Cargando…

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

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 ne...

Descripción completa

Detalles Bibliográficos
Autores principales: Brown, Jeffrey W., 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
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6306152/
https://www.ncbi.nlm.nih.gov/pubmed/30586424
http://dx.doi.org/10.1371/journal.pone.0208891
_version_ 1783382720007634944
author Brown, Jeffrey W.
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
author_facet Brown, Jeffrey W.
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
author_sort Brown, Jeffrey W.
collection PubMed
description 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 D(2)/D(3) 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 D(1) 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 D(2)/D(3) 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.
format Online
Article
Text
id pubmed-6306152
institution National Center for Biotechnology Information
language English
publishDate 2018
publisher Public Library of Science
record_format MEDLINE/PubMed
spelling pubmed-63061522019-01-08 A role for dopamine in the peripheral sensory processing of a gastropod mollusc Brown, Jeffrey W. 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 PLoS One Research Article 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 D(2)/D(3) 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 D(1) 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 D(2)/D(3) 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. Public Library of Science 2018-12-26 /pmc/articles/PMC6306152/ /pubmed/30586424 http://dx.doi.org/10.1371/journal.pone.0208891 Text en © 2018 Brown et al http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Brown, Jeffrey W.
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
title A role for dopamine in the peripheral sensory processing of a gastropod mollusc
title_full A role for dopamine in the peripheral sensory processing of a gastropod mollusc
title_fullStr A role for dopamine in the peripheral sensory processing of a gastropod mollusc
title_full_unstemmed A role for dopamine in the peripheral sensory processing of a gastropod mollusc
title_short A role for dopamine in the peripheral sensory processing of a gastropod mollusc
title_sort role for dopamine in the peripheral sensory processing of a gastropod mollusc
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6306152/
https://www.ncbi.nlm.nih.gov/pubmed/30586424
http://dx.doi.org/10.1371/journal.pone.0208891
work_keys_str_mv AT brownjeffreyw arolefordopamineintheperipheralsensoryprocessingofagastropodmollusc
AT schaubbrittanym arolefordopamineintheperipheralsensoryprocessingofagastropodmollusc
AT klusasbennettl arolefordopamineintheperipheralsensoryprocessingofagastropodmollusc
AT tranandrewx arolefordopamineintheperipheralsensoryprocessingofagastropodmollusc
AT dumanalexanderj arolefordopamineintheperipheralsensoryprocessingofagastropodmollusc
AT haneysamanthaj arolefordopamineintheperipheralsensoryprocessingofagastropodmollusc
AT borisabigailc arolefordopamineintheperipheralsensoryprocessingofagastropodmollusc
AT flanaganmeganp arolefordopamineintheperipheralsensoryprocessingofagastropodmollusc
AT delgadonadia arolefordopamineintheperipheralsensoryprocessingofagastropodmollusc
AT torresgrace arolefordopamineintheperipheralsensoryprocessingofagastropodmollusc
AT rolonmartinezsolymar arolefordopamineintheperipheralsensoryprocessingofagastropodmollusc
AT vaasjoleeo arolefordopamineintheperipheralsensoryprocessingofagastropodmollusc
AT millermarkw arolefordopamineintheperipheralsensoryprocessingofagastropodmollusc
AT gilletterhanor arolefordopamineintheperipheralsensoryprocessingofagastropodmollusc
AT brownjeffreyw rolefordopamineintheperipheralsensoryprocessingofagastropodmollusc
AT schaubbrittanym rolefordopamineintheperipheralsensoryprocessingofagastropodmollusc
AT klusasbennettl rolefordopamineintheperipheralsensoryprocessingofagastropodmollusc
AT tranandrewx rolefordopamineintheperipheralsensoryprocessingofagastropodmollusc
AT dumanalexanderj rolefordopamineintheperipheralsensoryprocessingofagastropodmollusc
AT haneysamanthaj rolefordopamineintheperipheralsensoryprocessingofagastropodmollusc
AT borisabigailc rolefordopamineintheperipheralsensoryprocessingofagastropodmollusc
AT flanaganmeganp rolefordopamineintheperipheralsensoryprocessingofagastropodmollusc
AT delgadonadia rolefordopamineintheperipheralsensoryprocessingofagastropodmollusc
AT torresgrace rolefordopamineintheperipheralsensoryprocessingofagastropodmollusc
AT rolonmartinezsolymar rolefordopamineintheperipheralsensoryprocessingofagastropodmollusc
AT vaasjoleeo rolefordopamineintheperipheralsensoryprocessingofagastropodmollusc
AT millermarkw rolefordopamineintheperipheralsensoryprocessingofagastropodmollusc
AT gilletterhanor rolefordopamineintheperipheralsensoryprocessingofagastropodmollusc