Early-in-life isoflurane exposure alters resting-state functional connectivity in juvenile non-human primates.


Journal

British journal of anaesthesia
ISSN: 1471-6771
Titre abrégé: Br J Anaesth
Pays: England
ID NLM: 0372541

Informations de publication

Date de publication:
12 2023
Historique:
received: 28 02 2023
revised: 20 07 2023
accepted: 26 07 2023
pmc-release: 01 12 2024
medline: 15 11 2023
pubmed: 16 9 2023
entrez: 15 9 2023
Statut: ppublish

Résumé

Clinical studies suggest that anaesthesia exposure early in life affects neurobehavioural development. We designed a non-human primate (NHP) study to evaluate cognitive, behavioural, and brain functional and structural alterations after isoflurane exposure during infancy. These NHPs displayed decreased close social behaviour and increased astrogliosis in specific brain regions, most notably in the amygdala. Here we hypothesise that resting-state functional connectivity MRI can detect alterations in connectivity of brain areas that relate to these social behaviours and astrogliosis. Imaging was performed in 2-yr-old NHPs under light anaesthesia, after early-in-life (postnatal days 6-12) exposure to 5 h of isoflurane either one or three times, or to room air. Brain images were segmented into 82 regions of interest; the amygdala and the posterior cingulate cortex were chosen for a seed-based resting-state functional connectivity MRI analysis. We found differences between groups in resting-state functional connectivity of the amygdala and the auditory cortices, medial premotor cortex, and posterior cingulate cortex. There were also alterations in resting-state functional connectivity between the posterior cingulate cortex and secondary auditory, polar prefrontal, and temporal cortices, and the anterior insula. Relationships were identified between resting-state functional connectivity alterations and the decrease in close social behaviour and increased astrogliosis. Early-in-life anaesthesia exposure in NHPs is associated with resting-state functional connectivity alterations of the amygdala and the posterior cingulate cortex with other brain regions, evident at the juvenile age of 2 yr. These changes in resting-state functional connectivity correlate with the decrease in close social behaviour and increased astrogliosis. Using resting-state functional connectivity MRI to study the neuronal underpinnings of early-in-life anaesthesia-induced behavioural alterations could facilitate development of a biomarker for anaesthesia-induced developmental neurotoxicity.

Sections du résumé

BACKGROUND
Clinical studies suggest that anaesthesia exposure early in life affects neurobehavioural development. We designed a non-human primate (NHP) study to evaluate cognitive, behavioural, and brain functional and structural alterations after isoflurane exposure during infancy. These NHPs displayed decreased close social behaviour and increased astrogliosis in specific brain regions, most notably in the amygdala. Here we hypothesise that resting-state functional connectivity MRI can detect alterations in connectivity of brain areas that relate to these social behaviours and astrogliosis.
METHODS
Imaging was performed in 2-yr-old NHPs under light anaesthesia, after early-in-life (postnatal days 6-12) exposure to 5 h of isoflurane either one or three times, or to room air. Brain images were segmented into 82 regions of interest; the amygdala and the posterior cingulate cortex were chosen for a seed-based resting-state functional connectivity MRI analysis.
RESULTS
We found differences between groups in resting-state functional connectivity of the amygdala and the auditory cortices, medial premotor cortex, and posterior cingulate cortex. There were also alterations in resting-state functional connectivity between the posterior cingulate cortex and secondary auditory, polar prefrontal, and temporal cortices, and the anterior insula. Relationships were identified between resting-state functional connectivity alterations and the decrease in close social behaviour and increased astrogliosis.
CONCLUSIONS
Early-in-life anaesthesia exposure in NHPs is associated with resting-state functional connectivity alterations of the amygdala and the posterior cingulate cortex with other brain regions, evident at the juvenile age of 2 yr. These changes in resting-state functional connectivity correlate with the decrease in close social behaviour and increased astrogliosis. Using resting-state functional connectivity MRI to study the neuronal underpinnings of early-in-life anaesthesia-induced behavioural alterations could facilitate development of a biomarker for anaesthesia-induced developmental neurotoxicity.

Identifiants

pubmed: 37714750
pii: S0007-0912(23)00444-0
doi: 10.1016/j.bja.2023.07.031
pmc: PMC10687619
pii:
doi:

Substances chimiques

Isoflurane CYS9AKD70P

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

1030-1042

Subventions

Organisme : NIH HHS
ID : P51 OD011092
Pays : United States

Commentaires et corrections

Type : CommentIn

Informations de copyright

Copyright © 2023 British Journal of Anaesthesia. Published by Elsevier Ltd. All rights reserved.

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Auteurs

Viola Neudecker (V)

Department of Anesthesiology, Columbia University Medical Center, New York, NY, USA.

Jose F Perez-Zoghbi (JF)

Department of Anesthesiology, Columbia University Medical Center, New York, NY, USA.

Oscar Miranda-Domínguez (O)

Clinical Behavioral Neuroscience Masonic Institute for the Developing Brain, Minneapolis, MN, USA.

Katie J Schenning (KJ)

Department of Anesthesiology and Perioperative Medicine, Oregon Health & Science University, Portland, OR, USA.

Julian Sb Ramirez (JS)

Department of Behavioral Neuroscience, Oregon Health & Science University, Portland, OR, USA.

A J Mitchell (AJ)

Department of Behavioral Neuroscience, Oregon Health & Science University, Portland, OR, USA.

Anders Perrone (A)

Clinical Behavioral Neuroscience Masonic Institute for the Developing Brain, Minneapolis, MN, USA.

Eric Earl (E)

Data Science and Sharing Team, National Institute of Mental Health, Bethesda, MD, USA.

Sam Carpenter (S)

Department of Behavioral Neuroscience, Oregon Health & Science University, Portland, OR, USA.

Lauren D Martin (LD)

Animal Resources & Research Support, Oregon National Primate Research Center, Oregon Health & Science University, Beaverton, OR, USA.

Kristine Coleman (K)

Division of Neuroscience, Oregon National Primate Research Center, Oregon Health & Science University, Portland, OR, USA.

Martha Neuringer (M)

Division of Neuroscience, Oregon National Primate Research Center, Oregon Health & Science University, Portland, OR, USA.

Christopher D Kroenke (CD)

Division of Neuroscience, Oregon National Primate Research Center, Oregon Health & Science University, Portland, OR, USA; Advanced Imaging Research Center, Oregon Health & Science University, Portland, OR, USA.

Gregory A Dissen (GA)

Division of Neuroscience, Oregon National Primate Research Center, Oregon Health & Science University, Portland, OR, USA.

Damien A Fair (DA)

Clinical Behavioral Neuroscience Masonic Institute for the Developing Brain, Minneapolis, MN, USA.

Ansgar M Brambrink (AM)

Department of Anesthesiology, Columbia University Medical Center, New York, NY, USA. Electronic address: amb2457@cumc.columbia.edu.

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