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Socially Mediated Shift in Neural Circuits Activation Regulated by Synergistic Neuromodulatory Signaling
Animals exhibit context-dependent behavioral decisions that are mediated by specific motor circuits. In social species these decisions are often influenced by social status. Although social status-dependent neural plasticity of motor circuits has been investigated in vertebrates, little is known of...
Autores principales: | , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Society for Neuroscience
2023
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10683552/ https://www.ncbi.nlm.nih.gov/pubmed/37914408 http://dx.doi.org/10.1523/ENEURO.0311-23.2023 |
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author | Clements, Katie N. Ahn, Sungwoo Park, Choongseok Heagy, Faith K. Miller, Thomas H. Kassai, Miki Issa, Fadi A. |
author_facet | Clements, Katie N. Ahn, Sungwoo Park, Choongseok Heagy, Faith K. Miller, Thomas H. Kassai, Miki Issa, Fadi A. |
author_sort | Clements, Katie N. |
collection | PubMed |
description | Animals exhibit context-dependent behavioral decisions that are mediated by specific motor circuits. In social species these decisions are often influenced by social status. Although social status-dependent neural plasticity of motor circuits has been investigated in vertebrates, little is known of how cellular plasticity translates into differences in motor activity. Here, we used zebrafish (Danio rerio) as a model organism to examine how social dominance influences the activation of swimming and the Mauthner-mediated startle escape behaviors. We show that the status-dependent shift in behavior patterns whereby dominants increase swimming and reduce sensitivity of startle escape while subordinates reduce their swimming and increase startle sensitivity is regulated by the synergistic interactions of dopaminergic, glycinergic, and GABAergic inputs to shift the balance of activation of the underlying motor circuits. This shift is driven by socially induced differences in expression of dopaminergic receptor type 1b (Drd1b) on glycinergic neurons and dopamine (DA) reuptake transporter (DAT). Second, we show that GABAergic input onto glycinergic neurons is strengthened in subordinates compared with dominants. Complementary neurocomputational modeling of the empirical results show that drd1b functions as molecular regulator to facilitate the shift between excitatory and inhibitory pathways. The results illustrate how reconfiguration in network dynamics serves as an adaptive strategy to cope with changes in social environment and are likely conserved and applicable to other social species. |
format | Online Article Text |
id | pubmed-10683552 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2023 |
publisher | Society for Neuroscience |
record_format | MEDLINE/PubMed |
spelling | pubmed-106835522023-11-30 Socially Mediated Shift in Neural Circuits Activation Regulated by Synergistic Neuromodulatory Signaling Clements, Katie N. Ahn, Sungwoo Park, Choongseok Heagy, Faith K. Miller, Thomas H. Kassai, Miki Issa, Fadi A. eNeuro Research Article: New Research Animals exhibit context-dependent behavioral decisions that are mediated by specific motor circuits. In social species these decisions are often influenced by social status. Although social status-dependent neural plasticity of motor circuits has been investigated in vertebrates, little is known of how cellular plasticity translates into differences in motor activity. Here, we used zebrafish (Danio rerio) as a model organism to examine how social dominance influences the activation of swimming and the Mauthner-mediated startle escape behaviors. We show that the status-dependent shift in behavior patterns whereby dominants increase swimming and reduce sensitivity of startle escape while subordinates reduce their swimming and increase startle sensitivity is regulated by the synergistic interactions of dopaminergic, glycinergic, and GABAergic inputs to shift the balance of activation of the underlying motor circuits. This shift is driven by socially induced differences in expression of dopaminergic receptor type 1b (Drd1b) on glycinergic neurons and dopamine (DA) reuptake transporter (DAT). Second, we show that GABAergic input onto glycinergic neurons is strengthened in subordinates compared with dominants. Complementary neurocomputational modeling of the empirical results show that drd1b functions as molecular regulator to facilitate the shift between excitatory and inhibitory pathways. The results illustrate how reconfiguration in network dynamics serves as an adaptive strategy to cope with changes in social environment and are likely conserved and applicable to other social species. Society for Neuroscience 2023-11-27 /pmc/articles/PMC10683552/ /pubmed/37914408 http://dx.doi.org/10.1523/ENEURO.0311-23.2023 Text en Copyright © 2023 Clements et al. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed. |
spellingShingle | Research Article: New Research Clements, Katie N. Ahn, Sungwoo Park, Choongseok Heagy, Faith K. Miller, Thomas H. Kassai, Miki Issa, Fadi A. Socially Mediated Shift in Neural Circuits Activation Regulated by Synergistic Neuromodulatory Signaling |
title | Socially Mediated Shift in Neural Circuits Activation Regulated by Synergistic Neuromodulatory Signaling |
title_full | Socially Mediated Shift in Neural Circuits Activation Regulated by Synergistic Neuromodulatory Signaling |
title_fullStr | Socially Mediated Shift in Neural Circuits Activation Regulated by Synergistic Neuromodulatory Signaling |
title_full_unstemmed | Socially Mediated Shift in Neural Circuits Activation Regulated by Synergistic Neuromodulatory Signaling |
title_short | Socially Mediated Shift in Neural Circuits Activation Regulated by Synergistic Neuromodulatory Signaling |
title_sort | socially mediated shift in neural circuits activation regulated by synergistic neuromodulatory signaling |
topic | Research Article: New Research |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10683552/ https://www.ncbi.nlm.nih.gov/pubmed/37914408 http://dx.doi.org/10.1523/ENEURO.0311-23.2023 |
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