Aperiodic EEG and 7T MRSI evidence for maturation of E/I balance supporting the development of working memory through adolescence.

Adolescent development Aperiodic activity EEG Excitation/Inhibition balance GABA Glutamate

Journal

Developmental cognitive neuroscience
ISSN: 1878-9307
Titre abrégé: Dev Cogn Neurosci
Pays: Netherlands
ID NLM: 101541838

Informations de publication

Date de publication:
03 Apr 2024
Historique:
received: 12 02 2024
revised: 01 04 2024
accepted: 02 04 2024
medline: 5 4 2024
pubmed: 5 4 2024
entrez: 4 4 2024
Statut: aheadofprint

Résumé

Adolescence has been hypothesized to be a critical period for the development of human association cortex and higher-order cognition. A defining feature of critical period development is a shift in the excitation: inhibition (E/I) balance of neural circuitry, however how changes in E/I may enhance cortical circuit function to support maturational improvements in cognitive capacities is not known. Harnessing ultra-high field 7 T MR spectroscopy and EEG in a large, longitudinal cohort of youth (N = 164, ages 10-32 years old, 347 neuroimaging sessions), we delineate biologically specific associations between age-related changes in excitatory glutamate and inhibitory GABA neurotransmitters and EEG-derived measures of aperiodic neural activity reflective of E/I balance in prefrontal association cortex. Specifically, we find that developmental increases in E/I balance reflected in glutamate:GABA balance are linked to changes in E/I balance assessed by the suppression of prefrontal aperiodic activity, which in turn facilitates robust improvements in working memory. These findings indicate a role for E/I-engendered changes in prefrontal signaling mechanisms in the maturation of cognitive maintenance. More broadly, this multi-modal imaging study provides evidence that human association cortex undergoes physiological changes consistent with critical period plasticity during adolescence.

Identifiants

pubmed: 38574406
pii: S1878-9293(24)00034-3
doi: 10.1016/j.dcn.2024.101373
pii:
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

101373

Informations de copyright

Copyright © 2024. Published by Elsevier Ltd.

Déclaration de conflit d'intérêts

Declaration of Competing Interest The authors declare no competing interests.

Auteurs

Shane D McKeon (SD)

Department of Bioengineering, University of Pittsburgh, PA, USA; The Center for the Neural Basis of Cognition, University of Pittsburgh, PA, USA. Electronic address: sdm63@pitt.edu.

Maria I Perica (MI)

The Center for the Neural Basis of Cognition, University of Pittsburgh, PA, USA; Department of Psychology, University of Pittsburgh, PA, USA.

Ashley C Parr (AC)

The Center for the Neural Basis of Cognition, University of Pittsburgh, PA, USA; Department of Psychiatry, University of Pittsburgh, PA, USA.

Finnegan J Calabro (FJ)

Department of Bioengineering, University of Pittsburgh, PA, USA; The Center for the Neural Basis of Cognition, University of Pittsburgh, PA, USA; Department of Psychiatry, University of Pittsburgh, PA, USA.

Will Foran (W)

Department of Psychiatry, University of Pittsburgh, PA, USA.

Hoby Hetherington (H)

Resonance Research Incorporated, Billerica, MA, USA; Department of Radiology, University of Missouri, Columbia, MO, USA.

Chan-Hong Moon (CH)

Department of Radiology, University of Pittsburgh, PA, USA.

Beatriz Luna (B)

The Center for the Neural Basis of Cognition, University of Pittsburgh, PA, USA; Department of Psychiatry, University of Pittsburgh, PA, USA. Electronic address: lunab@upmc.edu.

Classifications MeSH