Cortical thickness as a contributor to abnormal oscillations in schizophrenia?

Abstract

Introduction: Although brain rhythms depend on brain structure (e.g., gray and white matter), to our knowledge associations between brain oscillations and structure have not been investigated in healthy controls (HC) or in individuals with schizophrenia (SZ). Observing function-structure relationships, for example establishing an association between brain oscillations (defined in terms of amplitude or phase) and cortical gray matter, might inform models on the origins of psychosis. Given evidence of functional and structural abnormalities in primary/secondary auditory regions in SZ, the present study examined how superior temporal gyrus (STG) structure relates to auditory STG low-frequency and 40 Hz steady-state activity. Given changes in brain activity as a function of age, age-related associations in STG oscillatory activity were also examined.

Methods: Thirty-nine individuals with SZ and 29 HC were recruited. 40 Hz amplitude-modulated tones of 1 s duration were presented. MEG and T1-weighted sMRI data were obtained. Using the sources localizing 40 Hz evoked steady-state activity (300 to 950 ms), left and right STG total power and inter-trial coherence were computed. Time-frequency group differences and associations with STG structure and age were also examined.

Results: Decreased total power and inter-trial coherence in SZ were observed in the left STG for initial post-stimulus low-frequency activity (~ 50 to 200 ms, ~ 4 to 16 Hz) as well as 40 Hz steady-state activity (~ 400 to 1000 ms). Left STG 40 Hz total power and inter-trial coherence were positively associated with left STG cortical thickness in HC, not in SZ. Left STG post-stimulus low-frequency and 40 Hz total power were positively associated with age, again only in controls.

Discussion: Left STG low-frequency and steady-state gamma abnormalities distinguish SZ and HC. Disease-associated damage to STG gray matter in schizophrenia may disrupt the age-related left STG gamma-band function-structure relationships observed in controls.

Keywords: Alpha; Auditory; Gamma; Magnetoencephalography; Schizophrenia; Superior temporal gyrus; Theta.

Fig. 1

Total power family-wise corrected statistical maps for left and right STG (HC > SZ blue, SZ > HC red). Time is shown on the x axis and frequency on the y axis. The − 400 to − 200 ms period shows pre-stimulus total power without baseline subtraction. Insets show left STG post-stimulus low-frequency (4 to 12 Hz activity averaged from 25 to 150 ms) and 40 Hz steady-state (38 to 42 Hz activity averaged from 300 to 950 ms) total power values for each subject. In the inset, for each measure, colored lines show the mean and ± 2 SD.

Fig. 2

Inter-trial coherence family-wise corrected statistical maps for left and right STG (HC > SZ blue, SZ > HC red). Time is shown on the x axis and frequency on the y axis. Insets show left STG post-stimulus low-frequency (4 to 12 Hz activity averaged from 25 to 150 ms) and 40 Hz steady-state (38 to 42 Hz activity averaged from 300 to 950 ms) inter-trial coherence values for each subject. In the inset, for each measure, colored lines show the mean and ± 2 SD.

Fig. 3

Family-wise corrected statistical maps showing correlations between gray-matter cortical thickness and left STG total power (upper panel) and ITC (lower panel) for each group. Time is shown on the x axis and frequency on the y axis. Insets show scatterplots of gray-matter cortical thickness versus left STG low-frequency (4 to 16 Hz activity averaged from 25 to 150 ms) and 40 Hz ITC and total power (38 to 42 Hz activity averaged from 300 to 950 ms) for each group, with the R² values showing the percent variance explained.

Fig. 4

Family-wise corrected statistical maps showing correlations between age and left STG total power (upper panel) and ITC (lower panel) for each group. Time is shown on the x axis and frequency on the y axis. The − 400 to − 200 ms period shows pre-stimulus total power without baseline subtraction. Insets show scatterplots of age versus left STG low-frequency (4 to 16 Hz activity averaged from 25 to 150 ms) and 40 Hz ITC and total power (38 to 42 Hz activity averaged from 300 to 950 ms) for each group, with the R² values showing the percent variance explained.