Beyond the eye: Cortical differences in primary visual processing in children with cerebral palsy

Abstract

Despite the growing clinical recognition of visual impairments among people with cerebral palsy (CP), very few studies have evaluated the neurophysiology of the visual circuitry. To this end, the primary aim of this investigation was to use magnetoencephalography and beamforming methods to image the relative change in the alpha-beta and gamma occipital cortical oscillations induced by a spatial grating stimulus (e.g., visual contrast) that was viewed by a cohort of children with CP and typically-developing (TD) children. Our results showed that the high-contrast, visual gratings stimuli induced a decrease in alpha-beta (10 - 20 Hz) activity, and an increase in both low (40 - 56 Hz) and high (60 - 72 Hz) gamma oscillations in the occipital cortices. Compared with the TD children, the strength of the frequency specific cortical oscillations were significantly weaker in the children with CP, suggesting that they had deficient processing of the contrast stimulus. Although CP is largely perceived as a musculoskeletal centric disorder, our results fuel the growing impression that there may also be prominent visual processing deficiencies. These visual processing deficits likely impact the ability to perceive visual changes in the environment.

Keywords: Contrast; MEG; Magnetoencephalography; Spatial gratings; Vision; Visual perception.

Fig. 1

MEG visual task. Participants were positioned upright one meter from the stimulus screen and maintained visual fixation on the central red square throughout the task. A static spatial-grating stimulus was presented for 500 ms, with an interstimulus interval (ISI) of 2200–2600 ms. Each participant viewed 120 spatial-grating trials during the experiment. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)

Fig. 2

Time-frequency spectrogram from a gradiometer sensor located over the occipital cortex averaged across all participants. Time (in ms) is denoted on the x-axis, with 0 ms defined as the onset of the spatial grating. Spectral power is expressed as the difference from the baseline period (-350 to -50 ms). Separate components of significantly increased power were seen across the beta (20–36 Hz, 50 – 100 ms), low-gamma (40 – 56 Hz, 50 – 100 ms) and high-gamma (60 – 72 Hz, 50 – 350 ms) frequency bands. In addition, there was a significant decrease in power in the alpha–beta (10 – 20 Hz) frequency band during the latter time window (175 to 475 ms). Permutation testing indicated that all components were significant relative to baseline, p < 0.001, corrected.

Fig. 3

Alpha-beta (10 – 20 Hz) occipital cortical oscillations during the 175 to 475 ms time window. A) The grand-averaged beamformer image shows that the alpha–beta oscillations were centered on the occipital cortices. The pseudo-t color bar is shown to the right of the image. B) Relative response values (pseudo-t) averaged across participants per group, with * indicating p < 0.001. C) The neural time course was extracted from the peak voxel of each hemisphere, and then averaged across hemispheres for each group. The time series of the children with CP are plotted in red, while the TD participants are plotted in blue. Time (ms) is denoted on the x-axis with relative amplitude (%) shown on the y-axis. The visual stimulus was presented at 0 ms (dotted line), and the time–frequency window imaged is shown in the grayed area. The TD group demonstrated a stronger decrease in the alpha–beta occipital cortical oscillations throughout the stimulus presentation compared to the group with CP. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)

Fig. 4

Low-gamma (40 – 56 Hz) occipital responses during the 50 to100 ms time window. A) The grand-averaged beamformer image shows that the gamma increase was centered on the occipital cortices. B) Relative response values (pseudo-t) averaged across participants per group, with * indicating p = 0.01. C) The neural time course was extracted from the peak voxel of each hemisphere, and then averaged across hemispheres for each group. The time series for the group with CP are plotted in red, while the TD group are plotted in blue. Time (ms) is denoted on the x-axis with relative amplitude (%) shown on the y-axis. The visual stimulus was presented at 0 ms (dotted line), and the time–frequency window imaged is shown in the grayed area. The TD group had consistently stronger neural activity when compared with the group with CP. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)

Fig. 5

High-gamma (60 – 72 Hz) occipital responses during the 50 to 350 ms time window. A) The grand-averaged beamformer image shows that the induced change in high-gamma oscillations was centered on the occipital cortices. B) Relative response values (pseudo-t) averaged across participants per group, with * indicating p = 0.01C). The neural time course was extracted from the peak voxel of each hemisphere, and then averaged across hemispheres for each group. The time series of the children with CP are plotted in red, while the TD children are plotted in blue. Time (ms) is denoted on the x-axis with relative amplitude (%) shown on the y-axis. The visual stimulus was presented at 0 ms (dotted line), and the time–frequency window imaged is shown in the grayed area. The TD group had consistently stronger neural activity when compared to the group with CP. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)