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Developmental differences in amygdala projection neuron activation associated with isolation-driven changes in social preference

Adolescence is a developmental period characterized by brain maturation and changes in social engagement. Changes in the social environment influence social behaviors. Memories of social events, including remembering familiar individuals, require social engagement during encoding. Therefore, existin...

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Autores principales: Ferrara, Nicole C., Trask, Sydney, Ritger, Alexandra, Padival, Mallika, Rosenkranz, J. Amiel
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9449454/
https://www.ncbi.nlm.nih.gov/pubmed/36090658
http://dx.doi.org/10.3389/fnbeh.2022.956102
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author Ferrara, Nicole C.
Trask, Sydney
Ritger, Alexandra
Padival, Mallika
Rosenkranz, J. Amiel
author_facet Ferrara, Nicole C.
Trask, Sydney
Ritger, Alexandra
Padival, Mallika
Rosenkranz, J. Amiel
author_sort Ferrara, Nicole C.
collection PubMed
description Adolescence is a developmental period characterized by brain maturation and changes in social engagement. Changes in the social environment influence social behaviors. Memories of social events, including remembering familiar individuals, require social engagement during encoding. Therefore, existing differences in adult and adolescent social repertoires and environmentally-driven changes in social behavior may impact novel partner preference, associated with social recognition. Several amygdala subregions are sensitive to the social environment and can influence social behavior, which is crucial for novelty preference. Amygdala neurons project to the septum and nucleus accumbens (NAc), which are linked to social engagement. Here, we investigated how the social environment impacts age-specific social behaviors during social encoding and its subsequent impact on partner preference. We then examined changes in amygdala-septal and -NAc circuits that accompany these changes. Brief isolation can drive social behavior in both adults and adolescents and was used to increase social engagement during encoding. We found that brief isolation facilitates social interaction in adolescents and adults, and analysis across time revealed that partner discrimination was intact in all groups, but there was a shift in preference within isolated and non-isolated groups. We found that this same isolation preferentially increases basal amygdala (BA) activity relative to other amygdala subregions in adults, but activity among amygdala subregions was similar in adolescents, even when considering conditions (no isolation, isolation). Further, we identify isolation-driven increases in BA-NAc and BA-septal circuits in both adults and adolescents. Together, these results provide evidence for changes in neuronal populations within amygdala subregions and their projections that are sensitive to the social environment that may influence the pattern of social interaction within briefly isolated groups during development.
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spelling pubmed-94494542022-09-08 Developmental differences in amygdala projection neuron activation associated with isolation-driven changes in social preference Ferrara, Nicole C. Trask, Sydney Ritger, Alexandra Padival, Mallika Rosenkranz, J. Amiel Front Behav Neurosci Neuroscience Adolescence is a developmental period characterized by brain maturation and changes in social engagement. Changes in the social environment influence social behaviors. Memories of social events, including remembering familiar individuals, require social engagement during encoding. Therefore, existing differences in adult and adolescent social repertoires and environmentally-driven changes in social behavior may impact novel partner preference, associated with social recognition. Several amygdala subregions are sensitive to the social environment and can influence social behavior, which is crucial for novelty preference. Amygdala neurons project to the septum and nucleus accumbens (NAc), which are linked to social engagement. Here, we investigated how the social environment impacts age-specific social behaviors during social encoding and its subsequent impact on partner preference. We then examined changes in amygdala-septal and -NAc circuits that accompany these changes. Brief isolation can drive social behavior in both adults and adolescents and was used to increase social engagement during encoding. We found that brief isolation facilitates social interaction in adolescents and adults, and analysis across time revealed that partner discrimination was intact in all groups, but there was a shift in preference within isolated and non-isolated groups. We found that this same isolation preferentially increases basal amygdala (BA) activity relative to other amygdala subregions in adults, but activity among amygdala subregions was similar in adolescents, even when considering conditions (no isolation, isolation). Further, we identify isolation-driven increases in BA-NAc and BA-septal circuits in both adults and adolescents. Together, these results provide evidence for changes in neuronal populations within amygdala subregions and their projections that are sensitive to the social environment that may influence the pattern of social interaction within briefly isolated groups during development. Frontiers Media S.A. 2022-08-24 /pmc/articles/PMC9449454/ /pubmed/36090658 http://dx.doi.org/10.3389/fnbeh.2022.956102 Text en Copyright © 2022 Ferrara, Trask, Ritger, Padival and Rosenkranz. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Neuroscience
Ferrara, Nicole C.
Trask, Sydney
Ritger, Alexandra
Padival, Mallika
Rosenkranz, J. Amiel
Developmental differences in amygdala projection neuron activation associated with isolation-driven changes in social preference
title Developmental differences in amygdala projection neuron activation associated with isolation-driven changes in social preference
title_full Developmental differences in amygdala projection neuron activation associated with isolation-driven changes in social preference
title_fullStr Developmental differences in amygdala projection neuron activation associated with isolation-driven changes in social preference
title_full_unstemmed Developmental differences in amygdala projection neuron activation associated with isolation-driven changes in social preference
title_short Developmental differences in amygdala projection neuron activation associated with isolation-driven changes in social preference
title_sort developmental differences in amygdala projection neuron activation associated with isolation-driven changes in social preference
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9449454/
https://www.ncbi.nlm.nih.gov/pubmed/36090658
http://dx.doi.org/10.3389/fnbeh.2022.956102
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