Hand Motor Actions of Children With Cerebral Palsy Are Associated With Abnormal Sensorimotor Cortical Oscillations

Abstract

Background. The neuroimaging literature on cerebral palsy (CP) has predominantly focused on identifying the structural aberrations (eg, fiber track integrity), with very few studies examining neural activity within the key networks that serve the production of hand movements. Objective. We aimed to start to fill this knowledge gap by using magnetoencephalographic brain imaging to quantify the temporal dynamics of the sensorimotor oscillations during a hand motor action. Methods: Children with CP (n = 12; MACS [Manual Abilities Classification System] levels I-III) and typically developing (TD) children (n = 26) performed an arrow-based version of the Eriksen flanker task where a button press was performed with either the second or third digit of the right hand depending on the arrow’s direction. Results: Overall, the children with CP were less accurate and had slower reaction times compared with the TD children. These behavioral differences were closely linked with aberrant sensorimotor cortical oscillations seen in the children with CP. Compared with the TD children, the children with CP had a weaker gamma (68-82 Hz) response during motor execution and a weaker post-movement beta rebound (PMBR; 14-26 Hz) response on movement termination. Moreover, we observed a significant correlation between the amplitude of the gamma and PMBR with reaction time, with weaker gamma and PMBR responses being linked with slower reaction times. Conclusions: Overall, these results suggest that aberrations in motor-related gamma and beta cortical oscillations are associated with the impaired hand motor actions seen in children with CP.

Spinal Cord Microstructural Changes are Connected with the Aberrant Sensorimotor Cortical Oscillatory Activity in Adults with Cerebral Palsy

“…Our results also revealed that the PMBR was weaker for the adults with CP. This result is well aligned with our prior work, which has shown that the PMBR is weaker in youth with CP compared with controls when performing the same Eriksen anker task 50 . The PMBR is thought to re ect afferent sensory feedback upon completion of the motor action, 31,32 although other possible functions cannot be ruled out [33][34][35][36][37] .…”

“…In fact, only one study to date has quanti ed the strength of the PMBR and gamma ERS during upper extremity movements, and this study indicated weaker responses in youth with CP during performance of an arrow-based version of the Eriksen anker task 50 . Although these investigations have advanced our understanding of the impact of CP on sensorimotor cortical oscillations, we still have major knowledge gaps in our understanding of these cortical oscillations, especially in adults with CP, despite the overwhelming clinical impression that there is a decline in hand motor function throughout adulthood.…”

“…This went against our initial hypothesis, as our previous studies have repeatedly shown that the gamma ERS is reduced in youth with CP during both lower extremity tasks 47 and the same Eriksen Flanker task. 50 Prior pharmaco-MEG studies have shown that a N-methyl-Daspartate (NMDA) receptor antagonist can result in increased gamma ERS strength, while GABA agonists have no such effect 67,68,82 . Potentially, the amplitude differences seen across the respective studies for the youth and adults with CP might be NMDA receptor dependent.…”

“…We utilized the high temporal and spatial precision of MEG to investigate motor-related oscillations associated with performance of an arrow-based version of the Eriksen Flanker task. This cognitive-motor task was chosen as prior studies have demonstrated that it's associated with robust beta and gamma oscillatory activity 44,50 . Secondarily, we utilized MRI to investigate how the spinal cord microstructure may be related to the strength of sensorimotor cortical activity.…”

Stronger proprioceptive BOLD-responses in the somatosensory cortices reflect worse sensorimotor function in adolescents with and without cerebral palsy

“…In addition, Piitulainen et al (2018) suggested the impaired excitation-inhibition balance and Riquelme and Montoya (2010) enhanced excitability in the somatosensory cortices in CP. Moreover, post-movement beta rebound amplitude in the SM1 cortex correlates positively with higher GABA levels in the SM1 cortex ( Gaetz et al, 2011 , Cheng et al, 2017 ), and is weaker in individuals with CP participants ( Hoffman et al, 2019 ) and especially in their more affected side ( Pihko et al, 2014 ). Animal models of CP show hindered GABAergic inhibition and increased responsiveness of the SI cortex ( Coq et al, 2008 ) and post-mortem studies of neonates report loss of GABAergic neurons associated with the perinatal brain injury ( Robinson et al, 2006 , Stolp et al, 2019 ).…”