Resting-state oscillatory dynamics in sensorimotor cortex in benign epilepsy with centro-temporal spikes and typical brain development

Abstract

Benign Epilepsy with Centro-Temporal Spikes (BECTS) is a common childhood epilepsy associated with deficits in several neurocognitive domains. Neurophysiological studies in BECTS often focus on centro-temporal spikes, but these correlate poorly with morphology and cognitive impairments. To better understand the neural profile of BECTS, we studied background brain oscillations, thought to be integrally involved in neural network communication, in sensorimotor areas. We used independent component analysis of temporally correlated sources on magnetoencephalography recordings to assess sensorimotor resting-state network activity in BECTS patients and typically developing controls. We also investigated the variability of oscillatory characteristics within focal primary motor cortex (M1), localized with a separate finger abduction task. We hypothesized that background oscillations would differ between patients and controls in the sensorimotor network but not elsewhere, especially in the beta band (13-30 Hz) because of its role in network communication and motor processing. The results support our hypothesis: in the sensorimotor network, patients had a greater variability in oscillatory amplitude compared to controls, whereas there was no difference in the visual network. Network measures did not correlate with age. The coefficient of variation of resting M1 peak frequency correlated negatively with age in the beta band only, and was greater than average for a number of patients. Our results point toward a "disorganized" functional sensorimotor network in BECTS, supporting a neurodevelopmental delay in sensorimotor cortex. Our findings further suggest that investigating the variability of oscillatory peak frequency may be a useful tool to investigate deficits of disorganization in neurodevelopmental disorders.

Keywords: benign epilepsy with centro-temporal spikes; beta-band oscillations; magnetoencephalography; resting-state networks; sensorimotor cortex.

Figure 1

Sensorimotor (A, C, E) and visual (B, D, F) network independent components of temporally correlated oscillatory activity in the beta band (13–30 Hz) generated for the whole group (N=33). (A, B) Component images transformed to MNI space. Images show absolute ICA weights (in A.U.) thresholded at 0.5. (C, D) Group average ICA resting network component amplitude SDs (in A.U.). Error bars represent SDs of group mean. *P<0.05; n.s. = P>0.05. (E, F) Correlations of individual SDs with age. Data points represent subject's bootstrapped SD means with 95% confidence interval. [Color figure can be viewed in the online issue, which is available at http://wileyonlinelibrary.com.]

Figure 2

Group average t statistic images of the 60–90 Hz Movement‐Related Gamma Response paired t images obtained from the finger‐abduction data. Each panel shows a superior view of a group and finger‐abduction hand, as indicated. Insets are coronal sections at y=−10 mm. The images are normalized to the MNI template and thresholded at P=0.001 (voxel‐based corrected).

Figure 3

Group average CV oscillatory activity in motor cortex. Results are shown for six frequency bands of (A) amplitude and (B) peak frequency. Frequency bands are indicated by their Greek symbols (gamma 1/2/3 = 30–50 Hz, 50–90 Hz, 90–150 Hz). (C, D) Histograms of oscillatory peak frequency in motor cortex collapsed over groups. (C) The theta band (6–8 Hz) shows a non‐normal distribution skewed toward the lower frequencies. (D) The beta band (13–30 Hz) follows a normal distribution. (E) Negative correlation of motor cortex beta‐band peak frequency CV with age. All results are collapsed over hemispheres. Error bars represent SEM. *P<0.05. [Color figure can be viewed in the online issue, which is available at http://wileyonlinelibrary.com.]

Figure 4

Correlations of neural measures with neurocognitive tests for motor skills (MABC balance, top panels) and language skills (WIAT word reading, bottom panels). Correlations are displayed for sensorimotor network SD, visual network SD, and motor cortex (M1) beta‐band peak frequency CV. [Color figure can be viewed in the online issue, which is available at http://wileyonlinelibrary.com.]