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Motivating Motor Learning: The Role of Reward, Punishment and Dopamine

Periodic Reporting for period 4 - MotMotLearn (Motivating Motor Learning: The Role of Reward, Punishment and Dopamine)

Reporting period: 2020-04-01 to 2021-03-31

Motor learning (the ability of the brain to learn and update how an action is executed) is a fundamental process which influences many aspects of our lives such as learning to walk during childhood; the day-to-day behavioural adjustments required as an adult or in healthy ageing; and the rehabilitation process following an illness or injury. Despite the impact to society, it has proved extremely difficult to develop interventions that significantly enhance human motor learning. Therefore, devising protocols which optimise motor learning is a state-of-the-art research question that promises to deliver scientific, clinical and societal impact. Seeking reward and avoiding punishment are powerful factors in motivating humans to alter behaviour during cognition-based learning (selecting which action to perform), with sensitivity to reward and punishment being biased by the availability of dopamine in the brain. Intriguingly, reward and punishment are also known to affect generic motor learning (deciding how an action is executed) tasks which involve multiple underlying mechanisms. However to establish their potential for optimizing motor learning, we must understand how explicit reward- and punishment-based motivational feedback impact motor learning systems. Using an unprecedented combination of behavioural analysis, computational modelling, genetics and pharmacology, MotMotLearn will provide the first account of how reward, punishment and dopamine influence motor learning. This novel approach will enable MotMotLearn to develop protocols that utilise reward/punishment to optimise motor learning in healthy individuals and stroke patients suffering motor impairments. MotMotLearn will have a profound scientific impact in motor learning with applications to development, ageing, rehabilitation and sports.
The goal of MotMotLearn is understand how reward, punishment and dopamine influences motor learning. In total, 1450+ young healthy participants, 150+ older adults and 115+ clinical patients have been tested. After completion of the 5-year project, we have shown that motivational feedback has substantially differing effects depending on the type of motor learning being tested (Chen et al., 2017 & 2018). In addition, there also appears to be considerable individual differences between participants in terms of their ability to use reward-based feedback to learn new motor actions. Specifically, we found that only 2/3 of participants were able to learn with reward-based feedback (Holland et al., 2018; Codol et al., 2018). We have also begun to uncover the mechanisms which underlie the reward-based improvements in motor performance at a behavioural, neural and computational level (Codol et al., 2020; Codol et al., 2020). We examined whether genetic variability or working memory capacity could help explain individual differences in reward-based learning ability in a large cohort of participants (n=240). We found that working memory capacity, but not dopamine-related genetic variability, is predictive of reward-based motor learning ability (Holland et al., 2019). The role of dopamine has been examined using Parkinson’s disease patients and pharmacology. While Parkinson’s disease patients clearly show differences in reward/punishment sensitivity (Chen et al., 2020), we have been unable to modulate reward-based performance using Levodopa or Haloperidol (pharmacology) in young healthy adults (Sporn et al., in prep) or older healthy adults (Holland et al., in prep). In terms of stroke patients, we have shown that reward- and punishment-based feedback enhances the amount stroke patients (n=45) learn within a day and also how much they remember across days (Quattrocchi et al., 2017). We have also examined the improvements which occur in a large group (n=50) of stroke patients undergoing an intensive rehabilitation intervention with the goal being to understand the key aspects which reward could be used to improve (Dawson et al., in prep). In addition, we showed how reward can enhance performance of complex sequential actions and lead to long-term improvements in behaviour (Sporn et al., 2020). The final 12 months (including a 6 month extension) have been used to develop effective behavioural tasks that enables individuals to be assessed online (via smartphone and virtual reality devices). This promises to be an exciting avenue for future research in which this technology can be used to develop online rehabilitation interventions. Four exceptional team members made important contributions to the project and have all made successful transitions to the next stages of their career. Despite Covid, MotMotLearn has achieved its major planned deliverables of the project. This has delivered 10 influential research articles involving research staff from the grant and a further 11 involving the principal investigator, whilst research results have been presented at 13 international conferences and 13 world-leading Universities. The work from MotMotLearn led to an ERC proof-of-concept grant being awarded which aims to develop at-home reward-based interventions for stroke patients. Work from MotMotLearn has been presented at 10 outreach activities aimed to disseminate the results to the general public. In addition, MotMotLearn had its own webpage and regular updates were provided through twitter, YouTube and podcasts.
MotMotLearn has provided an in-depth account concerning the positive impact of reward, punishment and dopamine on the motor system in health and disease. Importantly, it has highlighted that we cannot simply apply reward/punishment feedback to every situation with the assumption that it is always beneficial. However, there have been setbacks in using genetics and pharmacology to enhance the effects of reward-based feedback on motor learning/performance. Despite this, MotMotLearn has provided essential details regarding the mechanisms which underlie reward-based improvements in motor performance. It has provided novel insight into the behavioural, physiological and neural mechanisms which underpin the beneficial effects of reward on motor performance, and revealed the benefits of reward-based feedback to motor learning in stroke patients. MotMotLearn examined the key aspects of stroke rehabilitation which reward-based feedback should be focussed on in addition to investigating the role of reward in improving motor behaviour in more complex actions more akin to activities of daily life. This had provided a comprehensive understanding of how and when reward-based feedback should be used to improve motor behaviour, in addition to the key factors which must be factored in when using this form of feedback. By defining the behavioural and theoretically boundaries in which motivation can have beneficial effects on motor learning and performance, MotMotLearn has created a roadmap which should enable these concepts to be applied to motor learning across the lifespan. Finally, MotMotLearn developed novel virtual reality technology which will allow novel reward-based interventions to be developed for ‘at home’ rehabilitation. This work was the basis of a successful ERC proof-of-concept grant which aims to develop these tasks and technology. This work not only has the clear societal impact but should also have the economic impact of identifying the situations where motivational feedback is a valid intervention.