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

Shane D McKeon; Maria I Perica; Ashley C Parr; Finnegan J Calabro; Will Foran; Hoby Hetherington; Chan-Hong Moon; Beatriz Luna

doi:10.1016/j.dcn.2024.101373

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

Dev Cogn Neurosci. 2024 Apr:66:101373. doi: 10.1016/j.dcn.2024.101373. Epub 2024 Apr 3.

Authors

Shane D McKeon¹, Maria I Perica², Ashley C Parr³, Finnegan J Calabro⁴, Will Foran⁵, Hoby Hetherington⁶, Chan-Hong Moon⁷, Beatriz Luna⁸

Affiliations

¹ 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.
² The Center for the Neural Basis of Cognition, University of Pittsburgh, PA, USA; Department of Psychology, University of Pittsburgh, PA, USA.
³ The Center for the Neural Basis of Cognition, University of Pittsburgh, PA, USA; Department of Psychiatry, University of Pittsburgh, PA, USA.
⁴ 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.
⁵ Department of Psychiatry, University of Pittsburgh, PA, USA.
⁶ Resonance Research Incorporated, Billerica, MA, USA; Department of Radiology, University of Missouri, Columbia, MO, USA.
⁷ Department of Radiology, University of Pittsburgh, PA, USA.
⁸ 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.

Abstract

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.

Keywords: Adolescent development; Aperiodic activity; EEG; Excitation/Inhibition balance; GABA; Glutamate.