Cortical plasticity is associated with blood-brain barrier modulation.

albumin blood–brain barrier caveolae-mediated transcytosis human magnetic resonance imaging neuroscience rat synaptic plasticity transforming growth factor β

Journal

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

Informations de publication

Date de publication:
18 Jul 2024
Historique:
medline: 18 7 2024
pubmed: 18 7 2024
entrez: 18 7 2024
Statut: epublish

Résumé

Brain microvessels possess the unique properties of a blood-brain barrier (BBB), tightly regulating the passage of molecules from the blood to the brain neuropil and vice versa. In models of brain injury, BBB dysfunction and the associated leakage of serum albumin to the neuropil have been shown to induce pathological plasticity, neuronal hyper-excitability, and seizures. The effect of neuronal activity on BBB function and whether it plays a role in plasticity in the healthy brain remain unclear. Here we show that neuronal activity induces modulation of microvascular permeability in the healthy brain and that it has a role in local network reorganization. Combining simultaneous electrophysiological recording and vascular imaging with transcriptomic analysis in rats, and functional and BBB-mapping MRI in human subjects, we show that prolonged stimulation of the limb induces a focal increase in BBB permeability in the corresponding somatosensory cortex that is associated with long-term synaptic plasticity. We further show that the increased microvascular permeability depends on neuronal activity and involves caveolae-mediated transcytosis and transforming growth factor β signaling. Our results reveal a role of BBB modulation in cortical plasticity in the healthy brain, highlighting the importance of neurovascular interactions for sensory experience and learning.

Identifiants

pubmed: 39024007
doi: 10.7554/eLife.89611
pii: 89611
doi:
pii:

Banques de données

GEO
['GSE223282']

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : Israel Science Foundation
ID : 717/15
Organisme : Israel Science Foundation
ID : 2254/20
Organisme : CIHR
ID : PJT 148896
Pays : Canada
Organisme : European Research Area Network
ID : NDD 168164

Informations de copyright

© 2023, Swissa et al.

Déclaration de conflit d'intérêts

ES, UM, LY, LS, LK, SM, IB, SU, RP, PS, OP, DK, AF No competing interests declared

Auteurs

Evyatar Swissa (E)

Department of Brain and Cognitive Sciences, The School of Brain Sciences and Cognition, Zlotowski Center for Neuroscience, Ben-Gurion University of the Negev, Beer-Sheva, Israel.

Uri Monsonego (U)

Department of Physiology and Cell Biology, Faculty of Health Sciences, Ben-Gurion University of the Negev, Beer-Sheva, Israel.

Lynn T Yang (LT)

Department of Integrative Biology, University of California, Berkeley, Berkeley, United States.
Helen Wills Neuroscience Institute, University of California, Berkeley, Berkeley, United States.

Lior Schori (L)

Department of Physiology and Cell Biology, Faculty of Health Sciences, Ben-Gurion University of the Negev, Beer-Sheva, Israel.

Lyna Kamintsky (L)

Department of Medical Neuroscience, Dalhousie University, Halifax, Canada.

Sheida Mirloo (S)

Department of Medical Neuroscience, Dalhousie University, Halifax, Canada.

Itamar Burger (I)

Department of Physiology and Cell Biology, Faculty of Health Sciences, Ben-Gurion University of the Negev, Beer-Sheva, Israel.

Sarit Uzzan (S)

Department of Clinical Biochemistry and Pharmacology, Faculty of Health Sciences, Ben-Gurion University of the Negev, Beer-Sheva, Israel.

Rishi Patel (R)

Department of Integrative Biology, University of California, Berkeley, Berkeley, United States.

Peter H Sudmant (PH)

Department of Integrative Biology, University of California, Berkeley, Berkeley, United States.

Ofer Prager (O)

Department of Brain and Cognitive Sciences, The School of Brain Sciences and Cognition, Zlotowski Center for Neuroscience, Ben-Gurion University of the Negev, Beer-Sheva, Israel.
Department of Physiology and Cell Biology, Faculty of Health Sciences, Ben-Gurion University of the Negev, Beer-Sheva, Israel.

Daniela Kaufer (D)

Department of Integrative Biology, University of California, Berkeley, Berkeley, United States.
Helen Wills Neuroscience Institute, University of California, Berkeley, Berkeley, United States.

Alon Friedman (A)

Department of Brain and Cognitive Sciences, The School of Brain Sciences and Cognition, Zlotowski Center for Neuroscience, Ben-Gurion University of the Negev, Beer-Sheva, Israel.
Department of Physiology and Cell Biology, Faculty of Health Sciences, Ben-Gurion University of the Negev, Beer-Sheva, Israel.
Department of Medical Neuroscience, Dalhousie University, Halifax, Canada.

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