Linking emotional valence and anxiety in a mouse insula-amygdala circuit

Abstract Responses of the insular cortex (IC) and amygdala to stimuli of positive and negative valence are altered in patients with anxiety disorders. However, neural coding of both anxiety and valence by IC neurons remains unknown. Using fiber photometry recordings in mice, we uncover a selective i...

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Main Authors: C. Nicolas, A. Ju, Y. Wu, H. Eldirdiri, S. Delcasso, Y. Couderc, C. Fornari, A. Mitra, L. Supiot, A. Vérité, M. Masson, S. Rodriguez-Rozada, D. Jacky, J. S. Wiegert, A. Beyeler
Format: Article
Language:English
Published: Nature Portfolio 2023-08-01
Series:Nature Communications
Online Access:https://doi.org/10.1038/s41467-023-40517-1
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author C. Nicolas
A. Ju
Y. Wu
H. Eldirdiri
S. Delcasso
Y. Couderc
C. Fornari
A. Mitra
L. Supiot
A. Vérité
M. Masson
S. Rodriguez-Rozada
D. Jacky
J. S. Wiegert
A. Beyeler
author_facet C. Nicolas
A. Ju
Y. Wu
H. Eldirdiri
S. Delcasso
Y. Couderc
C. Fornari
A. Mitra
L. Supiot
A. Vérité
M. Masson
S. Rodriguez-Rozada
D. Jacky
J. S. Wiegert
A. Beyeler
author_sort C. Nicolas
collection DOAJ
description Abstract Responses of the insular cortex (IC) and amygdala to stimuli of positive and negative valence are altered in patients with anxiety disorders. However, neural coding of both anxiety and valence by IC neurons remains unknown. Using fiber photometry recordings in mice, we uncover a selective increase of activity in IC projection neurons of the anterior (aIC), but not posterior (pIC) section, when animals are exploring anxiogenic spaces, and this activity is proportional to the level of anxiety of mice. Neurons in aIC also respond to stimuli of positive and negative valence, and the strength of response to strong negative stimuli is proportional to mice levels of anxiety. Using ex vivo electrophysiology, we characterized the IC connection to the basolateral amygdala (BLA), and employed projection-specific optogenetics to reveal anxiogenic properties of aIC-BLA neurons. Finally, we identified that aIC-BLA neurons are activated in anxiogenic spaces, as well as in response to aversive stimuli, and that both activities are positively correlated. Altogether, we identified a common neurobiological substrate linking negative valence with anxiety-related information and behaviors, which provides a starting point to understand how alterations of these neural populations contribute to psychiatric disorders.
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spelling doaj.art-d343d225f76144358dca29be4c5d848a2023-11-20T10:07:03ZengNature PortfolioNature Communications2041-17232023-08-0114111810.1038/s41467-023-40517-1Linking emotional valence and anxiety in a mouse insula-amygdala circuitC. Nicolas0A. Ju1Y. Wu2H. Eldirdiri3S. Delcasso4Y. Couderc5C. Fornari6A. Mitra7L. Supiot8A. Vérité9M. Masson10S. Rodriguez-Rozada11D. Jacky12J. S. Wiegert13A. Beyeler14Neurocentre Magendie, INSERM 1215, Université de BordeauxNeurocentre Magendie, INSERM 1215, Université de BordeauxNeurocentre Magendie, INSERM 1215, Université de BordeauxNeurocentre Magendie, INSERM 1215, Université de BordeauxNeurocentre Magendie, INSERM 1215, Université de BordeauxNeurocentre Magendie, INSERM 1215, Université de BordeauxNeurocentre Magendie, INSERM 1215, Université de BordeauxNeurocentre Magendie, INSERM 1215, Université de BordeauxNeurocentre Magendie, INSERM 1215, Université de BordeauxNeurocentre Magendie, INSERM 1215, Université de BordeauxNeurocentre Magendie, INSERM 1215, Université de BordeauxResearch Group Synaptic Wiring and Information Processing, Center for Molecular Neurobiology Hamburg, University Medical Center Hamburg-EppendorfNeurocentre Magendie, INSERM 1215, Université de BordeauxResearch Group Synaptic Wiring and Information Processing, Center for Molecular Neurobiology Hamburg, University Medical Center Hamburg-EppendorfNeurocentre Magendie, INSERM 1215, Université de BordeauxAbstract Responses of the insular cortex (IC) and amygdala to stimuli of positive and negative valence are altered in patients with anxiety disorders. However, neural coding of both anxiety and valence by IC neurons remains unknown. Using fiber photometry recordings in mice, we uncover a selective increase of activity in IC projection neurons of the anterior (aIC), but not posterior (pIC) section, when animals are exploring anxiogenic spaces, and this activity is proportional to the level of anxiety of mice. Neurons in aIC also respond to stimuli of positive and negative valence, and the strength of response to strong negative stimuli is proportional to mice levels of anxiety. Using ex vivo electrophysiology, we characterized the IC connection to the basolateral amygdala (BLA), and employed projection-specific optogenetics to reveal anxiogenic properties of aIC-BLA neurons. Finally, we identified that aIC-BLA neurons are activated in anxiogenic spaces, as well as in response to aversive stimuli, and that both activities are positively correlated. Altogether, we identified a common neurobiological substrate linking negative valence with anxiety-related information and behaviors, which provides a starting point to understand how alterations of these neural populations contribute to psychiatric disorders.https://doi.org/10.1038/s41467-023-40517-1
spellingShingle C. Nicolas
A. Ju
Y. Wu
H. Eldirdiri
S. Delcasso
Y. Couderc
C. Fornari
A. Mitra
L. Supiot
A. Vérité
M. Masson
S. Rodriguez-Rozada
D. Jacky
J. S. Wiegert
A. Beyeler
Linking emotional valence and anxiety in a mouse insula-amygdala circuit
Nature Communications
title Linking emotional valence and anxiety in a mouse insula-amygdala circuit
title_full Linking emotional valence and anxiety in a mouse insula-amygdala circuit
title_fullStr Linking emotional valence and anxiety in a mouse insula-amygdala circuit
title_full_unstemmed Linking emotional valence and anxiety in a mouse insula-amygdala circuit
title_short Linking emotional valence and anxiety in a mouse insula-amygdala circuit
title_sort linking emotional valence and anxiety in a mouse insula amygdala circuit
url https://doi.org/10.1038/s41467-023-40517-1
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