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

ABSTRACT: Cerebral palsy (CP) is a motor disorder where the motor defects are partly due to impaired proprioception. We studied cortical proprioceptive responses and sensorimotor performance in adolescents with CP and their typically-developed (TD) peers. Passive joint movements were used to stimulate proprioceptors during functional magnetic resonance imaging (fMRI) session to quantify the proprioceptive responses whose associations to behavioral sensorimotor performance were also examined. Twenty-three TD (15 females, age: mean ± standard deviation 14.2 ± 2.4 years) and 18 CP (12 females, age: mean ± standard deviation, 13.8 ± 2.3 years; 12 hemiplegic, 6 diplegic) participants were included in this study. Participants' index fingers and ankles were separately stimulated at 3 Hz and 1 Hz respectively with pneumatic movement actuators. Regions-of-interest were used to quantify BOLD-responses from the primary sensorimotor (SM1) and secondary (SII) somatosensory cortices and were compared across the groups. Associations between responses strengths and sensorimotor performance measures were also examined. Proprioceptive responses were stronger for the individuals with CP compared to their TD peers in SM1 (p < 0.001) and SII (p < 0.05) cortices contralateral to their more affected index finger. The ankle responses yielded no significant differences between the groups. The CP group had worse sensorimotor performance for hands and feet (p < 0.001). Stronger responses to finger stimulation in the dominant SM1 (p < 0.001) and both dominant and non-dominant SII (p < 0.01, p < 0.001) cortices were associated with the worse hand sensorimotor performance across all participants. Worse hand function was associated with stronger cortical activation to the proprioceptive stimulation. This association was evident both in adolescents with CP and their typically-developed controls, thus it likely reflects both clinical factors and normal variation in the sensorimotor function. The specific mechanisms need to be clarified in future studies.

SUBMITTER: Nurmi T

PROVIDER: S-EPMC8411230 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Key pointsIndividuals with cerebral palsy (CP) have a reduced somatosensory cortical response Somatosensory cortical response strength decreases from adolescence to early adulthood Somatosensory cortical responses in youth with CP are similar to adult controls Individuals with CP may have aberrant maturation of the somatosensory system ABSTRACT: Numerous studies have documented tactile and proprioceptive deficits in children with cerebral palsy (CP) and linked these with weaker somatosensory cortical activity. However, whether such aberrations in somatosensory processing extend and/or progress into adulthood remains poorly understood. In the current study, we used magnetoencephalography (MEG) to investigate the primary somatosensory responses in a sample of individuals with CP (N = 42; age = 9-28 years) and a cohort of healthy controls (N = 23; age range = 11-23 years). Briefly, transient electrical stimulation was applied to the right tibial nerve, and standardized low-resolution brain electromagnetic tomography (sLORETA) was used to image the dynamic somatosensory cortical response. We found that the strength of somatosensory cortical activity within the 112-252 ms time window was significantly reduced in the individuals with CP compared with the healthy controls (HC = 286.53 ± 30.51, 95% CI [226.74, 346.32]; CP = 208.30 ± 19.66,CI [169.77, 246.83], P = 0.0126). These results corroborate previous findings of aberrant somatosensory cortical activity in individuals with CP. Our results also suggest that the somatosensory cortical activity tends to become weaker with age, with a similar rate of neurophysiological change in individuals with CP and healthy controls (P = 0.8790). Visualization of regression models fitted to the data imply that youth with CP may have somatosensory cortical activity similar to adult controls. These findings suggest that some individuals with CP exhibit an aberrant developmental trajectory of their somatosensory system.

Project description:BACKGROUND:It is important to understand the motor deficits of children with Cerebral Palsy (CP). Our understanding of this motor disorder can be enriched by computational models of motor control. One crucial stage in generating movement involves combining uncertain information from different sources, and deficits in this process could contribute to reduced motor function in children with CP. Healthy adults can integrate previously-learned information (prior) with incoming sensory information (likelihood) in a close-to-optimal way when estimating object location, consistent with the use of Bayesian statistics. However, there are few studies investigating how children with CP perform sensorimotor integration. We compare sensorimotor estimation in children with CP and age-matched controls using a model-based analysis to understand the process. METHODS AND FINDINGS:We examined Bayesian sensorimotor integration in children with CP, aged between 5 and 12 years old, with Gross Motor Function Classification System (GMFCS) levels 1-3 and compared their estimation behavior with age-matched typically-developing (TD) children. We used a simple sensorimotor estimation task which requires participants to combine probabilistic information from different sources: a likelihood distribution (current sensory information) with a prior distribution (learned target information). In order to examine sensorimotor integration, we quantified how participants weighed statistical information from the two sources (prior and likelihood) and compared this to the statistical optimal weighting. We found that the weighing of statistical information in children with CP was as statistically efficient as that of TD children. CONCLUSIONS:We conclude that Bayesian sensorimotor integration is not impaired in children with CP and therefore, does not contribute to their motor deficits. Future research has the potential to enrich our understanding of motor disorders by investigating the stages of motor processing set out by computational models. Therapeutic interventions should exploit the ability of children with CP to use statistical information.

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

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