N, Torres, G, Rolón-Martínez, S, Vaasjo, LO, Miller, MW & Gillette, R 2018, 'A role for dopamine in the peripheral sensory processing of a gastropod mollusc', PloS one, vol. 13, no. 12, e0208891. https://doi.org/10.1371/journal.pone.0208891
Brown JW, Schaub BM, Klusas BL, Tran AX, Duman AJ, Haney SJ et al. A role for dopamine in the peripheral sensory processing of a gastropod mollusc. PloS one. 2018 Dec 1;13(12). e0208891. https://doi.org/10.1371/journal.pone.0208891
Brown, Jeffrey William ; Schaub, Brittany M. ; Klusas, Bennett L. ; Tran, Andrew X. ; Duman, Alexander J. ; Haney, Samantha J. ; Boris, Abigail C. ; Flanagan, Megan P. ; Delgado, Nadia ; Torres, Grace ; Rolón-Martínez, Solymar ; Vaasjo, Lee O. ; Miller, Mark W. ; Gillette, Rhanor. / A role for dopamine in the peripheral sensory processing of a gastropod mollusc. In: PloS one. 2018 ; Vol. 13, No. 12.
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