Spontaneous neural activity changes after bariatric surgery: A resting-state fMRI study.


Journal

NeuroImage
ISSN: 1095-9572
Titre abrégé: Neuroimage
Pays: United States
ID NLM: 9215515

Informations de publication

Date de publication:
01 11 2021
Historique:
received: 04 04 2021
revised: 24 06 2021
accepted: 20 07 2021
pubmed: 25 7 2021
medline: 21 10 2021
entrez: 24 7 2021
Statut: ppublish

Résumé

Metabolic disorders associated with obesity could lead to alterations in brain structure and function. Whether these changes can be reversed after weight loss is unclear. Bariatric surgery provides a unique opportunity to address these questions because it induces marked weight loss and metabolic improvements which in turn may impact the brain in a longitudinal fashion. Previous studies found widespread changes in grey matter (GM) and white matter (WM) after bariatric surgery. However, findings regarding changes in spontaneous neural activity following surgery, as assessed with the fractional amplitude of low frequency fluctuations (fALFF) and regional homogeneity of neural activity (ReHo), are scarce and heterogenous. In this study, we used a longitudinal design to examine the changes in spontaneous neural activity after bariatric surgery (comparing pre- to post-surgery), and to determine whether these changes are related to cardiometabolic variables. The study included 57 participants with severe obesity (mean BMI=43.1 ± 4.3 kg/m We found a global increase in the fALFF signal with greater increase within dorsolateral prefrontal cortex, precuneus, inferior temporal gyrus, and visual cortex. This effect was more significant 4 months after surgery. The increase within dorsolateral prefrontal cortex, temporal gyrus, and visual cortex was more limited after 12 months and only present in the visual cortex after 24 months. These increases in neural activity measured by fALFF were also significantly associated with the increase in GM density following surgery. Furthermore, the increase in neural activity was significantly related to post-surgery weight loss and improvement in cardiometabolic variables, such as blood pressure. In the independent HCP sample, normal-weight participants had higher global and regional fALFF signals, mainly in dorsolateral/medial frontal cortex, precuneus and middle/inferior temporal gyrus compared to the obese participants. These BMI-related differences in fALFF were associated with the increase in fALFF 4 months post-surgery especially in regions involved in control, default mode and dorsal attention networks. Bariatric surgery-induced weight loss and improvement in metabolic factors are associated with widespread global and regional increases in neural activity, as measured by fALFF signal. These findings alongside the higher fALFF signal in normal-weight participants compared to participants with severe obesity in an independent dataset suggest an early recovery in the neural activity signal level after the surgery.

Sections du résumé

BACKGROUND
Metabolic disorders associated with obesity could lead to alterations in brain structure and function. Whether these changes can be reversed after weight loss is unclear. Bariatric surgery provides a unique opportunity to address these questions because it induces marked weight loss and metabolic improvements which in turn may impact the brain in a longitudinal fashion. Previous studies found widespread changes in grey matter (GM) and white matter (WM) after bariatric surgery. However, findings regarding changes in spontaneous neural activity following surgery, as assessed with the fractional amplitude of low frequency fluctuations (fALFF) and regional homogeneity of neural activity (ReHo), are scarce and heterogenous. In this study, we used a longitudinal design to examine the changes in spontaneous neural activity after bariatric surgery (comparing pre- to post-surgery), and to determine whether these changes are related to cardiometabolic variables.
METHODS
The study included 57 participants with severe obesity (mean BMI=43.1 ± 4.3 kg/m
RESULTS
We found a global increase in the fALFF signal with greater increase within dorsolateral prefrontal cortex, precuneus, inferior temporal gyrus, and visual cortex. This effect was more significant 4 months after surgery. The increase within dorsolateral prefrontal cortex, temporal gyrus, and visual cortex was more limited after 12 months and only present in the visual cortex after 24 months. These increases in neural activity measured by fALFF were also significantly associated with the increase in GM density following surgery. Furthermore, the increase in neural activity was significantly related to post-surgery weight loss and improvement in cardiometabolic variables, such as blood pressure. In the independent HCP sample, normal-weight participants had higher global and regional fALFF signals, mainly in dorsolateral/medial frontal cortex, precuneus and middle/inferior temporal gyrus compared to the obese participants. These BMI-related differences in fALFF were associated with the increase in fALFF 4 months post-surgery especially in regions involved in control, default mode and dorsal attention networks.
CONCLUSIONS
Bariatric surgery-induced weight loss and improvement in metabolic factors are associated with widespread global and regional increases in neural activity, as measured by fALFF signal. These findings alongside the higher fALFF signal in normal-weight participants compared to participants with severe obesity in an independent dataset suggest an early recovery in the neural activity signal level after the surgery.

Identifiants

pubmed: 34302967
pii: S1053-8119(21)00694-7
doi: 10.1016/j.neuroimage.2021.118419
pii:
doi:

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

118419

Subventions

Organisme : CIHR
ID : TB2–138776
Pays : Canada

Informations de copyright

Copyright © 2021. Published by Elsevier Inc.

Auteurs

Yashar Zeighami (Y)

Montreal Neurological Institute, Department of Neurology and Neurosurgery, McGill University, Montreal, Canada; Ludmer Centre for Neuroinformatics and Mental Health, McGill University, Montreal, Canada.

Sylvain Iceta (S)

Centre de recherche de l'Institut universitaire de cardiologie et de pneumologie de Québec, Université Laval, Québec, Canada.

Mahsa Dadar (M)

CERVO Brain Research Center, Centre intégré universitaire santé et services sociaux de la Capitale Nationale, Université Laval, Québec, Canada.

Mélissa Pelletier (M)

Centre de recherche de l'Institut universitaire de cardiologie et de pneumologie de Québec, Université Laval, Québec, Canada.

Mélanie Nadeau (M)

Centre de recherche de l'Institut universitaire de cardiologie et de pneumologie de Québec, Université Laval, Québec, Canada.

Laurent Biertho (L)

Département de chirurgie générale, Institut universitaire de cardiologie et de pneumologie de Québec, Université Laval, Québec, Canada.

Annie Lafortune (A)

Département de chirurgie générale, Institut universitaire de cardiologie et de pneumologie de Québec, Université Laval, Québec, Canada.

André Tchernof (A)

Centre de recherche de l'Institut universitaire de cardiologie et de pneumologie de Québec, Université Laval, Québec, Canada.

Stephanie Fulton (S)

Centre de Recherche du CHUM and Montreal Diabetes Research Center, Montreal, QC, Canada.

Alan Evans (A)

Montreal Neurological Institute, Department of Neurology and Neurosurgery, McGill University, Montreal, Canada; Ludmer Centre for Neuroinformatics and Mental Health, McGill University, Montreal, Canada.

Denis Richard (D)

Centre de recherche de l'Institut universitaire de cardiologie et de pneumologie de Québec, Université Laval, Québec, Canada.

Alain Dagher (A)

Montreal Neurological Institute, Department of Neurology and Neurosurgery, McGill University, Montreal, Canada.

Andréanne Michaud (A)

Centre de recherche de l'Institut universitaire de cardiologie et de pneumologie de Québec, Université Laval, Québec, Canada. Electronic address: andreanne.michaud@fsaa.ulaval.ca.

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