Distinct mechanisms for online and offline motor skill learning across human development.

The human central nervous system (CNS) undergoes tremendous changes from childhood to adulthood and this may affect how individuals at different stages of development learn new skills. Here, we studied motor skill learning in children, adolescents, and young adults to test the prediction that differences in the maturation of different learning mechanisms lead to distinct temporal patterns of motor learning during practice and overnight. We found that overall learning did not differ between children, adolescents, and young adults. However, we demonstrate that adult-like skill learning is characterized by rapid and large improvements in motor performance during practice (i.e., online) that are susceptible to forgetting and decay over time (i.e., offline). On the other hand, child-like learning exhibits slower and less pronounced improvements in performance during practice, but these improvements are robust against forgetting and lead to gains in performance overnight without further practice. The different temporal dynamics of motor skill learning suggest an engagement of distinct learning mechanisms in the human CNS during development. In conclusion, adult-like skill learning mechanisms favor online improvements in motor performance whereas child-like learning mechanisms favors offline behavioral gains. RESEARCH HIGHLIGHTS: Many essential motor skills, like walking, talking, and writing, are acquired during childhood, and it is colloquially thought that children learn better than adults. We investigated dynamics of motor skill learning in children, adolescents, and young adults. Adults displayed substantial improvements during practice that was susceptible to forgetting over time. Children displayed smaller improvements during practice that were resilient against forgetting. The distinct age-related characteristics of these processes of acquisition and consolidation suggest that skill learning relies on different mechanisms in the immature and mature central nervous system.

Moving without sensory feedback: online TMS over the dorsal premotor cortex impairs motor performance during ischemic nerve block.

The study investigates the role of dorsal premotor cortex (PMd) in generating predicted sensory consequences of movements, i.e. corollary discharges. In 2 different sessions, we disrupted PMd and parietal hand's multisensory integration site (control area) with transcranial magnetic stimulation (TMS) during a finger-sequence-tapping motor task. In this TMS sham-controlled design, the task was performed with normal sensory feedback and during upper-limb ischemic nerve block (INB), in a time-window where participants moved without somatosensation. Errors and movement timing (objective measures) and ratings about movement perception (subjective measures) were collected. We found that INB overall worsens objective and subjective measures, but crucially in the PMd session, the absence of somatosensation together with TMS disruption induced more errors, less synchronized movements, and increased subjective difficulty ratings as compared with the parietal control session (despite a carryover effect between real and sham stimulation to be addressed in future studies). Contrarily, after parietal area interference session, when sensory information is already missing due to INB, motor performance was not aggravated. Altogether these findings suggest that the loss of actual (through INB) and predicted (through PMd disruption) somatosensory feedback degraded motor performance and perception, highlighting the crucial role of PMd in generating corollary discharge.

Valence, form, and content of self-talk predict sport type and level of performance.

In this paper, we aimed to test whether we could predict sport type (badminton or running) and marathon proficiency from the valence, form, and content of the athletes' self-reported inner speech. Additionally, we wanted to assess the difference between self-talk during high intensity and low intensity exercise. The present study corroborated existing research - we were able to predict both sport type in Study 1 and intensity level as well as marathon proficiency in Study 2 from questionnaire data using machine learning models. In Study 1, we found that badminton players engage more in worry and anxiety-control while runners are more prone to task disengagement. Interestingly, it seemed in Study 2 that the more participants engaged in condensed, positive, and repetitive self-talk when not pushing themselves, the slower their fastest marathons and half marathons were. We discuss potential explanations for these findings and make suggestions for future research.

Directed connectivity between primary and premotor areas underlying ankle force control in young and older adults.

The control of ankle muscle force is an integral component of walking and postural control. Aging impairs the ability to produce force steadily and accurately, which can compromise functional capacity and quality of life. Here, we hypothesized that reduced force control in older adults would be associated with altered cortico-cortical communication within a network comprising the primary motor area (M1), the premotor cortex (PMC), parietal, and prefrontal regions. We examined electroencephalographic (EEG) responses from fifteen younger (20-26 â€‹yr) and fifteen older (65-73 â€‹yr) participants during a unilateral dorsiflexion force-tracing task. Dynamic Causal Modelling (DCM) and Parametric Empirical Bayes (PEB) were used to investigate how directed connectivity between contralateral M1, PMC, parietal, and prefrontal regions was related to age group and precision in force production. DCM and PEB analyses revealed that the strength of connections between PMC and M1 were related to ankle force precision and differed by age group. For young adults, bidirectional PMC-M1 coupling was negatively related to task performance: stronger backward M1-PMC and forward PMC-M1 coupling was associated with worse force precision. The older group exhibited deviations from this pattern. For the PMC to M1 coupling, there were no age-group differences in coupling strength; however, within the older group, stronger coupling was associated with better performance. For the M1 to PMC coupling, older adults followed the same pattern as young adults - with stronger coupling accompanied by worse performance - but coupling strength was lower than in the young group. Our results suggest that bidirectional M1-PMC communication is related to precision in ankle force production and that this relationship changes with aging. We argue that the observed differences reflect compensatory reorganization that counteracts age-related sensorimotor declines and contributes to maintaining performance.

Spastic movement disorder: should we forget hyperexcitable stretch reflexes and start talking about inappropriate prediction of sensory consequences of movement?

Spastic movement disorder is characterized by reduced ability to selectively activate muscles with significant co-activation of antagonist muscles. It has traditionally been thought that hyperexcitable stretch reflexes have a central role in the pathophysiology and the clinical manifestations of the disorder. Here we argue that the main functional challenges for persons with spastic movement disorder are related to contractures, paresis, weak muscles and inappropriate central motor commands, whereas hyperexcitable reflexes play no or only an insignificant functional role. Co-activation of antagonist muscles and stiff posture and gait may rather be adaptations that aim to ensure joint and postural stability due to insufficient muscle strength. Aberrant (involuntary) muscle activity is likely related to an inadequate prediction of the sensory consequences of movement and a resulting impairment of muscle coordination. We argue that improvement of functional muscle strength and muscle coordination following central motor lesions may be achieved by optimizing integration of somatosensory information into central feedforward motor programs, whereas anti-spastic therapy that aims to reduce reflex activity may be less efficient. This opens for novel investigations into new treatment strategies that may improve functional control of movement and prevent reduced joint mobility in people with brain lesions.

Sense of agency for movements.

In this paper, we argue that the comparator model is not a satisfactory model of sense of agency (SoA). We present a theoretical argument and experimental studies. We show (1) most studies of SoA neglect a distinction between SoA associated with movements (narrow SoA) and SoA associated with environmental events (broad SoA); (2) the comparator model emerges from experimental studies of sensory consequences narrowly associated with movements; (3) narrow SoA can be explained by a comparator model, but a motor signal model is simpler and explain narrow SoA equally well; and (4) standard experimental paradigms study only broad SoA. Finally, we present results from two experiments, where we have failed to induce illusory narrow SoA in healthy participants. We believe our experimental approaches should have led to illusory SoA, if the comparator model of SoA was correct. The results challenge proponents of the comparator model of narrow SoA.

Tuning the Brake While Raising the Stake: Network Dynamics during Sequential Decision-Making.

UNLABELLED: When gathering valued goods, risk and reward are often coupled and escalate over time, for instance, during foraging, trading, or gambling. This escalating frame requires agents to continuously balance expectations of reward against those of risk. To address how the human brain dynamically computes these tradeoffs, we performed whole-brain fMRI while healthy young individuals engaged in a sequential gambling task. Participants were repeatedly confronted with the option to continue with throwing a die to accumulate monetary reward under escalating risk, or the alternative option to stop to bank the current balance. Within each gambling round, the accumulation of gains gradually increased reaction times for "continue" choices, indicating growing uncertainty in the decision to continue. Neural activity evoked by "continue" choices was associated with growing activity and connectivity of a cortico-subcortical "braking" network that positively scaled with the accumulated gains, including pre-supplementary motor area (pre-SMA), inferior frontal gyrus, caudate, and subthalamic nucleus (STN). The influence of the STN on continue-evoked activity in the pre-SMA was predicted by interindividual differences in risk-aversion attitudes expressed during the gambling task. Furthermore, activity in dorsal anterior cingulate cortex (ACC) reflected individual choice tendencies by showing increased activation when subjects made nondefault "continue" choices despite an increasing tendency to stop, but ACC activity did not change in proportion with subjective choice uncertainty. Together, the results implicate a key role of dorsal ACC, pre-SMA, inferior frontal gyrus, and STN in computing the trade-off between escalating reward and risk in sequential decision-making. SIGNIFICANCE STATEMENT: Using a paradigm where subjects experienced increasing potential rewards coupled with increasing risk, this study addressed two unresolved questions in the field of decision-making: First, we investigated an "inhibitory" network of regions that has so far been investigated with externally cued action inhibition. In this study, we show that the dynamics in this network under increasingly risky decisions are predictive of subjects' risk attitudes. Second, we contribute to a currently ongoing debate about the anterior cingulate cortex's role in sequential foraging decisions by showing that its activity is related to making nondefault choices rather than to choice uncertainty.

Modulation of fronto-parietal connections during the rubber hand illusion.

Accumulating evidence suggests that parieto-frontal connections play a role in adjusting body ownership during the Rubber Hand Illusion (RHI). Using a motor version of the rubber hand illusion paradigm, we applied single-site and dual-site transcranial magnetic stimulation (TMS) to investigate cortico-spinal and parietal-frontal connectivity during perceived rubber hand ownership. Healthy volunteers received a conditioning TMS pulse over left anterior intraparietal sulcus (aIPS) and a test TMS pulse over left primary motor cortex (M1). Motor Evoked Potentials (MEPs) were recorded at rest and during three RHI conditions: (i) agency and ownership, (ii) agency but no ownership and (iii) neither agency nor ownership. Parietal-motor communication differed among experimental conditions. The induction of action ownership was associated with an inhibitory parietal-to-motor connectivity, which was comparable to the aIPS-to-M1 inhibition present at rest. This aIPS-to-M1 inhibition disappeared during movement conditions not inducing ownership. Cortico-spinal excitability was not significantly modulated during the motor RHI as indicated by the task-constant MEP amplitude elicited by the M1 test pulse alone. Our results indicate that the perceived ownership over the rubber hand is associated with normal parietal-motor communication. This communication is disturbed if the sensorimotor conflict between one's own hand and the rubber hand is not resolved.

Dopamine replacement modulates oscillatory coupling between premotor and motor cortical areas in Parkinson's disease.

Efficient neural communication between premotor and motor cortical areas is critical for manual motor control. Here, we used high-density electroencephalography to study cortical connectivity in patients with Parkinson's disease (PD) and age-matched healthy controls while they performed repetitive movements of the right index finger at maximal repetition rate. Multiple source beamformer analysis and dynamic causal modeling were used to assess oscillatory coupling between the lateral premotor cortex (lPM), supplementary motor area (SMA), and primary motor cortex (M1) in the contralateral hemisphere. Elderly healthy controls showed task-related modulation in connections from lPM to SMA and M1, mainly within the γ-band (>30 Hz). Nonmedicated PD patients also showed task-related γ-γ coupling from lPM to M1, but γ coupling from lPM to SMA was absent. Levodopa reinstated physiological γ-γ coupling from lPM to SMA and significantly strengthened coupling in the feedback connection from M1 to lPM expressed as ß-ß as well as θ-ß coupling. Enhancement in cross-frequency θ-ß coupling from M1 to lPM was correlated with levodopa-induced improvement in motor function. The results show that PD is associated with an altered neural communication between premotor and motor cortical areas, which can be modulated by dopamine replacement.

The functional role of conscious sensation of movement.

This paper proposes a new framework for investigating neural signals sufficient for a conscious sensation of movement and their role in motor control. We focus on signals sufficient for proprioceptive awareness, particularly from muscle spindle activation and from primary motor cortex (M1). Our review of muscle vibration studies reveals that afferent signals alone can induce conscious sensations of movement. Similarly, studies employing peripheral nerve blocks suggest that efferent signals from M1 are sufficient for sensations of movement. On this basis, we show that competing theories of motor control assign different roles to sensation of movement. According to motor command theories, sensation of movement corresponds to an estimation of the current state based on afferent signals, efferent signals, and predictions. In contrast, within active inference architectures, sensations correspond to proprioceptive predictions driven by efferent signals from M1. The focus on sensation of movement provides a way to critically compare and evaluate the two theories. Our analysis offers new insights into the functional roles of movement sensations in motor control and consciousness.

Modulation of proprioceptive feedback during functional electrical stimulation: an fMRI study.

Functional electrical stimulation (FES) is sometimes used as a therapeutic modality in motor rehabilitation to augment voluntary motor drive to effect movement that would otherwise not be possible through voluntary activation alone. Effective motor rehabilitation should require that the central nervous system integrate efferent commands and appropriate afferent information to update the internal models of acquired skills. Here, we investigate whether FES-evoked (FES-ev) and FES-assisted (FES-as) movement are associated with the normal integration of motor commands and sensory feedback in a group of healthy participants during functional magnetic resonance imaging (fMRI). Sensory feedback was removed with a peripheral ischaemic nerve block while the participants performed voluntary (VOL), FES-ev or FES-as movement during fMRI. Before the peripheral nerve block, secondary somatosensory area (S2) activation was greater for the FES-ev and FES-as conditions than for the VOL condition. During the ischaemic nerve block, S2 activation was reduced for the FES-ev condition but not for FES-as and VOL conditions. The nerve block also reduced activation during FES in the primary somatosensory cortex and other motor areas including primary motor cortex, dorsal premotor cortex and supplementary motor area. In contrast, superior parietal lobule (area 7A) and precuneus activation was reduced as a consequence of the ischaemic nerve block in the VOL condition. These data suggest FES-related S2 activation is mainly a sensory phenomenon and does not reflect integration of sensory signals with motor commands.

Seeing or moving in parallel: the premotor cortex does both during bimanual coordination, while the cerebellum monitors the behavioral instability of symmetric movements.

The underlying neural mechanisms of a perceptual bias for in-phase bimanual coordination movements are not well understood. In the present study, we measured brain activity with functional magnetic resonance imaging in healthy subjects during a task, where subjects performed bimanual index finger adduction-abduction movements symmetrically or in parallel with real-time congruent or incongruent visual feedback of the movements. One network, consisting of bilateral superior and middle frontal gyrus and supplementary motor area (SMA), was more active when subjects performed parallel movements, whereas a different network, involving bilateral dorsal premotor cortex (PMd), primary motor cortex, and SMA, was more active when subjects viewed parallel movements while performing either symmetrical or parallel movements. Correlations between behavioral instability and brain activity were present in right lateral cerebellum during the symmetric movements. These findings suggest the presence of different error-monitoring mechanisms for symmetric and parallel movements. The results indicate that separate areas within PMd and SMA are responsible for both perception and performance of ongoing movements and that the cerebellum supports symmetric movements by monitoring deviations from the stable coordination pattern.

Mind over body: Interfering with the inner voice is detrimental to endurance performance.

In two preregistered experiments, we investigated whether covert language is involved in sustained physical efforts, specifically if people are less able to push themselves physically when distracted from using inner speech. In both experiments, participants performed 12 cycling trials (Experiment 1: N = 49; Experiment 2: N = 50), each lasting 1 min where participants were required to cycle as fast as possible while simultaneously engaging in either a visuospatial task, a verbal task or no interference. Experiment 1: Participants performed worse in the verbal interference condition compared with the control condition (d = 0.29) and verbal interference performance was numerically but not significantly worse than visuospatial interference (d = 0.22). Experiment 2: A more demanding interference task yielded significant slower cycling with verbal interference compared to both control (d = 1) and visuospatial interference (d = 0.43). These results indicate that inner speech plays a causal role in control of sustained physical efforts.

Interaction of electrical stimulation and voluntary hand movement in SII and the cerebellum during simulated therapeutic functional electrical stimulation in healthy adults.

The therapeutic application of functional electrical stimulation (FES) has shown promising clinical results in the rehabilitation of post-stroke hemiplegia. It appears that the effect is optimal when the patterned electrical stimulation is used in close synchrony with voluntary movement, although the neural mechanisms that underlie the clinical successes reported with therapeutic FES are unknown. One possibility is that therapeutic FES takes advantage of the sensory consequences of an internal model. Here, we investigate fMRI cortical activity when FES is combined with voluntary effort (FESVOL) and we compare this activity to that produced when FES and voluntary activity (VOL) are performed alone. FESVOL revealed greater cerebellar activity compared with FES alone and reduced activity bilaterally in secondary somatosensory areas (SII) compared with VOL alone. Reduced activity was also observed for FESVOL compared with FES alone in the angular gyrus, middle frontal gyrus and inferior frontal gyrus. These findings indicate that during the VOL condition the cerebellum predicts the sensory consequences of the movement and this reduces the subsequent activation in SII. The decreased SII activity may reflect a better match between the internal model and the actual sensory feedback. The greater cerebellar activity coupled with reduced angular gyrus activity in FESVOL compared with FES suggests that the cortex may interpret sensory information during the FES condition as an error-like signal due to the lack of a voluntary component in the movement.

Action-blindsight in healthy subjects after transcranial magnetic stimulation.

Clinical cases of blindsight have shown that visually guided movements can be accomplished without conscious visual perception. Here, we show that blindsight can be induced in healthy subjects by using transcranial magnetic stimulation over the visual cortex. Transcranial magnetic stimulation blocked the conscious perception of a visual stimulus, but subjects still corrected an ongoing reaching movement in response to the stimulus. The data show that correction of reaching movements does not require conscious perception of a visual target stimulus, even in healthy people. Our results support previous results suggesting that an efference copy is involved in movement correction, and this mechanism seems to be consistent even for movement correction without perception.

Premotor cortex modulates somatosensory cortex during voluntary movements without proprioceptive feedback.

Movement perception relies on sensory feedback, but the involvement of efference copies remains unclear. We investigated movements without proprioceptive feedback using ischemic nerve block during fMRI in healthy humans, and found preserved activation of the primary somatosensory cortex. This activation was associated with increased interaction with premotor cortex during voluntary movements, which demonstrates that perception of movements relies in part on predictions of sensory consequences of voluntary movements that are mediated by the premotor cortex.

Cortical signatures of precision grip force control in children, adolescents, and adults.

Human dexterous motor control improves from childhood to adulthood, but little is known about the changes in cortico-cortical communication that support such ontogenetic refinement of motor skills. To investigate age-related differences in connectivity between cortical regions involved in dexterous control, we analyzed electroencephalographic data from 88 individuals (range 8-30 years) performing a visually guided precision grip task using dynamic causal modelling and parametric empirical Bayes. Our results demonstrate that bidirectional coupling in a canonical 'grasping network' is associated with precision grip performance across age groups. We further demonstrate greater backward coupling from higher-order to lower-order sensorimotor regions from late adolescence in addition to differential associations between connectivity strength in a premotor-prefrontal network and motor performance for different age groups. We interpret these findings as reflecting greater use of top-down and executive control processes with development. These results expand our understanding of the cortical mechanisms that support dexterous abilities through development.

Measures of agency.

The sense of agency is typically defined as the experience of controlling one's own actions, and through them, changes in the external environment. It is often assumed that this experience is a single, unified construct that can be experimentally manipulated and measured in a variety of ways. In this article, we challenge this assumption. We argue that we should acknowledge four possible agency-related psychological constructs. Having a clear grasp of the possible constructs is important since experimental procedures are only able to target some but not all the possible constructs. The unacknowledged misalignment of the possible constructs of a sense of agency and the experimental procedures is a major theoretical and methodological obstacle to studying the sense of agency. Only if we recognize the nature of this obstacle will we be able to design the experimental paradigms that would enable us to study the responsible computational mechanisms.

Regional activation of the human medial temporal lobe during intentional encoding of objects and positions.

The medial temporal lobe (MTL) consists of several regions thought to be involved in learning and memory. However, the degree of functional specialization among these regions remains unclear. Previous studies have demonstrated effects of both content and processing stage, but findings have been inconsistent. In particular, studies have suggested that the perirhinal cortex is more involved in object processing than spatial processing, while other regions such as the parahippocampal cortex have been implicated in spatial processing. In this study, functional magnetic resonance imaging (fMRI) optimized for the MTL region was used to probe MTL activation during intentional encoding of object identities or positions. A region of interest analysis showed that object encoding evoked stronger activation than position encoding in bilateral perirhinal cortex, temporopolar cortex, parahippocampal cortex, hippocampus and amygdala. Results also indicate an unexpected significant correlation in activation level between anterior and posterior portions in both the left parahippocampal cortex and left hippocampus. Exploratory analysis did not show any regional content effects during preparation and rehearsal stages. These results provide additional evidence for functional specialization within the MTL, but were less clear regarding the specific nature of content specificity in these regions.

Brain correlates of aesthetic expertise: a parametric fMRI study.

Several studies have demonstrated that acquired expertise influences aesthetic judgments. In this paradigm we used functional magnetic resonance imaging (fMRI) to study aesthetic judgments of visually presented architectural stimuli and control-stimuli (faces) for a group of architects and a group of non-architects. This design allowed us to test whether level of expertise modulates neural activity in brain areas associated with either perceptual processing, memory, or reward processing. We show that experts and non-experts recruit bilateral medial orbitofrontal cortex (OFC) and subcallosal cingulate gyrus differentially during aesthetic judgment, even in the absence of behavioural aesthetic rating differences between experts and non-experts. By contrast, activity in nucleus accumbens (NAcc) exhibits a differential response profile compared to OFC and subcallosal cingulate gyrus, suggesting a dissociable role between these regions in the reward processing of expertise. Finally, categorical responses (irrespective of aesthetic ratings) resulted in expertise effects in memory-related areas such as hippocampus and precuneus. These results highlight the fact that expertise not only modulates cognitive processing, but also modulates the response in reward related brain areas.