Cargando…

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...

Descripción completa

Detalles Bibliográficos
Autores principales: Clements, Katie N., Ahn, Sungwoo, Park, Choongseok, Heagy, Faith K., Miller, Thomas H., Kassai, Miki, Issa, Fadi A.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Society for Neuroscience 2023
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
_version_ 1785151221323005952
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
work_keys_str_mv AT clementskatien sociallymediatedshiftinneuralcircuitsactivationregulatedbysynergisticneuromodulatorysignaling
AT ahnsungwoo sociallymediatedshiftinneuralcircuitsactivationregulatedbysynergisticneuromodulatorysignaling
AT parkchoongseok sociallymediatedshiftinneuralcircuitsactivationregulatedbysynergisticneuromodulatorysignaling
AT heagyfaithk sociallymediatedshiftinneuralcircuitsactivationregulatedbysynergisticneuromodulatorysignaling
AT millerthomash sociallymediatedshiftinneuralcircuitsactivationregulatedbysynergisticneuromodulatorysignaling
AT kassaimiki sociallymediatedshiftinneuralcircuitsactivationregulatedbysynergisticneuromodulatorysignaling
AT issafadia sociallymediatedshiftinneuralcircuitsactivationregulatedbysynergisticneuromodulatorysignaling