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Neural control of olfaction and tentacle movements by serotonin and dopamine in terrestrial snail

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Abstract

We investigated the role of serotonin (5HT) and dopamine (DA) in the regulation of olfactory system function and odor-evoked tentacle movements in the snail Helix. Preparations of the posterior tentacle (including sensory pad, tentacular ganglion and olfactory nerve) or central ganglia with attached posterior tentacles were exposed to cineole odorant and the evoked responses were affected by prior application of 5HT or DA or their precursors 5-hydroxytryptophan (5HTP) and l-DOPA, respectively. 5HT applications decreased cineole-evoked responses recorded in the olfactory nerve and hyperpolarized the identified tentacle retractor muscle motoneuron MtC3, while DA applications led to the opposite changes. 5HTP and l-DOPA modified MtC3 activity comparable to 5HT and DA action. DA was also found to decrease the amplitude of spontaneous local field potential oscillations in the procerebrum, a central olfactory structure. In vivo studies demonstrated that injection of 5HTP in freely moving snails reduced the tentacle withdrawal response to aversive ethyl acetate odorant, whereas the injection of l-DOPA increased responses to “neutral” cineole and aversive ethyl acetate odorants. Our data suggest that 5HT and DA affect the peripheral (sensory epithelium and tentacular ganglion), the central (procerebrum), and the single motor neuron (withdrawal motoneuron MtC3) level of the snail’s nervous system.

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Abbreviations

5HT:

Serotonin

5HTP:

5-hydroxy-l-tryptophan

DA:

Dopamine

l-DOPA:

3,4-Dihydroxy-l-phenylalanine

LFP:

Local field potential

MtC3:

Identified metacerebral neuron #3

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Acknowledgments

Authors are thankful to R. Boyle, E.S. Nikitin, A.Y. Malyshev, I.S. Zakharov, and T.A. Korshunova for discussions and help in experiments. This study was supported by grants from Russian Foundation for Basic Research, Council for Grants of the President of RF, Program of Physiology Division of Russian Academy of Sciences, and Federal Program of Russian Ministry of Education and Science. The Ethics Commission of Institute of Higher Nervous Activity, Russian Academy of Sciences, approved the experimental protocol. Experimental procedures are in compliance with the Guide for the care and use of Laboratory animals published by the National Institutes of Health (USA).

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  1. Institute of Higher Nervous Activity and Neurophysiology, Russian Academy of Science, Butlerova 5a, Moscow, 117485, Russia

    Matvey Roshchin & Pavel M. Balaban

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  1. Matvey Roshchin
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  2. Pavel M. Balaban
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Correspondence to Pavel M. Balaban.

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Roshchin, M., Balaban, P.M. Neural control of olfaction and tentacle movements by serotonin and dopamine in terrestrial snail. J Comp Physiol A 198, 145–158 (2012). https://doi.org/10.1007/s00359-011-0695-9

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  • DOI: https://doi.org/10.1007/s00359-011-0695-9

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