Reward and punishment: the neural correlates of reinforcement feedback during motor learning

‘By the carrot or the stick’ reward or punishment has been contemplated by instructors to motivate their pupils to learn a new motor skill. The reinforcements of reward and punishment have demonstrated dissociable effects on motor learning with punishment enhancing the learning rate and reward increasing retention of the motor task. However it is still unclear how the brain processes reward and punishment during motor learning. This study sought to investigate the role of reinforcement feedback in cortical neural activity associated with motor learning. A novel visuomotor rotation task was employed with reward punishment or null feedback as the participants adapted their movement to a 30-degree counter-clockwise rotation. We measured movement time and task accuracy throughout the task. Surface electroencephalography was utilized to record cortical neural activity throughout the learning and retention of the motor task. Event-related potentials (ERPs) were calculated to assess how the brain processes the reinforcement feedback and prepares for movement. Repeated measures ANOVAs were utilized to detect differences in the movement parameters and ERP amplitudes. This study found that reward and punishment feedback did not produce different effects on the rate of task learning. However punishment feedback impaired the retention (memory) of the motor task. These behavioral effects were accompanied by changes in the amplitude of ERPs during feedback presentation and movement preparation. These results suggest that punishment feedback alters brain processes involved in memory formation during motor learning

Effects of Positive Social Comparative Feedback During Practice on Motor Sequence Learning, Performance Expectancies, and Resting State Connectivity

Positive social comparative feedback indicates to the learner that they are performing better than others. While this type feedback supports motor skill learning in some tasks, the effect of social comparative feedback on motor sequence learning remains unknown. In addition, the OPTIMAL theory predicts that positive social comparative feedback may trigger a dopaminergic response in the brain. However, no studies have utilized neuroimaging techniques to investigate this question. Therefore, the aim of these studies was to determine the effect of positive social comparative feedback on motor sequence learning, performance expectancies, and resting state connectivity of dopaminergic neural pathways. In the first study, forty-eight individuals practiced a joystick-based sequence task and were divided into three feedback groups: CONTROL (no performance feedback), RT ONLY (response time only feedback), and RT+POS (response time plus positive social comparison). Participants attended sessions on two consecutive days: Day 1 for motor skill acquisition and Day 2 for retention testing. Performance related expectancies were measured before and after motor practice and at retention. The RT+POS and CONTROL group showed better overall performance/learning compared with the RT ONLY group. However, the RT+POS showed the highest peak velocities, and the CONTOL group showed the shortest path distances. Overall, the RT+POS and CONTROL showed increases in perceived competence while the RT ONLY group did not. The results of this study suggest that feedback content is an important consideration during motor practice, since feedback without social context (RT ONLY) was detrimental, and since feedback may be leveraged to bias motor practice towards higher movement speeds versus spatial accuracy. In the second study, thirty individuals practiced the same motor task and were divided into two feedback groups: RT ONLY and RT+POS. The study protocol was similar, with magnetic resonance imaging added before and after motor practice. The RT+POS group showed an increase in functional connectivity between the ventral tegmental area and the left nucleus accumbens, brain regions along the mesolimbic dopamine pathway. The RT+POS group showed better overall performance than the RT ONLY group at acquisition. Similar to the first study, the RT+POS showed higher peak velocities than the RT ONLY group. Overall, both groups showed increases in performance expectancies that were not different by group. The results of the brain connectivity analysis support the OPTIMAL theory prediction that positive social comparative feedback may trigger a dopaminergic response in the brain

Differential impact of reward and punishment on functional connectivity after skill learning

Reward and punishment shape behavior, but the mechanisms underlying their effect on skill learning are not well understood. Here, we tested whether the functional connectivity of premotor cortex (PMC), a region known to be critical for learning of sequencing skills, is altered after training when reward or punishment is given during training. Resting-state fMRI was collected in two experiments before and after participants trained on either a serial reaction time task (SRTT; n = 36) or force-tracking task (FTT; n = 36) with reward, punishment, or control feedback. In each experiment, training-related change in PMC functional connectivity was compared across feedback groups. In both tasks, we found that reward and punishment differentially affected PMC functional connectivity. On the SRTT, participants trained with reward showed an increase in functional connectivity between PMC and cerebellum as well as PMC and striatum, while participants trained with punishment showed an increase in functional connectivity between PMC and medial temporal lobe connectivity. After training on the FTT, subjects trained with control and reward showed increases in PMC connectivity with parietal and temporal cortices after training, while subjects trained with punishment showed increased PMC connectivity with ventral striatum. While the results from the two experiments overlapped in some areas, including ventral pallidum, temporal lobe, and cerebellum, these regions showed diverging patterns of results across the two tasks for the different feedback conditions. These findings suggest that reward and punishment strongly influence spontaneous brain activity after training, and that the regions implicated depend on the task learned

When motor control hangs in the balance: Sensorimotor learning during balance-challenging conditions

Maintaining balance while moving is fundamental for safe and successful motor performance. However, this aspect of daily movement is often overlooked in experimental paradigms that assess adaptation during constrained and/or isolated tasks. Consequently, we cannot easily extrapolate the results from these studies to naturalistic motor behaviours. The goal of this thesis is to determine how the necessity to maintain balance during unconstrained movement affects sensorimotor learning. For my first study, I assessed how challenging balance during adaptation affects generalization of learning. Four groups of participants adapted to a new visuomotor mapping induced by prism lenses while performing either a standing-based reaching or walking task, with or without a manipulation that challenged balance. To assess generalization, participants performed a single trial of each of the other group’s tasks without the prisms. I found that both the reaching and walking balance-challenged groups showed greater generalization to their equivalent, non-adapted task compared to the balance-unchallenged groups. I also found that challenging balance modulated generalization across the reaching and walking tasks. For my second study, I tested how challenging balance affected motor memory retention. To do this, the same four groups of participants returned to the lab and repeated their adaptation protocol one week later. I found that only the walking groups demonstrated faster relearning (or savings) during re-exposure to the prisms. Crucially, I found that challenging balance significantly enhanced savings during walking. In my third study, I determined how a stability consequence associated with movement errors affected sensorimotor learning. Two groups of participants adapted to a new visuomotor mapping while performing a precision walking task either with or without the possibility of experiencing a slip perturbation when making errors. I assessed generalization of learning across two visually guided walking tasks and motor memory consolidation. To assess consolidation, I introduced an opposite direction visuomotor mapping following adaptation and evaluated relearning one week later. I found that the experiencing a physical consequence when making errors enhanced generalization and motor memory consolidation. Overall, this thesis provides a novel perspective on how the necessity for balance control contributes to sensorimotor learning, which has intriguing implications for the development of rehabilitation interventions

Differential impact of reward and punishment on functional connectivity after skill learning

Reward and punishment shape behavior, but the mechanisms underlying their effect on skill learning are not well understood. Here, we tested whether the functional connectivity of premotor cortex (PMC), a region known to be critical for learning of sequencing skills, is altered after training when reward or punishment is given during training. Resting-state fMRI was collected in two experiments before and after participants trained on either a serial reaction time task (SRTT; n = 36) or force-tracking task (FTT; n = 36) with reward, punishment, or control feedback. In each experiment, training-related change in PMC functional connectivity was compared across feedback groups. In both tasks, we found that reward and punishment differentially affected PMC functional connectivity. On the SRTT, participants trained with reward showed an increase in functional connectivity between PMC and cerebellum as well as PMC and striatum, while participants trained with punishment showed an increase in functional connectivity between PMC and medial temporal lobe connectivity. After training on the FTT, subjects trained with control and reward showed increases in PMC connectivity with parietal and temporal cortices after training, while subjects trained with punishment showed increased PMC connectivity with ventral striatum. While the results from the two experiments overlapped in some areas, including ventral pallidum, temporal lobe, and cerebellum, these regions showed diverging patterns of results across the two tasks for the different feedback conditions. These findings suggest that reward and punishment strongly influence spontaneous brain activity after training, and that the regions implicated depend on the task learned