Efficient musculoskeletal annotation using free-form deformation.

Traditionally, constructing training datasets for automatic muscle segmentation from medical images involved skilled operators, leading to high labor costs and limited scalability. To address this issue, we developed a tool that enables efficient annotation by non-experts and assessed its effectiveness for training an automatic segmentation network. Our system allows users to deform a template three-dimensional (3D) anatomical model to fit a target magnetic-resonance image using free-form deformation with independent control points for axial, sagittal, and coronal directions. This method simplifies the annotation process by allowing non-experts to intuitively adjust the model, enabling simultaneous annotation of all muscles in the template. We evaluated the quality of the tool-assisted segmentation performed by non-experts, which achieved a Dice coefficient greater than 0.75 compared to expert segmentation, without significant errors such as mislabeling adjacent muscles or omitting musculature. An automatic segmentation network trained with datasets created using this tool demonstrated performance comparable to or superior to that of networks trained with expert-generated datasets. This innovative tool significantly reduces the time and labor costs associated with dataset creation for automatic muscle segmentation, potentially revolutionizing medical image annotation and accelerating the development of deep learning-based segmentation networks in various clinical applications.

Decision uncertainty as a context for motor memory.

The current view of perceptual decision-making suggests that once a decision is made, only a single motor programme associated with the decision is carried out, irrespective of the uncertainty involved in decision making. In contrast, we show that multiple motor programmes can be acquired on the basis of the preceding uncertainty of the decision, indicating that decision uncertainty functions as a contextual cue for motor memory. The actions learned after making certain (uncertain) decisions are only partially transferred to uncertain (certain) decisions. Participants were able to form distinct motor memories for the same movement on the basis of the preceding decision uncertainty. Crucially, this contextual effect generalizes to novel stimuli with matched uncertainty levels, demonstrating that decision uncertainty is itself a contextual cue. These findings broaden the understanding of contextual inference in motor memory, emphasizing that it extends beyond direct motor control cues to encompass the decision-making process.

Transition between individually different and common features in skilled drumming movements.

Why do professional athletes and musicians exhibit individually different motion patterns? For example, baseball pitchers generate various pitching forms, e.g., variable wind-up, cocking, and follow-through forms. However, they commonly rotate their wrists and fingers at increasingly high speeds via shoulder and trunk motions. Despite the universality of common and individually different motion patterns in skilled movements, the abovementioned question remains unanswered. Here, we focus on a motion required to hit a snare drum, including the indirect phase of task achievement (i.e., the early movement and mid-flight phases) and the direct phase of task achievement (i.e., the hit phase). We apply tensor decomposition to collected kinematic data for the drum-hitting motion, enabling us to decompose high-dimensional and time-varying motion data into individually different and common movement patterns. As a result, individually different motion patterns emerge during the indirect phase of task achievement, and common motion patterns are evident in the direct phase of task achievement. Athletes and musicians are thus possibly allowed to perform individually different motion patterns during the indirect phase of task achievement. Additionally, they are required to exhibit common patterns during the direct phase of task achievement.

Validity of Freehand 3-D Ultrasound System in Measurement of the 3-D Surface Shape of Shoulder Muscles.

Freehand 3-D ultrasound (3DUS) system is a promising technique for accurately assessing muscle morphology. However, its accuracy has been validated mainly in terms of volume by examining lower limb muscles. This study was aimed at validating 3DUS in the measurements of 3-D surface shape and volume by comparing them with magnetic resonance imaging (MRI) measurements while ensuring the reproducibility of participant posture by focusing on the shoulder muscles. The supraspinatus, infraspinatus and posterior deltoid muscles of 10 healthy men were scanned using 3DUS and MRI while secured by an immobilization support customized for each participant. A 3-D surface model of each muscle was created from the 3DUS and MRI methods, and the agreement between them was assessed. For the muscle volume, the mean difference between the two models was within -0.51 cm3. For the 3-D surface shape, the distances between the closest points of the two models and the Dice similarity coefficient were calculated. The results indicated that the median surface distance was less than 1.12 mm and the Dice similarity coefficient was larger than 0.85. These results suggest that, given the aforementioned error is permitted, 3DUS can be used as an alternative to MRI in measuring volume and surface shape, even for the shoulder muscles.

Neural Network Models for Spinal Implementation of Muscle Synergies.

Muscle synergies have been proposed as functional modules to simplify the complexity of body motor control; however, their neural implementation is still unclear. Converging evidence suggests that output projections of the spinal premotor interneurons (PreM-INs) underlie the formation of muscle synergies, but they exhibit a substantial variation across neurons and exclude standard models assuming a small number of unitary "modules" in the spinal cord. Here we compared neural network models for muscle synergies to seek a biologically plausible model that reconciles previous clinical and electrophysiological findings. We examined three neural network models: one with random connections (non-synergy model), one with a small number of spinal synergies (simple synergy model), and one with a large number of spinal neurons representing muscle synergies with a certain variation (population synergy model). We found that the simple and population synergy models emulate the robustness of muscle synergies against cortical stroke observed in human stroke patients. Furthermore, the size of the spinal variation of the population synergy matched well with the variation in spinal PreM-INs recorded in monkeys. These results suggest that a spinal population with moderate variation is a biologically plausible model for the neural implementation of muscle synergies.

Neurological and behavioral features of locomotor imagery in the blind.

In people with normal sight, mental simulation (motor imagery) of an experienced action involves a multisensory (especially kinesthetic and visual) emulation process associated with the action. Here, we examined how long-term blindness influences sensory experience during motor imagery and its neuronal correlates by comparing data obtained from blind and sighted people. We scanned brain activity with functional magnetic resonance imaging (fMRI) while 16 sighted and 14 blind male volunteers imagined either walking or jogging around a circle of 2 m radius. In the training before fMRI, they performed these actions with their eyes closed. During scanning, we explicitly instructed the blindfolded participants to generate kinesthetic motor imagery. After the experimental run, they rated the degree to which their motor imagery became kinesthetic or spatio-visual. The imagery of blind people was more kinesthetic as per instructions, while that of the sighted group became more spatio-visual. The imagery of both groups commonly activated bilateral frontoparietal cortices including supplementary motor areas (SMA). Despite the lack of group differences in degree of brain activation, we observed stronger functional connectivity between the SMA and cerebellum in the blind group compared to that in the sighted group. To conclude, long-term blindness likely changes sensory emulation during motor imagery to a more kinesthetic mode, which may be associated with stronger functional coupling in kinesthetic brain networks compared with that in sighted people. This study adds valuable knowledge on motor cognition and mental imagery processes in the blind.

Individuals physically interacting in a group rapidly coordinate their movement by estimating the collective goal.

How can a human collective coordinate, for example to move a banquet table, when each person is influenced by the inertia of others who may be inferior at the task? We hypothesized that large groups cannot coordinate through touch alone, accruing to a zero-sum scenario where individuals inferior at the task hinder superior ones. We tested this hypothesis by examining how dyads, triads and tetrads, whose right hands were physically coupled together, followed a common moving target. Surprisingly, superior individuals followed the target accurately even when coupled to an inferior group, and the interaction benefits increased with the group size. A computational model shows that these benefits arose as each individual uses their respective interaction force to infer the collective's target and enhance their movement planning, which permitted coordination in seconds independent of the collective's size. By estimating the collective's movement goal, its individuals make physical interaction beneficial, swift and scalable.

Tagging motor memories with transcranial direct current stimulation allows later artificially-controlled retrieval.

We demonstrate that human motor memories can be artificially tagged and later retrieved by noninvasive transcranial direct current stimulation (tDCS). Participants learned to adapt reaching movements to two conflicting dynamical environments that were each associated with a different tDCS polarity (anodal or cathodal tDCS) on the sensorimotor cortex. That is, we sought to determine whether divergent background activity levels within the sensorimotor cortex (anodal: higher activity; cathodal: lower activity) give rise to distinct motor memories. After a training session, application of each tDCS polarity automatically resulted in the retrieval of the motor memory corresponding to that polarity. These results reveal that artificial modulation of neural activity in the sensorimotor cortex through tDCS can act as a context for the formation and recollection of motor memories.

Visuomotor Map Determines How Visually Guided Reaching Movements are Corrected Within and Across Trials.

When a visually guided reaching movement is unexpectedly perturbed, it is implicitly corrected in two ways: immediately after the perturbation by feedback control (online correction) and in the next movement by adjusting feedforward motor commands (offline correction or motor adaptation). Although recent studies have revealed a close relationship between feedback and feedforward controls, the nature of this relationship is not yet fully understood. Here, we show that both implicit online and offline movement corrections utilize the same visuomotor map for feedforward movement control that transforms the spatial location of visual objects into appropriate motor commands. First, we artificially distorted the visuomotor map by applying opposite visual rotations to the cursor representing the hand position while human participants reached for two different targets. This procedure implicitly altered the visuomotor map so that changes in the movement direction to the target location were more insensitive or more sensitive. Then, we examined how such visuomotor map distortion influenced online movement correction by suddenly changing the target location. The magnitude of online movement correction was altered according to the shape of the visuomotor map. We also examined offline movement correction; the aftereffect induced by visual rotation in the previous trial was modulated according to the shape of the visuomotor map. These results highlighted the importance of the visuomotor map as a foundation for implicit motor control mechanisms and the intimate relationship between feedforward control, feedback control, and motor adaptation.

How does the brain solve muscle redundancy? Filling the gap between optimization and muscle synergy hypotheses.

The question of how the central nervous system coordinates redundant muscles has been a long-standing problem in motor neuroscience. The optimization hypothesis posits that the brain can select the muscle activation pattern that minimizes the motor effort cost from among many solutions that satisfy the requirements of the task. On the other hand, the muscle-synergy hypothesis proposes that neurally established functional groupings of muscles alleviate the computational burden associated with motor control and learning. Although the two hypotheses are not mutually exclusive, the relationship between them has not been well analyzed. This is probably because both hypotheses are formulated mathematically without a clear concept of their neural implementation. Here, we introduce a biologically plausible hypothesis ("the forgetting hypothesis") for how optimization is realized by a population of neurons. We further demonstrate that low-dimensional structure can be detected in an optimal network even if no muscle-synergies are explicitly assumed. Finally, we briefly discuss an inherent difficulty in testing the muscle-synergy hypothesis, which arises when population level optimization is assumed.

Prospective errors determine motor learning.

Diverse features of motor learning have been reported by numerous studies, but no single theoretical framework concurrently accounts for these features. Here, we propose a model for motor learning to explain these features in a unified way by extending a motor primitive framework. The model assumes that the recruitment pattern of motor primitives is determined by the predicted movement error of an upcoming movement (prospective error). To validate this idea, we perform a behavioural experiment to examine the model's novel prediction: after experiencing an environment in which the movement error is more easily predictable, subsequent motor learning should become faster. The experimental results support our prediction, suggesting that the prospective error might be encoded in the motor primitives. Furthermore, we demonstrate that this model has a strong explanatory power to reproduce a wide variety of motor-learning-related phenomena that have been separately explained by different computational models.

Functional modulation of corticospinal excitability with adaptation of wrist movements to novel dynamical environments.

Adaptation of reaching movements to a novel dynamic environment is associated with changes in neuronal activity in the primary motor cortex (M1), suggesting that M1 neurons are part of the internal model. Here, we investigated whether such changes in neuronal activity, resulting from motor adaptation, were also accompanied by changes in human corticospinal excitability, which reflects M1 activity at a macroscopic level. Participants moved a cursor on a display using the right wrist joint from the starting position toward one of eight equally spaced peripheral targets. Motor-evoked potentials (MEPs) were elicited from the wrist muscles by transcranial magnetic stimulation delivered over the left M1 before and after adaptation to a clockwise velocity-dependent force field. We found that the MEP elicited even during the preparatory period exhibited a directional tuning property, and that the preferred direction shifted clockwise after adaptation to the force field. In a subsequent experiment, participants simultaneously adapted an identical wrist movement to two opposing force fields, each of which was associated with unimanual or bimanual contexts, and the MEP during the preparatory period was flexibly modulated, depending on the context. In contrast, such modulation of the MEP was not observed when participants tried to adapt to two opposing force fields that were each associated with a target color. These results suggest that the internal model formed in the M1 is retrieved flexibly even during the preparatory period, and that the MEP could be a very useful probe for evaluating the formation and retrieval of motor memory.

Lateralized sensitivity of motor memories to the kinematics of the opposite arm reveals functional specialization during bimanual actions.

It is generally believed that the dominant arm exhibits greater functional advantages over the nondominant arm in every respect, including muscular strength and movement accuracy. Recent studies have proposed that this laterality is due to different underlying control strategies for each limb rather than different limb capabilities constraining performance. However, the functional role and mechanisms of these different control strategies have yet to be elucidated. Here, we report a specialized function of the nondominant arm that plays a significant role only during bimanual movements. Right-handed human participants performed bimanual reaching movements while only one arm was subjected to a force field. Consistent with our previous study, adaptation to the force field decreased gradually as the movement direction of the opposite arm deviated from the trained direction. We also observed that the decrement of the adaptation was significantly greater for the nondominant left arm. According to our previously proposed theory, this poorer generalization of the left arm originated from a difference in parameters characterizing motor memory; the nondominant arm's motor memory was more strongly influenced by the opposite arm's kinematics. Remarkably, a model incorporating this lateralized memory predicted that the nondominant arm would demonstrate greater adaptability to force fields associated with the opposite arm's movement. We confirmed this prediction experimentally and found that this advantage of the left arm disappeared in left-handed human participants. We concluded that the secondary supporting role often played by the nondominant arm in bimanual actions reflects its specialization rather than its inferiority.

Decomposition of spontaneous movements of infants as combinations of limb synergies.

We hypothesized that a variety of limb movements in infants, including spontaneous movements and movements during interactions with the environment, can be represented as combinations of limb synergies, which are building blocks for generating coordinated movements of multiple limbs. A decomposition algorithm based on a nonnegative matrix factorization was applied to the discrete data segments taken from continuous data of limb movements in 298 infants (age, 3-4 months). The data were linearly decomposed into bases, which were referred to as synergies. The results showed that approximately 70% of the variance in the velocity profiles of the data segments of the four limbs can be explained by a set of five simple synergies that represent single-limb movements and the synchronous movement of all limbs. The present method showed that the complex properties of limb movements can be represented as combinations of synergies. Furthermore, comparisons of movement patterns across different age groups showed that in older infants, the contribution ratios of each synergy were different between spontaneous movements and movements during playing with a toy, whereas in younger infants, there were no differences in the contribution ratios between the different movement conditions. These results demonstrate that decomposition into limb synergies is useful for determining the spatiotemporal properties of interlimb coordination during spontaneous movements and task-constrained movements in infants.

Precursors of dancing and singing to music in three- to four-months-old infants.

Dancing and singing to music involve auditory-motor coordination and have been essential to our human culture since ancient times. Although scholars have been trying to understand the evolutionary and developmental origin of music, early human developmental manifestations of auditory-motor interactions in music have not been fully investigated. Here we report limb movements and vocalizations in three- to four-months-old infants while they listened to music and were in silence. In the group analysis, we found no significant increase in the amount of movement or in the relative power spectrum density around the musical tempo in the music condition compared to the silent condition. Intriguingly, however, there were two infants who demonstrated striking increases in the rhythmic movements via kicking or arm-waving around the musical tempo during listening to music. Monte-Carlo statistics with phase-randomized surrogate data revealed that the limb movements of these individuals were significantly synchronized to the musical beat. Moreover, we found a clear increase in the formant variability of vocalizations in the group during music perception. These results suggest that infants at this age are already primed with their bodies to interact with music via limb movements and vocalizations.

Simultaneous processing of information on multiple errors in visuomotor learning.

The proper association between planned and executed movements is crucial for motor learning because the discrepancies between them drive such learning. Our study explored how this association was determined when a single action caused the movements of multiple visual objects. Participants reached toward a target by moving a cursor, which represented the right hand's position. Once every five to six normal trials, we interleaved either of two kinds of visual perturbation trials: rotation of the cursor by a certain amount (±15°, ±30°, and ±45°) around the starting position (single-cursor condition) or rotation of two cursors by different angles (+15° and -45°, 0° and 30°, etc.) that were presented simultaneously (double-cursor condition). We evaluated the aftereffects of each condition in the subsequent trial. The error sensitivity (ratio of the aftereffect to the imposed visual rotation) in the single-cursor trials decayed with the amount of rotation, indicating that the motor learning system relied to a greater extent on smaller errors. In the double-cursor trials, we obtained a coefficient that represented the degree to which each of the visual rotations contributed to the aftereffects based on the assumption that the observed aftereffects were a result of the weighted summation of the influences of the imposed visual rotations. The decaying pattern according to the amount of rotation was maintained in the coefficient of each imposed visual rotation in the double-cursor trials, but the value was reduced to approximately 40% of the corresponding error sensitivity in the single-cursor trials. We also found a further reduction of the coefficients when three distinct cursors were presented (e.g., -15°, 15°, and 30°). These results indicated that the motor learning system utilized multiple sources of visual error information simultaneously to correct subsequent movement and that a certain averaging mechanism might be at work in the utilization process.

Learning with slight forgetting optimizes sensorimotor transformation in redundant motor systems.

Recent theoretical studies have proposed that the redundant motor system in humans achieves well-organized stereotypical movements by minimizing motor effort cost and motor error. However, it is unclear how this optimization process is implemented in the brain, presumably because conventional schemes have assumed a priori that the brain somehow constructs the optimal motor command, and largely ignored the underlying trial-by-trial learning process. In contrast, recent studies focusing on the trial-by-trial modification of motor commands based on error information suggested that forgetting (i.e., memory decay), which is usually considered as an inconvenient factor in motor learning, plays an important role in minimizing the motor effort cost. Here, we examine whether trial-by-trial error-feedback learning with slight forgetting could minimize the motor effort and error in a highly redundant neural network for sensorimotor transformation and whether it could predict the stereotypical activation patterns observed in primary motor cortex (M1) neurons. First, using a simple linear neural network model, we theoretically demonstrated that: 1) this algorithm consistently leads the neural network to converge at a unique optimal state; 2) the biomechanical properties of the musculoskeletal system necessarily determine the distribution of the preferred directions (PD; the direction in which the neuron is maximally active) of M1 neurons; and 3) the bias of the PDs is steadily formed during the minimization of the motor effort. Furthermore, using a non-linear network model with realistic musculoskeletal data, we demonstrated numerically that this algorithm could consistently reproduce the PD distribution observed in various motor tasks, including two-dimensional isometric torque production, two-dimensional reaching, and even three-dimensional reaching tasks. These results may suggest that slight forgetting in the sensorimotor transformation network is responsible for solving the redundancy problem in motor control.

Adaptation to visual feedback delay influences visuomotor learning.

Computational theory of motor control suggests that the brain continuously monitors motor commands, to predict their sensory consequences before actual sensory feedback becomes available. Such prediction error is a driving force of motor learning, and therefore appropriate associations between motor commands and delayed sensory feedback signals are crucial. Indeed, artificially introduced delays in visual feedback have been reported to degrade motor learning. However, considering our perceptual ability to causally bind our own actions with sensory feedback, demonstrated by the decrease in the perceived time delay following repeated exposure to an artificial delay, we hypothesized that such perceptual binding might alleviate deficits of motor learning associated with delayed visual feedback. Here, we evaluated this hypothesis by investigating the ability of human participants to adapt their reaching movements in response to a novel visuomotor environment with 3 visual feedback conditions--no-delay, sudden-delay, and adapted-delay. To introduce novelty into the trials, the cursor position, which originally indicated the hand position in baseline trials, was rotated around the starting position. In contrast to the no-delay condition, a 200-ms delay was artificially introduced between the cursor and hand positions during the presence of visual rotation (sudden-delay condition), or before the application of visual rotation (adapted-delay condition). We compared the learning rate (representing how the movement error modifies the movement direction in the subsequent trial) between the 3 conditions. In comparison with the no-delay condition, the learning rate was significantly degraded for the sudden-delay condition. However, this degradation was significantly alleviated by prior exposure to the delay (adapted-delay condition). Our data indicate the importance of appropriate temporal associations between motor commands and sensory feedback in visuomotor learning. Moreover, they suggest that the brain is able to account for such temporal associations in a flexible manner.

Distinct motor plans form and retrieve distinct motor memories for physically identical movements.

We can adapt movements to a novel dynamic environment (e.g., tool use, microgravity, and perturbation) by acquiring an internal model of the dynamics. Although multiple environments can be learned simultaneously if each environment is experienced with different limb movement kinematics, it is controversial as to whether multiple internal models for a particular movement can be learned and flexibly retrieved according to behavioral contexts. Here, we address this issue by using a novel visuomotor task. While participants reached to each of two targets located at a clockwise or counter-clockwise position, a gradually increasing visual rotation was applied in the clockwise or counter-clockwise direction, respectively, to the on-screen cursor representing the unseen hand position. This procedure implicitly led participants to perform physically identical pointing movements irrespective of their intentions (i.e., movement plans) to move their hand toward two distinct visual targets. Surprisingly, if each identical movement was executed according to a distinct movement plan, participants could readily adapt these movements to two opposing force fields simultaneously. The results demonstrate that multiple motor memories can be learned and flexibly retrieved, even for physically identical movements, according to distinct motor plans in a visual space.