The Amount and Pattern of Reciprocal Compensations Predict Performance Stability in a Visually Guided Finger Force Production Task.

Previous work suggests that synergistic activity among motor elements implicated in force production tasks underlies enhanced performance stability associated with visual feedback. A hallmark of synergistic activity is reciprocal compensation, that is, covariation in the states of motor elements that stabilizes critical performance variables. The present study examined if characteristics of reciprocal compensation are indicators of individuals' capacity to respond adaptively to variations in the resolution of visual feedback about criterion performance. Twenty healthy adults (19.25 ± 1.25 years; 15 females and five males) pressed two sensors with their index fingers to produce a total target force equivalent to 20% of their maximal voluntary contraction under nine conditions that differed in the spatial resolution of real-time feedback about their performance. By combining within-trial uncontrolled manifold and sample entropy analyses, we quantified the amount and degree of irregularity (i.e., non-repetitiveness) of reciprocal compensations over time. We found a U-shaped relationship between performance stability and gain. Importantly, this relationship was moderated by the degree of irregularity of reciprocal compensation. Lower irregularity in reciprocal compensation patterns was related to individuals' capacity to maintain (or minimize losses in) performance under changes in feedback resolution. Results invite future investigation into how interindividual variations in reciprocal compensation patterns relate to differences in control strategies supporting adaptive responses in complex, visually guided motor tasks.

Prior uncertainty impedes discrete locomotor adaptation.

The impact of environmental uncertainty on locomotor adaptation remains unclear. Environmental uncertainty could either aid locomotor adaptation by prompting protective control strategies that stabilize movements to assist learning or impede adaptation by reducing error sensitivity and fostering hesitance to pursue corrective movements. To explore this, we investigated participants' adaptation to a consistent force field after experiencing environmental uncertainty in the form of unpredictable balance perturbations. We compared the performance of this group (Perturbation) to the adaptive performance of a group that did not experience any unpredictable perturbations (Non-Perturbation). Perturbations were delivered using a cable-driven robotic device applying lateral forces to the pelvis. We assessed whole-body center of mass (COM) trajectory (COM signed deviation), anticipatory postural adjustments (COM lateral offset), and first step width. The Perturbation group exhibited larger disruptions in COM trajectory (greater COM signed deviations) than the Non-Perturbation group when first walking in the force field. While the COM signed deviations of both groups decreased towards baseline values, only the Non-Perturbation group returned to baseline levels. The Perturbation groups COM signed deviations remained higher, indicating they failed to fully adapt to the force field before the end. The Perturbation group also did not adapt their COM lateral offset to counter the predictable effects of the force field as the Non-Perturbation group did, and their first step width increased more slowly. Our findings suggest that exposure to unpredictable perturbations impeded future sensorimotor adaptations to consistent perturbations.

Increased paired stimuli enhance corticospinal-motoneuronal plasticity in humans with spinal cord injury.

Paired corticospinal-motoneuronal stimulation (PCMS) has been used to enhance corticospinal excitability and functional outcomes in humans with spinal cord injury (SCI). Here, we examined the effect of increasing the number of paired pulses on PCMS-induced plasticity. During PCMS, corticospinal volleys evoked by transcranial magnetic stimulation (TMS) over the hand motor cortex were timed to arrive at corticospinal-motoneuronal synapses of the first dorsal interosseous (FDI) muscle 1-2 ms before the arrival of antidromic potentials elicited in motoneurons by electrical stimulation of the ulnar nerve. We tested motor-evoked potentials (MEPs) elicited by TMS over the hand motor cortex and electrical stimulation at the cervicomedullary junction (CMEPs) in the FDI muscle before and after 180 paired pulses (PCMS-180) followed up by another 180 paired pulses (PCMS-360) in humans with and without chronic incomplete cervical SCI. The nine-hole-peg-test (9HPT) was measured before and after PCMS paired pulses in individuals with SCI. We found that the size of MEPs and CMEPs increased after PCMS-180 in both groups compared with baseline and further increased after PCMS-360 in participants with SCI, suggesting a spinal origin for these effects. Notably, in people with SCI, the time to complete the 9HPT decreased after PCMS-180 and further decreased after PCMS-360 compared with baseline but not when the 9HPT was repeated overtime. Our findings demonstrate that increasing the number of PCMS paired pulses potentiates corticospinal excitability and voluntary motor output after SCI, likely through spinal plasticity. This proof-of-principle study suggests that increasing the PCMS dose represents a strategy to boost voluntary motor output after SCI.NEW & NOTEWORTHY Paired corticospinal-motoneuronal stimulation (PCMS) has been used to enhance corticospinal excitability and functional outcomes in humans with spinal cord injury (SCI). Here, we demonstrate that 360 paired pulses resulted in larger increases in motor-evoked potential size in a hand muscle and in a better ability to complete the nine-hold-peg-test compared with 180 paired pulses in people with SCI. This proof-of-principle study suggests that increasing the PCMS dose represents a strategy to boost motor output after SCI.

A Dynamical Approach to the Uncontrolled Manifold: Predicting Performance Error During Steady-State Isometric Force Production.

The uncontrolled manifold (UCM) approach quantifies the presence of compensatory variability between musculoskeletal elements involved in a motor task. This approach has proved useful for identifying synergistic control strategies for a variety of everyday motor tasks and for investigating how control strategies are affected by motor pathology. However, the UCM approach is limited in its ability to relate compensatory motor variance directly to task performance because variability along the UCM is mathematically agnostic to performance. We present a new approach to UCM analysis that quantifies patterns of irregularity in the compensatory variability between motor elements over time. In a bimanual isometric force stabilization task, irregular patterns of compensation between index fingers predicted greater performance error associated with difficult task conditions, in particular for individuals who exploited a larger set of compensatory strategies (i.e., a larger subspace of the UCM). This relationship between the amount and structure of compensatory motor variance might be an expression of underlying processes supporting performance resilience.

Grip force anticipation of nonlinear, underactuated load force.

Feedforward internal model-based control enabled by efference copies of motor commands is the prevailing theoretical account of motor anticipation. Grip force control during object manipulation-a paradigmatic example of motor anticipation-is a key line of evidence for that account. However, the internal model approach has not addressed the computational challenges faced by the act of manipulating mechanically complex objects with nonlinear, underactuated degrees of freedom. These objects exhibit complex and unpredictable load force dynamics which cannot be encoded by efference copies of underlying motor commands, leading to the prediction from the perspective of an efference copy-enabled feedforward control scheme that grip force should either lag or fail to coordinate with changes in load force. In contrast to that prediction, we found evidence for strong, precise, anticipatory grip force control during manipulations of a complex object. The results are therefore inconsistent with the internal forward model approach and suggest that efference copies of motor commands are not necessary to enable anticipatory control during active object manipulation.NEW & NOTEWORTHY From the perspective of feedforward internal model-based control, precise, anticipatory grip force (GF) control when manipulating a complex object should not be possible as the object's changing load forces (LFs) cannot be encoded by efference copies of the underlying movements. However, we observed that GF exhibited strong, precise, anticipatory coupling with LF during extended manipulations of a complex object. These findings suggest that an alternative theoretical framework is needed to account for anticipatory GF control.

Early learning differences between intra- and interpersonal interlimb coordination.

Intrinsic coordination patterns exist between limbs such that 1) coordination at these states is inherently stable, 2) any other pattern requires learning to produce, and 3) this learning is subject to interference from a systemic bias towards intrinsic patterns. The dynamics that govern intrapersonal interlimb coordination also govern interpersonal coordination. However, intrapersonal coordination exhibits greater coupling strength and thus more stable intrinsic dynamics than interpersonal coordination. Because the strength of intrinsic coordination tendencies has consequences for learning coordination patterns, the differences in coupling strength between intra- and interpersonal coordination should impact the ability to perform new coordination patterns via greater or less interference from intrinsic dynamics. This was investigated by measuring participants' performance as they learned a new coordination pattern alone (intrapersonal) or in pairs (interpersonal). Participants were implicitly tasked with learning the pattern as they separately controlled the vertical and horizontal position of an on-screen cursor to trace a circling target. We observed better performance of dyads on first trial and steeper learning trajectories for individuals. Overall, these results indicate that individuals experienced greater interference from stronger intrinsic coordination dynamics during early learning but could overcome this interference and achieve similar performance to that of dyads with very little practice.

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

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.

Grip Force-Load Force Coupling Is Influenced by Altered Visual Feedback about Object Kinematics.

Recent evidence suggests that visual feedback influences the adjustment of grip force to the changing load force exerted by a grasped object as it is manipulated. The current project investigated how visual feedback of object kinematics affects the coupling of grip force to load force by scaling the apparent displacements of the object viewed in virtual reality. Participants moved the object to manually track a moving virtual target. The predictability of the changing load force exerted by the object was also manipulated by altering the nature of target trajectories (and therefore the nature of object motions). When apparent object displacements increased in magnitude, grip force became more tightly coupled to load force over time. Furthermore, when load force variations were less predictable, the magnitude of apparent object displacements affected the relative degree of continuous versus intermittent coupling of grip force to load force. These findings show that visual feedback of object motion affects the ongoing dynamical coupling between grip force control and load force experienced during manipulation of a grasped object.

Flexible organization of grip force control during movement frequency scaling.

The grip force applied to maintain grasp of a handheld object has been typically reported as tightly coupled to the load force exerted by the object as it is actively manipulated, occurring proportionally and consistently in phase with changes in load force. However, continuous grip force-load force coupling breaks down when overall load force levels and oscillation amplitudes are lower (Grover F, Lamb M, Bonnette S, Silva PL, Lorenz T, Riley MA. Exp Brain Res 236: 2531-2544, 2018) or more predictable (Grover FM, Nalepka P, Silva PL, Lorenz T, Riley MA. Exp Brain Res 237: 687-703, 2019). Under these circumstances, grip force is instead only intermittently coupled to load force; continuous coupling is prompted only when load force levels or variations become sufficiently high or unpredictable. The current study investigated the nature of the transition between continuous and intermittent modes of grip force control by scaling the load force level and the oscillation amplitude continuously in time by means of scaling the required frequency of movement oscillations. Participants grasped a cylindrical object between the thumb and forefinger and oscillated their arm about the shoulder in the sagittal plane. Oscillation frequencies were paced with a metronome that scaled through an ascending or descending frequency progression. Due to greater accelerations, faster frequencies produced greater overall load force levels and more pronounced load oscillations. We observed smooth but nonlinear transitions between clear regimes of intermittent and continuous grip force-load force coordination, for both scaling directions, indicating that grip force control can flexibly reorganize as parameters affecting grasp (e.g., variations in load force) change over time.NEW & NOTEWORTHY Grip force (GF) is synchronously coupled to changing load forces (LF) during object manipulation when LF levels are high or unpredictable, but only intermittently coupled to LF during less challenging grasp conditions. This study characterized the nature of transitions between synchronous and intermittent GF-LF coupling, revealing a smooth but nonlinear change in intermittent GF modulation in response to continuous scaling of LF amplitude. Intermittent, "drift-and-act" control may provide an alternative framework for understanding GF-LF coupling.

Variable and intermittent grip force control in response to differing load force dynamics.

A recent study (Grover et al. Exp Brain Res 236(10):2531-2544, 2018) found that the grip force applied to maintain grasp of a hand-held object exhibited intermittent coupling to the changing load forces exerted by the object as it was oscillated. In particular, the strength and consistency of grip force response to load force oscillations was tied to overall load force levels and the prominence of load force oscillations. This contrasts with previous reports of grip force-load force coupling as generally continuous and stable and, therefore, has implications for theoretical accounts of grip force control that are predicated on these prior understandings of the coupling. The finding of intermittency additionally raises questions about the consistency of the temporal relation (i.e., lead/lag) between grip force and load force over time. The objective of the current study was, therefore, to investigate how the time-varying pattern (i.e., the regularity vs. complexity) of load force variations contribute to shifts between more intermittent and more continuous grip force control, and to determine the temporal consistency of the coupling. It was found that grip force became more tightly and continuously responsive to load force as load force changes became less predictable. Additionally, we report strong evidence that the temporal (i.e., lead/lag) relation between grip force and load force and the strength of their coupling vary substantially over time.