Deficient auditory gamma-BOLD coupling in schizophrenia is related to sensory gating deficits

Abstract

Background: Schizophrenia is associated with aberrant gamma band power, hypothesized to reflect imbalance in the excitation-inhibition (E/I) ratio and undermine neural signal efficiency. Relationships between resting-state gamma, E/I balance, and regional hemodynamics from the fMRI BOLD signal are unknown. Methods: We recorded simultaneous EEG-fMRI at rest, with eyes open, in people with schizophrenia (n= 57) and people without a psychiatric diagnosis (n= 46) and identified gamma and aperiodic EEG parameters associated with E/I balance. Measures from all EEG channels were entered into a whole-brain, parametric modulation analysis followed by statistical correction for multiple comparisons. Sensory gating was assessed using the Sensory Gating Inventory, and psychotic symptoms were assessed using the Positive and Negative Syndrome Scale. Results: Across groups, gamma power modestly predicts a steeper aperiodic slope (greater inhibition), without group differences in either gamma power or aperiodic slope. In schizophrenia, gamma-BOLD coupling was reduced in bilateral auditory regions of the superior temporal gyri and inversely correlated with sensory gating deficits and symptom severity. Analysis of the spectral features of scanner sounds revealed distinct peaks in the gamma range, reflecting a rapidly repeating scanner pulse sound present throughout the resting state recording. Conclusion: Regional hemodynamic support for putative inhibitory and excitatory contributions to resting EEG are aberrant in SZ. Deficient gamma coupling to auditory BOLD may reflect impaired gating of fMRI-scanner sound.

Unveiling the hidden electroencephalographical rhythms during development: aperiodic and periodic activity in healthy subjects

“…The exponent is mainly distributed over fronto-central and parietal areas on the midline of the scalp and presents higher posterior values. These findings confirm recent studies in EEG (Hill et al, 2022;Jacob et al, 2021) and MEG (Donoghue et al, 2020a).…”

“…1 in Gómez et al, 2006;Rodríguez-Martínez et al, 2012. Similar patterns have been observed in magnetoencephalography (MEG) (Donohue et al, 2020a;Jacob et al, 2021) and electroencephalography (Hill et al, 2022) studies, showing power concentration for delta at frontal areas, theta at the central midline, alpha in posterior areas, beta centered on sensorimotor areas and gamma bi-temporally (Jacob et al, 2021;Niso et al, 2016). However, a more detailed topographical correlational analysis suggests that canonical topographies are more dominated by the AP PSD component than by the P PSD component, except for alpha and low-beta in which the topography correlational analysis suggests an important contribution of P PSD.…”

“…to neuroanatomical (He et al, 2019;Jacob et al, 2021) and neurochemical (Buzsáki et al, 2012;Cohen Kadosh et al, 2015) changes. While our results align with these findings:…”

“…We analyzed the topographic distribution of the AP component parameters (offset and exponent) and different topographic distributions were observed (Hill et al, 2022;Jacob et al, 2021). The offset and exponent topographies were maintained throughout maturation.…”