Aerobic exercise reverses aging-induced depth-dependent decline in cerebral microcirculation.

aging cerebral microcirculation cerebral oxygenation exercise mouse neuroscience two-photon microscopy white matter

Journal

eLife
ISSN: 2050-084X
Titre abrégé: Elife
Pays: England
ID NLM: 101579614

Informations de publication

Date de publication:
04 07 2023
Historique:
received: 20 01 2023
accepted: 16 06 2023
medline: 6 7 2023
pubmed: 4 7 2023
entrez: 4 7 2023
Statut: epublish

Résumé

Aging is a major risk factor for cognitive impairment. Aerobic exercise benefits brain function and may promote cognitive health in older adults. However, underlying biological mechanisms across cerebral gray and white matter are poorly understood. Selective vulnerability of the white matter to small vessel disease and a link between white matter health and cognitive function suggests a potential role for responses in deep cerebral microcirculation. Here, we tested whether aerobic exercise modulates cerebral microcirculatory changes induced by aging. To this end, we carried out a comprehensive quantitative examination of changes in cerebral microvascular physiology in cortical gray and subcortical white matter in mice (3-6 vs. 19-21 months old), and asked whether and how exercise may rescue age-induced deficits. In the sedentary group, aging caused a more severe decline in cerebral microvascular perfusion and oxygenation in deep (infragranular) cortical layers and subcortical white matter compared with superficial (supragranular) cortical layers. Five months of voluntary aerobic exercise partly renormalized microvascular perfusion and oxygenation in aged mice in a depth-dependent manner, and brought these spatial distributions closer to those of young adult sedentary mice. These microcirculatory effects were accompanied by an improvement in cognitive function. Our work demonstrates the selective vulnerability of the deep cortex and subcortical white matter to aging-induced decline in microcirculation, as well as the responsiveness of these regions to aerobic exercise.

Identifiants

pubmed: 37402178
doi: 10.7554/eLife.86329
pii: 86329
pmc: PMC10319437
doi:
pii:

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

Subventions

Organisme : NIH HHS
ID : U24EB028941
Pays : United States
Organisme : NIH HHS
ID : U19NS123717
Pays : United States
Organisme : NIH HHS
ID : U01HL133362
Pays : United States
Organisme : NIH HHS
ID : R00MH120053
Pays : United States
Organisme : NIH HHS
ID : R01NS115401
Pays : United States
Organisme : NIH HHS
ID : RF1NS121095
Pays : United States
Organisme : NIH HHS
ID : R01AG055413
Pays : United States

Commentaires et corrections

Type : UpdateOf

Informations de copyright

© 2023, Shin et al.

Déclaration de conflit d'intérêts

PS, QP, HI, GH, EM, SG, BF, MA, SA, IŞ, BL, CR, SV, CA, EL, KA, AD, SS No competing interests declared

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Auteurs

Paul Shin (P)

Athinoula A Martinos Center for Biomedical Imaging, Massachusetts General Hospital, Harvard Medical School, Charlestown, United States.

Qi Pian (Q)

Athinoula A Martinos Center for Biomedical Imaging, Massachusetts General Hospital, Harvard Medical School, Charlestown, United States.

Hidehiro Ishikawa (H)

Neuroprotection Research Laboratory, Departments of Radiology and Neurology, Massachusetts General Hospital, Harvard Medical School, Charlestown, United States.

Gen Hamanaka (G)

Neuroprotection Research Laboratory, Departments of Radiology and Neurology, Massachusetts General Hospital, Harvard Medical School, Charlestown, United States.

Emiri T Mandeville (ET)

Neuroprotection Research Laboratory, Departments of Radiology and Neurology, Massachusetts General Hospital, Harvard Medical School, Charlestown, United States.

Shuzhen Guo (S)

Neuroprotection Research Laboratory, Departments of Radiology and Neurology, Massachusetts General Hospital, Harvard Medical School, Charlestown, United States.

Buyin Fu (B)

Athinoula A Martinos Center for Biomedical Imaging, Massachusetts General Hospital, Harvard Medical School, Charlestown, United States.

Mohammed Alfadhel (M)

Athinoula A Martinos Center for Biomedical Imaging, Massachusetts General Hospital, Harvard Medical School, Charlestown, United States.
Department of Bioengineering, Northeastern University, Boston, United States.

Srinivasa Rao Allu (SR)

Department of Biochemistry and Biophysics, University of Pennsylvania, Philadelphia, United States.
Department of Chemistry, University of Pennsylvania, Philadelphia, United States.

Ikbal Şencan-Eğilmez (I)

Athinoula A Martinos Center for Biomedical Imaging, Massachusetts General Hospital, Harvard Medical School, Charlestown, United States.
Biophotonics Research Center, Mallinckrodt Institute of Radiology, Department of Radiology, Washington University School of Medicine, St. Louis, United States.

Baoqiang Li (B)

Athinoula A Martinos Center for Biomedical Imaging, Massachusetts General Hospital, Harvard Medical School, Charlestown, United States.
Brain Cognition and Brain Disease Institute, Shenzhen Institute of Advanced Technology, Chinese Academy of Sciences, Shenzhen, China.

Chongzhao Ran (C)

Athinoula A Martinos Center for Biomedical Imaging, Massachusetts General Hospital, Harvard Medical School, Charlestown, United States.

Sergei A Vinogradov (SA)

Department of Biochemistry and Biophysics, University of Pennsylvania, Philadelphia, United States.
Department of Chemistry, University of Pennsylvania, Philadelphia, United States.

Cenk Ayata (C)

Neurovascular Research Laboratory, Department of Radiology, Massachusetts General Hospital, Harvard Medical School, Charlestown, United States.
Stroke Service, Department of Neurology, Massachusetts General Hospital, Harvard Medical School, Charlestown, United States.

Eng Lo (E)

Neuroprotection Research Laboratory, Departments of Radiology and Neurology, Massachusetts General Hospital, Harvard Medical School, Charlestown, United States.

Ken Arai (K)

Neuroprotection Research Laboratory, Departments of Radiology and Neurology, Massachusetts General Hospital, Harvard Medical School, Charlestown, United States.

Anna Devor (A)

Athinoula A Martinos Center for Biomedical Imaging, Massachusetts General Hospital, Harvard Medical School, Charlestown, United States.
Department of Biomedical Engineering, Boston University, Boston, United States.

Sava Sakadžić (S)

Athinoula A Martinos Center for Biomedical Imaging, Massachusetts General Hospital, Harvard Medical School, Charlestown, United States.

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