Neuronal correlates of memory formation in motor cortex after adaptation to force field.

Activity of single neurons in the motor cortex has been shown to change during acquisition of motor skills. We previously reported that the combined activity of cell ensembles in the motor cortex of monkeys (Macaca fascicularis) evolves during adaptation to a novel force field perturbation to encode the direction of compensatory force when reaching to visual targets. We also showed that the population directional signal was altered by the available sensory feedback. Here, we examined whether traces of such activity would linger on to later constitute motor memories of the newly acquired skill and whether memory traces would differ depending on feedback. We found that motor-cortical cell ensembles retained features of their adaptive activity pattern in the absence of perturbation when reaching to both learned and unlearned targets. Moreover, the preferred directions of these cells rotated in the direction of force field while the entire population of cells produced no net rotation of preferred direction when returning to null-field reaches. Whereas the activity pattern and preferred direction rotations were comparable with and without visual feedback, changes in tuning amplitudes differed across feedback conditions. Last, savings in behavioral performance and neuronal activity during later reexposure to force field were apparent. Overall, the findings reflect a novel representation of motor memory by cell ensembles and indicate a putative role of the motor cortex in early acquisition of motor memory.

Combined adaptiveness of specific motor cortical ensembles underlies learning.

Learning motor skills entails adaptation of neural computations that can generate or modify associations between sensations and actions. Indeed, humans can use different strategies when adapting to dynamic loads depending on available sensory feedback. Here, we examined how neural activity in motor cortex was modified when monkeys made arm reaches to a visual target and locally adapted to curl force field with or without visual trajectory feedback. We found that firing rates of a large subpopulation of cells were consistently modulated depending on the distance of their preferred direction from the learned movement direction. The newly acquired activity followed a cosine-like function, with maximal increase in directions that opposed the perturbing force and decrease in opposite directions. As a result, the combined neuronal activity generated an adapted population vector. The results suggest that this could be achieved without changing the tuning properties of the cells. This population directional signal was however altered in the absence of visual feedback; while the cosine pattern of modulation was maintained, the population distributions of modulated cells differed across feedback consistent with the different trajectory shapes. Finally, we predicted generalization patterns of force-field learning based on the cosine-like modulation. These conformed to reported features of generalization in humans, suggesting that the generalization function was related to the observed rate modulations in the motor cortex. Overall, the findings suggest that the new combined activation of neuronal ensembles could underlie the change in the internal model of movement dynamics in a way that depends on available sensory feedback and chosen strategy.

Discordant Tasks and Motor Adjustments Affect Interactions between Adaptations to Altered Kinematics and Dynamics.

Motor control and adaptation are multi-determinate processes with complex interactions. This is reflected for example in the ambiguous nature of interactions during sequential adaptation of reaching under kinematics and dynamics perturbations. It has been suggested that perturbations based on the same kinematic parameter interfere. Others posited that opposing motor adjustments underlie interference. Here, we examined the influence of discordances in task and in motor adjustments on sequential adaptations to visuomotor rotation and viscous force field perturbations. These two factors - perturbation direction and task discordance - have been examined separately by previous studies, thus the inherent difficulty to identify the roots of interference. Forty-eight human subjects adapted sequentially to one or two types of perturbations, of matched or conflicting directions. We found a gradient of interaction effects based on perturbation direction and task discordance. Perturbations of matched directions showed facilitation while perturbations of opposite directions, which required opposing motor adjustments, interfered with each other. Further, interaction effects increased with greater task discordance. We also found that force field and visuomotor rotation had mutual anterograde and retrograde effects. However, we found independence between anterograde and retrograde interferences between similar tasks. The results suggest that the newly acquired internal models of kinematic and dynamic perturbations are not independent but they share common neuronal resources and interact between them. Such overlap does not necessarily imply competition of resources. Rather, our results point to an additional principle of sensorimotor adaptation allowing the system to tap or harness common features across diverse sensory inputs and task contexts whenever available.

Differences in context and feedback result in different trajectories and adaptation strategies in reaching.

Computational models of motor control have often explained the straightness of horizontal planar reaching movements as a consequence of optimal control. Departure from rectilinearity is thus regarded as sub-optimal. Here we examine if subjects may instead select to make curved trajectories following adaptation to force fields and visuomotor rotations. Separate subjects adapted to force fields with or without visual feedback of their hand trajectory and were retested after 24 hours. Following adaptation, comparable accuracies were achieved in two ways: with visual feedback, adapted trajectories in force fields were straight whereas without it, they remained curved. The results suggest that trajectory shape is not always straight, but is also influenced by the calibration of available feedback signals for the state estimation required by the task. In a follow-up experiment, where additional subjects learned a visuomotor rotation immediately after force field, the trajectories learned in force fields (straight or curved) were transferred when directions of the perturbations were similar but not when directions were opposing. This demonstrates a strong bias by prior experience to keep using a recently acquired control policy that continues to produce successful performance inspite of differences in tasks and feedback conditions. On relearning of force fields on the second day, facilitation by intervening visuomotor rotations occurred only when required motor adjustments and calibration of feedback signals were similar in both tasks. These results suggest that both the available feedback signals and prior history of learning influence the choice and maintenance of control policy during adaptations.

The scaling of postural adjustments during bimanual load-lifting in traumatic brain-injured adults.

Previous postural studies of traumatic brain injury (TBI) patients have been limited to identifying deficits in static and quasi-dynamic postural control tasks such as weight shifting. In this study, we examined whether or not patients with TBI are able to scale adequately their postural adjustments during the performance of the dynamic task of bimanual load-lifting. An age matched group of healthy adults served as controls. We used the Tetrax posturography system that calculates a stability score (ST) based on fluctuations in vertical ground reaction forces, normalized for body weight. During quiet standing, the ST scores of the TBI group were significantly higher than the control group. Forward weight shift and percentage change in the vertical ground reaction forces (lift postural adjustment (LPA) and post-lift postural adjustment (PLPA) scores) linearly increased with increasing load weight in both healthy and TBI subjects. Group differences were found in the magnitude of forward weight shift but not in the relative increase of the LPA and PLPA scores during the lifting and post-lifting phases respectively. The forward weight shift of the TBI group was lower-than-normal and asymmetrical--there was significantly less forward weight shift on the more affected than on the less affected limb. In addition, a significant amplitude coupling was found between the scaling of the weight shift of the heel and forefoot of each limb. However, no coupling was found between the weight shift amplitudes of homologous parts of both limbs in the TBI group. The results showed that scaling based on prior experience was preserved in the TBI group, though some TBI subjects demonstrated absent scaling in either the more affected or less affected heel or forefoot. The differences between the normal and TBI groups in postural adjustments are not necessarily a sign of pathology; rather they may represent a deliberate choice of the central nervous system to counteract predictable disturbances.