Regional gray matter oligodendrocyte- and myelin-related measures are associated with differential susceptibility to stress-induced behavior in rats and humans.


Journal

Translational psychiatry
ISSN: 2158-3188
Titre abrégé: Transl Psychiatry
Pays: United States
ID NLM: 101562664

Informations de publication

Date de publication:
13 12 2021
Historique:
received: 06 07 2021
accepted: 23 11 2021
revised: 30 10 2021
entrez: 14 12 2021
pubmed: 15 12 2021
medline: 1 2 2022
Statut: epublish

Résumé

Individual reactions to traumatic stress vary dramatically, yet the biological basis of this variation remains poorly understood. Recent studies demonstrate the surprising plasticity of oligodendrocytes and myelin with stress and experience, providing a potential mechanism by which trauma induces aberrant structural and functional changes in the adult brain. In this study, we utilized a translational approach to test the hypothesis that gray matter oligodendrocytes contribute to traumatic-stress-induced behavioral variation in both rats and humans. We exposed adult, male rats to a single, severe stressor and used a multimodal approach to characterize avoidance, startle, and fear-learning behavior, as well as oligodendrocyte and myelin basic protein (MBP) content in multiple brain areas. We found that oligodendrocyte cell density and MBP were correlated with behavioral outcomes in a region-specific manner. Specifically, stress-induced avoidance positively correlated with hippocampal dentate gyrus oligodendrocytes and MBP. Viral overexpression of the oligodendrogenic factor Olig1 in the dentate gyrus was sufficient to induce an anxiety-like behavioral phenotype. In contrast, contextual fear learning positively correlated with MBP in the amygdala and spatial-processing regions of the hippocampus. In a group of trauma-exposed US veterans, T1-/T2-weighted magnetic resonance imaging estimates of hippocampal and amygdala myelin associated with symptom profiles in a region-specific manner that mirrored the findings in rats. These results demonstrate a species-independent relationship between region-specific, gray matter oligodendrocytes and differential behavioral phenotypes following traumatic stress exposure. This study suggests a novel mechanism for brain plasticity that underlies individual variance in sensitivity to traumatic stress.

Identifiants

pubmed: 34903726
doi: 10.1038/s41398-021-01745-5
pii: 10.1038/s41398-021-01745-5
pmc: PMC8668977
doi:

Substances chimiques

Myelin Basic Protein 0

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

631

Subventions

Organisme : NIMH NIH HHS
ID : R01 MH115020
Pays : United States
Organisme : U.S. Department of Health & Human Services | NIH | National Institute of Mental Health (NIMH)
ID : R01MH115020

Informations de copyright

© 2021. The Author(s).

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Auteurs

Kimberly L P Long (KLP)

Helen Wills Neuroscience Institute, University of California, Berkeley, Berkeley, CA, 94720, USA.
Department of Psychiatry and Behavioral Sciences, University of California, SanFrancisco, San Francisco, CA, 94143, USA.

Linda L Chao (LL)

Department of Radiology & Biomedical Imaging, University of California, San Francisco, San Francisco, CA, 94143, USA.
Department of Psychiatry and Behavioral Sciences, University of California, San Francisco, San Francisco, CA, 94143, USA.

Yurika Kazama (Y)

Helen Wills Neuroscience Institute, University of California, Berkeley, Berkeley, CA, 94720, USA.

Anjile An (A)

Helen Wills Neuroscience Institute, University of California, Berkeley, Berkeley, CA, 94720, USA.
Division of Biostatistics, Department of Population Health Sciences, Weill Cornell Medicine, New York, NY, 10065, USA.

Kelsey Y Hu (KY)

Helen Wills Neuroscience Institute, University of California, Berkeley, Berkeley, CA, 94720, USA.

Lior Peretz (L)

Department of Molecular, Cellular, and Developmental Biology, University of California, Los Angeles, Los Angeles, CA, 90095, USA.

Dyana C Y Muller (DCY)

Department of Computer Science, University of Arizona, Tucson, AZ, 85721, USA.

Vivian D Roan (VD)

Helen Wills Neuroscience Institute, University of California, Berkeley, Berkeley, CA, 94720, USA.

Rhea Misra (R)

Helen Wills Neuroscience Institute, University of California, Berkeley, Berkeley, CA, 94720, USA.

Claire E Toth (CE)

Helen Wills Neuroscience Institute, University of California, Berkeley, Berkeley, CA, 94720, USA.

Jocelyn M Breton (JM)

Helen Wills Neuroscience Institute, University of California, Berkeley, Berkeley, CA, 94720, USA.
Department of Psychiatry, Columbia University, New York, NY, 10027, USA.

William Casazza (W)

Department of Statistics and Department of Medical Genetics, University of British Columbia, Vancouver, BC, V6T 1Z4, Canada.

Sara Mostafavi (S)

Department of Statistics and Department of Medical Genetics, University of British Columbia, Vancouver, BC, V6T 1Z4, Canada.
Canadian Institute for Advanced Research, Toronto, ON, M5G 1M1, Canada.

Bertrand R Huber (BR)

Department of Neurology, Boston University, Boston, MA, 02215, USA.
National Center for PTSD, VA New England Health Care System, Boston, MA, 02130, USA.

Steven H Woodward (SH)

National Center for PTSD, VA Palo Alto Health Care System, Palo Alto, CA, 94304, USA.

Thomas C Neylan (TC)

Department of Psychiatry and Behavioral Sciences, University of California, San Francisco, San Francisco, CA, 94143, USA.
San Francisco VA Health Care System, San Francisco, CA, 94121, USA.

Daniela Kaufer (D)

Helen Wills Neuroscience Institute, University of California, Berkeley, Berkeley, CA, 94720, USA. danielak@berkeley.edu.
Canadian Institute for Advanced Research, Toronto, ON, M5G 1M1, Canada. danielak@berkeley.edu.
Department of Integrative Biology, University of California, Berkeley, Berkeley, CA, 94720, USA. danielak@berkeley.edu.

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