Level of decision confidence shapes motor memory.

Decision making is often necessary before performing an action. Traditionally, it has been assumed that decision making and motor control are independent, sequential processes. Ogasa et al. challenge this view, and demonstrate that the decision-making process significantly impacts on the formation and retrieval of motor memory by tagging it with the level of confidence.

Divisively normalized neuronal processing of uncertain visual feedback for visuomotor learning.

When encountering a visual error during a reaching movement, the motor system improves the motor command for the subsequent trial. This improvement is impaired by visual error uncertainty, which is considered evidence that the motor system optimally estimates the error. However, how such statistical computation is accomplished remains unclear. Here, we propose an alternative scheme implemented with a divisive normalization (DN): the responses of neuronal elements are normalized by the summed activity of the population. This scheme assumes that when an uncertain visual error is provided by multiple cursors, the motor system processes the error conveyed by each cursor and integrates the information using DN. The DN model reproduced the patterns of learning response to 1-3 cursor errors and the impairment of learning response with visual error uncertainty. This study provides a new perspective on how the motor system updates motor commands according to uncertain visual error information.

Shouting strengthens voluntary force during sustained maximal effort through enhancement of motor system state via motor commands.

Previous research indicates that shouting during momentary maximal exertion effort potentiates the maximal voluntary force through the potentiation of motor cortical excitability. However, the muscular force-enhancing effects of shouting on sustained maximal force production remain unclear. We investigated the effect of shouting on the motor system state by examining motor evoked potentials in response to transcranial magnetic stimulation applied over the hand area of the contralateral primary motor cortex (M1) during sustained maximal voluntary contraction, and by assessing handgrip maximal voluntary force. We observed that shouting significantly increased handgrip maximal voluntary force and reduced the silent period. Our results indicate that shouting increased handgrip voluntary force during sustained maximal exertion effort through the reduced silent period. This is the first objective evidence that the muscular force of shouting during maximal force exertion is associated with the potentiation of motor system activity produced by the additional drive of shouting operating on the motor system (i.e., shouting-induced excitatory input to M1).

The unconscious mental inhibiting process of human maximal voluntary contraction.

Human maximal voluntary contraction (MVC) is believed to be limited by neural inhibition. Motivational goal priming alters background states of the motor system, leading to enhanced MVC. However, the mechanisms that determine the constant inhibition of force exertion in the motor system remain unclear. The primary behavioural goal of MVC is maximal voluntary force exertion. The final expected or desired state of this behavioural goal is explicitly demonstrated with words related to physical exertion, such as 'maximal', irrespective of the possibility of demand-like properties in participants' minds, such as attainability and/or desirability of the goal. For the primed maximal goal state, most trial results fail to meet expectations, demonstrating negative affect that, without awareness, contributes to the mentioned inhibitory mechanism underlying MVC. We therefore speculated that the behavioural goal of MVC contributes to neural inhibitory mechanisms underlying MVC. In our study, we used a previously developed paradigm (Takarada and Nozaki in Scientific Reports 8: 10135, 2018) in which subliminal visual priming stimuli such as the physical exertion-related words "perform" and "exert" were presented to 12 healthy participants and were followed by supraliminal words that were the word "maximal" or neutral.We found that when combined with the term 'maximal' in the consciously visible form, the effect of this subliminal motor-goal priming in inducing pupil dilation and stronger action preparation/execution was abolished without conscious awareness. This is the first objective evidence of motor inhibitory effect-predicting patterns of pupil-linked noradrenergic activity as a signature of a type of mental inhibition underlying the MVC behavioural goal.

Effects of Simulated Microgravity and Hypergravity Conditions on Arm Movements in Normogravity.

The human sensorimotor control has evolved in the Earth's environment where all movement is influenced by the gravitational force. Changes in this environmental force can severely impact the performance of arm movements which can be detrimental in completing certain tasks such as piloting or controlling complex vehicles. For this reason, subjects that are required to perform such tasks undergo extensive training procedures in order to minimize the chances of failure. We investigated whether local gravity simulation of altered gravitational conditions on the arm would lead to changes in kinematic parameters comparable to the full-body experience of microgravity and hypergravity onboard a parabolic flight. To see if this would be a feasible approach for on-ground training of arm reaching movements in altered gravity conditions we developed a robotic device that was able to apply forces at the wrist in order to simulate micro- or hypergravity conditions for the arm while subjects performed pointing movements on a touch screen. We analyzed and compared the results of several kinematic parameters along with muscle activity using this system with data of the same subjects being fully exposed to microgravity and hypergravity conditions on a parabolic flight. Both in our simulation and in-flight, we observed a significant increase in movement durations in microgravity conditions and increased velocities in hypergravity for upward movements. Additionally, we noted a reduced accuracy of pointing both in-flight and in our simulation. These promising results suggest, that locally simulated altered gravity can elicit similar changes in some movement characteristics for arm reaching movements. This could potentially be exploited as a means of developing devices such as exoskeletons to aid in training individuals prior to undertaking tasks in changed gravitational conditions.

Effects of Local Gravity Compensation on Motor Control During Altered Environmental Gravity.

Our sensorimotor control is well adapted to normogravity environment encountered on Earth and any change in gravity significantly disturbs our movement. In order to produce appropriate motor commands for aimed arm movements such as pointing or reaching, environmental changes have to be taken into account. This adaptation is crucial when performing successful movements during microgravity and hypergravity conditions. To mitigate the effects of changing gravitational levels, such as the changed movement duration and decreased accuracy, we explored the possible beneficial effects of gravity compensation on movement. Local gravity compensation was achieved using a motorized robotic device capable of applying precise forces to the subject's wrist that generated a normogravity equivalent torque at the shoulder joint during periods of microgravity and hypergravity. The efficiency of the local gravity compensation was assessed with an experiment in which participants performed a series of pointing movements toward the target on a screen during a parabolic flight. We compared movement duration, accuracy, movement trajectory, and muscle activations of movements during periods of microgravity and hypergravity with conditions when local gravity compensation was provided. The use of local gravity compensation at the arm mitigated the changes in movement duration, accuracy, and muscle activity. Our results suggest that the use of such an assistive device helps with movements during unfamiliar environmental gravity.

Shouting strengthens maximal voluntary force and is associated with augmented pupillary dilation.

Previous research has demonstrated that human maximal voluntary force is generally limited by neural inhibition. Producing a shout during maximal exertion effort enhances the force levels of maximal voluntary contraction. However, the mechanisms underlying this enhancement effect on force production remain unclear. We investigated the influence of producing a shout on the pupil-linked neuromodulatory system state by examining pupil size. We also examined its effects on the motor system state by examining motor evoked potentials in response to transcranial magnetic stimulation applied over the contralateral primary motor cortex, and by evaluating handgrip maximal voluntary force. Analysis revealed that producing a shout significantly increased handgrip maximal voluntary force, followed by an increase in pupil size and a reduction of the cortical silent period. Our results indicate that producing a shout increased handgrip maximal voluntary force through the enhancement of motor cortical excitability, possibly via the enhancement of noradrenergic system activity. This study provides evidence that the muscular force-enhancing effect of shouting during maximal force exertion is related to both the motor system state and the pupil-linked neuromodulatory system state.

Cosine tuning determines plantarflexors' activities during human upright standing and is affected by incomplete spinal cord injury.

Plantarflexors such as the soleus (SOL) and medial gastrocnemius (MG) play key roles in controlling bipedal stance; however, how the central nervous system controls the activation levels of these plantarflexors is not well understood. Here we investigated how the central nervous system controls the plantarflexors' activation level during quiet standing in a cosine tuning manner where the maximal activation is achieved in a preferred direction (PD). Furthermore, we investigated how spinal cord injury affects these plantarflexors' activations. Thirteen healthy adults (AB) and thirteen individuals with chronic, incomplete spinal cord injury (iSCI) performed quiet standing trials. Their body kinematics and kinetics as well as electromyography signals from the MG and SOL were recorded. In the AB group, we found that the plantarflexors followed the cosine tuning manner during quiet standing. That is, MG was most active when the ratio of plantarflexion torque to knee extension torque was ~2:-3, whereas SOL was most active when the ratio was ~2:1. This suggests that the SOL muscle, despite being a monoarticular muscle, is sensitive to both ankle plantarflexion and knee extension during quiet standing. The difference in the PDs accounts for the phasic activity of MG and for the tonic activity of SOL. Unlike the AB group, the MG's activity was similar to the SOL's activity in the iSCI group, and the SOL PDs were similar to those in the AB group. This result suggests that chronic iSCI affects the control strategy, i.e., cosine tuning, for MG, which may affect standing balance in individuals with iSCI.NEW & NOTEWORTHY Soleus muscle shows a tonic activity whereas medial gastrocnemius muscle shows a phasic activity during quiet standing. Cosine tuning and their preferred direction account for the different muscle activation patterns between these two muscles. In individuals with chronic incomplete spinal cord injury, the preferred direction of gastrocnemius medial head is affected, which may result in their deteriorated standing balance.

"Paralympic Brain". Compensation and Reorganization of a Damaged Human Brain with Intensive Physical Training.

The main aim of the study was to evaluate how the brain of a Paralympic athlete with severe disability due to cerebral palsy has reorganized after continuous training geared to enhance performance. Both corticospinal excitability of upper-limb muscles and electromyographic activity during swimming were investigated for a Paralympic gold medalist in swimming competitions. Transcranial magnetic stimulation (TMS) to the affected and intact hand motor cortical area revealed that the affected side finger muscle cortical representation area shifted towards the temporal side, and cortico-spinal excitability of the target muscle was prominently facilitated, i.e., the maximum motor evoked potential in the affected side, 6.11 ± 0.19 mV was greater than that in the intact side, 4.52 ± 0.39 mV (mean ± standard error). Electromyographic activities during swimming demonstrated well-coordinated patterns as compared with rather spastic activities observed in the affected side during walking on land. These results suggest that the ability of the brain to reorganize through intensive training in Paralympic athletes can teach interesting lessons to the field neurorehabilitation.

Divisively Normalized Integration of Multisensory Error Information Develops Motor Memories Specific to Vision and Proprioception.

Both visual and proprioceptive information contribute to the accuracy of limb movement, but the mechanism of integration of these different modality signals for movement control and learning remains controversial. We aimed to elucidate the mechanism of multisensory integration for motor adaptation by evaluating single-trial adaptation (i.e., aftereffect) induced by visual and proprioceptive perturbations while male and female human participants performed reaching movements. The force-channel method was used to precisely impose several combinations of visual and proprioceptive perturbations (i.e., error), including an instance when the directions of perturbation in both stimuli opposed each another. In the subsequent probe force-channel trial, the lateral force against the channel was quantified as the aftereffect to clarify the mechanism by which the motor adaptation system corrects movement in the event of visual and proprioceptive errors. We observed that the aftereffects had complex dependence on the visual and proprioceptive errors. Although this pattern could not be explained by previously proposed computational models based on the reliability of sensory information, we found that it could be reasonably explained by a mechanism known as divisive normalization, which was the reported mechanism underlying the integration of multisensory signals in neurons. Furthermore, we discovered evidence that the motor memory for each sensory modality developed separately in accordance with a divisive normalization mechanism and that the outputs of both memories were integrated. These results provide a novel view of the utilization and integration of different sensory modality signals in motor adaptation.SIGNIFICANCE STATEMENT The mechanism of utilization of multimodal sensory information by the motor control system to perform limb movements with accuracy is a fundamental question. However, the mechanism of integration of these different sensory modalities for movement control and learning remains highly debatable. Herein, we demonstrate that multisensory integration in the motor learning system can be reasonably explained by divisive normalization, a canonical computation, ubiquitously observed in the brain (Carandini and Heeger, 2011). Moreover, we provide evidence of a novel idea that integration does not occur at the sensory information processing level, but at the motor execution level, after the motor memory for each sensory modality is separately created.

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.

Motivational goal-priming with or without awareness produces faster and stronger force exertion.

Previous research has demonstrated that barely visible (subliminal) goal-priming with motivational reward can alter the state of the motor system and enhance motor output. Research shows that these affective-motivational effects result from associations between goal representations and positive affect without conscious awareness. Here, we tested whether motivational priming can increase motor output even if the priming is fully visible (supraliminal), and whether the priming effect occurs through increased cortical excitability. Groups of participants were primed with either barely visible or fully visible words related to effort and control sequences of random letters that were each followed by fully visible positively reinforcing words. The priming effect was measured behaviourally by handgrip force and reaction time to the grip cue after the priming was complete. Physiologically, the effects were measured by pupil dilation and motor-evoked potentials (MEPs) in response to transcranial magnetic stimulation during the priming task. Analysis showed that for both the supraliminal and subliminal conditions, reaction time decreased and total force, MEP magnitude, and pupil dilation increased. None of the priming-induced changes in behaviour or physiology differed significantly between the supraliminal and the subliminal groups, indicating that implicit motivation towards motor goals might not require conscious perception of the goals.

Pupil dilations induced by barely conscious reward goal-priming.

The topic of unconscious influences on behavior has long been explored as a way of understanding human performance and the neurobiological correlates of intention, motivation and action. Previous research using transcranial magnetic stimulation has demonstrated that barely visible priming of an action concept, when combined with reward in the form of a consciously perceived positive stimulus, can alter the state of the motor system and enhance the maximal voluntary force level. One possible explanation is that positive stimulus-induced reward signals are processed by the dopaminergic system in the basal ganglia, motivating individuals to increase the effort they invest in particular behaviors, or to recruit the resources necessary for maintaining those behaviors. If so, given that the dopaminergic system has functionally and anatomically close connections with the noradrenergic system, we hypothesize that the state of the noradrenergic system may be enhanced by the same process. In accord with this hypothesis, we observed that barely visible goal priming with reward caused pupil dilation, suggesting that activity in the noradrenergic system increased. Importantly, this enhancement was accompanied by an unconscious increase in handgrip force. This is the first objective evidence that the pupil-linked neuromodulatory system is related to implicit learning of the link between physical exertion and reward, probably in the noradrenergic system, resulting in more forceful voluntary motor action in the absence of conscious awareness.

Improving a Bimanual Motor Skill Through Unimanual Training.

When we learn a bimanual motor skill (e.g., rowing a boat), we often break it down into unimanual practices (e.g., a rowing drill with the left or right arm). Such unimanual practice is thought to be useful for learning bimanual motor skills efficiently because the learner can concentrate on learning to perform a simpler component. However, it is not so straightforward to assume that unimanual training (UT) improves bimanual performance. We have previously demonstrated that motor memories for reaching movements consist of three different parts: unimanual-specific, bimanual-specific, and overlapping parts. According to this scheme, UT appears to be less effective, as its training effect is only partially transferred to the same limb for bimanual movement. In the present study, counter-intuitively, we demonstrate that, even after the bimanual skill is almost fully learned by means of bimanual training (BT), additional UT could further improve bimanual skill. We hypothesized that this effect occurs because UT increases the memory content in the overlapping part, which might contribute to an increase in the memory for bimanual movement. To test this hypothesis, we examined whether the UT performed after sufficient BT could improve the bimanual performance. Participants practiced performing bimanual reaching movements (BM) in the presence of a novel force-field imposed only on their left arm. As an index for the motor performance, we used the error-clamp method (i.e., after-effect of the left arm) to evaluate the force output to compensate for the force-field during the reaching movement. After sufficient BT, the training effect reached a plateau. However, UT performed subsequently improved the bimanual performance significantly. In contrast, when the same amount of BT was continued, the bimanual performance remained unchanged, highlighting the beneficial effect of UT on bimanual performance. Considering memory structure, we also expected that BT could improve unimanual performance, which was confirmed by another experiment. These results provide a new interpretation of why UT was useful for improving a bimanual skill, and propose a practical strategy for enhancing performance by performing training in various contexts.

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.

Learning feedback and feedforward control in a mirror-reversed visual environment.

When we learn a novel task, the motor system needs to acquire both feedforward and feedback control. Currently, little is known about how the learning of these two mechanisms relate to each other. In the present study, we tested whether feedforward and feedback control need to be learned separately, or whether they are learned as common mechanism when a new control policy is acquired. Participants were trained to reach to two lateral and one central target in an environment with mirror (left-right)-reversed visual feedback. One group was allowed to make online movement corrections, whereas the other group only received visual information after the end of the movement. Learning of feedforward control was assessed by measuring the accuracy of the initial movement direction to lateral targets. Feedback control was measured in the responses to sudden visual perturbations of the cursor when reaching to the central target. Although feedforward control improved in both groups, it was significantly better when online corrections were not allowed. In contrast, feedback control only adaptively changed in participants who received online feedback and remained unchanged in the group without online corrections. Our findings suggest that when a new control policy is acquired, feedforward and feedback control are learned separately, and that there may be a trade-off in learning between feedback and feedforward controllers.

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.

Maximal voluntary force strengthened by the enhancement of motor system state through barely visible priming words with reward.

The topic of unconscious influences on behaviour has long been explored as a means of understanding human performance and the neurobiological correlates of intention, motivation, and action. However, what is relatively unknown is whether subconsciously delivered priming stimuli, with or without rewards, can affect individuals' maximum level of force produced with their best effort. We demonstrated using transcranial magnetic stimulation that barely visible priming of an action concept, when combined with a reward in the form of a consciously visible positive stimulus, could alter the state of the motor system. In accordance with this neurophysiological alteration, the prime-plus-reward stimuli significantly increased the hand-grip force level of maximum voluntary contraction with little conscious awareness. This is the first objective evidence that the barely conscious presence of a behavioral goal can influence the state of the motor system and arouse latent ability for human force exertion.

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.