Effects of noninvasive neuromodulation targeting the spinal cord on early learning of force control by the digits.

AIMS: Control of finger forces underlies our capacity for skilled hand movements acquired during development and reacquired after neurological injury. Learning force control by the digits, therefore, predicates our functional independence. Noninvasive neuromodulation targeting synapses that link corticospinal neurons onto the final common pathway via spike-timing-dependent mechanisms can alter distal limb motor output on a transient basis, yet these effects appear subject to individual differences. Here, we investigated how this form of noninvasive neuromodulation interacts with task repetition to influence early learning of force control during precision grip. METHODS: The unique effects of neuromodulation, task repetition, and neuromodulation coinciding with task repetition were tested in three separate conditions using a within-subject, cross-over design (n = 23). RESULTS: We found that synchronizing depolarization events within milliseconds of stabilizing precision grip accelerated learning but only after accounting for individual differences through inclusion of subjects who showed upregulated corticospinal excitability at 2 of 3 time points following conditioning stimulation (n = 19). CONCLUSIONS: Our findings provide insights into how the state of the corticospinal system can be leveraged to drive early motor skill learning, further emphasizing individual differences in the response to noninvasive neuromodulation. We interpret these findings in the context of biological mechanisms underlying the observed effects and implications for emerging therapeutic applications.

Consistent Individual Tendencies in Motor Speed-Accuracy Trade-Off.

The literature on speed-accuracy trade-off (SAT) in motor control has evidenced individuality in how individuals trade moments (e.g., mean and variance) of spatial and temporal errors. These individual tendencies could grasp tendencies of the system given previous experiences and constraints of the organism, a signature of the system control. Nonetheless, such tendency must be robust to small perturbations. Thirty participants performed nine conditions with different time and spatial criteria over 2 days (scanning). In between these scanning conditions, individuals performed a practice condition that required modifications of the individuals' preferred spatial and temporal tendency in the SAT. Our results demonstrated that there were no systematic effects of practice in SAT preferences. However, individual analyses demonstrated significant changes for 25 out of 30 individuals. The latter either attests against a consistent preference or to a more complex characterization of individual SAT tendencies.

Force oscillations underlying precision grip in humans with lesioned corticospinal tracts.

Stability of precision grip depends on the ability to regulate forces applied by the digits. Increased frequency composition and temporal irregularity of oscillations in the force signal are associated with enhanced force stability, which is thought to result from increased voluntary drive along the corticospinal tract (CST). There is limited knowledge of how these oscillations in force output are regulated in the context of dexterous hand movements like precision grip, which are often impaired by CST damage due to stroke. The extent of residual CST volume descending from primary motor cortex may help explain the ability to modulate force oscillations at higher frequencies. Here, stroke survivors with longstanding hand impairment (n = 17) and neurologically-intact controls (n = 14) performed a precision grip task requiring dynamic and isometric muscle contractions to scale and stabilize forces exerted on a sensor by the index finger and thumb. Diffusion spectrum imaging was used to quantify total white matter volume within the residual and intact CSTs of stroke survivors (n = 12) and CSTs of controls (n = 14). White matter volumes within the infarct region and an analogous portion of overlap with the CST, mirrored onto the intact side, were also quantified in stroke survivors. We found reduced ability to stabilize force and more restricted frequency ranges in force oscillations of stroke survivors relative to controls; though, more broadband, irregular output was strongly related to force-stabilizing ability in both groups. The frequency composition and temporal irregularity of force oscillations observed in stroke survivors did not correlate with maximal precision grip force, suggesting that it is not directly related to impaired force-generating capacity. The ratio of residual to intact CST volumes contained within infarct and mirrored compartments was associated with more broadband, irregular force oscillations in stroke survivors. Our findings provide insight into granular aspects of dexterity altered by corticospinal damage and supply preliminary evidence to support that the ability to modulate force oscillations at higher frequencies is explained, at least in part, by residual CST volume in stroke survivors.

Task and Informational Constraints on Search Strategies: Testing the Idea of Convergence to Tolerant Regions.

The experiment reported was designed to investigate the interaction of information and force variability on the evolving search strategy, specifically testing the hypothesis of convergence to tolerant regions. Participants were required to produce proportional bimanual isometric force output over three days of practice, with no prespecified force target and where performance was more tolerant to force variability at higher forces. The duration of intermittent visual feedback was manipulated to test the effects of information and force variability on the search process and the resulting sensitivity to tolerant regions of the task space. The findings showed that just under half of the participants exploited more tolerant regions and that this was predicted by the initial force conditions. Different characterizations of the individual search patterns were also predicted by inherent force-dependent variability and initial force conditions. Visual intermittency feedback did not affect the time-dependent properties of the search process but did influence the within-trial variability. Our findings suggest that the attraction to tolerant regions needs to be considered within the interactions of the different categories of constraints on the search process.

Instructions on Task Constraints Mediate Perceptual-Motor Search and How Movement Variability Relates to Performance Outcome.

Movement variability has been postulated to afford perception of the perceptual motor workspace and to be directly linked to improved performance. Here, we investigated how instructions mediate the search process and the relation between performance outcome and movement variability. We used a novel bimanual force tracking task where zero error was achieved via proportional output between the hands. Participants were either instructed or not as to how to coordinate their force output to achieve this goal, but the goal to minimize error was explained to all participants. The provision of instructions restricted the overall area of the task space that was searched. Moreover, the time dependent properties of the search were influenced; where instructions increased the likelihood that participants would produce a higher force level over practice. Multiple regression revealed that variability was positively correlated with performance outcome, but the strength of this relation was dependent on instructions and individual search strategies. The findings are consistent with the view that information through instructions shapes individual emergent perceptual-motor search strategies that in turn mediate how movement variability relates to performance outcome.

Search Strategies in the Perceptual-Motor Workspace and the Acquisition of Coordination, Control, and Skill.

In this paper we re-visit and elaborate-on the theoretical framework of learning as searching within the perceptual-motor workspace for a solution to the task. The central focus is the nature of search strategies to locate and create stable equilibrium regions in the perceptual-motor workspace and how these strategies relate to the emergent movement forms in the acquisition of coordination, control, and skill. In the ecological theory of perception and action, the enhanced stability of performance occurs through the attunement of the perceptual systems to the task dynamics together with modifications of action as task and intrinsic dynamics cooperate and/or compete. Thus, through practice in this search process, individuals adapt to the pick-up of task relevant perceptual variables and change their movement form according to the stability of the performed action and its outcome in relation to the task demands. Contemporary experimental findings have revealed features of the search process given the interaction of individual intrinsic dynamics in the context of task requirements and principles that drive the change - e.g., exploitation of more tolerant task-space solutions and emergence of compensatory mechanisms. Finally, we outline how the search strategy framework relates to traditional learning-related phenomena: including the dynamical pathways of learning, learning curves, factors of learning, individuality, motor development, and sport and rehabilitation interventions.

Bimanual coordination and the intermittency of visual information in isometric force tracking.

The effect of the intermittency of visual information in the bimanual coordination of an isometric force coordination task was investigated as a function of criterion force level. Eight levels of visual information intermittency (.2-25.6 Hz) were used in blocked fashion at each force level. Participants were required to produce a constant force output matching as accurately as possible the criterion force target. The results showed that performance improved as the intermittency of visual information was reduced-this effect being a function of force level. The distribution of the relative phase through the trial revealed a preference for the two hands to be coupled together (in-phase) at the slower rates of visual presentation (~.2 Hz). However, as the rate of visual feedback was increased (up to ~25.6 Hz), there was a transition to predominantly a negative correlation pattern (anti-phase). The pattern of bimanual coordination in this isometric tracking task is driven by the availability of information for error correction and the interactive influence of perceptual-motor constraints.

Adapting relative phase of bimanual isometric force coordination through scaling visual information intermittency.

Visual information plays an adaptive role in the relation between bimanual force coupling and error corrective processes of isometric force control. In the present study, the evolving distribution of the relative phase properties of bimanual isometric force coupling was examined by scaling within a trial the temporal feedback rate of visual intermittency (short to long presentation intervals and vice versa). The force error (RMSE) was reduced, and time-dependent irregularity (SampEn) of the force output was increased with greater amounts of visual information (shorter intermittency). Multi-stable coordination patterns of bimanual isometric force control were differentially shifted toward and away from the intrinsic dynamics by the changing the intermittency of visual information. The distribution of Hilbert transformed relative phase values showed progressively a predominantly anti-phase mode under less intermittent visual information to predominantly an in-phase mode with limited (almost no) visual information. Correlation between the hands showed a continuous reduction, rather than abrupt "transition," with increase in visual information, although no mean negative correlation was realized, despite the tendency towards an anti-phase distribution. Lastly, changes in both the performance outcome and bimanual isometric force coordination occurred at visual feedback rates faster than the minimal visual processing times established from single limb movement and isometric force protocols.