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Sensory-thresholded switch of neural firing states in a computational model of the ventromedial hypothalamus

The mouse ventromedial hypothalamus (VMH) is both necessary and sufficient for defensive responses to predator and social threats. Defensive behaviors typically involve cautious approach toward potentially threatening stimuli aimed at obtaining information about the risk involved, followed by sudden...

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Autores principales: Rahy, Ryan, Asari, Hiroki, Gross, Cornelius T.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9491323/
https://www.ncbi.nlm.nih.gov/pubmed/36157840
http://dx.doi.org/10.3389/fncom.2022.964634
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author Rahy, Ryan
Asari, Hiroki
Gross, Cornelius T.
author_facet Rahy, Ryan
Asari, Hiroki
Gross, Cornelius T.
author_sort Rahy, Ryan
collection PubMed
description The mouse ventromedial hypothalamus (VMH) is both necessary and sufficient for defensive responses to predator and social threats. Defensive behaviors typically involve cautious approach toward potentially threatening stimuli aimed at obtaining information about the risk involved, followed by sudden avoidance and flight behavior to escape harm. In vivo neural recording studies in mice have identified two major populations of VMH neurons that either increase their firing activity as the animal approaches the threat (called Assessment+ cells) or increase their activity as the animal flees the threat (called Flight+ cells). Interestingly, Assessment+ and Flight+ cells abruptly decrease and increase their firing activity, respectively, at the decision point for flight, creating an escape-related “switch” in functional state. This suggests that the activity of the two cell types in VMH is coordinated and could result from local circuit interactions. Here, we used computational modeling to test if a local inhibitory feedback circuit could give rise to key features of the neural activity seen in VMH during the approach-to-flight transition. Starting from a simple dual-population inhibitory feedback circuit receiving repeated trains of monotonically increasing sensory input to mimic approach to threat, we tested the requirement for balanced sensory input, balanced feedback, short-term synaptic plasticity, rebound excitation, and inhibitory feedback exclusivity to reproduce an abrupt, sensory-thresholded reciprocal firing change that resembles Assessment+ and Flight+ cell activity seen in vivo. Our work demonstrates that a relatively simple local circuit architecture is sufficient for the emergence of firing patterns similar to those seen in vivo and suggests that a reiterative process of experimental and computational work may be a fruitful avenue for better understanding the functional organization of mammalian instinctive behaviors at the circuit level.
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spelling pubmed-94913232022-09-22 Sensory-thresholded switch of neural firing states in a computational model of the ventromedial hypothalamus Rahy, Ryan Asari, Hiroki Gross, Cornelius T. Front Comput Neurosci Neuroscience The mouse ventromedial hypothalamus (VMH) is both necessary and sufficient for defensive responses to predator and social threats. Defensive behaviors typically involve cautious approach toward potentially threatening stimuli aimed at obtaining information about the risk involved, followed by sudden avoidance and flight behavior to escape harm. In vivo neural recording studies in mice have identified two major populations of VMH neurons that either increase their firing activity as the animal approaches the threat (called Assessment+ cells) or increase their activity as the animal flees the threat (called Flight+ cells). Interestingly, Assessment+ and Flight+ cells abruptly decrease and increase their firing activity, respectively, at the decision point for flight, creating an escape-related “switch” in functional state. This suggests that the activity of the two cell types in VMH is coordinated and could result from local circuit interactions. Here, we used computational modeling to test if a local inhibitory feedback circuit could give rise to key features of the neural activity seen in VMH during the approach-to-flight transition. Starting from a simple dual-population inhibitory feedback circuit receiving repeated trains of monotonically increasing sensory input to mimic approach to threat, we tested the requirement for balanced sensory input, balanced feedback, short-term synaptic plasticity, rebound excitation, and inhibitory feedback exclusivity to reproduce an abrupt, sensory-thresholded reciprocal firing change that resembles Assessment+ and Flight+ cell activity seen in vivo. Our work demonstrates that a relatively simple local circuit architecture is sufficient for the emergence of firing patterns similar to those seen in vivo and suggests that a reiterative process of experimental and computational work may be a fruitful avenue for better understanding the functional organization of mammalian instinctive behaviors at the circuit level. Frontiers Media S.A. 2022-09-07 /pmc/articles/PMC9491323/ /pubmed/36157840 http://dx.doi.org/10.3389/fncom.2022.964634 Text en Copyright © 2022 Rahy, Asari and Gross. https://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
Rahy, Ryan
Asari, Hiroki
Gross, Cornelius T.
Sensory-thresholded switch of neural firing states in a computational model of the ventromedial hypothalamus
title Sensory-thresholded switch of neural firing states in a computational model of the ventromedial hypothalamus
title_full Sensory-thresholded switch of neural firing states in a computational model of the ventromedial hypothalamus
title_fullStr Sensory-thresholded switch of neural firing states in a computational model of the ventromedial hypothalamus
title_full_unstemmed Sensory-thresholded switch of neural firing states in a computational model of the ventromedial hypothalamus
title_short Sensory-thresholded switch of neural firing states in a computational model of the ventromedial hypothalamus
title_sort sensory-thresholded switch of neural firing states in a computational model of the ventromedial hypothalamus
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9491323/
https://www.ncbi.nlm.nih.gov/pubmed/36157840
http://dx.doi.org/10.3389/fncom.2022.964634
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