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Galea, J. M.

Publications and source records attributed to Galea, J. M..

16 recordsLinked to original sources

Differential impact of ageing on reward driven changes in motor control

Abstract Background: Reward can influence both the selection and execution of goal-directed actions. Healthy ageing is associated with changes in reward processing, raising the possibility that reward effects on motor control may be reduced in older adults. Objective: This study examined how monetary reward affects action execution and action selection during reaching movements and whether these effects differ between younger and older adults. Methods: 28 younger adults and 28 older adults performed a reward-based reaching task. Behaviourally non-distracted trials were used to assess action execution, whereas distractor-containing trials were used to assess action selection. Outcomes included maximum velocity, movement time, endpoint error, reaction time, and selection accuracy. Results: Reward increased maximum velocity and reduced movement time in both age groups without increasing error. These reward-related changes in movement vigour were larger in younger adults. During action selection, reward shortened reaction time but reduced selection accuracy in both groups, indicating faster but less accurate responses. The reward-related changes in reaction time and selection accuracy did not differ significantly between age groups. Conclusion: Ageing did not produce a uniform reduction in reward responsiveness. Instead, ageing attenuated reward-driven movement invigoration, while reward-related changes in action-selection behaviour were similar across age groups. These findings may inform the design of reward-based interventions that promote movement vigour without encouraging speed at the expense of accurate action selection.

neuroscience↗

Bilateral Intracortical Inhibition during Unilateral Motor Preparation and Sequence Learning

Motor sequence learning gradually quickens reaction time, suggesting that sequence learning alters motor preparation processes. Interestingly, evidence has shown that preparing sequence movements decreases short intracortical inhibition (SICI) in the contralateral motor cortex (M1), but also that sequence learning alters motor preparation processes in both the contralateral and ipsilateral M1s. Therefore, one possibility is that sequence learning alters the SICI decreases occurring during motor preparation in bilateral M1s. To examine this, two novel hypotheses were tested: unilateral sequence preparation would decrease SICI in bilateral M1s, and sequence learning would alter such bilateral SICI responses. Paired-pulse transcranial magnetic stimulation was delivered over the contralateral and ipsilateral M1s to assess SICI in an index finger muscle during the preparation of sequences initiated by either the right index or little finger. In the absence of sequence learning, SICI decreased in both the contralateral and ipsilateral M1s during the preparation of sequences initiated by the right index finger, suggesting that SICI decreases in bilateral M1s during unilateral motor preparation. As sequence learning progressed, SICI decreased in the contralateral M1 whilst it increased in the ipsilateral M1. Moreover, these bilateral SICI responses were observed at the onset of motor preparation, suggesting that sequence learning altered baseline SICI levels rather than the SICI decreases occurring during motor preparation per se. Altogether, these results suggest that SICI responses in bilateral M1s reflect two motor processes: an acute decrease of inhibition during motor preparation, and a cooperative but bidirectional shift of baseline inhibition levels as sequence learning progresses.

neuroscience↗

Dopaminergic manipulations affect the modulation and meta-modulation of movement speed: evidence from two pharmacological interventions

A body of research implicates dopamine in the average speed of simple movements. However, naturalistic movements span a range of different shaped trajectories and rarely proceed at a single constant speed; instead, speed is reduced when drawing "corners" compared to "straights" (i.e., speed-modulation), and the extent of this slowing down is dependent upon the global shape of the movement trajectory (i.e., speed-meta-modulation) - for example whether the shape is an ellipse or a rounded square. By employing two pharmacological intervention studies - individuals with Parkinsons both ON and OFF dopaminergic medication (N = 32) and members of the general population on a D2 receptor blocker (haloperidol) versus placebo (N = 43) - we implicate dopamine in speed, speed-modulation and speed-meta-modulation. Our findings move beyond vigour models implicating dopamine in average movement speed, and towards a conceptualisation that involves the modulation of speed as a function of contextual information.

neuroscience↗

Reward-based improvements in motor sequence learning are differentially affected by dopamine

Reward is a powerful tool to enhance human motor behaviour with research showing that it promotes motor sequence learning through increases in both motor vigour and movement fusion. Specifically, during a sequential reaching movement, monetary incentive leads to increased speed of each movement (vigour effect), whilst reward-based performance feedback increases speed of transition between movements (fusion effect). Therefore, motor sequence learning can be driven by distinct reward types with dissociable underlying processes. The neurotransmitter dopamine has been implicated to modulate motor vigour and regulate movement fusion. However, in humans, it is unclear if the same dopaminergic mechanism underlies both processes. To address this, we used a complex sequential reaching task in which rewards were based on movement times (MT). Crucially, MTs could be reduced via : 1) enhanced speed of individual movements (vigour effect) and/or 2) enhanced speed of transition between movements (fusion effect). 92 participants were randomly assigned to a reward and no reward group and were given either 2.5mg of the dopamine antagonist haloperidol or a placebo. Our results demonstrate that haloperidol impaired the reward-based effects on motor vigour whilst not affecting movement fusion. Thus, we illustrate that whilst both strategies are reward sensitive, they rely on dissociable mechanisms.

neuroscience↗

A Methodological Framework to Assess the Accuracy of Virtual Reality Hand-Tracking Systems: A case study with the Oculus Quest 2

Optical marker-less hand-tracking systems incorporated into virtual reality (VR) headsets are transforming the ability to assess motor skills, including hand movements, in VR. This promises to have far-reaching implications for the increased applicability of VR across scientific, industrial and clinical settings. However, so far, there is little data regarding the accuracy, delay and overall performance of these types of hand-tracking systems. Here we present a novel methodological framework which can be easily applied to measure these systems absolute positional error, temporal delay and finger joint-angle accuracy. We used this framework to evaluate the Meta Quest 2 hand-tracking system. Our results showed an average fingertip positional error of 1.1cm, an average finger joint angle error of 9.6o and an average temporal delay of 38.0ms. Finally, a novel approach was developed to correct for these positional errors based on a lens distortion model. This methodological framework provides a powerful tool to ensure the reliability and validity of data originating from VR-based, marker-less hand-tracking systems.

neuroscience↗

Age-Related Differences in Reward-Based Modulation of Sequential Reaching Performance

Reward can increase the speed and accuracy of movements in both simple and sequential reaching tasks. Two mechanisms are thought to be responsible for this: an increase in maximum velocity, due to increased muscle stiffness, resulting in faster, but energetically inefficient, individual movements; or coarticulation - the blending of sub-movements into single, smoother, more energetically efficient movements. Older adults have shown reduced sensitivity to reward in decision paradigms, but there is little research relating reward and motor performance in older adults. Using a novel online sequential reaching task, we compared the effects of reward on motor performance between young (18-23 years) and older (65-79 years) participants. We found that movement time decreased across training in all groups, and reward invigorated this decrease in both age groups. This suggests that reward is a viable facilitator of motor performance to compensate for age-related motor decline and has the potential for use in the design of rehabilitation programmes for age-related motor deficits or disease.

neuroscience↗

The dissociable effects of reward on sequential motor behaviour

Reward has consistently been shown to enhance motor performance however its beneficial effects appear to be largely unspecific. While reward has been shown to invigorate performance, it also enhances learning and/or retention. Therefore, a mechanistic account of the effects of reward on motor behaviour is lacking. Here we tested the hypothesis that these distinct reward-based improvements are driven by dissociable reward types: explicit reward (i.e. money) and performance feedback (i.e. points). Experiment 1 showed that explicit reward instantaneously improved movement times (MT) using a novel sequential reaching task. In contrast, performance-based feedback led to learning-related improvements. Importantly, pairing both maximised MT performance gains and accelerated movement fusion. Fusion describes an optimisation process during which neighbouring sequential movements blend together to form singular actions. Results from experiment 2 served as a replication and showed that fusion led to enhanced performance speed whilst also improving movement efficiency through increased smoothness. Finally, experiment 3 showed that these improvements in performance persist for 24 hours even without reward availability. This highlights the dissociable impact of explicit reward and performance feedback, with their combination maximising performance gains and leading to stable improvements in the speed and efficiency of sequential actions.

neuroscience↗

Reward-based invigoration of sequential reaching

Seeking reward is a powerful tool for shaping human behaviour. While it has been demonstrated that reward invigorates performance of simple movements, its effect on more complex sequential actions is less clear. In addition, it is unknown why reward-based improvements for discrete actions are transient, i.e. performance gains are lost once reward is removed, but appear long lasting for sequential actions. We show across three experiments that reward invigorates sequential reaching performance. Driven by a reward-based increase in speed, movements also exhibited greater coarticulation, smoothness and a closer alignment to a minimum jerk trajectory. Critically, these performance gains were maintained across multiple days even after the removal of reward. We propose that coarticulation, the blending together of sub-movements into a single continuous action, provides a mechanism by which reward can invigorate sequential performance whilst also increasing efficiency. This change in efficiency appears essential for the retention of reward-based improvements in motor behaviour.

neuroscience↗

Reward-driven enhancements in motor control are robust to TMS manipulation

A wealth of evidence describes the strong positive impact that reward has on motor control at the behavioural level. However, surprisingly little is known regarding the neural mechanisms which underpin these effects, beyond a reliance on the dopaminergic system. In recent work, we developed a task that enabled the dissociation of the selection and execution components of an upper limb reaching movement. Our results demonstrated that both selection and execution are concommitently enhanced by immediate reward availability. Here, we investigate what the neural underpinnings of each component may be. To this end, we disrupted activity of the ventromedial prefrontal cortex and supplementary motor area using continuous theta-burst transcranial magnetic stimulation (cTBS) in a within-participant design (N=23). Both cortical areas are involved in reward processing and motor control, and we hypothesised that disruption of their activity would result in disruption of the reward-driven effects on action selection and execution, respectively. To increase statistical power, participants were pre-selected based on their sensitivity to reward in the reaching task. While reward did lead to enhanced perforance during the cTBS sessions and a control sham session, cTBS was ineffective in altering these effects. These results may provide evidence that other areas, such as the primary motor cortex or the premotor area, may drive the reward-based enhancements of motor performance.

neuroscience↗

Reward-based improvements in motor control are driven by multiple error-reducing mechanisms

Reward has a remarkable ability to invigorate motor behaviour, enabling individuals to select and execute actions with greater precision and speed. However, if reward is to be exploited in applied settings such as rehabilitation, a thorough understanding of its underlying mechanisms is required. Although reward-driven enhancement of movement execution has been proposed to occur through enhanced feedback control, an untested alternative is that it is driven by increased arm stiffness, an energy-consuming process that increases limb stability. First, we demonstrate that during reaching reward improves selection and execution performance concomitantly without interference. Computational analysis revealed that reward led to both an increase in feedback correction during movement and a reduction in motor noise near the target. We provide novel evidence that this noise reduction is driven by a reward-dependent increase in arm stiffness. Therefore, reward drives multiple error-reduction mechanisms which enable individuals to invigorate motor performance without compromising accuracy.

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Dopamine-dependent loss aversion during effort-based decision-making

From psychology to economics there has been substantial interest in how costs (e.g., delay, risk) are represented asymmetrically during decision-making when attempting to gain reward or to avoid punishment. For example, in decision-making under risk, individuals show a tendency to prefer to avoid punishment than to acquire the equivalent reward (loss aversion). Although the cost of physical effort has received significant recent attention due to the evaluation of motor costs being crucial in our daily decisions, it remains unclear whether loss aversion exists during effort-based decision-making. On the one hand, loss aversion may be hardwired due to asymmetric evolutionary pressure on losses and gains and therefore exists across decision-making contexts. On the other hand, distinct brain regions are involved with different decision costs, making it questionable whether similar asymmetries exist. Here, we demonstrate that young healthy participants exhibit loss aversion during effort-based decision-making by exerting more physical effort in order to avoid punishment than to gain a same-size reward. Next, we show that medicated Parkinsons disease (PD) patients show a reduction in loss aversion compared to age-matched controls. Behavioural and computational analysis revealed that people with PD exerted similar physical effort in return for a reward, but were less willing to produce effort in order to avoid punishment. Therefore, loss aversion is present during effort-based decision-making and can be modulated by altered dopaminergic state. This finding could have important implications for our understanding of clinical disorders that show a reduced willingness to exert effort in the pursuit of reward.\n\nSignificance StatementLoss aversion - preferring to avoid punishment than to acquire equivalent reward - is an important concept in decision-making under risk. However, little is known about whether loss aversion also exists during decisions where the cost is physical effort. This is surprising given that motor cost shapes human behaviour, and a reduced willingness to exert effort is a characteristic of many clinical disorders. Here, we show that healthy individuals exert more effort to minimise punishment than to maximise reward (loss aversion). We also demonstrate that loss aversion is modulated by altered dopaminergic state by showing that medicated Parkinsons disease patients exert similar effort to gain reward but less effort to avoid punishment. Therefore, dopamine-dependent loss aversion is crucial for explaining effort-based decision-making.

animal behavior and cognition↗

Domain-specific working memory, but not dopamine-related genetic variability, shapes reward-based motor learning

The addition of rewarding feedback to motor learning tasks has been shown to increase the retention of learning, spurring interest in the possible utility for rehabilitation. However, laboratory-based motor tasks employing rewarding feedback have repeatedly been shown to lead to great inter-individual variability in performance. Understanding the causes of such variability is vital for maximising the potential benefits of reward-based motor learning. Thus, in this pre-registered study, we assessed whether spatial (SWM), verbal (VWM) and mental rotation (RWM) working memory capacity as well as dopamine-related genetic profiles could predict performance in two reward-based motor tasks, using a large cohort of participants (N=241). The first task assessed participants ability to follow a hidden and slowly shifting reward region based on hit/miss (binary) feedback. The second task investigated participants capacity to preserve performance with binary feedback after adapting to the shift with full visual feedback. Our results demonstrate that SWM strongly predicts a participants capacity to reliably reproduce a successful motor action, measured as change in reach angle following reward, while RWM predicted a participants propensity to express an explicit strategy when required to make large adjustments in reach angle. Therefore, both SWM and RWM were reliable predictors of success during reward-based motor learning. Change in reach direction following failure was also a strong predictor of success rate, although we observed no consistent relationship with any type of working memory. Surprisingly, no dopamine-related genotypes predicted performance. Therefore, working memory capacity plays a pivotal in determining individual ability in reward-based motor learning.\n\nSignificance statementReward-based motor learning tasks have repeatedly been shown to lead to idiosyncratic behaviours that cause varying degrees of task success. Yet, the factors determining an individuals capacity to use reward-based feedback are unclear. Here, we assessed a wide range of possible candidate predictors, and demonstrate that domain-specific working memory plays an essential role in determining individual capacity to use reward-based feedback. Surprisingly, genetic variations in dopamine availability were not found to play a role. This is in stark contrast with seminal work in the reinforcement and decision-making literature, which show strong and replicated effects of the same dopaminergic genes in decision-making. Therefore, our results provide novel insights in reward-based motor learning, highlighting a key role for domain-specific working memory capacity.

neuroscience↗

The role of explicit strategies during reinforcement-based motor learning

Despite increasing interest in the role of reward in motor learning, the underlying mechanisms remain ill-defined. In particular, the relevance of explicit strategies to reward-based motor learning is unclear. To address this, we examined subjects (n=30) ability to learn to compensate for a gradually introduced 25{degrees} visuomotor rotation with only reward-based feedback (binary success/failure). Only two-thirds of subjects (n=20) were successful at the maximum angle. The remaining subjects initially follow the rotation but after a variable number of trials begin to reach at an insufficiently large angle and subsequently return to near baseline performance (n=10). Furthermore, those that were successful accomplished this largely via the use of strategies, evidenced by a large reduction in reach angle when asked to remove any strategy they employed. However, both groups display a small degree of remaining retention even after the removal of strategies. All subjects made greater and more variable changes in reach angle following incorrect (unrewarded) trials. However, subjects who failed to learn showed decreased sensitivity to errors, even in the initial period in which they followed the rotation, a pattern previously found in Parkinsonian patients. In a second experiment, the addition of a secondary mental rotation task completely abolished learning (n=10), whilst a control group replicated the results of the first experiment (n=10). These results emphasize a pivotal role of strategy-use during reinforcement-based motor learning and the susceptibility of this form of learning to disruption has important implications for its potential therapeutic benefits.

neuroscience↗

The relationship between reinforcement and explicit strategies during visuomotor adaptation

The motor systems ability to adapt to changes in the environment is essential for maintaining accurate movements. During such adaptation several distinct systems are recruited: cerebellar sensory-prediction error learning, success-based reinforcement, and explicit strategy-use. Although much work has focused on the relationship between cerebellar learning and strategy-use, there is little research regarding how reinforcement and strategy-use interact. To address this, participants first learnt a 20{degrees} visuomotor displacement. After reaching asymptotic performance, binary, hit-or-miss feedback (BF) was introduced either with or without visual feedback, the latter promoting reinforcement. Subsequently, retention was assessed using no-feedback trials, with half of the participants in each group being instructed to stop using any strategy. Although BF led to an increase in retention of the visuomotor displacement, instructing participants to remove their strategy nullified this effect, suggesting strategy-use is critical to BF-based reinforcement. In a second experiment, we prevented the expression or development of a strategy during BF performance, by either constraining participants to a short preparation time (expression) or by introducing the displacement gradually (development). As both strongly impaired BF performance, it suggests reinforcement requires both the development and expression of a strategy. These results emphasise a pivotal role of strategy-use during reinforcement-based motor learning.

neuroscience↗

Age-dependent Pavlovian biases influence motor decision-making

Healthy ageing is associated with decreased risk taking in motor1 and economic2-4 decision-making. However, it is unknown whether a single underlying mechanism explains these changes. Age-related changes in economic risk taking are explained by reduced Pavlovian biases that promote action toward reward2, 5, 6. Although Pavlovian biases also promote inaction in the face of punishment, the role such Pavlovian biases play in motor decision-making, which additionally depends on estimating the probability of successfully executing an action7-10, is unknown. To address this, we developed a novel app-based motor decision-making task to measure sensitivity to reward and punishment when subjects (n=26,532) made a go/no-go motor gamble based on the perceived ability to execut ...

neuroscience↗

Reward and punishment enhance motor adaptation in stroke

The effects of motor learning, such as motor adaptation, in stroke rehabilitation are often transient, thus mandating approaches that enhance the amount of learning and retention. Previously, we showed in young individuals that reward-and punishment-feedback have dissociable effects on motor adaptation, with punishment improving adaptation and reward enhancing retention. If these findings were able to generalise to stroke patients, they would provide a way to optimize motor learning in these patients. Therefore, we tested this in 45 chronic stroke patients allocated in three groups. Patients performed reaching movements with their paretic arm with a robotic manipulandum. After training (day 1), day 2 involved adapting to a novel force-field. During this adaptation phase, patients received performance-based feedback according to the group they were allocated: reward, punishment or no feedback (neutral). On day 3, patients readapted to the force-field but all groups now received neutral feedback. All patients adapted, with reward and punishment groups displaying greater adaptation and readaptation than the neutral group, irrespective of demographic, cognitive or functional differences. Remarkably, the reward and punishment groups adapted to similar degree as healthy controls. Finally, the reward group showed greater retention. This study provides, for the first time, evidence that reward and punishment can enhance motor adaptation in stroke patients. Further research on reinforcement-based motor learning regimes is warranted to translate these promising results into clinical practice and improve motor rehabilitation outcomes in stroke patients.

neuroscience↗