Aging, brain plasticity, and motor learning.

Motor skill learning, the process of acquiring new motor skills, is critically important across the lifespan, from early development through adulthood and into older age, as well as in pathological conditions (i.e., rehabilitation). Extensive research has demonstrated that motor skill acquisition in young adults is accompanied by significant neuroplastic changes, including alterations in brain structure (gray and white matter), function (i.e., activity and connectivity), and neurochemistry (i.e., levels of neurotransmitters). In the aging population, motor performance typically declines, characterized by slower and less accurate movements. However, despite these age-related changes, older adults maintain the capacity for skill improvement through training. In this review, we explore the extent to which the aging brain retains the ability to adapt in response to motor learning, specifically whether skill acquisition is accompanied by neural changes. Furthermore, we discuss the associations between inter-individual variability in brain structure and function and the potential for future learning in older adults. Finally, we consider the use of non-invasive brain stimulation techniques aimed at optimizing motor learning in this population. Our review provides insights into the neurobiological underpinnings of motor learning in older adults and emphasizes strategies to enhance their motor skill acquisition.

Enhancing motor skill learning through multiple sessions of online high-definition transcranial direct current stimulation in healthy adults: insights from EEG power spectrum.

The purpose of this study was to evaluate the influence of high-definition transcranial direct current stimulation (HD-tDCS) on finger motor skill acquisition. Thirty-one healthy adult males were randomly assigned to one of three groups: online HD-tDCS (administered during motor skill learning), offline HD-tDCS (delivered before motor skill learning), and a sham group. Participants engaged in a visual isometric pinch task for three consecutive days. Overall motor skill learning and speed-accuracy tradeoff function were used to evaluate the efficacy of tDCS. Electroencephalography was recorded and power spectral density was calculated. Both online and offline HD-tDCS total motor skill acquisition was significantly higher than the sham group (P < 0.001 and P < 0.05, respectively). Motor skill acquisition in the online group was higher than offline (P = 0.132, Cohen's d = 1.46). Speed-accuracy tradeoff function in the online group was higher than both offline and sham groups in the post-test. The online group exhibited significantly lower electroencephalography activity in the frontal, fronto-central, and centro-parietal alpha band regions compared to the sham (P < 0.05). The findings suggest that HD-tDCS application can boost finger motor skill acquisition, with online HD-tDCS displaying superior facilitation. Furthermore, online HD-tDCS reduces the power of alpha rhythms during motor skill execution, enhancing information processing and skill learning efficiency.

Experience-driven competition in neural reorganization after stroke.

Behavioural experiences interact with regenerative responses to shape patterns of neural reorganization after stroke. This review is focused on the competitive nature of these behavioural experience effects. Interactions between learning-related plasticity and regenerative reactions have been found to underlie the establishment of new compensatory behaviours and the efficacy of motor rehabilitative training in rodent stroke models. Learning in intact brains depends on competitive and cooperative mechanisms of synaptic plasticity. Synapses are added in response to learning and selectively maintained and strengthened via activity-dependent competition. Long-term memories for experiences that occur closely in time can be weakened or enhanced by competitive or cooperative interactions in the time-dependent process of stabilizing synaptic changes. Rodent stroke model findings suggest that compensatory reliance on the non-paretic hand after stroke can shape and stabilize synaptic reorganization patterns in both hemispheres, to compete with the capacity for experiences of the paretic side to do so. However, the competitive edge of the non-paretic side can be countered by overlapping experiences of the paretic hand, and might even be shifted in a cooperative direction with skilfully coordinated bimanual experience. Advances in the basic understanding of learning-related synaptic competition are helping to inform the basis of experience-dependent variations in stroke outcome.

Association Between Physical Activity and Performance in Skill Learning Among Older Adults Based on Cognitive Function.

BACKGROUND/OBJECTIVES: Most older adults experience cognitive and physical functioning problems; however, they require the ability to learn skills in response to age-related or social environmental changes for independent living. This study aimed to clarify the associations between age-related physical activity and performance in skill learning tasks based on cognitive function. METHODS: Fifty-eight adults participated in this study and were divided into two groups: the control group (aged under 65 years) and older adult group (aged over 65). All the participants performed two-skill learning exercises based on cognitive function. Habitual exercise was measured using an accelerometer and a self-reported questionnaire. RESULTS: At baseline, the scores on skill tasks were lower in the older adult group than in the control group and were associated with habitual exercise and motor performance. Skill acquisition, observed in both groups, was associated with age and self-reported physical activity. Retention of the acquired skill was not associated with habitual exercise, and it declined significantly in the older group. CONCLUSIONS: Skill acquisition was maintained regardless of age; however, the ability to retain the acquired skills decreased among the older adults. Habitual physical activity was associated with skill acquisition but not the retention of the acquired skill. Significance/Implications: The study findings highlight the association between habitual exercise and motor skill learning in older adults, providing insight for practitioners in the rehabilitation and health care fields.

Different delayed consequences of attaining a plateau phase in practicing a simple (finger-tapping sequence learning) and a complex (Tower of Hanoi puzzle) task.

In practicing a new task, the initial performance gains, across consecutive trials, decrease; in the following phase, performance tends to plateau. However, after a long delay additional performance improvements may emerge (delayed/ "offline" gains). It has been suggested that the attainment of the plateau phase is a necessary condition for the triggering of skill consolidation processes that lead to the expression of delayed gains. Here we compared the effect of a long-delay (24-48 h) interval following each of the two within-session phases, on performance in a simple motor task, the finger-tapping sequence learning (FTSL), and in a conceptually complex task, the Tower of Hanoi puzzle (TOHP). In Experiment 1 we determined the amount of practice leading to the plateau phase within a single practice session (long practice), in each task. Experiment 2 consisted of three consecutive sessions with long-delay intervals in between; in the first session, participants underwent a short practice without attaining the plateau phase, but in the next two sessions, participants received long practice, attaining the plateau phase. In the FTSL, short practice resulted in no delayed gains after the long delay, but after 24-48 h following long practice, task performance was further improved. In contrast, no delayed gains evolved in the TOHP during the 24- to 48-h delay following long practice. We propose that the attainment of a plateau phase can indicate either the attainment of a comprehensive task solution routine (achievable for simple tasks) or a preservation of work-in-progress task solution routine (complex tasks); performance after a long post-practice interval can differentiate these two states.

Practice Reshapes the Geometry and Dynamics of Task-tailored Representations.

Extensive practice makes task performance more efficient and precise, leading to automaticity. However, theories of automaticity differ on which levels of task representations (e.g., low-level features, stimulus-response mappings, or high-level conjunctive memories of individual events) change with practice, despite predicting the same pattern of improvement (e.g., power law of practice). To resolve this controversy, we built on recent theoretical advances in understanding computations through neural population dynamics. Specifically, we hypothesized that practice optimizes the neural representational geometry of task representations to minimally separate the highest-level task contingencies needed for successful performance. This involves efficiently reaching conjunctive neural states that integrate task-critical features nonlinearly while abstracting over non-critical dimensions. To test this hypothesis, human participants (n = 40) engaged in extensive practice of a simple, context-dependent action selection task over 3 days while recording EEG. During initial rapid improvement in task performance, representations of the highest-level, context-specific conjunctions of task-features were enhanced as a function of the number of successful episodes. Crucially, only enhancement of these conjunctive representations, and not lower-order representations, predicted the power-law improvement in performance. Simultaneously, over sessions, these conjunctive neural states became more stable earlier in time and more aligned, abstracting over redundant task features, which correlated with offline performance gain in reducing switch costs. Thus, practice optimizes the dynamic representational geometry as task-tailored neural states that minimally tesselate the task space, taming their high-dimensionality.

Task-dependent coarticulation of movement sequences.

Combining individual actions into sequences is a hallmark of everyday activities. Classical theories propose that the motor system forms a single specification of the sequence as a whole, leading to the coarticulation of the different elements. In contrast, recent neural recordings challenge this idea and suggest independent execution of each element specified separately. Here, we show that separate or coarticulated sequences can result from the same task-dependent controller, without implying different representations in the brain. Simulations show that planning for multiple reaches simultaneously allows separate or coarticulated sequences depending on instructions about intermediate goals. Human experiments in a two-reach sequence task validated this model. Furthermore, in co-articulated sequences, the second goal influenced long-latency stretch responses to external loads applied during the first reach, demonstrating the involvement of the sensorimotor network supporting fast feedback control. Overall, our study establishes a computational framework for sequence production that highlights the importance of feedback control in this essential motor skill.

Properties of layer V pyramidal neurons in the primary motor cortex that represent acquired motor skills.

Layer V neurons in primary motor cortex (M1) are required for motor skill learning. We analyzed training-induced plasticity using a whole-cell slice patch-clamp technique with a rotor rod task, and found that training induces diverse changes in intrinsic properties and synaptic plasticity in M1 layer V neurons. Although the causal relationship between specific cellular changes and motor performance is unclear, by linking individual motor performance to cellular/synaptic functions, we identified several cellular and synaptic parameters that represent acquired motor skills. With respect to cellular properties, motor performance was positively correlated with resting membrane potential and fast afterhyperpolarization, but not with the membrane resistance, capacitance, or threshold. With respect to synaptic function, the performance was positively correlated with AMPA receptor-mediated postsynaptic currents, but not with GABAA receptor-mediated postsynaptic currents. With respect to live imaging analysis in Thy1-YFP mice, we further demonstrated a cross-correlation between motor performance, spine head volume, and self-entropy per spine. In the present study, we identified several changes in M1 layer V pyramidal neurons after motor training that represent acquired motor skills. Furthermore, training increased extracellular acetylcholine levels known to promote synaptic plasticity, which is correlated with individual motor performance. These results suggest that systematic control of specific intracellular parameters and enhancement of synaptic plasticity in M1 layer V neurons may be useful for improving motor skills.

Different time courses of maturation for learning and generalization following auditory training in children.

OBJECTIVE: We recently demonstrated that learning abilities among school-age children vary following frequency discrimination (FD) training, with some exhibiting mature adult-like learning while others performing poorly (non-adult-like learners). This study tested the hypothesis that children's post-training generalisation is related to their learning maturity. Additionally, it investigated how training duration influences children's generalisation, considering the observed decrease with increased training in adults. DESIGN: Generalisation to the untrained ear and untrained 2000 Hz frequency was assessed following single-session or nine-session 1000 Hz FD training, using an adaptive forced-choice procedure. Two additional groups served as controls for the untrained frequency. STUDY SAMPLE: Fifty-four children aged 7-9 years and 59 adults aged 18-30 years. RESULTS: (1) Only adult-like learners generalised their learning gains across frequency or ear, albeit less efficiently than adults; (2) As training duration increased children experienced reduced generalisation, similar to adults; (3) Children's performance in the untrained tasks correlated strongly with their trained task performance after the first training session. CONCLUSIONS: Auditory skill learning and its generalisation do not necessarily mature contemporaneously, although mature learning is a prerequisite for mature generalisation. Furthermore, in children, as in adults, more practice makes rather specific experts. These findings should be considered when designing training programs.

From task-general towards task-specific cognitive operations in a few minutes? Working memory performance as an adaptive process.

Measurement of cognitive functions is typically based on the implicit assumption that the mental architecture underlying cognitive task performance is constant throughout the task. In contrast, skill learning theory implies that cognitively demanding task performance is an adaptive process that progresses from initial heavy engagement of effortful and task-general metacognitive and executive control processes towards more automatic and task-specific performance. However, this hypothesis is rarely applied to the short time spans of traditional cognitive tasks such as working memory (WM) tasks. We utilised longitudinal structural equation models on two well-powered data sets to test the hypothesis that the initial stages of WM task performances load heavily on a task-general g-factor and then start to diverge towards factors specific to task structure. In line with the hypothesis, data from the first experiment (N = 296) were successfully fitted in a model with task-initial unity of the WM paradigm-specific latent factors, after which their intercorrelations started to diverge. The second experiment (N = 201) replicated this pattern except for one paradigm-specific latent factor. These preliminary results suggest that the processes underlying WM task performance tend to progress rapidly from more task-general towards task-specific, in line with the cognitive skill learning framework. Such task-internal dynamics has important implications for the measurement of complex cognitive functions.

The effects of reward and punishment on the performance of ping-pong ball bouncing.

Introduction: Reward and punishment modulate behavior. In real-world motor skill learning, reward and punishment have been found to have dissociable effects on optimizing motor skill learning, but the scientific basis for these effects is largely unknown. Methods: In the present study, we investigated the effects of reward and punishment on the performance of real-world motor skill learning. Specifically, three groups of participants were trained and tested on a ping-pong ball bouncing task for three consecutive days. The training and testing sessions were identical across the three days: participants were trained with their right (dominant) hand each day under conditions of either reward, punishment, or a neutral control condition (neither). Before and after the training session, all participants were tested with their right and left hands without any feedback. Results: We found that punishment promoted early learning, while reward promoted late learning. Reward facilitated short-term memory, while punishment impaired long-term memory. Both reward and punishment interfered with long-term memory gains. Interestingly, the effects of reward and punishment transferred to the left hand. Discussion: The results show that reward and punishment have different effects on real-world motor skill learning. The effects change with training and transfer readily to novel contexts. The results suggest that reward and punishment may act on different learning processes and engage different neural mechanisms during real-world motor skill learning. In addition, high-level metacognitive processes may be enabled by the additional reinforcement feedback during real-world motor skill learning. Our findings provide new insights into the mechanisms underlying motor learning, and may have important implications for practical applications such as sports training and motor rehabilitation.

Effect of Laterality in Microsurgery: Comparative Study of an Expert and a Novice.

Background: Hand laterality has an impact on surgical gestures. In this study, we sought to measure the multi-parameter variability of the microsurgical gesture depending on the hand used and the differences between expert microsurgeons and novices. Methods: Ten experienced microsurgeons and twenty medical students with no prior microsurgical experience performed arterial anastomosis on a chicken wing artery using dominant and non-dominant hands. We measured time and force using a homemade force-sensing microsurgical needle holder, heart rate variability with a Polar H10 chest strap, anxiety with the STAI-Y questionnaire and anastomosis quality using the MARS 10 scale. Results: In the microsurgeons' group, duration of anastomosis (p = 0.037), force applied to the needle holder (p = 0.047), anxiety (p = 0.05) and MARS10 (p = 0.291) were better with the dominant hand. For novices, there was no difference between the dominant and non-dominant hand pertaining to force, time and stress level. There were no differences between microsurgeons and novices pertaining to force and anxiety using the non-dominant hand. Conclusions: The study highlighted a marked laterality among microsurgical experts, a finding that may be explained by current learning methods. Surprisingly, no laterality is observed in students, suggesting that for a specific gesture completely different from everyday tasks, laterality is not predefined. Ambidexterity training in the residency curriculum seems relevant and may help microsurgeons improve performance and postoperative outcomes.

Alternative muscle synergy patterns of upper limb amputees.

Myoelectric hand prostheses are effective tools for upper limb amputees to regain hand functions. Much progress has been made with pattern recognition algorithms to recognize surface electromyography (sEMG) patterns, but few attentions was placed on the amputees' motor learning process. Many potential myoelectric prostheses users could not fully master the control or had declined performance over time. It is possible that learning to produce distinct and consistent muscle activation patterns with the residual limb could help amputees better control the myoelectric prosthesis. In this study, we observed longitudinal effect of motor skill learning with 2 amputees who have developed alternative muscle activation patterns in response to the same set of target prosthetic actions. During a 10-week program, amputee participants were trained to produce distinct and constant muscle activations with visual feedback of live sEMG and without interaction with prosthesis. At the end, their sEMG patterns were different from each other and from non-amputee control groups. For certain intended hand motion, gradually reducing root mean square (RMS) variance was observed. The learning effect was also assessed with a CNN-LSTM mixture classifier designed for mobile sEMG pattern recognition. The classification accuracy had a rising trend over time, implicating potential performance improvement of myoelectric prosthesis control. A follow-up session took place 6 months after the program and showed lasting effect of the motor skill learning in terms of sEMG pattern classification accuracy. The results indicated that with proper feedback training, amputees could learn unique muscle activation patterns that allow them to trigger intended prosthesis functions, and the original motor control scheme is updated. The effect of such motor skill learning could help to improve myoelectric prosthetic control performance.

Neural Filtering of Physiological Tremor Oscillations to Spinal Motor Neurons Mediates Short-Term Acquisition of a Skill Learning Task.

The acquisition of a motor skill involves adaptations of spinal and supraspinal pathways to alpha motoneurons. In this study, we estimated the shared synaptic contributions of these pathways to understand the neural mechanisms underlying the short-term acquisition of a new force-matching task. High-density surface electromyography (HDsEMG) was acquired from the first dorsal interosseous (FDI; 7 males and 6 females) and tibialis anterior (TA; 7 males and 4 females) during 15 trials of an isometric force-matching task. For two selected trials (pre- and post-skill acquisition), we decomposed the HDsEMG into motor unit spike trains, tracked motor units between trials, and calculated the mean discharge rate and the coefficient of variation of interspike interval (COVISI). We also quantified the post/pre ratio of motor units' coherence within delta, alpha, and beta bands. Force-matching improvements were accompanied by increased mean discharge rate and decreased COVISI for both muscles. Moreover, the area under the curve within alpha band decreased by ∼22% (TA) and ∼13% (FDI), with no delta or beta bands changes. These reductions correlated significantly with increased coupling between force/neural drive and target oscillations. These results suggest that short-term force-matching skill acquisition is mediated by attenuation of physiological tremor oscillations in the shared synaptic inputs. Supported by simulations, a plausible mechanism for alpha band reductions may involve spinal interneuron phase-cancelling descending oscillations. Therefore, during skill learning, the central nervous system acts as a matched filter, adjusting synaptic weights of shared inputs to suppress neural components unrelated to the specific task.

How did you perform? Investigating football players' perception of self-regulated passing performances under auditory noise environments.

Introduction: This paper deals with the question on how sport performances may be influenced by internal, emotional processes, which stem from outside feedback. Methods: In terms of methods, players' subjective performance ratings for four experimental auditory cue conditions were examined; these included both 'positive' and 'negative' stadium noise, 'no (auditory) conditions,' and a control/'baseline' condition. This resulted in a qualitative-analytic data set that was obtained succeeding each auditory cue condition using a unique football training machine (i.e., known as 'Footbonaut'). Without having received any coaching/performance feedback, players were asked to rate and individually comment on their perceived performance ratings for each experimental auditory condition. Results: Findings indicate stronger and more significant correlations between auditory conditions and subjective ratings compared to the non-auditory condition and its subjective rating. Furthermore, data provides initial insight into players' emotional experiences during each of the practice conditions. Discussion: These noteworthy findings on players' abilities to accurately judge their performances based on selfmonitoring and intrinsic feedback are discussed from an Ecological Dynamics perspective, linked to a Nonlinear Pedagogy for coaching. Here, representative and affective learning designs for skill learning and performance preparation are presented. Finally, a hypothetical catalyst effect of auditory stadium noise on subjective performance rating is proposed.

Cholecystokinin facilitates motor skill learning by modulating neuroplasticity in the motor cortex.

Cholecystokinin (CCK) is an essential modulator for neuroplasticity in sensory and emotional domains. Here, we investigated the role of CCK in motor learning using a single pellet reaching task in mice. Mice with a knockout of Cck gene (Cck-/-) or blockade of CCK-B receptor (CCKBR) showed defective motor learning ability; the success rate of retrieving reward remained at the baseline level compared to the wildtype mice with significantly increased success rate. We observed no long-term potentiation upon high-frequency stimulation in the motor cortex of Cck-/- mice, indicating a possible association between motor learning deficiency and neuroplasticity in the motor cortex. In vivo calcium imaging demonstrated that the deficiency of CCK signaling disrupted the refinement of population neuronal activity in the motor cortex during motor skill training. Anatomical tracing revealed direct projections from CCK-expressing neurons in the rhinal cortex to the motor cortex. Inactivation of the CCK neurons in the rhinal cortex that project to the motor cortex bilaterally using chemogenetic methods significantly suppressed motor learning, and intraperitoneal application of CCK4, a tetrapeptide CCK agonist, rescued the motor learning deficits of Cck-/- mice. In summary, our results suggest that CCK, which could be provided from the rhinal cortex, may surpport motor skill learning by modulating neuroplasticity in the motor cortex.

Information flow between motor cortex and striatum reverses during skill learning.

The coordination of neural activity across brain areas during a specific behavior is often interpreted as neural communication involved in controlling the behavior. However, whether information relevant to the behavior is actually transferred between areas is often untested. Here, we used information-theoretic tools to quantify how motor cortex and striatum encode and exchange behaviorally relevant information about specific reach-to-grasp movement features during skill learning in rats. We found a temporal shift in the encoding of behaviorally relevant information during skill learning, as well as a reversal in the primary direction of behaviorally relevant information flow, from cortex-to-striatum during naive movements to striatum-to-cortex during skilled movements. Standard analytical methods that quantify the evolution of overall neural activity during learning-such as changes in neural signal amplitude or the overall exchange of information between areas-failed to capture these behaviorally relevant information dynamics. Using these standard methods, we instead found a consistent coactivation of overall neural signals during movement production and a bidirectional increase in overall information propagation between areas during learning. Our results show that skill learning is achieved through a transformation in how behaviorally relevant information is routed across cortical and subcortical brain areas and that isolating the components of neural activity relevant to and informative about behavior is critical to uncover directional interactions within a coactive and coordinated network.

Dopamine Receptor-Expressing Neurons Are Differently Distributed throughout Layers of the Motor Cortex to Control Dexterity.

The motor cortex comprises the primary descending circuits for flexible control of voluntary movements and is critically involved in motor skill learning. Motor skill learning is impaired in patients with Parkinson's disease, but the precise mechanisms of motor control and skill learning are still not well understood. Here we have used transgenic mice, electrophysiology, in situ hybridization, and neural tract-tracing methods to target genetically defined cell types expressing D1 and D2 dopamine receptors in the motor cortex. We observed that putative D1 and D2 dopamine receptor-expressing neurons (D1+ and D2+, respectively) are organized in highly segregated, nonoverlapping populations. Moreover, based on ex vivo patch-clamp recordings, we showed that D1+ and D2+ cells have distinct morphological and electrophysiological properties. Finally, we observed that chemogenetic inhibition of D2+, but not D1+, neurons disrupts skilled forelimb reaching in adult mice. Overall, these results demonstrate that dopamine receptor-expressing cells in the motor cortex are highly segregated and play a specialized role in manual dexterity.

The Effects of Different Motor Teaching Strategies on Learning a Complex Motor Task.

During the learning of a new sensorimotor task, individuals are usually provided with instructional stimuli and relevant information about the target task. The inclusion of haptic devices in the study of this kind of learning has greatly helped in the understanding of how an individual can improve or acquire new skills. However, the way in which the information and stimuli are delivered has not been extensively explored. We have designed a challenging task with nonintuitive visuomotor perturbation that allows us to apply and compare different motor strategies to study the teaching process and to avoid the interference of previous knowledge present in the naïve subjects. Three subject groups participated in our experiment, where the learning by repetition without assistance, learning by repetition with assistance, and task Segmentation Learning techniques were performed with a haptic robot. Our results show that all the groups were able to successfully complete the task and that the subjects' performance during training and evaluation was not affected by modifying the teaching strategy. Nevertheless, our results indicate that the presented task design is useful for the study of sensorimotor teaching and that the presented metrics are suitable for exploring the evolution of the accuracy and precision during learning.

Strategy use and its evolvement in word list learning: a replication study.

Spontaneous strategy employment is important for memory performance, but systematic research on strategy use and within-task evolvement is limited. This online study aimed to replicate three main findings by Waris and colleagues in Quarterly Journal of Experimental Psychology (2021): in word-list learning, spontaneous strategy use (1) predicts better task performance, (2) stabilizes along the task, and (3) increases during the first two task blocks. We administered a shortened version of their original real-word list-learning task to 209 neurotypical adults. Their first finding was partly replicated: manipulation strategies (grouping, visualization, association, narrative, other strategy) but not maintenance strategies (rehearsal/repetition, selective focus) were associated with superior word recall. The second finding on the decrease in strategy changers over task blocks was replicated. The third finding turned out to be misguided: neither our nor the original study showed task-initial increase in strategy use in the real-word learning condition. Our results confirm the important role of spontaneous strategies in understanding memory performance and the existence of task-initial dynamics in strategy employment. They support the general conclusions by Waris and colleagues: task demands can trigger strategy use even in a familiar task like learning a list of common words, and evolution of strategy use during a memory task reflects cognitive skill learning.