Cargando…

Specific configurations of electrical synapses filter sensory information to drive choices in behavior

Synaptic configurations in precisely wired circuits underpin how sensory information is processed by the nervous system, and the emerging animal behavior. This is best understood for chemical synapses, but far less is known about how electrical synaptic configurations modulate, in vivo and in specif...

Descripción completa

Detalles Bibliográficos
Autores principales: Almoril-Porras, Agustin, Calvo, Ana C., Niu, Longgang, Beagan, Jonathan, Hawk, Josh D., Aljobeh, Ahmad, Wisdom, Elias M., Ren, Ivy, Díaz-García, Malcom, Wang, Zhao-Wen, Colón-Ramos, Daniel A.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Cold Spring Harbor Laboratory 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10418224/
https://www.ncbi.nlm.nih.gov/pubmed/37577611
http://dx.doi.org/10.1101/2023.08.01.551556
_version_ 1785088218447740928
author Almoril-Porras, Agustin
Calvo, Ana C.
Niu, Longgang
Beagan, Jonathan
Hawk, Josh D.
Aljobeh, Ahmad
Wisdom, Elias M.
Ren, Ivy
Díaz-García, Malcom
Wang, Zhao-Wen
Colón-Ramos, Daniel A.
author_facet Almoril-Porras, Agustin
Calvo, Ana C.
Niu, Longgang
Beagan, Jonathan
Hawk, Josh D.
Aljobeh, Ahmad
Wisdom, Elias M.
Ren, Ivy
Díaz-García, Malcom
Wang, Zhao-Wen
Colón-Ramos, Daniel A.
author_sort Almoril-Porras, Agustin
collection PubMed
description Synaptic configurations in precisely wired circuits underpin how sensory information is processed by the nervous system, and the emerging animal behavior. This is best understood for chemical synapses, but far less is known about how electrical synaptic configurations modulate, in vivo and in specific neurons, sensory information processing and context-specific behaviors. We discovered that INX-1, a gap junction protein that forms electrical synapses, is required to deploy context-specific behavioral strategies during C. elegans thermotaxis behavior. INX-1 couples two bilaterally symmetric interneurons, and this configuration is required for the integration of sensory information during migration of animals across temperature gradients. In inx-1 mutants, uncoupled interneurons display increased excitability and responses to subthreshold temperature stimuli, resulting in abnormally longer run durations and context-irrelevant tracking of isotherms. Our study uncovers a conserved configuration of electrical synapses that, by increasing neuronal capacitance, enables differential processing of sensory information and the deployment of context-specific behavioral strategies.
format Online
Article
Text
id pubmed-10418224
institution National Center for Biotechnology Information
language English
publishDate 2023
publisher Cold Spring Harbor Laboratory
record_format MEDLINE/PubMed
spelling pubmed-104182242023-08-12 Specific configurations of electrical synapses filter sensory information to drive choices in behavior Almoril-Porras, Agustin Calvo, Ana C. Niu, Longgang Beagan, Jonathan Hawk, Josh D. Aljobeh, Ahmad Wisdom, Elias M. Ren, Ivy Díaz-García, Malcom Wang, Zhao-Wen Colón-Ramos, Daniel A. bioRxiv Article Synaptic configurations in precisely wired circuits underpin how sensory information is processed by the nervous system, and the emerging animal behavior. This is best understood for chemical synapses, but far less is known about how electrical synaptic configurations modulate, in vivo and in specific neurons, sensory information processing and context-specific behaviors. We discovered that INX-1, a gap junction protein that forms electrical synapses, is required to deploy context-specific behavioral strategies during C. elegans thermotaxis behavior. INX-1 couples two bilaterally symmetric interneurons, and this configuration is required for the integration of sensory information during migration of animals across temperature gradients. In inx-1 mutants, uncoupled interneurons display increased excitability and responses to subthreshold temperature stimuli, resulting in abnormally longer run durations and context-irrelevant tracking of isotherms. Our study uncovers a conserved configuration of electrical synapses that, by increasing neuronal capacitance, enables differential processing of sensory information and the deployment of context-specific behavioral strategies. Cold Spring Harbor Laboratory 2023-08-03 /pmc/articles/PMC10418224/ /pubmed/37577611 http://dx.doi.org/10.1101/2023.08.01.551556 Text en https://creativecommons.org/licenses/by-nc/4.0/This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License (https://creativecommons.org/licenses/by-nc/4.0/) , which allows reusers to distribute, remix, adapt, and build upon the material in any medium or format for noncommercial purposes only, and only so long as attribution is given to the creator.
spellingShingle Article
Almoril-Porras, Agustin
Calvo, Ana C.
Niu, Longgang
Beagan, Jonathan
Hawk, Josh D.
Aljobeh, Ahmad
Wisdom, Elias M.
Ren, Ivy
Díaz-García, Malcom
Wang, Zhao-Wen
Colón-Ramos, Daniel A.
Specific configurations of electrical synapses filter sensory information to drive choices in behavior
title Specific configurations of electrical synapses filter sensory information to drive choices in behavior
title_full Specific configurations of electrical synapses filter sensory information to drive choices in behavior
title_fullStr Specific configurations of electrical synapses filter sensory information to drive choices in behavior
title_full_unstemmed Specific configurations of electrical synapses filter sensory information to drive choices in behavior
title_short Specific configurations of electrical synapses filter sensory information to drive choices in behavior
title_sort specific configurations of electrical synapses filter sensory information to drive choices in behavior
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10418224/
https://www.ncbi.nlm.nih.gov/pubmed/37577611
http://dx.doi.org/10.1101/2023.08.01.551556
work_keys_str_mv AT almorilporrasagustin specificconfigurationsofelectricalsynapsesfiltersensoryinformationtodrivechoicesinbehavior
AT calvoanac specificconfigurationsofelectricalsynapsesfiltersensoryinformationtodrivechoicesinbehavior
AT niulonggang specificconfigurationsofelectricalsynapsesfiltersensoryinformationtodrivechoicesinbehavior
AT beaganjonathan specificconfigurationsofelectricalsynapsesfiltersensoryinformationtodrivechoicesinbehavior
AT hawkjoshd specificconfigurationsofelectricalsynapsesfiltersensoryinformationtodrivechoicesinbehavior
AT aljobehahmad specificconfigurationsofelectricalsynapsesfiltersensoryinformationtodrivechoicesinbehavior
AT wisdomeliasm specificconfigurationsofelectricalsynapsesfiltersensoryinformationtodrivechoicesinbehavior
AT renivy specificconfigurationsofelectricalsynapsesfiltersensoryinformationtodrivechoicesinbehavior
AT diazgarciamalcom specificconfigurationsofelectricalsynapsesfiltersensoryinformationtodrivechoicesinbehavior
AT wangzhaowen specificconfigurationsofelectricalsynapsesfiltersensoryinformationtodrivechoicesinbehavior
AT colonramosdaniela specificconfigurationsofelectricalsynapsesfiltersensoryinformationtodrivechoicesinbehavior