scholarly journals Modulation of neural activity in frontopolar cortex drives reward-based motor learning

2020 ◽  
Author(s):  
M Herrojo Ruiz ◽  
T Maudrich ◽  
B Kalloch ◽  
D Sammler ◽  
R Kenville ◽  
...  

AbstractDecision-making is increasingly being recognised to play a role in learning motor skills. Understanding the neural processes regulating motor decision-making is therefore essential to identify mechanisms that contribute to motor skill learning. In decision-making tasks, the frontopolar cortex (FPC) is involved in tracking the reward of different alternative choices, as well as their reliability. Whether this FPC function extends to reward landscapes associated with a continuous movement dimension remains unknown. Here we used anodal transcranial direct current stimulation (tDCS) over the right FPC to investigate its role in reward-based motor learning. Nineteen healthy human participants completed a motor sequence learning task using trial-wise reward feedback to discover a hidden performance goal along a continuous dimension: timing. As a control condition, we modulated contralateral motor cortex (left M1) activity with tDCS, which has been shown to benefit motor skill learning but less consistently reward-based motor learning. Each active tDCS condition was contrasted to sham stimulation. Right FPC-tDCS led to faster learning primarily through a regulation of exploration, without concurrent modulation of motor noise. A Bayesian computational model revealed that following rFPC-tDCS, participants had a higher expectation of reward, consistent with their faster learning. These higher reward estimates were inferred to be less volatile, and thus participants under rFPC-tDCS deemed the mapping between movement and reward to be more stable. Relative to sham, lM1-tDCS did not significantly modulate main behavioral outcomes. The results indicate that brain regions previously linked to decision-making, such as the FPC, are relevant for motor skill learning.

2020 ◽  
Vol 2 (2) ◽  
Author(s):  
Svenja Espenhahn ◽  
Holly E Rossiter ◽  
Bernadette C M van Wijk ◽  
Nell Redman ◽  
Jane M Rondina ◽  
...  

Abstract Recovery of skilled movement after stroke is assumed to depend on motor learning. However, the capacity for motor learning and factors that influence motor learning after stroke have received little attention. In this study, we first compared motor skill acquisition and retention between well-recovered stroke patients and age- and performance-matched healthy controls. We then tested whether beta oscillations (15–30 Hz) from sensorimotor cortices contribute to predicting training-related motor performance. Eighteen well-recovered chronic stroke survivors (mean age 64 ± 8 years, range: 50–74 years) and 20 age- and sex-matched healthy controls were trained on a continuous tracking task and subsequently retested after initial training (45–60 min and 24 h later). Scalp electroencephalography was recorded during the performance of a simple motor task before each training and retest session. Stroke patients demonstrated capacity for motor skill learning, but it was diminished compared to age- and performance-matched healthy controls. Furthermore, although the properties of beta oscillations prior to training were comparable between stroke patients and healthy controls, stroke patients did show less change in beta measures with motor learning. Lastly, although beta oscillations did not help to predict motor performance immediately after training, contralateral (ipsilesional) sensorimotor cortex post-movement beta rebound measured after training helped predict future motor performance, 24 h after training. This finding suggests that neurophysiological measures such as beta oscillations can help predict response to motor training in chronic stroke patients and may offer novel targets for therapeutic interventions.


1992 ◽  
Vol 12 (1) ◽  
pp. 110-119 ◽  
Author(s):  
Krystyna R. Isaacs ◽  
Brenda J. Anderson ◽  
Adriana A. Alcantara ◽  
James E. Black ◽  
William T. Greenough

This study compared the morphology of cerebellar cortex in adult female rats exposed for 1 month to repetitive exercise, motor learning, or an inactive condition. In the exercise conditions, rats that were run on a treadmill or housed with access to a running wheel had a shorter diffusion distance from blood vessels in the molecular layer of the paramedian lobule when compared to rats housed individually or rats that participated in a motor skill learning task. Rats taught complex motor skills substantially increased the volume of the molecular layer per Purkinje neuron and increased blood vessel number sufficiently to maintain the diffusion distance. These results dissociate angiogenesis associated with increased neuropil volume (as seen in the motor learning group) from angiogenesis associated with increased metabolic demands (as seen in the exercise groups). While the volume fraction of mitochondria did not differ among groups, the mitochondrial volume fraction per Purkinje cell was significantly increased in the motor skill rats. This appears to parallel the previously reported increase in synapses and associated neuropil volume change.


2021 ◽  
Vol 11 (1) ◽  
Author(s):  
M. Herrojo Ruiz ◽  
T. Maudrich ◽  
B. Kalloch ◽  
D. Sammler ◽  
R. Kenville ◽  
...  

AbstractThe frontopolar cortex (FPC) contributes to tracking the reward of alternative choices during decision making, as well as their reliability. Whether this FPC function extends to reward gradients associated with continuous movements during motor learning remains unknown. We used anodal transcranial direct current stimulation (tDCS) over the right FPC to investigate its role in reward-based motor learning. Nineteen healthy human participants practiced novel sequences of finger movements on a digital piano with corresponding auditory feedback. Their aim was to use trialwise reward feedback to discover a hidden performance goal along a continuous dimension: timing. We additionally modulated the contralateral motor cortex (left M1) activity, and included a control sham stimulation. Right FPC-tDCS led to faster learning compared to lM1-tDCS and sham through regulation of motor variability. Bayesian computational modelling revealed that in all stimulation protocols, an increase in the trialwise expectation of reward was followed by greater exploitation, as shown previously. Yet, this association was weaker in lM1-tDCS suggesting a less efficient learning strategy. The effects of frontopolar stimulation were dissociated from those induced by lM1-tDCS and sham, as motor exploration was more sensitive to inferred changes in the reward tendency (volatility). The findings suggest that rFPC-tDCS increases the sensitivity of motor exploration to updates in reward volatility, accelerating reward-based motor learning.


2014 ◽  
Vol 112 (1) ◽  
pp. 156-164 ◽  
Author(s):  
James P. Coxon ◽  
Nicola M. Peat ◽  
Winston D. Byblow

Motor learning requires practice over a period of time and depends on brain plasticity, yet even for relatively simple movements, there are multiple practice strategies that can be used for skill acquisition. We investigated the role of intracortical inhibition in the primary motor cortex (M1) during motor skill learning. Event-related transcranial magnetic stimulation (TMS) was used to assess corticomotor excitability and inhibition thought to involve synaptic and extrasynaptic γ-aminobutyric acid (GABA). Short intracortical inhibition (SICI) was assessed using 1- and 2.5-ms interstimulus intervals (ISIs). Participants learned a novel, sequential pinch-grip task on a computer in either a repetitive or interleaved practice structure. Both practice structures showed equivalent levels of motor performance at the end of acquisition and at retention 1 wk later. There was a novel task-related modulation of 1-ms SICI. Repetitive practice elicited a greater reduction of 1- and 2.5-ms SICI, i.e., disinhibition, between rest and task acquisition, compared with interleaved practice. These novel findings support the use of a repetitive practice structure for motor learning because the associated effects within M1 have relevance for motor rehabilitation.


2005 ◽  
Vol 28 (1) ◽  
pp. 70-71 ◽  
Author(s):  
Luca A. Finelli ◽  
Terrence J. Sejnowski

Learning procedural skills involves improvement in speed and accuracy. Walker proposes two stages of memory consolidation: enhancement, which requires sleep, and stabilization, which does not require sleep. Speed improvement for a motor learning task but not accuracy occurs after sleep-dependent enhancement. We discuss this finding in the context of computational models and underlying sleep mechanisms.


2009 ◽  
Vol 89 (4) ◽  
pp. 370-383 ◽  
Author(s):  
Catherine F Siengsukon ◽  
Lara A Boyd

Sleep following motor skill practice has repeatedly been demonstrated to enhance motor skill learning off-line (continued overnight improvements in motor skill that are not associated with additional physical practice) for young people who are healthy. Mounting evidence suggests that older people who are healthy fail to demonstrate sleep-dependent off-line motor learning. However, little is known regarding the influence of sleep on motor skill enhancement following damage to the brain. Emerging evidence suggests that individuals with brain damage, particularly following stroke, do benefit from sleep to promote off-line motor skill learning. Because rehabilitation following stroke requires learning new, and re-learning old, motor skills, awareness that individuals with stroke benefit from a period of sleep following motor skill practice to enhance skill learning could affect physical therapist practice. The objective of this article is to present the evidence demonstrating sleep-dependent off-line motor learning in young people who are healthy and the variables that may influence this beneficial sleep-dependent skill enhancement. In young people who are healthy, these variables include the stages of memory formation, the type of memory, the type of instruction provided (implicit versus explicit learning), and the task utilized. The neural mechanisms thought to be associated with sleep-dependent off-line motor learning also are considered. Research examining whether older adults who are healthy show the same benefits of sleep as do younger adults is discussed. The data suggest that older adults who are healthy do not benefit from sleep to promote off-line skill enhancement. A possible explanation for the apparent lack of sleep-dependent off-line motor learning by older adults who are healthy is presented. Last, emerging evidence showing that individuals with chronic stroke demonstrate sleep-dependent off-line motor skill learning and some of the possible mechanisms for this effect are considered.


BMJ Open ◽  
2021 ◽  
Vol 11 (7) ◽  
pp. e045841
Author(s):  
David Matthews ◽  
Edith Elgueta Cancino ◽  
Deborah Falla ◽  
Ali Khatibi

IntroductionMotor skill learning is intrinsic to living. Pain demands attention and may disrupt non-pain-related goals such as learning new motor skills. Although rehabilitation approaches have used motor skill learning for individuals in pain, there is uncertainty on the impact of pain on learning motor skills.Methods and analysisThe protocol of this systematic review has been designed and is reported in accordance with criteria set out by the Preferred Reporting Items for Systematic Review and Meta-Analysis Protocols guidelines. Web of Science, Scopus, MEDLINE, Embase and CINAHL databases; key journals; and grey literature will be searched up until March 2021, using subject-specific searches. Two independent assessors will oversee searching, screening and extracting of data and assessment of risk of bias. Both behavioural and activity-dependent plasticity outcome measures of motor learning will be synthesised and presented. The quality of evidence will be assessed using the Grading of Recommendations Assessment, Development and Evaluation approach.Ethics and disseminationNo patient data will be collected, and therefore, ethical approval was not required for this review. The results of this review will provide further understanding into the complex effects of pain and may guide clinicians in their use of motor learning strategies for the rehabilitation of individuals in pain. The results of this review will be published in a peer-reviewed journal and presented at scientific conferences.PROSPERO registration numberCRD42020213240.


2021 ◽  
Author(s):  
Pierre Vassiliadis ◽  
Gerard Derosiere ◽  
Cecile Dubuc ◽  
Aegryan Lete ◽  
Frederic Crevecoeur ◽  
...  

AbstractBesides relying heavily on sensory and reinforcement feedback, motor skill learning may also depend on the level of motivation experienced during training. Yet, how motivation by reward modulates motor learning remains unclear. In 90 healthy subjects, we investigated the net effect of motivation by reward on motor learning while controlling for the sensory and reinforcement feedback received by the participants. Reward improved motor skill learning beyond performance-based reinforcement feedback. Importantly, the beneficial effect of reward involved a specific potentiation of reinforcement-related adjustments in motor commands, which concerned primarily the most relevant motor component for task success and persisted on the following day in the absence of reward. We propose that the long-lasting effects of motivation on motor learning may entail a form of associative learning resulting from the repetitive pairing of the reinforcement feedback and reward during training, a mechanism that may be exploited in future rehabilitation protocols.


2021 ◽  
Author(s):  
Maria Herrojo Ruiz ◽  
Tom Maudrich ◽  
Benjamin Kalloch ◽  
Daniela Sammler ◽  
Rouven Kenville ◽  
...  

Abstract The frontopolar cortex (FPC) contributes to tracking the reward of alternative choices during decision making, as well as their reliability. Whether this FPC function extends to reward gradients associated with continuous movements during motor learning remains unknown. We used anodal transcranial direct current stimulation (tDCS) over the right FPC to investigate its role in reward-based motor learning. Nineteen healthy human participants completed a motor sequence learning task using trialwise reward feedback to discover a hidden goal along a continuous dimension: timing. As additional conditions, we modulated the contralateral motor cortex (left M1) activity, and included a control sham stimulation. Right FPC-tDCS led to faster learning compared to lM1-tDCS and sham through regulation of motor variability. Computational modelling revealed that in all stimulation protocols, an increase in the trialwise expectation of reward was followed by greater exploitation, as shown previously. Yet, this association was weaker in lM1-tDCS suggesting a less efficient learning strategy. The effects of frontopolar stimulation were dissociated from those induced by lM1-tDCS and sham, as motor exploration was more sensitive to inferred changes in the reward tendency (volatility). The findings suggest that rFPC-tDCS increases the sensitivity of motor exploration to updates in reward volatility, accelerating reward-based motor learning.


2021 ◽  
Vol 118 (23) ◽  
pp. e2102242118
Author(s):  
Jasmine Herszage ◽  
Haggai Sharon ◽  
Nitzan Censor

Learning motor skills commonly requires repeated execution to achieve gains in performance. Motivated by memory reactivation frameworks predominantly originating from fear-conditioning studies in rodents, which have extended to humans, we asked the following: Could motor skill learning be achieved by brief memory reactivations? To address this question, we had participants encode a motor sequence task in an initial test session, followed by brief task reactivations of only 30 s each, conducted on separate days. Learning was evaluated in a final retest session. The results showed that these brief reactivations induced significant motor skill learning gains. Nevertheless, the efficacy of reactivations was not consistent but determined by the number of consecutive correct sequences tapped during memory reactivations. Highly continuous reactivations resulted in higher learning gains, similar to those induced by full extensive practice, while lower continuity reactivations resulted in minimal learning gains. These results were replicated in a new independent sample of subjects, suggesting that the quality of memory reactivation, reflected by its continuity, regulates the magnitude of learning gains. In addition, the change in noninvasive brain stimulation measurements of corticospinal excitability evoked by transcranial magnetic stimulation over primary motor cortex between pre- and postlearning correlated with retest and transfer performance. These results demonstrate a unique form of rapid motor skill learning and may have far-reaching implications, for example, in accelerating motor rehabilitation following neurological injuries.


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