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The Influence of Environmental Enrichment on Affective and Neural Consequences of Social Isolation Across Development

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Abstract

Social stress is associated with depression and anxiety, physiological disruptions, and altered brain morphology in central stress circuitry across development. Environmental enrichment strategies may improve responses to social stress. Socially monogamous prairie voles exhibit analogous social and emotion-related behaviors to humans, with potential translational insight into interactions of social stress, age, and environmental enrichment. This study explored the effects of social isolation and environmental enrichment on behaviors related to depression and anxiety, physiological indicators of stress, and dendritic structural changes in amygdala and hippocampal subregions in young adult and aging prairie voles. Forty-nine male prairie voles were assigned to one of six groups divided by age (young adult vs. aging), social structure (paired vs. isolated), and housing environment (enriched vs. non-enriched). Following 4 weeks of these conditions, behaviors related to depression and anxiety were investigated in the forced swim test and elevated plus maze, body and adrenal weights were evaluated, and dendritic morphology analyses were conducted in hippocampus and amygdala subregions. Environmental enrichment decreased immobility duration in the forced swim test, increased open arm exploration in the elevated plus maze, and reduced adrenal/body weight ratio in aging and young adult prairie voles. Age and social isolation influenced dendritic morphology in the basolateral amygdala. Age, but not social isolation, influenced dendritic morphology in the hippocampal dentate gyrus. Environmental enrichment did not influence dendritic morphology in either brain region. These data may inform interventions to reduce the effects of social stressors and age-related central changes associated with affective behavioral consequences in humans.

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Acknowledgements

The authors would like to thank the following individuals for valuable assistance: Sarah Ciosek, William Colburn, Miranda Cox, Nicole Holzapfel, Blessy Johnson, Meredith McCormick, Marigny Normann, Cassidy Padal, Samantha Sujet, and Cynthia Sanchez-Vazquez. Thank you to the Northern Illinois University College of Liberal Arts and Sciences Instrumentation Shop for technical assistance.

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Correspondence to Angela J. Grippo.

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Funding Information

This research was funded in part by National Institutes of Health grants HL112350 and HL147179. The funder had no role in the study design, data collection, data analysis and interpretation, writing of the report, or decision to submit the article for publication.

Conflicts of Interest

The authors declare no competing interests.

Data Availability

Data for the project can be obtained here: https://osf.io/d29zg/.

Author Contributions

All authors contributed significantly to the study conceptualization, study design, data collection, analyses, interpretation, and/or writing of the manuscript. All authors have approved the final version of the submitted manuscript.

Ethical Approval

All procedures described in this manuscript were approved by the Northern Illinois University Institutional Animal Care and Use Committee, and are in compliance with all federal guidelines. The methods conform to the Guide for the Care and Use of Laboratory Animals from the Institute of Laboratory Animal Research. All efforts were made to ensure that procedures were conducted in a responsible and ethical manner in the context of the Three Rs (replacement, reduction, and refinement).

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Not applicable.

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Handling Editor: Forrest Dylan Rogers

Open Access

(1) Data and/or materials are not available per the Level 2 TOP guidelines.

(2) These experiments were not preregistered.

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Akinbo, O.I., McNeal, N., Hylin, M. et al. The Influence of Environmental Enrichment on Affective and Neural Consequences of Social Isolation Across Development. Affec Sci 3, 713–733 (2022). https://doi.org/10.1007/s42761-022-00131-8

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  • DOI: https://doi.org/10.1007/s42761-022-00131-8

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