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A dual-pathway architecture enables chronic stress to promote habit formation

Chronic stress can change how we learn and, thus, how we make decisions by promoting the formation of inflexible, potentially maladaptive, habits. Here we investigated the neuronal circuit mechanisms that enable this. Using a multifaceted approach in male and female mice, we reveal a dual pathway, a...

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Autores principales: Giovanniello, Jacqueline R., Paredes, Natalie, Wiener, Anna, Ramírez-Armenta, Kathia, Oragwam, Chukwuebuka, Uwadia, Hanniel O., Lim, Kayla, Nnamdi, Gift, Wang, Alicia, Sehgal, Megha, Reis, Fernando MCV, Sias, Ana C., Silva, Alcino J., Adhikari, Avishek, Malvaez, Melissa, Wassum, Kate M.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Cold Spring Harbor Laboratory 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10592885/
https://www.ncbi.nlm.nih.gov/pubmed/37873076
http://dx.doi.org/10.1101/2023.10.03.560731
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author Giovanniello, Jacqueline R.
Paredes, Natalie
Wiener, Anna
Ramírez-Armenta, Kathia
Oragwam, Chukwuebuka
Uwadia, Hanniel O.
Lim, Kayla
Nnamdi, Gift
Wang, Alicia
Sehgal, Megha
Reis, Fernando MCV
Sias, Ana C.
Silva, Alcino J.
Adhikari, Avishek
Malvaez, Melissa
Wassum, Kate M.
author_facet Giovanniello, Jacqueline R.
Paredes, Natalie
Wiener, Anna
Ramírez-Armenta, Kathia
Oragwam, Chukwuebuka
Uwadia, Hanniel O.
Lim, Kayla
Nnamdi, Gift
Wang, Alicia
Sehgal, Megha
Reis, Fernando MCV
Sias, Ana C.
Silva, Alcino J.
Adhikari, Avishek
Malvaez, Melissa
Wassum, Kate M.
author_sort Giovanniello, Jacqueline R.
collection PubMed
description Chronic stress can change how we learn and, thus, how we make decisions by promoting the formation of inflexible, potentially maladaptive, habits. Here we investigated the neuronal circuit mechanisms that enable this. Using a multifaceted approach in male and female mice, we reveal a dual pathway, amygdala-striatal, neuronal circuit architecture by which a recent history of chronic stress shapes learning to disrupt flexible goal-directed behavior in favor of inflexible habits. Chronic stress inhibits activity of basolateral amygdala projections to the dorsomedial striatum to impede the action-outcome learning that supports flexible, goal-directed decisions. Stress also increases activity in direct central amygdala projections to the dorsomedial striatum to promote the formation of rigid, inflexible habits. Thus, stress exerts opposing effects on two amygdala-striatal pathways to promote premature habit formation. These data provide neuronal circuit insights into how chronic stress shapes learning and decision making, and help understand how stress can lead to the disrupted decision making and pathological habits that characterize substance use disorders and other psychiatric conditions.
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spelling pubmed-105928852023-10-24 A dual-pathway architecture enables chronic stress to promote habit formation Giovanniello, Jacqueline R. Paredes, Natalie Wiener, Anna Ramírez-Armenta, Kathia Oragwam, Chukwuebuka Uwadia, Hanniel O. Lim, Kayla Nnamdi, Gift Wang, Alicia Sehgal, Megha Reis, Fernando MCV Sias, Ana C. Silva, Alcino J. Adhikari, Avishek Malvaez, Melissa Wassum, Kate M. bioRxiv Article Chronic stress can change how we learn and, thus, how we make decisions by promoting the formation of inflexible, potentially maladaptive, habits. Here we investigated the neuronal circuit mechanisms that enable this. Using a multifaceted approach in male and female mice, we reveal a dual pathway, amygdala-striatal, neuronal circuit architecture by which a recent history of chronic stress shapes learning to disrupt flexible goal-directed behavior in favor of inflexible habits. Chronic stress inhibits activity of basolateral amygdala projections to the dorsomedial striatum to impede the action-outcome learning that supports flexible, goal-directed decisions. Stress also increases activity in direct central amygdala projections to the dorsomedial striatum to promote the formation of rigid, inflexible habits. Thus, stress exerts opposing effects on two amygdala-striatal pathways to promote premature habit formation. These data provide neuronal circuit insights into how chronic stress shapes learning and decision making, and help understand how stress can lead to the disrupted decision making and pathological habits that characterize substance use disorders and other psychiatric conditions. Cold Spring Harbor Laboratory 2023-10-03 /pmc/articles/PMC10592885/ /pubmed/37873076 http://dx.doi.org/10.1101/2023.10.03.560731 Text en https://creativecommons.org/licenses/by-nc-nd/4.0/This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License (https://creativecommons.org/licenses/by-nc-nd/4.0/) , which allows reusers to copy and distribute the material in any medium or format in unadapted form only, for noncommercial purposes only, and only so long as attribution is given to the creator.
spellingShingle Article
Giovanniello, Jacqueline R.
Paredes, Natalie
Wiener, Anna
Ramírez-Armenta, Kathia
Oragwam, Chukwuebuka
Uwadia, Hanniel O.
Lim, Kayla
Nnamdi, Gift
Wang, Alicia
Sehgal, Megha
Reis, Fernando MCV
Sias, Ana C.
Silva, Alcino J.
Adhikari, Avishek
Malvaez, Melissa
Wassum, Kate M.
A dual-pathway architecture enables chronic stress to promote habit formation
title A dual-pathway architecture enables chronic stress to promote habit formation
title_full A dual-pathway architecture enables chronic stress to promote habit formation
title_fullStr A dual-pathway architecture enables chronic stress to promote habit formation
title_full_unstemmed A dual-pathway architecture enables chronic stress to promote habit formation
title_short A dual-pathway architecture enables chronic stress to promote habit formation
title_sort dual-pathway architecture enables chronic stress to promote habit formation
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10592885/
https://www.ncbi.nlm.nih.gov/pubmed/37873076
http://dx.doi.org/10.1101/2023.10.03.560731
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