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Serotonergic Modulation of Sensory Neuron Activity and Behavior in Apteronotus albifrons

Organisms must constantly adapt to changes in their environment to survive. It is thought that neuromodulators such as serotonin enable sensory neurons to better process input encountered during different behavioral contexts. Here, we investigated how serotonergic innervation affects neural and beha...

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Autores principales: Marquez, Mariana M., Chacron, Maurice J.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7358949/
https://www.ncbi.nlm.nih.gov/pubmed/32733214
http://dx.doi.org/10.3389/fnint.2020.00038
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author Marquez, Mariana M.
Chacron, Maurice J.
author_facet Marquez, Mariana M.
Chacron, Maurice J.
author_sort Marquez, Mariana M.
collection PubMed
description Organisms must constantly adapt to changes in their environment to survive. It is thought that neuromodulators such as serotonin enable sensory neurons to better process input encountered during different behavioral contexts. Here, we investigated how serotonergic innervation affects neural and behavioral responses to behaviorally relevant envelope stimuli in the weakly electric fish species Apteronotus albifrons. Under baseline conditions, we found that exogenous serotonin application within the electrosensory lateral line lobe increased sensory neuron excitability, thereby promoting burst firing. We found that serotonin enhanced the responses to envelope stimuli of pyramidal cells within the lateral segment of the electrosensory lateral line lobe (ELL) by increasing sensitivity, with the increase more pronounced for stimuli with higher temporal frequencies (i.e., >0.2 Hz). Such increases in neural sensitivity were due to increased burst firing. At the organismal level, bilateral serotonin application within the ELL lateral segment enhanced behavioral responses to sensory input through increases in sensitivity. Similar to what was observed for neural responses, increases in behavioral sensitivity were more pronounced for higher (i.e., >0.2 Hz) temporal frequencies. Surprisingly, a comparison between our results and previous ones obtained in the closely related species A. leptorhynchus revealed that, while serotonin application gave rise to similar effects on neural excitability and responses to sensory input, serotonin application also gave rise to marked differences in behavior. Specifically, behavioral responses in A. leptorhynchus were increased primarily for lower (i.e., ≤0.2 Hz) rather than for higher temporal frequencies. Thus, our results strongly suggest that there are marked differences in how sensory neural responses are processed downstream to give rise to behavior across both species. This is even though previous results have shown that the behavioral responses of both species to envelope stimuli were identical when serotonin is not applied.
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spelling pubmed-73589492020-07-29 Serotonergic Modulation of Sensory Neuron Activity and Behavior in Apteronotus albifrons Marquez, Mariana M. Chacron, Maurice J. Front Integr Neurosci Neuroscience Organisms must constantly adapt to changes in their environment to survive. It is thought that neuromodulators such as serotonin enable sensory neurons to better process input encountered during different behavioral contexts. Here, we investigated how serotonergic innervation affects neural and behavioral responses to behaviorally relevant envelope stimuli in the weakly electric fish species Apteronotus albifrons. Under baseline conditions, we found that exogenous serotonin application within the electrosensory lateral line lobe increased sensory neuron excitability, thereby promoting burst firing. We found that serotonin enhanced the responses to envelope stimuli of pyramidal cells within the lateral segment of the electrosensory lateral line lobe (ELL) by increasing sensitivity, with the increase more pronounced for stimuli with higher temporal frequencies (i.e., >0.2 Hz). Such increases in neural sensitivity were due to increased burst firing. At the organismal level, bilateral serotonin application within the ELL lateral segment enhanced behavioral responses to sensory input through increases in sensitivity. Similar to what was observed for neural responses, increases in behavioral sensitivity were more pronounced for higher (i.e., >0.2 Hz) temporal frequencies. Surprisingly, a comparison between our results and previous ones obtained in the closely related species A. leptorhynchus revealed that, while serotonin application gave rise to similar effects on neural excitability and responses to sensory input, serotonin application also gave rise to marked differences in behavior. Specifically, behavioral responses in A. leptorhynchus were increased primarily for lower (i.e., ≤0.2 Hz) rather than for higher temporal frequencies. Thus, our results strongly suggest that there are marked differences in how sensory neural responses are processed downstream to give rise to behavior across both species. This is even though previous results have shown that the behavioral responses of both species to envelope stimuli were identical when serotonin is not applied. Frontiers Media S.A. 2020-07-07 /pmc/articles/PMC7358949/ /pubmed/32733214 http://dx.doi.org/10.3389/fnint.2020.00038 Text en Copyright © 2020 Marquez and Chacron. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Neuroscience
Marquez, Mariana M.
Chacron, Maurice J.
Serotonergic Modulation of Sensory Neuron Activity and Behavior in Apteronotus albifrons
title Serotonergic Modulation of Sensory Neuron Activity and Behavior in Apteronotus albifrons
title_full Serotonergic Modulation of Sensory Neuron Activity and Behavior in Apteronotus albifrons
title_fullStr Serotonergic Modulation of Sensory Neuron Activity and Behavior in Apteronotus albifrons
title_full_unstemmed Serotonergic Modulation of Sensory Neuron Activity and Behavior in Apteronotus albifrons
title_short Serotonergic Modulation of Sensory Neuron Activity and Behavior in Apteronotus albifrons
title_sort serotonergic modulation of sensory neuron activity and behavior in apteronotus albifrons
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7358949/
https://www.ncbi.nlm.nih.gov/pubmed/32733214
http://dx.doi.org/10.3389/fnint.2020.00038
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