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Influence of the corticospinal tract wiring pattern on sensorimotor functional connectivity and clinical correlates of upper limb function in unilateral cerebral palsy.

ABSTRACT: In children with unilateral cerebral palsy (uCP), the corticospinal tract (CST)-wiring patterns may differ (contralateral, ipsilateral or bilateral), partially determining motor deficits. However, the impact of such CST-wiring on functional connectivity remains unknown. Here, we explored resting-state sensorimotor functional connectivity in 26 uCP with periventricular white matter lesions (mean age (standard deviation): 12.87?m (±4.5), CST wiring: 9 contralateral, 9 ipsilateral, 6 bilateral) compared to 60 healthy controls (mean age (standard deviation): 14.54 (±4.8)), and between CST-wiring patterns. Functional connectivity from each M1 to three bilateral sensorimotor regions of interest (primary sensory cortex, dorsal and ventral premotor cortex) and the supplementary motor area was compared between groups (controls vs. uCP; and controls vs. each CST-wiring group). Seed-to-voxel analyses from bilateral M1 were compared between groups. Additionally, relations with upper limb motor deficits were explored. Aberrant sensorimotor functional connectivity seemed to be CST-dependent rather than specific from all the uCP population: in the dominant hemisphere, the contralateral CST group showed increased connectivity between M1 and premotor cortices, whereas the bilateral CST group showed higher connectivity between M1 and somatosensory association areas. These results suggest that functional connectivity of the sensorimotor network is CST-wiring-dependent, although the impact on upper limb function remains unclear.

SUBMITTER: Simon-Martinez C

PROVIDER: S-EPMC6547689 | biostudies-literature | 2019 Jun

REPOSITORIES: biostudies-literature

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Influence of the corticospinal tract wiring pattern on sensorimotor functional connectivity and clinical correlates of upper limb function in unilateral cerebral palsy.

Simon-Martinez Cristina C Jaspers Ellen E Alaerts Kaat K Ortibus Els E Balsters Joshua J Mailleux Lisa L Blommaert Jeroen J Sleurs Charlotte C Klingels Katrijn K Amant Frédéric F Uyttebroeck Anne A Wenderoth Nicole N Feys Hilde H

Scientific reports 20190603 1

In children with unilateral cerebral palsy (uCP), the corticospinal tract (CST)-wiring patterns may differ (contralateral, ipsilateral or bilateral), partially determining motor deficits. However, the impact of such CST-wiring on functional connectivity remains unknown. Here, we explored resting-state sensorimotor functional connectivity in 26 uCP with periventricular white matter lesions (mean age (standard deviation): 12.87 m (±4.5), CST wiring: 9 contralateral, 9 ipsilateral, 6 bilateral) com ...[more]

PMID: 31160679

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Project description:Brain lesion characteristics (timing, location, and extent) and the type of corticospinal tract (CST) wiring have been proposed as determinants of upper limb (UL) motor function in unilateral cerebral palsy (uCP), yet an investigation of the relative combined impact of these factors on both motor and sensory functions is still lacking. Here, we first investigated whether structural brain lesion characteristics could predict the underlying CST wiring and we explored the role of CST wiring and brain lesion characteristics to predict UL motor and sensory functions in uCP. Fifty-two participants with uCP (mean age (SD): 11 y and 3 m (3 y and 10 m)) underwent a single-pulse Transcranial Magnetic Stimulation session to determine CST wiring between the motor cortex and the more affected hand (n = 17 contralateral, n = 19 ipsilateral, and n = 16 bilateral) and an MRI to determine lesion timing (n = 34 periventricular (PV) lesion, n = 18 corticosubcortical (CSC) lesion), location, and extent. Lesion location and extent were evaluated with a semiquantitative scale. A standardized protocol included UL motor (grip strength, unimanual capacity, and bimanual performance) and sensory measures. A combination of lesion locations (damage to the PLIC and frontal lobe) significantly contributed to differentiate between the CST wiring groups, reclassifying the participants in their original group with 57% of accuracy. Motor and sensory functions were influenced by each of the investigated neurological factors. However, multiple regression analyses showed that motor function was predicted by the CST wiring (more preserved in individuals with contralateral CST (p < 0.01)), lesion extent, and damage to the basal ganglia and thalamus. Sensory function was predicted by the combination of a large and later lesion and an ipsilateral or bilateral CST wiring, which led to increased sensory deficits (p < 0.05). These novel insights contribute to a better understanding of the underlying pathophysiology of UL function and may be useful to delineate individualized treatment strategies.

Project description:Background: In children with unilateral cerebral palsy (uCP) virtually nothing is known on the relation between structural brain damage and upper limb (UL) kinematics quantified with three-dimensional movement analysis (3DMA). This explorative study aimed to (1) investigate differences in UL kinematics between children with different lesion timings, i.e., periventricular white matter (PWM) vs. cortical and deep gray matter (CDGM) lesions and (2) to explore the relation between UL kinematics and lesion location and extent within each lesion timing group. Methods: Forty-eight children (age 10.4 ± 2.7 year; 29 boys; 21 right-sided; 33 PWM; 15 CDGM) underwent an UL 3DMA during a reach-to-grasp task. Spatiotemporal parameters [movement duration, (timing of) maximum velocity, trajectory straightness], the Arm Profile Score (APS) and Arm Variable Scores (AVS) were extracted. The APS and AVS refer to the total amount of movement pathology and movement deviations of the wrist, elbow, shoulder, scapula and trunk respectively. Brain lesion location and extent were scored based on FLAIR-images using a semi-quantitative MRI-scale. Results: Children with CDGM lesions showed more aberrant spatiotemporal parameters (p < 0.03) and more movement pathology (APS, p = 0.003) compared to the PWM group, mostly characterized by increased wrist flexion (p = 0.01). In the CDGM group, moderate to high correlations were found between lesion location and extent and duration, timing of maximum velocity and trajectory straightness (r = 0.53-0.90). Lesion location and extent were further moderately correlated with distal UL movement pathology (wrist flexion/extension, elbow pronation/supination, elbow flexion/extension; r = 0.50-0.65) and with the APS (r = 0.51-0.63). In the PWM group, only a few and low correlations were observed, mostly between damage to the PLIC and higher AVS of elbow flexion/extension, shoulder elevation and trunk rotation (r = 0.35-0.42). Regression analysis revealed damage to the temporal lobe with lesion timing as interactor (27%, p = 0.002) and the posterior limb of the internal capsule (PLIC) (7%, p = 0.04) as the strongest predictors, explaining 34% of the variance in APS. Conclusion: UL kinematic deviations are more influenced by lesion location and extent in children with later (CDGM) versus earlier lesions (PWM), except for proximal movement pathology. Damage to the PLIC is a significant predictor for UL movement pathology irrespective of lesion timing.

Project description:Background/Objectives: Intensive training of the more affected upper extremity (UE) has been shown to be effective for children with unilateral spastic cerebral palsy (USCP). Two types of UE training have been particularly successful: Constraint-Induced Movement Therapy (CIMT) and Bimanual training. Reorganization of the corticospinal tract (CST) early during development often occurs in USCP. Prior studies have suggested that children with an ipsilateral CST controlling the affected UE may improve less following CIMT than children with a contralateral CST. We tested the hypothesis that improvements in UE function after intensive training depend on CST laterality. Study Participants and Setting: Eighty-two children with USCP, age 5 years 10 months to 17 years, University laboratory setting. Materials/Methods: Single-pulse transcranial magnetic stimulation (TMS) was used to determine each child's CST connectivity pattern. Children were stratified by age, sex, baseline hand function and CST connectivity pattern, and randomized to receive either CIMT or Bimanual training, each of which were provided in a day-camp setting (90 h). Hand function was tested before, immediately and 6 months after the intervention with the Jebsen-Taylor Test of Hand Function, the Assisting Hand Assessment, the Box and Block Test, and ABILHAND-Kids. The Canadian Occupational Performance Measure was used to track goal achievement and the Pediatric Evaluation of Disability Inventory was used to assess functioning in daily living activities at home. Results: In contrast to our hypothesis, participants had statistically similar improvements for both CIMT and Bimanual training for all measures independent of their CST connectivity pattern (contralateral, ipsilateral, or bilateral) (p < 0.05 in all cases). Conclusions/Significance: The efficacy of CIMT and Bimanual training is independent of CST connectivity pattern. Children with an ipsilateral CST, previously thought to be maladaptive, have the capacity to improve as well as children with a contralateral or bilateral CST following intensive CIMT or Bimanual training. Clinical Trial Registration: www.ClinicalTrials.gov, identifier NCT02918890.

Project description:AimTo explore cortical activation during bimanual tasks and functional correlates in unilateral cerebral palsy (CP).MethodThis cross-sectional study included eight participants with unilateral CP (six females, two males; mean age [SD] 20y 10mo [5y 10mo], 13y 8mo-31y 6mo) in Manual Ability Classification System levels II to III and nine age-matched participants with typical development (seven females, two males; mean age [SD] 17y 8mo [5y 7mo], 9y 4mo-24y 2mo). They performed bimanual symmetric squeezing (BSS) and bimanual asymmetric squeezing (BAS) tasks at 1Hz, and a pouring task with dominant hand (DPour) and a pouring task with non-dominant hand (NDPour) at 0.67Hz, all while a custom array of functional near-infrared spectroscopy (fNIRS) optodes were placed over their sensorimotor area. Mixed-effects were used to contrast groups, tasks, and hemispheres (corrected p-values [q] reported). Analysis of variance and t-tests compared performance measures across groups and tasks.ResultsParticipants with unilateral CP showed greater activation in both hemispheres during BAS (non-lesioned: q<0.001; lesioned: q<0.001), and in the lesioned hemisphere during BSS (q<0.001), DPour (q=0.02), and NDPour (q=0.02) than those with typical development. The lesioned hemisphere in unilateral CP showed more activity than the non-lesioned one (BSS: q=0.01; BAS: q=0.009; NDPour: q=0.04). During BAS, higher cortical activity correlated with more synchronous arm activation (r=0.79; p=0.02); activity lateralized towards the non-lesioned hemisphere correlated with better Pediatric Evaluation of Disability Inventory computer adaptive test scores (r=0.81; p=0.03).InterpretationResults suggest abnormally increased sensorimotor cortical activity in unilateral CP, with implications to be investigated.What this paper addsCortical activity in manual tasks is described with functional near-infrared spectroscopy in typical and atypical cohorts. Activation levels in unilateral cerebral palsy appear to escalate with task difficulty. Increased brain activity may be associated with poorer selective manual control. Specific patterns of brain activity may be related to impaired bimanual function.

Dataset Information

Influence of the corticospinal tract wiring pattern on sensorimotor functional connectivity and clinical correlates of upper limb function in unilateral cerebral palsy.

Publications

Influence of the corticospinal tract wiring pattern on sensorimotor functional connectivity and clinical correlates of upper limb function in unilateral cerebral palsy.

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