Neurophysiological abnormalities in the sensorimotor cortices during the motor planning and movement execution stages of children with cerebral palsy

A considerable amount of research effort has been placed on cataloging and quantifying the impairments seen in the final motor output of children with cerebral palsy (CP). These efforts have revealed that children with CP may present a wide variety of musculoskeletal impairments, and this has promoted the idea that the movement deficits seen in these children primarily reside in the musculoskeletal machinery. Unfortunately, treatment strategies that have focused on musculoskeletal impairments (i.e. surgical and strength training) have had mixed results, and their outcomes have not been clearly successful.1,2 More recent therapeutic trends have shifted toward a task-orientated approach that focuses on the neurological impairments first, with the musculoskeletal impairments resulting from the neurological insult as a secondary issue. This approach places greater emphasis on the neurological basis for the impaired timing of the muscle activation patterns that result in co-contractions, spasticity, and weakness.3 Despite this new paradigm shift, there is still only limited insight into the neurological foundation for how children plan and execute their movements. Neural oscillatory activity in the sensorimotor cortices has received significant attention in electrophysiological studies of the motor system because it has been linked to the processes that occur during the planning and execution stages of movements. A plethora of electroencephalography (EEG) and magnetoencephalography (MEG) experiments have shown that cortical oscillatory activity across the sensorimotor cortices decreases in the beta frequency range (15–30Hz) before the onset of movement.4–8 This decrease in the power of the beta band frequency, commonly termed beta desynchronization, is thought to reflect task-related changes in the firing rate of local populations of neurons as they begin to prepare for the specific demands of the pending movement. The consensus is that this beta event-related desynchronization (ERD) is related to the formulation of a motor plan, because it occurs well before the onset of movement and is influenced by the certainty of the movement pattern to be performed.4–8 Invasive electrocorticographic (ECoG) studies have also shown that the beta ERD is followed by an increase (or synchronization) in the high gamma frequency range (~50Hz) as the motor plan is executed.9 This high frequency activity is restricted to a smaller population of neurons within the primary motor cortex and appears to follow the homuncular organization common in rolandic regions. Only within the past 5 years have MEG studies reported gamma-band neural oscillatory activity during movement, and the few studies that exist have shown that gamma band oscillations are concentrated in the pre-central gyrus and closely yoked to the onset of muscular activation.5,6,10 Based on these initial findings, it has been proposed that the rapid and temporally succinct gamma response reflects the motor command execution signal. While the central role of beta and gamma neural oscillatory activity before and at the movement onset is well appreciated, there has been limited effort to use this knowledge to more precisely characterize the neurological basis of motor deficits seen in children with CP. Applying this knowledge has the potential to elucidate whether children with CP have motor planning deficits, or whether their poor motor control partly resides in the feed-forward motor execution command, or whether both of these alternatives play a significant role. In this investigation, we used high-density MEG and beamforming methodology to examine the stage-like neural oscillatory activity in the sensorimotor cortices of children with CP, and children with typical development as they initiated the extension of their knee joint to a physical target. The knee joint was selected for this investigation because it is well recognized as a critical factor that limits the mobility of children with CP.11 Our primary hypothesis was that children with CP would have altered beta ERD during the motor planning stage. Our secondary hypothesis was that children with CP would have an altered gamma ERS at the onset of the movement.