Children with cerebral palsy have altered oscillatory activity in the motor and visual cortices during a knee motor task

Abstract

The neuroimaging literature on cerebral palsy (CP) has predominantly focused on identifying structural aberrations within the white matter (e.g., fiber track integrity), with very few studies examining neural activity within the key networks that serve the production of motor actions. The current investigation used high-density magnetoencephalography to begin to fill this knowledge gap by quantifying the temporal dynamics of the alpha and beta cortical oscillations in children with CP (age = 15.5 ± 3 years; GMFCS levels II-III) and typically developing (TD) children (age = 14.1 ± 3 years) during a goal-directed isometric target-matching task using the knee joint. Advanced beamforming methods were used to image the cortical oscillations during the movement planning and execution stages. Compared with the TD children, our results showed that the children with CP had stronger alpha and beta event-related desynchronization (ERD) within the primary motor cortices, premotor area, inferior parietal lobule, and inferior frontal gyrus during the motor planning stage. Differences in beta ERD amplitude extended through the motor execution stage within the supplementary motor area and premotor cortices, and a stronger alpha ERD was detected in the anterior cingulate. Interestingly, our results also indicated that alpha and beta oscillations were weaker in the children with CP within the occipital cortices and visual MT area during movement execution. These altered alpha and beta oscillations were accompanied by slower reaction times and substantial target matching errors in the children with CP. We also identified that the strength of the alpha and beta ERDs during the motor planning and execution stages were correlated with the motor performance. Lastly, our regression analyses suggested that the beta ERD within visual areas during motor execution primarily predicted the amount of motor errors. Overall, these data suggest that uncharacteristic alpha and beta oscillations within visuomotor cortical networks play a prominent role in the atypical motor actions exhibited by children with CP.

Keywords: Isometric; Lower extremity; Magnetoencephalography; Vision.

Fig. 1

A) Depiction of the custom-built pneumatic force transducer that is positioned just proximal to the lateral malleolus of the child. B) The isometric knee extension force generated by the child animates the yellow box to ascend vertically to match the green target box. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)

Fig. 2

(A) Time-frequency spectrogram for a representative typically-developing participant. Frequency (Hz) is shown on the y-axis and time (s) is denoted on the x-axis, with 0.0 s defined as the onset of the isometric force. The event-related spectral changes during the isometric knee task are expressed as the percent difference from baseline (− 3.6 to − 3.1 s), with the scale shown to the far right. The MEG sensor with the greatest response amplitude is shown, which was located near the sensorimotor cortices and contralateral to the leg generating the force. As can be discerned, there was a strong decrease in the alpha (8–14 Hz) and beta (16–24 Hz) bands that started about 0.5 s prior to the initiation of the isometric force. The alpha band decrease (desynchronization) ceased at about 0.8 s, while the beta band activity was sustained while the participant attempted to match the prescribed targets. (B) A 2D map of the sensor array is shown to illustrate the gradiometer sensors where significant alpha (8–14 Hz) and beta (16–24 Hz) responses were detected, with a color legend to the far right. As shown, significant beta and alpha responses clustered around the sensorimotor cortices, and stretched toward the occipital cortices, with the beta-only sensors clustering anteriorly (near motor regions) and alpha-only sensors clustering posteriorly (near occipital cortex). Between these two extremes, many sensors contained both significant alpha and beta responses. Note that the black sensor-chip was not included in the sensor-level statistical analyses, as it was bad in several participants.

Fig. 3

Statistical parametric maps (SPMs) of the group effect for alpha activity (8–14 Hz) during the motor planning stage (− 0.5 to 0 s) and motor execution stage (0 to 0.5 s) of the isometric knee target force matching task. The images have been thresholded at (P < 0.01, corrected) and are displayed following the radiological convention (R = L). As shown in panel A, there were wide spread significant differences in alpha event-related desynchronization (ERD) responses between the children with cerebral palsy and the typically-developing children within the bilateral primary motor cortices, left pre-motor cortices, right inferior parietal lobule and right premotor cortices during the planning of a motor action. All of these results indicated that the children with cerebral palsy had a stronger alpha ERD within the respective cortical areas during the motor planning stage. As shown in panel B, there were significant alpha differences in the occipital cortices bilaterally between the children with cerebral palsy and the typically developing children during movement execution. These results indicated that the children with cerebral palsy had a weaker alpha ERD within the occipital cortices during the motor execution stage.

Fig. 4

Statistical parametric maps (SPMs) of the group effect for beta oscillations (16–24 Hz) during the motor planning (− 0.5 to 0 s) and execution stages (0 to 0.5 s) of the isometric knee target force matching task. The images have been thresholded at (P < 0.01, corrected) and are displayed following the radiological convention (R = L). As shown in panel A, there were significant differences in beta event-related desynchronization (ERD) responses between the children with cerebral palsy and the typically developing children within the leg area of the primary motor cortices, left inferior frontal gyrus, and left premotor cortex while planning the movements. These results indicated that the children with cerebral palsy had a stronger beta ERD within the respective cortical areas during the motor planning stage. As shown in panel B, there were significant beta differences between the children with cerebral palsy and the typically developing children within the supplementary motor area and left premotor cortices while executing the movement. These results indicated that the children with cerebral palsy had a stronger beta ERD within the respective cortical areas during the motor execution stage.

Fig. 5

Statistical parametric maps (SPMs) of the group effect for beta oscillatory activity (16–24 Hz) in the occipital cortices during the motor execution stage (0 to 0.5 s). This image has been thresholded at (P < 0.01, corrected) and is displayed following the radiological convention (R = L). As shown, children with cerebral palsy had a weaker beta event-related desynchronization relative to typically developing children within the occipital cortices and visual MT area.