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A synaptic threshold mechanism for computing escape decisions

Escaping from imminent danger is an instinctive behaviour fundamental for survival that requires classifying sensory stimuli as harmless or threatening. The absence of threat allows animals to forage for essential resources, but as the level of threat and potential for harm increases, they have to d...

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Autores principales: Evans, D.A, Stempel, A.V., Vale, R., Ruehle, S., Lefler, Y., Branco, T.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6235113/
https://www.ncbi.nlm.nih.gov/pubmed/29925954
http://dx.doi.org/10.1038/s41586-018-0244-6
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author Evans, D.A
Stempel, A.V.
Vale, R.
Ruehle, S.
Lefler, Y.
Branco, T.
author_facet Evans, D.A
Stempel, A.V.
Vale, R.
Ruehle, S.
Lefler, Y.
Branco, T.
author_sort Evans, D.A
collection PubMed
description Escaping from imminent danger is an instinctive behaviour fundamental for survival that requires classifying sensory stimuli as harmless or threatening. The absence of threat allows animals to forage for essential resources, but as the level of threat and potential for harm increases, they have to decide whether or not to seek safety1. Despite previous work on instinctive defensive behaviours in rodents2–11, little is known about how the brain computes the threat level for initiating escape. Here we show that the probability and vigour of escape in mice scale with the saliency of innate threats, and are well described by a model that computes the distance between threat level and an escape threshold. Calcium imaging and optogenetics in the midbrain of freely behaving mice show that the activity of excitatory neurons in the deep layers of the medial superior colliculus (mSC) represents the threat stimulus saliency and is predictive of escape, whereas dorsal periaqueductal gray (dPAG) glutamatergic neurons encode exclusively the escape choice and control escape vigour. We demonstrate a feed-forward monosynaptic excitatory connection from mSC to dPAG neurons that is weak and unreliable – yet necessary for escape behaviour – which provides a synaptic threshold for dPAG activation and the initiation of escape. This threshold can be overcome by high mSC network activity because of short-term synaptic facilitation and recurrent excitation within the mSC, which amplifies and sustains synaptic drive to the dPAG. Thus, dPAG glutamatergic neurons compute escape decisions and vigour using a synaptic mechanism to threshold threat information received from the mSC, and provide a biophysical model of how the brain performs a critical behavioural computation.
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spelling pubmed-62351132018-12-20 A synaptic threshold mechanism for computing escape decisions Evans, D.A Stempel, A.V. Vale, R. Ruehle, S. Lefler, Y. Branco, T. Nature Article Escaping from imminent danger is an instinctive behaviour fundamental for survival that requires classifying sensory stimuli as harmless or threatening. The absence of threat allows animals to forage for essential resources, but as the level of threat and potential for harm increases, they have to decide whether or not to seek safety1. Despite previous work on instinctive defensive behaviours in rodents2–11, little is known about how the brain computes the threat level for initiating escape. Here we show that the probability and vigour of escape in mice scale with the saliency of innate threats, and are well described by a model that computes the distance between threat level and an escape threshold. Calcium imaging and optogenetics in the midbrain of freely behaving mice show that the activity of excitatory neurons in the deep layers of the medial superior colliculus (mSC) represents the threat stimulus saliency and is predictive of escape, whereas dorsal periaqueductal gray (dPAG) glutamatergic neurons encode exclusively the escape choice and control escape vigour. We demonstrate a feed-forward monosynaptic excitatory connection from mSC to dPAG neurons that is weak and unreliable – yet necessary for escape behaviour – which provides a synaptic threshold for dPAG activation and the initiation of escape. This threshold can be overcome by high mSC network activity because of short-term synaptic facilitation and recurrent excitation within the mSC, which amplifies and sustains synaptic drive to the dPAG. Thus, dPAG glutamatergic neurons compute escape decisions and vigour using a synaptic mechanism to threshold threat information received from the mSC, and provide a biophysical model of how the brain performs a critical behavioural computation. 2018-06-20 2018-06 /pmc/articles/PMC6235113/ /pubmed/29925954 http://dx.doi.org/10.1038/s41586-018-0244-6 Text en Users may view, print, copy, and download text and data-mine the content in such documents, for the purposes of academic research, subject always to the full Conditions of use:http://www.nature.com/authors/editorial_policies/license.html#terms
spellingShingle Article
Evans, D.A
Stempel, A.V.
Vale, R.
Ruehle, S.
Lefler, Y.
Branco, T.
A synaptic threshold mechanism for computing escape decisions
title A synaptic threshold mechanism for computing escape decisions
title_full A synaptic threshold mechanism for computing escape decisions
title_fullStr A synaptic threshold mechanism for computing escape decisions
title_full_unstemmed A synaptic threshold mechanism for computing escape decisions
title_short A synaptic threshold mechanism for computing escape decisions
title_sort synaptic threshold mechanism for computing escape decisions
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6235113/
https://www.ncbi.nlm.nih.gov/pubmed/29925954
http://dx.doi.org/10.1038/s41586-018-0244-6
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