Long-term changes of parvalbumin- and somatostatin-positive interneurons of the primary motor cortex after chronic social defeat stress depend on individual stress-vulnerability

Chronic stress is a major risk factor for developing mental illnesses and cognitive deficiencies although stress-susceptibility varies individually. In a recent study, we established the connection between chronic social defeat stress (CSDS) and impaired motor learning abilities accompanied by chron...

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Main Authors: Maria L. Serradas, Valentin Stein, Anne-Kathrin Gellner
Format: Article
Language:English
Published: Frontiers Media S.A. 2022-07-01
Series:Frontiers in Psychiatry
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fpsyt.2022.946719/full
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author Maria L. Serradas
Valentin Stein
Anne-Kathrin Gellner
author_facet Maria L. Serradas
Valentin Stein
Anne-Kathrin Gellner
author_sort Maria L. Serradas
collection DOAJ
description Chronic stress is a major risk factor for developing mental illnesses and cognitive deficiencies although stress-susceptibility varies individually. In a recent study, we established the connection between chronic social defeat stress (CSDS) and impaired motor learning abilities accompanied by chronically disturbed structural neuroplasticity in the primary motor cortex (M1) of mice. In this study, we further investigated the long-term effects of CSDS exposure on M1, focusing on the interneuronal cell population. We used repeated CSDS to elicit effects across behavioral, endocrinological, and metabolic parameters in mice. Susceptible and resilient phenotypes were discriminated by symptom load and motor learning abilities were assessed on the rotarod. Structural changes in interneuronal circuits of M1 were studied by immunohistochemistry using parvalbumin (PV+) and somatostatin (SST+) markers. Stress-susceptible mice had a blunted stress hormone response and impaired motor learning skills. These mice presented reduced numbers of both interneuron populations in M1 with layer-dependent distribution, while alterations in cell size and immunoreactivity were found in both susceptible and resilient individuals. These results, together with our previous data, suggest that stress-induced cell loss and degeneration of the GABAergic interneuronal network of M1 could underlay impaired motor learning, due to their role in controlling the excitatory output and spine dynamics of principal neurons required for this task. Our study further highlights the importance of long-term outcomes of chronically stressed individuals which are translationally important due to the long timecourses of stress-induced neuropsychiatric disorders.
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spelling doaj.art-efa4fb66b691436084b5559e5e301d572022-12-22T01:39:08ZengFrontiers Media S.A.Frontiers in Psychiatry1664-06402022-07-011310.3389/fpsyt.2022.946719946719Long-term changes of parvalbumin- and somatostatin-positive interneurons of the primary motor cortex after chronic social defeat stress depend on individual stress-vulnerabilityMaria L. Serradas0Valentin Stein1Anne-Kathrin Gellner2Institute of Physiology II, Medical Faculty, University of Bonn, Bonn, GermanyInstitute of Physiology II, Medical Faculty, University of Bonn, Bonn, GermanyDepartment of Psychiatry and Psychotherapy, University Hospital Bonn, Bonn, GermanyChronic stress is a major risk factor for developing mental illnesses and cognitive deficiencies although stress-susceptibility varies individually. In a recent study, we established the connection between chronic social defeat stress (CSDS) and impaired motor learning abilities accompanied by chronically disturbed structural neuroplasticity in the primary motor cortex (M1) of mice. In this study, we further investigated the long-term effects of CSDS exposure on M1, focusing on the interneuronal cell population. We used repeated CSDS to elicit effects across behavioral, endocrinological, and metabolic parameters in mice. Susceptible and resilient phenotypes were discriminated by symptom load and motor learning abilities were assessed on the rotarod. Structural changes in interneuronal circuits of M1 were studied by immunohistochemistry using parvalbumin (PV+) and somatostatin (SST+) markers. Stress-susceptible mice had a blunted stress hormone response and impaired motor learning skills. These mice presented reduced numbers of both interneuron populations in M1 with layer-dependent distribution, while alterations in cell size and immunoreactivity were found in both susceptible and resilient individuals. These results, together with our previous data, suggest that stress-induced cell loss and degeneration of the GABAergic interneuronal network of M1 could underlay impaired motor learning, due to their role in controlling the excitatory output and spine dynamics of principal neurons required for this task. Our study further highlights the importance of long-term outcomes of chronically stressed individuals which are translationally important due to the long timecourses of stress-induced neuropsychiatric disorders.https://www.frontiersin.org/articles/10.3389/fpsyt.2022.946719/fullchronic stressparvalbuminmotor learningdepressionsomatostatininterneuron
spellingShingle Maria L. Serradas
Valentin Stein
Anne-Kathrin Gellner
Long-term changes of parvalbumin- and somatostatin-positive interneurons of the primary motor cortex after chronic social defeat stress depend on individual stress-vulnerability
Frontiers in Psychiatry
chronic stress
parvalbumin
motor learning
depression
somatostatin
interneuron
title Long-term changes of parvalbumin- and somatostatin-positive interneurons of the primary motor cortex after chronic social defeat stress depend on individual stress-vulnerability
title_full Long-term changes of parvalbumin- and somatostatin-positive interneurons of the primary motor cortex after chronic social defeat stress depend on individual stress-vulnerability
title_fullStr Long-term changes of parvalbumin- and somatostatin-positive interneurons of the primary motor cortex after chronic social defeat stress depend on individual stress-vulnerability
title_full_unstemmed Long-term changes of parvalbumin- and somatostatin-positive interneurons of the primary motor cortex after chronic social defeat stress depend on individual stress-vulnerability
title_short Long-term changes of parvalbumin- and somatostatin-positive interneurons of the primary motor cortex after chronic social defeat stress depend on individual stress-vulnerability
title_sort long term changes of parvalbumin and somatostatin positive interneurons of the primary motor cortex after chronic social defeat stress depend on individual stress vulnerability
topic chronic stress
parvalbumin
motor learning
depression
somatostatin
interneuron
url https://www.frontiersin.org/articles/10.3389/fpsyt.2022.946719/full
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AT valentinstein longtermchangesofparvalbuminandsomatostatinpositiveinterneuronsoftheprimarymotorcortexafterchronicsocialdefeatstressdependonindividualstressvulnerability
AT annekathringellner longtermchangesofparvalbuminandsomatostatinpositiveinterneuronsoftheprimarymotorcortexafterchronicsocialdefeatstressdependonindividualstressvulnerability