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Social Isolation in Adolescence Disrupts Cortical Development and Goal-Dependent Decision-Making in Adulthood, Despite Social Reintegration

The social environment influences neurodevelopment. Investigations using rodents to study this phenomenon commonly isolate subjects, then assess neurobehavioral consequences while animals are still isolated. This approach precludes one from dissociating the effects of on-going versus prior isolation...

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Autores principales: Hinton, Elizabeth A., Li, Dan C., Allen, Aylet G., Gourley, Shannon L.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Society for Neuroscience 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6757188/
https://www.ncbi.nlm.nih.gov/pubmed/31527057
http://dx.doi.org/10.1523/ENEURO.0318-19.2019
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author Hinton, Elizabeth A.
Li, Dan C.
Allen, Aylet G.
Gourley, Shannon L.
author_facet Hinton, Elizabeth A.
Li, Dan C.
Allen, Aylet G.
Gourley, Shannon L.
author_sort Hinton, Elizabeth A.
collection PubMed
description The social environment influences neurodevelopment. Investigations using rodents to study this phenomenon commonly isolate subjects, then assess neurobehavioral consequences while animals are still isolated. This approach precludes one from dissociating the effects of on-going versus prior isolation, hindering our complete understanding of the consequences of social experience during particular developmental periods. Here, we socially isolated adolescent mice from postnatal day (P)31 to P60, then re-housed them into social groups. We tested their ability to select actions based on expected outcomes using multiple reinforcer devaluation and instrumental contingency degradation techniques. Social isolation in adolescence (but not adulthood) weakened instrumental response updating, causing mice to defer to habit-like behaviors. Habit biases were associated with glucocorticoid insufficiency in adolescence, oligodendrocyte marker loss throughout cortico-striatal regions, and dendritic spine and synaptic marker excess in the adult orbitofrontal cortex (OFC). Artificial, chemogenetic stimulation of the ventrolateral OFC in typical, healthy mice recapitulated response biases following isolation, causing habit-like behaviors. Meanwhile, correcting dendritic architecture by inhibiting the cytoskeletal regulatory protein ROCK remedied instrumental response updating defects in socially isolated mice. Our findings suggest that adolescence is a critical period during which social experience optimizes one’s ability to seek and attain goals later in life. Age-typical dendritic spine elimination appears to be an essential factor, and in its absence, organisms may defer to habit-based behaviors.
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spelling pubmed-67571882019-09-24 Social Isolation in Adolescence Disrupts Cortical Development and Goal-Dependent Decision-Making in Adulthood, Despite Social Reintegration Hinton, Elizabeth A. Li, Dan C. Allen, Aylet G. Gourley, Shannon L. eNeuro Confirmation The social environment influences neurodevelopment. Investigations using rodents to study this phenomenon commonly isolate subjects, then assess neurobehavioral consequences while animals are still isolated. This approach precludes one from dissociating the effects of on-going versus prior isolation, hindering our complete understanding of the consequences of social experience during particular developmental periods. Here, we socially isolated adolescent mice from postnatal day (P)31 to P60, then re-housed them into social groups. We tested their ability to select actions based on expected outcomes using multiple reinforcer devaluation and instrumental contingency degradation techniques. Social isolation in adolescence (but not adulthood) weakened instrumental response updating, causing mice to defer to habit-like behaviors. Habit biases were associated with glucocorticoid insufficiency in adolescence, oligodendrocyte marker loss throughout cortico-striatal regions, and dendritic spine and synaptic marker excess in the adult orbitofrontal cortex (OFC). Artificial, chemogenetic stimulation of the ventrolateral OFC in typical, healthy mice recapitulated response biases following isolation, causing habit-like behaviors. Meanwhile, correcting dendritic architecture by inhibiting the cytoskeletal regulatory protein ROCK remedied instrumental response updating defects in socially isolated mice. Our findings suggest that adolescence is a critical period during which social experience optimizes one’s ability to seek and attain goals later in life. Age-typical dendritic spine elimination appears to be an essential factor, and in its absence, organisms may defer to habit-based behaviors. Society for Neuroscience 2019-09-20 /pmc/articles/PMC6757188/ /pubmed/31527057 http://dx.doi.org/10.1523/ENEURO.0318-19.2019 Text en Copyright © 2019 Hinton et al. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.
spellingShingle Confirmation
Hinton, Elizabeth A.
Li, Dan C.
Allen, Aylet G.
Gourley, Shannon L.
Social Isolation in Adolescence Disrupts Cortical Development and Goal-Dependent Decision-Making in Adulthood, Despite Social Reintegration
title Social Isolation in Adolescence Disrupts Cortical Development and Goal-Dependent Decision-Making in Adulthood, Despite Social Reintegration
title_full Social Isolation in Adolescence Disrupts Cortical Development and Goal-Dependent Decision-Making in Adulthood, Despite Social Reintegration
title_fullStr Social Isolation in Adolescence Disrupts Cortical Development and Goal-Dependent Decision-Making in Adulthood, Despite Social Reintegration
title_full_unstemmed Social Isolation in Adolescence Disrupts Cortical Development and Goal-Dependent Decision-Making in Adulthood, Despite Social Reintegration
title_short Social Isolation in Adolescence Disrupts Cortical Development and Goal-Dependent Decision-Making in Adulthood, Despite Social Reintegration
title_sort social isolation in adolescence disrupts cortical development and goal-dependent decision-making in adulthood, despite social reintegration
topic Confirmation
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6757188/
https://www.ncbi.nlm.nih.gov/pubmed/31527057
http://dx.doi.org/10.1523/ENEURO.0318-19.2019
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