Corrigendum: Motor learning in developmental coordination disorder: behavioral and neuroimaging study.

[This corrects the article DOI: 10.3389/fnins.2023.1187790.].

Interlimb transfer of sequential motor learning between upper and lower effectors.

BACKGROUND: Interlimb transfer of sequential motor learning (SML) refers to the positive influence of prior experiences in performing the same sequential movements using different effectors. Despite evidence from intermanual SML, and while most daily living activities involve interlimb cooperation and coordination between the four limbs, nothing is known about bilateral SML transfer between the upper and lower limbs. RESEARCH QUESTION: We examined the transfer of bilateral SML from the upper to the lower limbs and vice versa. METHODS: Twenty-four participants had to learn an initial bilateral SML task using the upper limbs and then performed the same sequence using the lower limbs during a transfer SML task. They performed the reversed situation 1 month apart. The performance was evaluated at the beginning and the end of both initial and transfer SML practice phases. RESULTS: Significant and reciprocal transfer gains in performance were observed regardless of the effectors. Greater transfer gains in performance were observed at the beginning of the transfer SML from the lower to the upper limbs (44 %) but these gains vanished after practice with the transfer effectors (5 %). Although smaller gains were initially achieved in the transfer of SML from the upper to the lower limbs (15 %), these gains persisted and remained significant (9 %) after practice with the transfer effectors. SIGNIFICANCE: Our results provide evidence of a reciprocal and asymmetrical interlimb transfer of bilateral SML between the upper and lower limbs. These findings could be leveraged as a relevant strategy in the context of sports and functional rehabilitation.

Fundamental processes in sensorimotor learning: Reasoning, refinement, and retrieval.

Motor learning is often viewed as a unitary process that operates outside of conscious awareness. This perspective has led to the development of sophisticated models designed to elucidate the mechanisms of implicit sensorimotor learning. In this review, we argue for a broader perspective, emphasizing the contribution of explicit strategies to sensorimotor learning tasks. Furthermore, we propose a theoretical framework for motor learning that consists of three fundamental processes: reasoning, the process of understanding action-outcome relationships; refinement, the process of optimizing sensorimotor and cognitive parameters to achieve motor goals; and retrieval, the process of inferring the context and recalling a control policy. We anticipate that this '3R' framework for understanding how complex movements are learned will open exciting avenues for future research at the intersection between cognition and action.

Corticospinal excitability at rest outside of a task does not differ from task intertrial intervals in healthy adults.

Human corticospinal excitability (CSE) modulates during movement, when muscles are active, but also at rest, when muscles are not active. These changes in resting motor system excitability can be transient or longer lasting. Evidence from transcranial magnetic stimulation (TMS) studies suggests even relatively short periods of motor learning on the order of minutes can have lasting effects on resting CSE. Whether individuals are able to return CSE to out-of-task resting levels during the intertrial intervals (ITI) of behavioral tasks that do not include an intended motor learning component is an important question. Here, in twenty-five healthy young adults, we used single-pulse TMS and electromyography (EMG) to measure motor evoked potentials (MEPs) during two different resting contexts: (1) prior to engaging in the response task during which participants were instructed only to rest (out-of-task), and (2) ITI of a choice-reaction time task (in-task). In both contexts, five TMS intensities were used to evaluate possible differences in recruitment of corticospinal (CS) output across a range of inputs. We hypothesized resting state CSE would be greater during ITI than out-of-task rest, reflected in larger MEP amplitudes. Contrary to our hypothesis, we observed no significant difference in MEP amplitudes between out-of-task rest and in-task ITI, and instead found evidence of equivalence, indicating that humans are able to return to a stable motor resting state within seconds after a response. These data support the interpretation that rest is a uniform motor state in the healthy nervous system. In the future, our data may be a useful reference for motor disorder populations with an impaired ability to return to rest.

Differential Components of Bradykinesia in Parkinson Disease Revealed by Deep Brain Stimulation.

Bradykinesia is a term describing several manifestations of movement disruption caused by Parkinson's disease (PD), including movement slowing, amplitude reduction, and gradual decrease of speed and amplitude over multiple repetitions of the same movement. Deep brain stimulation (DBS) of the subthalamic nucleus (STN) improves bradykinesia in patients with PD. We examined the effect of DBS on specific components of bradykinesia when applied at two locations within the STN, using signal processing techniques to identify the time course of amplitude and frequency of repeated hand pronation-supination movements performed by participants with and without PD. Stimulation at either location increased movement amplitude, increased frequency, and decreased variability, though not to the range observed in the control group. Amplitude and frequency showed decrement within trials, which was similar in PD and control groups and did not change with DBS. Decrement across trials, by contrast, differed between PD and control groups, and was reduced by stimulation. We conclude that DBS improves specific aspects of movement that are disrupted by PD, whereas it does not affect short-term decrement that could reflect muscular fatigue.

Structural Learning Benefits in a Visuomotor Adaptation Task Generalize to a Contralateral Effector.

Structural learning is characterized by facilitated adaptation following training on a set of sensory perturbations all belonging to the same structure (e.g., 'visuomotor rotations'). This generalization of learning is a core feature of the motor system and is often studied in the context of interlimb transfer. However, such transfer has only been demonstrated when participants learn to counter a specific perturbation in the sensory feedback of their movements; we determined whether structural learning in one limb generalized to the contralateral limb. We trained 13 participants to counter random visual feedback rotations between +/-90 degrees with the right hand and subsequently tested the left hand on a fixed rotation. The structural training group showed faster adaptation in the left hand in both feedforward and feedback components of reaching compared to 13 participants who trained with veridical reaching, with lower initial reaching error, and straighter, faster, and smoother movements than in the control group. The transfer was ephemeral - benefits were confined to roughly the first 20 trials. The results demonstrate that the motor system can extract invariant properties of seemingly random environments in one limb, and that this information can be accessed by the contralateral limb.

Sensorimotor Challenges in Minimally Invasive Surgery: A Theoretically-Oriented Review.

OBJECTIVE: This review surveys the literature on sensorimotor challenges impacting performance in laparoscopic minimally invasive surgery (MIS). BACKGROUND: Despite its well-known benefits for patients, achieving proficiency in MIS can be challenging for surgeons due to many factors including altered visual perspectives and fulcrum effects in instrument handling. Research on these and other sensorimotor challenges has been hindered by imprecise terminology and the lack of a unified theoretical framework to guide research questions in the field. METHOD: We conducted a systematic survey of the MIS literature, focusing on studies investigating sensorimotor challenges affecting laparoscopic performance. To provide a common foundation for cross-study comparisons, we propose a standardized taxonomy that distinguishes between different experimental paradigms used in the literature. We then show how the computational motor learning perspective provides a unifying theoretical framework for the field that can facilitate progress and motivate future research along clearer, hypothesis-driven lines. RESULTS: The survey identified diverse sensorimotor perturbations in MIS, which can be effectively categorized according to our proposed taxonomy. Studies investigating monitor-, camera-, and tool-based perturbations were systematically analyzed, elucidating their impact on surgical performance. We also show how the computational motor learning perspective provides deeper insights and potential strategies to mitigate challenges. CONCLUSION: Sensorimotor challenges significantly impact MIS, necessitating a systematic, empirically informed approach. Our proposed taxonomy and theoretical framework shed light on the complexities involved, paving the way for more structured research and targeted training approaches to enhance surgical proficiency. APPLICATION: Understanding the sensorimotor challenges inherent to MIS can guide the design of improved training curricula and inform the configuration of setups in the operating room to enhance surgeon performance and ultimately patient outcomes. This review offers key insights for surgeons, educators, and researchers in surgical performance and technology development.

Concerto of movement: how expertise shapes the synergistic control of upper limb muscles in complex motor tasks with varying tempo and dynamics.

Objective. This research aims to reveal how the synergistic control of upper limb muscles adapts to varying requirements in complex motor tasks and how expertise shapes the motor modules.Approach. We study the muscle synergies of a complex, highly skilled and flexible task-piano playing-and characterize expertise-related muscle-synergy control that permits the experts to effortlessly execute the same task at different tempo and force levels. Surface EMGs (28 muscles) were recorded from adult novice (N= 10) and expert (N= 10) pianists as they played scales and arpeggios at different tempo-force combinations. Muscle synergies were factorized from EMGs.Main results. We found that experts were able to cover both tempo and dynamic ranges using similar synergy selections and achieved better performance, while novices altered synergy selections more to adapt to the changing tempi and keystroke intensities compared with experts. Both groups relied on fine-tuning the muscle weights within specific synergies to accomplish the different task styles, while the experts could tune the muscles in a greater number of synergies, especially when changing the tempo, and switch tempo over a wider range.Significance. Our study sheds light on the control mechanism underpinning expertise-related motor flexibility in highly skilled motor tasks that require decade-long training. Our results have implications on musical and sports training, as well as motor prosthetic design.

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.

Online reach adjustments induced by real-time movement sonification.

Movement sonification can improve motor control in both healthy subjects (e.g., learning or refining a sport skill) and those with sensorimotor deficits (e.g., stroke patients and deafferented individuals). It is not known whether improved motor control and learning from movement sonification are driven by feedback-based real-time ("online") trajectory adjustments, adjustments to internal models over multiple trials, or both. We searched for evidence of online trajectory adjustments (muscle twitches) in response to movement sonification feedback by comparing the kinematics and error of reaches made with online (i.e., real-time) and terminal sonification feedback. We found that reaches made with online feedback were significantly more jerky than reaches made with terminal feedback, indicating increased muscle twitching (i.e., online trajectory adjustment). Using a between-subject design, we found that online feedback was associated with improved motor learning of a reach path and target over terminal feedback; however, using a within-subjects design, we found that switching participants who had learned with online sonification feedback to terminal feedback was associated with a decrease in error. Thus, our results suggest that, with our task and sonification, movement sonification leads to online trajectory adjustments which improve internal models over multiple trials, but which themselves are not helpful online corrections.

Sensing, feeling and regulating: investigating the association of focal brain damage with voluntary respiratory and motor control.

Breathing is a complex, vital function that can be modulated to influence physical and mental well-being. However, the role of cortical and subcortical brain regions in voluntary control of human respiration is underexplored. Here we investigated the influence of damage to human frontal, temporal or limbic regions on the sensation and regulation of breathing patterns. Participants performed a respiratory regulation task across regular and irregular frequencies ranging from 6 to 60 breaths per minute (bpm), with a counterbalanced hand motor control task. Interoceptive and affective states induced by each condition were assessed via questionnaire, and autonomic signals were indexed via skin conductance. Participants with focal lesions to the bilateral frontal lobe, right insula/basal ganglia and left medial temporal lobe showed reduced performance relative to individually matched healthy comparisons during the breathing and motor tasks. They also reported significantly higher anxiety during the 60 bpm regular and irregular breathing trials, with anxiety correlating with difficulty in rapid breathing specifically within this group. This study demonstrates that damage to frontal, temporal or limbic regions is associated with abnormal voluntary respiratory and motor regulation and tachypnoea-related anxiety, highlighting the role of the forebrain in affective and motor responses during breathing. This article is part of the theme issue 'Sensing and feeling: an integrative approach to sensory processing and emotional experience'.

Response inhibition in premotor cortex corresponds to a complex reshuffle of the mesoscopic information network.

Recent studies have explored functional and effective neural networks in animal models; however, the dynamics of information propagation among functional modules under cognitive control remain largely unknown. Here, we addressed the issue using transfer entropy and graph theory methods on mesoscopic neural activities recorded in the dorsal premotor cortex of rhesus monkeys. We focused our study on the decision time of a Stop-signal task, looking for patterns in the network configuration that could influence motor plan maturation when the Stop signal is provided. When comparing trials with successful inhibition to those with generated movement, the nodes of the network resulted organized into four clusters, hierarchically arranged, and distinctly involved in information transfer. Interestingly, the hierarchies and the strength of information transmission between clusters varied throughout the task, distinguishing between generated movements and canceled ones and corresponding to measurable levels of network complexity. Our results suggest a putative mechanism for motor inhibition in premotor cortex: a topological reshuffle of the information exchanged among ensembles of neurons.

In this study, we investigated the dynamics of information transfer among functionally identified neural modules during cognitive motor control. Our focus was on mesoscopic neural activities in the dorsal premotor cortex of rhesus monkeys engaged in a Stop-signal task. Leveraging multivariate transfer entropy and graph theory, we uncovered insights on how behavioral control shapes the topology of information transmission in a local brain network. Task phases modulated the strength and hierarchy of information exchange between modules, revealing the nuanced interplay between neural populations during generated and canceled movements. Notably, during successful inhibition, the network displayed a distinctive configuration, unveiling a novel mechanism for motor inhibition in the premotor cortex: a topological reshuffle of information among neuronal ensembles.

Sensorimotor Feedback Control Dysfunction as a Marker of Posttraumatic Stress Disorder.

BACKGROUND: Posttraumatic stress disorder (PTSD) is characterized not only by its direct association with traumatic events but also by a potential deficit in inhibitory control across emotional, cognitive, and sensorimotor domains. Recent research has shown that a continuous sensorimotor feedback control task, the rapid assessment of motor processing (RAMP) paradigm, can yield reliable measures of individual sensorimotor control performance. This study used this paradigm to investigate control deficits in PTSD relative to both healthy volunteer and a non-PTSD psychiatric comparison group. METHODS: We examined control processing using the RAMP paradigm in a sample of 40 individuals with PTSD, along with matched groups of 40 individuals with mood and anxiety (MA) complaints and 40 healthy controls (HC). We estimated Kp (drive) and Kd (damping) parameters using a proportion-derivative (PD) control modeling approach. RESULTS: The Kp parameter was lower in the PTSD group compared to the HC (Cohen's d = .86) and MA groups (Cohen's d = 0.63). After controlling for color-word inhibition, Kp remained lower in the PTSD group versus HC (Cohen's d = 0.79) and versus MA (Cohen's d = 0.62). Mediation analysis showed that Kd significantly mediated the relationship between PTSD and control deficits in the Kp parameter, with 96% of the effect mediated by Kd. CONCLUSIONS: These findings underscore the potential of using dynamic control paradigms to elucidate the control dysfunctions in PTSD and suggests that different psychiatric conditions may distinctly influence subcomponents of sensorimotor control.

MotorNet, a Python toolbox for controlling differentiable biomechanical effectors with artificial neural networks.

Artificial neural networks (ANNs) are a powerful class of computational models for unravelling neural mechanisms of brain function. However, for neural control of movement, they currently must be integrated with software simulating biomechanical effectors, leading to limiting impracticalities: (1) researchers must rely on two different platforms and (2) biomechanical effectors are not generally differentiable, constraining researchers to reinforcement learning algorithms despite the existence and potential biological relevance of faster training methods. To address these limitations, we developed MotorNet, an open-source Python toolbox for creating arbitrarily complex, differentiable, and biomechanically realistic effectors that can be trained on user-defined motor tasks using ANNs. MotorNet is designed to meet several goals: ease of installation, ease of use, a high-level user-friendly application programming interface, and a modular architecture to allow for flexibility in model building. MotorNet requires no dependencies outside Python, making it easy to get started with. For instance, it allows training ANNs on typically used motor control models such as a two joint, six muscle, planar arm within minutes on a typical desktop computer. MotorNet is built on PyTorch and therefore can implement any network architecture that is possible using the PyTorch framework. Consequently, it will immediately benefit from advances in artificial intelligence through PyTorch updates. Finally, it is open source, enabling users to create and share their own improvements, such as new effector and network architectures or custom task designs. MotorNet's focus on higher-order model and task design will alleviate overhead cost to initiate computational projects for new researchers by providing a standalone, ready-to-go framework, and speed up efforts of established computational teams by enabling a focus on concepts and ideas over implementation.

Motor learning alters vision, but vision does not alter motor learning.

During visuomotor learning, improvements in motor performance accompany changes in how people use vision. However, the dependencies between altered visual reliance and improvements in motor skill is unclear. The present studies used an online sequence learning task to quantify how changing the availability of visual information affected motor skill learning (Study One) and how changing motor skill affected visual reliance (Study Two). Participants used their keyboard to respond to targets falling vertically down a game screen. In Study One (n=49), the availability of visual information was altered by manipulating where the targets were visible on the screen. Three experimental groups practiced the task during full or limited vision conditions (when the targets were only visible in specific areas). We hypothesized that limiting visual information would reduce motor learning (i.e. the rate of improvement during training trial blocks). Instead, while participants performed worse during limited vision trials (p<0.001), there was no difference in learning rate (p=0.87). In Study Two (n=119), all participants practiced the task with full vision and their visual reliance (i.e., their performance change between full and limited vision conditions) was quantified before and after training. We hypothesized that with motor learning, visual reliance on future targets would increase, while visual reliance on the current targets would decrease. The results of Study Two partially support our hypotheses with visual reliance decreasing for all visual areas (p<0.001). Together, the results suggest changing motor skill alters how people use vision, but changing visual availability does not affect motor learning.

Boundaries of task-specificity: bimanual finger dexterity is reduced in musician's dystonia.

Task-specific dystonia leads to loss of sensorimotor control for a particular motor skill. Although focal in nature, it is hugely disabling and can terminate professional careers in musicians. Biomarkers for underlying mechanism and severity are much needed. In this study, we designed a keyboard device that measured the forces generated at all fingertips during individual finger presses. By reliably quantifying overflow to other fingers in the instructed (enslaving) and contralateral hand (mirroring) we explored whether this task could differentiate between musicians with and without dystonia. 20 right-handed professional musicians (11 with dystonia) generated isometric flexion forces with the instructed finger to match 25%, 50% or 75% of maximal voluntary contraction for that finger. Enslaving was estimated as a linear slope of the forces applied across all instructed/uninstructed finger combinations. Musicians with dystonia had a small but robust loss of finger dexterity. There was increased enslaving and mirroring, primarily during use of the symptomatic hand (enslaving p = 0.003; mirroring p = 0.016), and to a lesser extent with the asymptomatic hand (enslaving p = 0.052; mirroring p = 0.062). Increased enslaving and mirroring were seen across all combinations of finger pairs. In addition, enslaving was exaggerated across symptomatic fingers when more than one finger was clinically affected. Task-specific dystonia therefore appears to express along a gradient, most severe in the affected skill with subtle and general motor control dysfunction in the background. Recognition of this provides a more nuanced understanding of the sensorimotor control deficits at play and can inform therapeutic options for this highly disabling disorder.

Identical movement control exercises with and without synchronized breathing for chronic non-specific low back pain:A randomized pilot trial.

BACKGROUND: Exercise is a first-line treatment for chronic non-specific low back pain (CNSLBP). Exercise combined with specific breathing techniques have the potential to improve multifactorial outcomes. No previous studies, however, have compared outcomes between identical exercises with or without a specific breathing protocol in a uniform clinical study setting. OBJECTIVES: 1) To investigate the feasibility of combining synchronized breathing with movement control exercises and evaluate eligibility criteria, randomization procedures, and dropout rates. 2) To study the preliminary efficacy of the interventions on multifactorial outcome measures. METHODS: Thirty subjects with CNSLBP were randomized into two groups. Both groups had four contact clinic visits where they received personalized home movement control exercises to practice over two months. The experimental group included a movement control exercise intervention combined with synchronized breathing techniques. Trial registration number: NCT05268822. RESULTS: Feasibility was demonstrated by meeting the recruitment goal of 30 subjects within the pre-specified timeframe with enrolment rate of 24.8% (30/121). Synchronized breathing techniques were successfully adhered by participants. Home exercise adherence was nearly identical between the groups without any adverse events. Preliminary efficacy findings on pain intensity, disability, and self-efficacy in the experimental group exceeded the minimal clinically important difference. No such findings were observed in any outcome measures within the control group. Overall, multifactorial differences were consistent because nine out of eleven outcome measures showed greater improvements for the experimental group. CONCLUSION: The synchronized breathing with movement control exercises protocol was feasible and may be more beneficial for improving multifactorial outcomes compared to identical exercises alone. Results suggested progression to a full-scale trial.

Cortico-basal ganglia plasticity in motor learning.

One key function of the brain is to control our body's movements, allowing us to interact with the world around us. Yet, many motor behaviors are not innate but require learning through repeated practice. Among the brain's motor regions, the cortico-basal ganglia circuit is particularly crucial for acquiring and executing motor skills, and neuronal activity in these regions is directly linked to movement parameters. Cell-type-specific adaptations of activity patterns and synaptic connectivity support the learning of new motor skills. Functionally, neuronal activity sequences become structured and associated with learned movements. On the synaptic level, specific connections become potentiated during learning through mechanisms such as long-term synaptic plasticity and dendritic spine dynamics, which are thought to mediate functional circuit plasticity. These synaptic and circuit adaptations within the cortico-basal ganglia circuitry are thus critical for motor skill acquisition, and disruptions in this plasticity can contribute to movement disorders.

Subthalamic DBS does not restore deficits in corticospinal suppression during movement preparation in Parkinson's disease.

OBJECTIVE: Parkinson's disease (PD) patients exhibit changes in mechanisms underlying movement preparation, particularly the suppression of corticospinal excitability - termed "preparatory suppression" - which is thought to facilitate movement execution in healthy individuals. Deep brain stimulation (DBS) of the subthalamic nucleus (STN) being an attractive treatment for advanced PD, we aimed to study the potential contribution of this nucleus to PD-related changes in such corticospinal dynamics. METHODS: On two consecutive days, we applied single-pulse transcranial magnetic stimulation to the primary motor cortex of 20 advanced PD patients treated with bilateral STN-DBS (ON vs. OFF), as well as 20 healthy control subjects. Motor-evoked potentials (MEPs) were elicited at rest or during movement preparation in an instructed-delay choice reaction time task including left- or right-hand responses. Preparatory suppression was assessed by expressing MEPs during movement preparation relative to rest. RESULTS: PD patients exhibited a deficit in preparatory suppression when it was probed on the responding hand side, particularly when this corresponded to their most-affected hand, regardless of their STN-DBS status. CONCLUSIONS: Advanced PD patients displayed a reduction in preparatory suppression which was not restored by STN-DBS. SIGNIFICANCE: The current findings confirm that PD patients lack preparatory suppression, as previously reported. Yet, the fact that this deficit was not responsive to STN-DBS calls for future studies on the neural source of this regulatory mechanism during movement preparation.

Movement-related increases in subthalamic activity optimize locomotion.

The subthalamic nucleus (STN) is traditionally thought to restrict movement. Lesion or prolonged STN inhibition increases movement vigor and propensity, while optogenetic excitation has opposing effects. However, STN neurons often exhibit movement-related increases in firing. To address this paradox, STN activity was recorded and manipulated in head-fixed mice at rest and during self-initiated and self-paced treadmill locomotion. We found that (1) most STN neurons (type 1) exhibit locomotion-dependent increases in activity, with half firing preferentially during the propulsive phase of the contralateral locomotor cycle; (2) a minority of STN neurons exhibit dips in activity or are uncorrelated with movement; (3) brief optogenetic inhibition of the lateral STN (where type 1 neurons are concentrated) slows and prematurely terminates locomotion; and (4) in Q175 Huntington's disease mice, abnormally brief, low-velocity locomotion is associated with type 1 hypoactivity. Together, these data argue that movement-related increases in STN activity contribute to optimal locomotor performance.