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Effects of maternal social isolation on adult rodent offspring cognition

Prenatal experiences can influence offspring physiology and behaviour through the lifespan. Various forms of prenatal stress impair adult learning and memory function and can lead to increased occurrence of anxiety and depression. Clinical work suggests that prenatal stress and maternal depression l...

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Autores principales: McDonald, Robert J., Hong, Nancy S., Trow, Jan S., Kaupp, Chelsea, Balog, R. J., Gokarn, London, Falkenberg, Erin A., McCreary, Keiko J., Soltanpour, Nasrin, Witbeck, Carter, McKenna, Aimee, Metz, Gerlinde A. S.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10177704/
https://www.ncbi.nlm.nih.gov/pubmed/37173349
http://dx.doi.org/10.1038/s41598-023-34834-0
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author McDonald, Robert J.
Hong, Nancy S.
Trow, Jan S.
Kaupp, Chelsea
Balog, R. J.
Gokarn, London
Falkenberg, Erin A.
McCreary, Keiko J.
Soltanpour, Nasrin
Witbeck, Carter
McKenna, Aimee
Metz, Gerlinde A. S.
author_facet McDonald, Robert J.
Hong, Nancy S.
Trow, Jan S.
Kaupp, Chelsea
Balog, R. J.
Gokarn, London
Falkenberg, Erin A.
McCreary, Keiko J.
Soltanpour, Nasrin
Witbeck, Carter
McKenna, Aimee
Metz, Gerlinde A. S.
author_sort McDonald, Robert J.
collection PubMed
description Prenatal experiences can influence offspring physiology and behaviour through the lifespan. Various forms of prenatal stress impair adult learning and memory function and can lead to increased occurrence of anxiety and depression. Clinical work suggests that prenatal stress and maternal depression lead to similar outcomes in children and adolescents, however the long-term effects of maternal depression are less established, particularly in well controlled animal models. Social isolation is common in depressed individuals and during the recent COVID-19 pandemic. Accordingly, for this study we were interested in the effects of maternal stress induced via social isolation on adult offspring cognitive functions including spatial, stimulus–response, and emotional learning and memory that are mediated by different networks centered on the hippocampus, dorsal striatum, and amygdala, respectively. Tasks included a discriminative contextual fear conditioning task and cue-place water task. Pregnant dams in the social isolation group were single housed prior to and throughout gestation. Once offspring reached adulthood the male offspring were trained on a contextual fear conditioning task in which rats were trained to associate one of two contexts with an aversive stimulus and the opposing context remained neutral. Afterwards a cue-place water task was performed during which they were required to navigate to both a visible and invisible platform. Fear conditioning results revealed that the adult offspring of socially isolated mothers, but not controls, were impaired in associating a specific context with a fear-inducing stimulus as assessed by conditioned freezing and avoidance. Results from the water task indicate that adult offspring of mothers that were socially isolated showed place learning deficits but not stimulus-response habit learning on the same task. These cognitive impairments, in the offspring of socially isolated dams, occurred in the absence of maternal elevated stress hormone levels, anxiety, or altered mothering. Some evidence suggested that maternal blood-glucose levels were altered particularly during gestation. Our results provide further support for the idea that learning and memory networks, centered on the amygdala and hippocampus are particularly susceptible to the negative impacts of maternal social isolation and these effects can occur without elevated glucocorticoid levels associated with other forms of prenatal stress.
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spelling pubmed-101777042023-05-14 Effects of maternal social isolation on adult rodent offspring cognition McDonald, Robert J. Hong, Nancy S. Trow, Jan S. Kaupp, Chelsea Balog, R. J. Gokarn, London Falkenberg, Erin A. McCreary, Keiko J. Soltanpour, Nasrin Witbeck, Carter McKenna, Aimee Metz, Gerlinde A. S. Sci Rep Article Prenatal experiences can influence offspring physiology and behaviour through the lifespan. Various forms of prenatal stress impair adult learning and memory function and can lead to increased occurrence of anxiety and depression. Clinical work suggests that prenatal stress and maternal depression lead to similar outcomes in children and adolescents, however the long-term effects of maternal depression are less established, particularly in well controlled animal models. Social isolation is common in depressed individuals and during the recent COVID-19 pandemic. Accordingly, for this study we were interested in the effects of maternal stress induced via social isolation on adult offspring cognitive functions including spatial, stimulus–response, and emotional learning and memory that are mediated by different networks centered on the hippocampus, dorsal striatum, and amygdala, respectively. Tasks included a discriminative contextual fear conditioning task and cue-place water task. Pregnant dams in the social isolation group were single housed prior to and throughout gestation. Once offspring reached adulthood the male offspring were trained on a contextual fear conditioning task in which rats were trained to associate one of two contexts with an aversive stimulus and the opposing context remained neutral. Afterwards a cue-place water task was performed during which they were required to navigate to both a visible and invisible platform. Fear conditioning results revealed that the adult offspring of socially isolated mothers, but not controls, were impaired in associating a specific context with a fear-inducing stimulus as assessed by conditioned freezing and avoidance. Results from the water task indicate that adult offspring of mothers that were socially isolated showed place learning deficits but not stimulus-response habit learning on the same task. These cognitive impairments, in the offspring of socially isolated dams, occurred in the absence of maternal elevated stress hormone levels, anxiety, or altered mothering. Some evidence suggested that maternal blood-glucose levels were altered particularly during gestation. Our results provide further support for the idea that learning and memory networks, centered on the amygdala and hippocampus are particularly susceptible to the negative impacts of maternal social isolation and these effects can occur without elevated glucocorticoid levels associated with other forms of prenatal stress. Nature Publishing Group UK 2023-05-12 /pmc/articles/PMC10177704/ /pubmed/37173349 http://dx.doi.org/10.1038/s41598-023-34834-0 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
McDonald, Robert J.
Hong, Nancy S.
Trow, Jan S.
Kaupp, Chelsea
Balog, R. J.
Gokarn, London
Falkenberg, Erin A.
McCreary, Keiko J.
Soltanpour, Nasrin
Witbeck, Carter
McKenna, Aimee
Metz, Gerlinde A. S.
Effects of maternal social isolation on adult rodent offspring cognition
title Effects of maternal social isolation on adult rodent offspring cognition
title_full Effects of maternal social isolation on adult rodent offspring cognition
title_fullStr Effects of maternal social isolation on adult rodent offspring cognition
title_full_unstemmed Effects of maternal social isolation on adult rodent offspring cognition
title_short Effects of maternal social isolation on adult rodent offspring cognition
title_sort effects of maternal social isolation on adult rodent offspring cognition
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10177704/
https://www.ncbi.nlm.nih.gov/pubmed/37173349
http://dx.doi.org/10.1038/s41598-023-34834-0
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