Cargando…

Brain-wide perception of the emotional valence of light is regulated by distinct hypothalamic neurons

Salient sensory stimuli are perceived by the brain, which guides both the timing and outcome of behaviors in a context-dependent manner. Light is such a stimulus, which is used in treating mood disorders often associated with a dysregulated hypothalamic-pituitary-adrenal stress axis. Relationships b...

Descripción completa

Detalles Bibliográficos
Autores principales: Wagle, Mahendra, Zarei, Mahdi, Lovett-Barron, Matthew, Poston, Kristina Tyler, Xu, Jin, Ramey, Vince, Pollard, Katherine S., Prober, David A., Schulkin, Jay, Deisseroth, Karl, Guo, Su
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9613822/
https://www.ncbi.nlm.nih.gov/pubmed/35484242
http://dx.doi.org/10.1038/s41380-022-01567-x
_version_ 1784820056720408576
author Wagle, Mahendra
Zarei, Mahdi
Lovett-Barron, Matthew
Poston, Kristina Tyler
Xu, Jin
Ramey, Vince
Pollard, Katherine S.
Prober, David A.
Schulkin, Jay
Deisseroth, Karl
Guo, Su
author_facet Wagle, Mahendra
Zarei, Mahdi
Lovett-Barron, Matthew
Poston, Kristina Tyler
Xu, Jin
Ramey, Vince
Pollard, Katherine S.
Prober, David A.
Schulkin, Jay
Deisseroth, Karl
Guo, Su
author_sort Wagle, Mahendra
collection PubMed
description Salient sensory stimuli are perceived by the brain, which guides both the timing and outcome of behaviors in a context-dependent manner. Light is such a stimulus, which is used in treating mood disorders often associated with a dysregulated hypothalamic-pituitary-adrenal stress axis. Relationships between the emotional valence of light and the hypothalamus, and how they interact to exert brain-wide impacts remain unclear. Employing larval zebrafish with analogous hypothalamic systems to mammals, we show in free-swimming animals that hypothalamic corticotropin releasing factor (CRF(Hy)) neurons promote dark avoidance, and such role is not shared by other hypothalamic peptidergic neurons. Single-neuron projection analyses uncover processes extended by individual CRF(Hy) neurons to multiple targets including sensorimotor and decision-making areas. In vivo calcium imaging uncovers a complex and heterogeneous response of individual CRF(Hy) neurons to the light or dark stimulus, with a reduced overall sum of CRF neuronal activity in the presence of light. Brain-wide calcium imaging under alternating light/dark stimuli further identifies distinct and distributed photic response neuronal types. CRF(Hy) neuronal ablation increases an overall representation of light in the brain and broadly enhances the functional connectivity associated with an exploratory brain state. These findings delineate brain-wide photic perception, uncover a previously unknown role of CRF(Hy) neurons in regulating the perception and emotional valence of light, and suggest that light therapy may alleviate mood disorders through reducing an overall sum of CRF neuronal activity.
format Online
Article
Text
id pubmed-9613822
institution National Center for Biotechnology Information
language English
publishDate 2022
publisher Nature Publishing Group UK
record_format MEDLINE/PubMed
spelling pubmed-96138222022-12-01 Brain-wide perception of the emotional valence of light is regulated by distinct hypothalamic neurons Wagle, Mahendra Zarei, Mahdi Lovett-Barron, Matthew Poston, Kristina Tyler Xu, Jin Ramey, Vince Pollard, Katherine S. Prober, David A. Schulkin, Jay Deisseroth, Karl Guo, Su Mol Psychiatry Article Salient sensory stimuli are perceived by the brain, which guides both the timing and outcome of behaviors in a context-dependent manner. Light is such a stimulus, which is used in treating mood disorders often associated with a dysregulated hypothalamic-pituitary-adrenal stress axis. Relationships between the emotional valence of light and the hypothalamus, and how they interact to exert brain-wide impacts remain unclear. Employing larval zebrafish with analogous hypothalamic systems to mammals, we show in free-swimming animals that hypothalamic corticotropin releasing factor (CRF(Hy)) neurons promote dark avoidance, and such role is not shared by other hypothalamic peptidergic neurons. Single-neuron projection analyses uncover processes extended by individual CRF(Hy) neurons to multiple targets including sensorimotor and decision-making areas. In vivo calcium imaging uncovers a complex and heterogeneous response of individual CRF(Hy) neurons to the light or dark stimulus, with a reduced overall sum of CRF neuronal activity in the presence of light. Brain-wide calcium imaging under alternating light/dark stimuli further identifies distinct and distributed photic response neuronal types. CRF(Hy) neuronal ablation increases an overall representation of light in the brain and broadly enhances the functional connectivity associated with an exploratory brain state. These findings delineate brain-wide photic perception, uncover a previously unknown role of CRF(Hy) neurons in regulating the perception and emotional valence of light, and suggest that light therapy may alleviate mood disorders through reducing an overall sum of CRF neuronal activity. Nature Publishing Group UK 2022-04-28 2022 /pmc/articles/PMC9613822/ /pubmed/35484242 http://dx.doi.org/10.1038/s41380-022-01567-x Text en © The Author(s) 2022, corrected publication 2022 https://creativecommons.org/licenses/by/4.0/This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. (https://creativecommons.org/licenses/by/4.0/)
spellingShingle Article
Wagle, Mahendra
Zarei, Mahdi
Lovett-Barron, Matthew
Poston, Kristina Tyler
Xu, Jin
Ramey, Vince
Pollard, Katherine S.
Prober, David A.
Schulkin, Jay
Deisseroth, Karl
Guo, Su
Brain-wide perception of the emotional valence of light is regulated by distinct hypothalamic neurons
title Brain-wide perception of the emotional valence of light is regulated by distinct hypothalamic neurons
title_full Brain-wide perception of the emotional valence of light is regulated by distinct hypothalamic neurons
title_fullStr Brain-wide perception of the emotional valence of light is regulated by distinct hypothalamic neurons
title_full_unstemmed Brain-wide perception of the emotional valence of light is regulated by distinct hypothalamic neurons
title_short Brain-wide perception of the emotional valence of light is regulated by distinct hypothalamic neurons
title_sort brain-wide perception of the emotional valence of light is regulated by distinct hypothalamic neurons
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9613822/
https://www.ncbi.nlm.nih.gov/pubmed/35484242
http://dx.doi.org/10.1038/s41380-022-01567-x
work_keys_str_mv AT waglemahendra brainwideperceptionoftheemotionalvalenceoflightisregulatedbydistincthypothalamicneurons
AT zareimahdi brainwideperceptionoftheemotionalvalenceoflightisregulatedbydistincthypothalamicneurons
AT lovettbarronmatthew brainwideperceptionoftheemotionalvalenceoflightisregulatedbydistincthypothalamicneurons
AT postonkristinatyler brainwideperceptionoftheemotionalvalenceoflightisregulatedbydistincthypothalamicneurons
AT xujin brainwideperceptionoftheemotionalvalenceoflightisregulatedbydistincthypothalamicneurons
AT rameyvince brainwideperceptionoftheemotionalvalenceoflightisregulatedbydistincthypothalamicneurons
AT pollardkatherines brainwideperceptionoftheemotionalvalenceoflightisregulatedbydistincthypothalamicneurons
AT proberdavida brainwideperceptionoftheemotionalvalenceoflightisregulatedbydistincthypothalamicneurons
AT schulkinjay brainwideperceptionoftheemotionalvalenceoflightisregulatedbydistincthypothalamicneurons
AT deisserothkarl brainwideperceptionoftheemotionalvalenceoflightisregulatedbydistincthypothalamicneurons
AT guosu brainwideperceptionoftheemotionalvalenceoflightisregulatedbydistincthypothalamicneurons