Children and adolescents with cerebral palsy flexibly adapt grip control in response to variable task demands

Highlights

• Children with cerebral palsy demonstrate task-dependent grip control strategies

• Grip impairments were more apparent under more predictable task conditions.

• Unpredictable task demands attenuated grip control impairments.

Abstract

Background

Children and adolescents with cerebral palsy demonstrate impairments in grip control with associated limitations in functional grasp. Previous work in cerebral palsy has focused on grip control using relatively predictable task demands, a feature which may limit generalizability of those study results in light of recent evidence in typically developing adults suggesting that grip control strategies are task-dependent. The purpose of this study was to determine whether and how varying upper extremity task demands affect grip control in children and adolescents with cerebral palsy.

Methods

Children and adolescents with mild spastic cerebral palsy (n = 10) and age- and gender-matched typically developing controls (n = 10) participated. Participants grasped an object while immersed in a virtual environment displaying a moving target and a virtual representation of the held object. Participants aimed to track the target by maintaining the position of the virtual object within the target as it moved in predictable and unpredictable trajectories.

Findings

Grip control in children with cerebral palsy was less efficient and less responsive to object load force than in typically developing children, but only in the predictable trajectory condition. Both groups of participants demonstrated more responsive grip control in the unpredictable compared to the predictable trajectory condition.

Interpretation

Grip control impairments in children with cerebral palsy are task-dependent. Children and adolescents with cerebral palsy demonstrated commonly observed grip impairments in the predictable trajectory condition. Unpredictable task demands, however, appeared to attenuate impairments and, thus, could be exploited in the design of therapeutic interventions.

Introduction

During active object manipulation, successful grasp requires individuals to adapt grip force (GF) to the weight and changing inertial forces of the held object (i.e., load force; LF). While initial studies of GF-LF coupling suggested that GF is continuously modulated in-phase with changing LF (Blank et al., 2001; Flanagan and Wing, 1993; Viviani and Lacquaniti, 2015), recent studies of grip control in typically developing (TD) adults indicate that GF-LF coordination patterns are flexibly organized as a function of task demands (Grover et al., 2018; Grover et al., 2019a; Grover et al., 2019b; Grover et al., 2020). Participants in those studies shifted from more continuous (i.e., strongly coordinated and responsive) to more intermittent (i.e., less responsive) GF-LF coupling when the magnitude of LFs experienced at the point of grasp decreased (Grover et al., 2018, Grover et al., 2019b) and when task requirements involved more predictable upper extremity (UE) movements and, thus, more predictable LF variations (Grover et al., 2019a). An important lesson from these studies is that it is critical to systematically vary task demands to reveal the full range of grip control strategies.

This lesson may be particularly important for efforts to characterize grip control impairments that result from pathology, like cerebral palsy (CP). Grip control in children with CP has been previously examined during the performance of sequential lifts involving a single, predictable UE trajectory (i.e., grip-lift-hold) (Duff and Gordon, 2003; Eliasson et al., 1992; Gordon and Duff, 1999). GF in the affected hands of children with CP has been characterized as excessive (i.e., greater force production) and less responsive to LF changes compared to TD peers, with a GF-LF coordination pattern resembling that of infants less than one year old (Eliasson et al., 1991). It is unknown if CP-related grip impairments occur under less predictable task conditions, which are known to promote more continuous GF-LF coupling in TD adults (Grover et al., 2019a). Additionally, previous findings of an apparent lack of GF-LF coordination in CP (e.g., Eliasson et al., 1992) may reflect differences in UE kinematics between children with CP and TD children. In that study (see their Fig. 2D, in particular the 400 g condition), children with CP produced lower UE accelerations than TD children. Because LF is proportional to acceleration, this means they experienced lower LF than TD children. The apparent non-responsiveness of GF to changing LF observed in children with CP may, therefore, be related to reduced task demands (i.e., lower LF), since lower LFs are associated with more intermittent (i.e., non-responsive) GF-LF coupling in TD adults compared to higher LFs (Grover et al., 2018, Grover et al., 2019a, Grover et al., 2019b).

The present study was designed to determine whether and how the demands imposed on UE kinematics affect grip control in children and adolescents with CP. We used a virtual reality target tracking task (cf. Grover et al., 2019a) to control UE kinematics in order to create comparable patterns of LF for participants with CP and TD peers. The virtual target moved along unpredictable trajectories (more demanding and previously associated with more continuous GF-LF coupling; Grover et al., 2019a) or predictable trajectories (associated with more intermittent GF-LF coupling). We also manipulated mass of the grasped object; lower mass leads to lower LF and was previously associated with more intermittent GF-LF coupling (Grover et al., 2018). We hypothesized that differences in grip control between children with CP and TD children would be attenuated under conditions that promote more continuous GF-LF coupling in TD adults.