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Aversive stimuli drive hypothalamus-to-habenula excitation to promote escape behavior

A sudden aversive event produces escape behaviors, an innate response essential for survival in virtually all-animal species. Nuclei including the lateral habenula (LHb), the lateral hypothalamus (LH), and the midbrain are not only reciprocally connected, but also respond to negative events contribu...

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Autores principales: Lecca, Salvatore, Meye, Frank Julius, Trusel, Massimo, Tchenio, Anna, Harris, Julia, Schwarz, Martin Karl, Burdakov, Denis, Georges, Francois, Mameli, Manuel
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5606847/
https://www.ncbi.nlm.nih.gov/pubmed/28871962
http://dx.doi.org/10.7554/eLife.30697
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author Lecca, Salvatore
Meye, Frank Julius
Trusel, Massimo
Tchenio, Anna
Harris, Julia
Schwarz, Martin Karl
Burdakov, Denis
Georges, Francois
Mameli, Manuel
author_facet Lecca, Salvatore
Meye, Frank Julius
Trusel, Massimo
Tchenio, Anna
Harris, Julia
Schwarz, Martin Karl
Burdakov, Denis
Georges, Francois
Mameli, Manuel
author_sort Lecca, Salvatore
collection PubMed
description A sudden aversive event produces escape behaviors, an innate response essential for survival in virtually all-animal species. Nuclei including the lateral habenula (LHb), the lateral hypothalamus (LH), and the midbrain are not only reciprocally connected, but also respond to negative events contributing to goal-directed behaviors. However, whether aversion encoding requires these neural circuits to ultimately prompt escape behaviors remains unclear. We observe that aversive stimuli, including foot-shocks, excite LHb neurons and promote escape behaviors in mice. The foot-shock-driven excitation within the LHb requires glutamatergic signaling from the LH, but not from the midbrain. This hypothalamic excitatory projection predominates over LHb neurons monosynaptically innervating aversion-encoding midbrain GABA cells. Finally, the selective chemogenetic silencing of the LH-to-LHb pathway impairs aversion-driven escape behaviors. These findings unveil a habenular neurocircuitry devoted to encode external threats and the consequent escape; a process that, if disrupted, may compromise the animal’s survival.
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spelling pubmed-56068472017-09-25 Aversive stimuli drive hypothalamus-to-habenula excitation to promote escape behavior Lecca, Salvatore Meye, Frank Julius Trusel, Massimo Tchenio, Anna Harris, Julia Schwarz, Martin Karl Burdakov, Denis Georges, Francois Mameli, Manuel eLife Neuroscience A sudden aversive event produces escape behaviors, an innate response essential for survival in virtually all-animal species. Nuclei including the lateral habenula (LHb), the lateral hypothalamus (LH), and the midbrain are not only reciprocally connected, but also respond to negative events contributing to goal-directed behaviors. However, whether aversion encoding requires these neural circuits to ultimately prompt escape behaviors remains unclear. We observe that aversive stimuli, including foot-shocks, excite LHb neurons and promote escape behaviors in mice. The foot-shock-driven excitation within the LHb requires glutamatergic signaling from the LH, but not from the midbrain. This hypothalamic excitatory projection predominates over LHb neurons monosynaptically innervating aversion-encoding midbrain GABA cells. Finally, the selective chemogenetic silencing of the LH-to-LHb pathway impairs aversion-driven escape behaviors. These findings unveil a habenular neurocircuitry devoted to encode external threats and the consequent escape; a process that, if disrupted, may compromise the animal’s survival. eLife Sciences Publications, Ltd 2017-09-05 /pmc/articles/PMC5606847/ /pubmed/28871962 http://dx.doi.org/10.7554/eLife.30697 Text en © 2017, Lecca et al http://creativecommons.org/licenses/by/4.0/ http://creativecommons.org/licenses/by/4.0/This article is distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Neuroscience
Lecca, Salvatore
Meye, Frank Julius
Trusel, Massimo
Tchenio, Anna
Harris, Julia
Schwarz, Martin Karl
Burdakov, Denis
Georges, Francois
Mameli, Manuel
Aversive stimuli drive hypothalamus-to-habenula excitation to promote escape behavior
title Aversive stimuli drive hypothalamus-to-habenula excitation to promote escape behavior
title_full Aversive stimuli drive hypothalamus-to-habenula excitation to promote escape behavior
title_fullStr Aversive stimuli drive hypothalamus-to-habenula excitation to promote escape behavior
title_full_unstemmed Aversive stimuli drive hypothalamus-to-habenula excitation to promote escape behavior
title_short Aversive stimuli drive hypothalamus-to-habenula excitation to promote escape behavior
title_sort aversive stimuli drive hypothalamus-to-habenula excitation to promote escape behavior
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5606847/
https://www.ncbi.nlm.nih.gov/pubmed/28871962
http://dx.doi.org/10.7554/eLife.30697
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