Attenuation of implicit motor learning with consecutive exposure to visual errors.

Visual errors induced by movement drive implicit corrections of that movement. When similar errors are experienced consecutively, does sensitivity to the error remain consistent each time? This study aimed to investigate the modulation of implicit error sensitivity through continuous exposure to the same errors. In the reaching task using visual error-clamp feedback, participants were presented with the same error in direction and magnitude for four consecutive trials. We found that implicit error sensitivity decreased after exposure to the second error. These results indicate that when visual errors occur consecutively, the sensorimotor system exhibits different responses, even for identical errors. The continuity of errors may be a factor that modulates error sensitivity.

Implicit motor adaptation driven by intermittent and invariant errors.

Our movements and movement outcomes are disturbed by environmental changes, leading to errors. During ongoing environmental changes, people should correct their movement using sensory feedback. However, when the changes are momentary, corrections based on sensory feedback are undesirable. Previous studies have suggested that implicit motor adaptation takes place despite the realization that the presented visual feedback should be ignored. Although these studies created experimental situations in which participants had to continuously ignore the presented visual feedback, in daily lives, people intermittently encounter opportunities to ignore sensory feedback. In this study, by intermittently presenting visual error clamp feedback, always offset from a target by 16° counterclockwise, regardless of the actual movement in a reaching experiment, we provided intermittent opportunities to ignore the visual feedback. We found that in the trials conducted immediately after presenting the visual error clamp feedback, reaching movements shifted in the direction opposite to the feedback, which is a hallmark of implicit motor adaptation. Moreover, the magnitude of the shift was significantly correlated with the rate of motor adaptation to gradual changes in the environment. Therefore, the results suggest that people unintentionally react to momentary environmental changes, which should be ignored. In addition, the sensitivity to momentary changes is greater in people who can quickly adapt to gradual environmental changes.

Error Size Shape Relationships between Motor Variability and Implicit Motor Adaptation.

Previous studies have demonstrated the effects of motor variability on motor adaptation. However, their findings have been inconsistent, suggesting that various factors affect the relationship between motor variability and adaptation. This study focused on the size of errors driving motor adaptation as one of the factors and examined the relationship between different error sizes. Thirty-one healthy young adults participated in a visuomotor task in which they made fast-reaching movements toward a target. Motor variability was measured in the baseline phase when a veridical feedback cursor was presented. In the adaptation phase, the feedback cursor was sometimes not reflected in the hand position and deviated from the target by 0°, 3°, 6°, or 12° counterclockwise or clockwise (i.e., error-clamp feedback). Movements during trials following trials with error-clamp feedback were measured to quantify implicit adaptation. Implicit adaptation was driven by errors presented through error-clamp feedback. Moreover, motor variability significantly correlated with implicit adaptation driven by a 12° error. The results suggested that motor variability accelerates implicit adaptation when a larger error occurs. As such a trend was not observed when smaller errors occurred, the relationship between motor variability and motor adaptation might have been affected by the error size driving implicit adaptation.

Neural correlates of online cooperation during joint force production.

During joint action, two or more persons depend on each other to accomplish a goal. This mutual recursion, or circular dependency, is one of the characteristics of cooperation. To evaluate the neural substrates of cooperation, we conducted a hyperscanning functional MRI study in which 19 dyads performed a joint force-production task. The goal of the task was to match their average grip forces to the target value (20% of their maximum grip forces) through visual feedback over a 30-s period; the task required taking into account other-produced force to regulate the self-generated one in real time, which represented cooperation. Time-series data of the dyad's exerted grip forces were recorded, and the noise contribution ratio (NCR), a measure of influence from the partner, was computed using a multivariate autoregressive model to identify the degree to which each participant's grip force was explained by that of their partner's, i.e., the degree of cooperation. Compared with the single force-production task, the joint task enhanced the NCR and activated the mentalizing system, including the medial prefrontal cortex, precuneus, and bilateral posterior subdivision of the temporoparietal junction (TPJ). In addition, specific activation of the anterior subdivision of the right TPJ significantly and positively correlated with the NCR across participants during the joint task. The effective connectivity of the anterior to posterior TPJ was upregulated when participants coordinated their grip forces. Finally, the joint task enhanced cross-brain functional connectivity of the right anterior TPJ, indicating shared attention toward the temporal patterns of the motor output of the partner. Since the posterior TPJ is part of the mentalizing system for tracking the intention of perceived agents, our findings indicate that cooperation, i.e., the degree of adjustment of individual motor output depending on that of the partner, is mediated by the interconnected subdivisions of the right TPJ.

Ankle muscle co-contractions during quiet standing are associated with decreased postural steadiness in the elderly.

It has been reported that the elderly use co-contraction of the tibialis anterior (TA) and plantarflexor muscles for longer duration during quiet standing than the young. However, the particular role of ankle muscle co-contractions in the elderly during quiet standing remains unclear. Therefore, the objective of this study was to investigate the association between ankle muscle co-contractions and postural steadiness during standing in the elderly. Twenty-seven young (27.2±4.5yrs) and twenty-three elderly (66.2±5.0yrs) subjects were asked to stand quietly on a force plate for five trials. The center of pressure (COP) trajectory and its velocity (COPv) as well as the center of mass (COM) trajectory and its velocity (COMv) and acceleration (ACC) were calculated using the force plate outputs. Electromyograms were obtained from the right TA, soleus (SOL), and medial gastrocnemius (MG) muscles. Periods of TA activity (TAon) and inactivity (TAoff) were determined using an EMG threshold based on TA resting level. Our results indicate that, in the elderly, the COPv, COMv, and ACC variability were significantly larger during TAon periods compared to TAoff periods. However, in the young, no significant association between respective variability and TA activity was found. We conclude that ankle muscle co-contractions in the elderly are not associated with an increase, but a decrease in postural steadiness. Future studies are needed to clarify the causal relationship between (1) ankle muscle co-contractions and (2) joint stiffness and multi-segmental actions during standing as well as their changes with aging.

Neuromotor Noise Is Malleable by Amplifying Perceived Errors.

Variability in motor performance results from the interplay of error correction and neuromotor noise. This study examined whether visual amplification of error, previously shown to improve performance, affects not only error correction, but also neuromotor noise, typically regarded as inaccessible to intervention. Seven groups of healthy individuals, with six participants in each group, practiced a virtual throwing task for three days until reaching a performance plateau. Over three more days of practice, six of the groups received different magnitudes of visual error amplification; three of these groups also had noise added. An additional control group was not subjected to any manipulations for all six practice days. The results showed that the control group did not improve further after the first three practice days, but the error amplification groups continued to decrease their error under the manipulations. Analysis of the temporal structure of participants' corrective actions based on stochastic learning models revealed that these performance gains were attained by reducing neuromotor noise and, to a considerably lesser degree, by increasing the size of corrective actions. Based on these results, error amplification presents a promising intervention to improve motor function by decreasing neuromotor noise after performance has reached an asymptote. These results are relevant for patients with neurological disorders and the elderly. More fundamentally, these results suggest that neuromotor noise may be accessible to practice interventions.

Heel strike detection using split force-plate treadmill.

A common source of error when detecting heel-strike moments utilizing split force-plate treadmills is unwillingly stepping on contra-lateral force-plate. In this study, we quantified this error when heel-strike was detected based on such erroneous data and compared three methods to investigate how well the heel-strikes and stride-intervals were detected with erroneous data. Eleven subjects walked on a split force-plate treadmill for more than 20min. We used 20N and 50% body-weight thresholds to detect the heel-strike moments (HS20N and HS50%, respectively). Besides, we used linear approximation to estimate the unaffected force profile from affected force-plate data, and subsequently to detect the heel-strike moments (HSest). We used heel-strike moments detected by a foot-switch as a reference to compare accuracy of HS20N, HS50% and HSest. HS20N and HSest detected heel-strike moments accurately for unaffected force-plate data (median(max) errors for all subjects: 9(23) and 9(37) ms) but HS50% showed significantly larger errors (52(74) ms). Unlike HS50% and HSest, HS20N was considerably affected by the affected force-plate data (23(68) ms). The error in stride-interval measurement was relatively small using any methods for unaffected force-plate data (3(7), 6(8), and 6(12) ms), while stride-interval errors were large for some subjects when using HS20N for affected data (6(175) ms). We concluded that unwillingly stepping on contra-lateral force-plate occurred a few percent and up to 37.7% of all strides (median: 12.9%). Our proposed method (HSest) robustly showed small errors for heel-strike detection and stride-interval calculation consistently among subjects, while HS50% and HS20N showed large errors depending on subjects.

Center of pressure velocity reflects body acceleration rather than body velocity during quiet standing.

The purpose of this study was to test the hypothesis that the center of pressure (COP) velocity reflects the center of mass (COM) acceleration due to a large derivative gain in the neural control system during quiet standing. Twenty-seven young (27.2±4.5 years) and twenty-three elderly (66.2±5.0 years) subjects participated in this study. Each subject was requested to stand quietly on a force plate for five trials, each 90 s long. The COP and COM displacements, the COP and COM velocities, and the COM acceleration were acquired via a force plate and a laser displacement sensor. The amount of fluctuation of each variable was quantified using the root mean square. Following the experimental study, a simulation study was executed to investigate the experimental findings. The experimental results revealed that the COP velocity was correlated with the COM velocity, but more highly correlated with the COM acceleration. The equation of motion of the inverted pendulum model, however, accounts only for the correlation between the COP and COM velocities. These experimental results can be meaningfully explained by the simulation study, which indicated that the neural motor command presumably contains a significant portion that is proportional to body velocity. In conclusion, the COP velocity fluctuation reflects the COM acceleration fluctuation rather than the COM velocity fluctuation, implying that the neural motor command controlling quiet standing posture contains a significant portion that is proportional to body velocity.

Modulation between bilateral legs and within unilateral muscle synergists of postural muscle activity changes with development and aging.

The effect of development and aging on common modulation between bilateral plantarflexors (i.e., the right and left soleus, and the right and left medial gastrocnemius) (bilateral comodulation) and within plantarflexors in one leg (i.e., the right soleus and the right medial gastrocnemius) (unilateral comodulation) was investigated during bipedal quiet standing by comparing electromyography-electromyography (EMG) coherence among three age groups: adult (23-35 years), child (6-8 years), and elderly (60-80 years). The results demonstrate that there was significant coherence between bilateral plantarflexors and within plantarflexors in one leg in the 0- to 4-Hz frequency region in all three age groups. Coherence in this frequency region was stronger in the elderly group than in the adult group, while no difference was found between the adult and child groups. Of particular interest was the finding of significant coherence in bilateral and unilateral EMG recordings in the 8- to 12-Hz frequency region in some subjects in the elderly group, whereas it was not observed in the adult and child groups. These results suggest that aging affects the organization of bilateral and unilateral postural muscle activities (i.e., bilateral and unilateral comodulation) in the plantarflexors during quiet standing.

Directionality in distribution and temporal structure of variability in skill acquisition.

Observable structure of variability presents a window into the underlying processes of skill acquisition, especially when the task affords a manifold of solutions to the desired task result. This study examined skill acquisition by analyzing variability in both its distributional and temporal structure. Using a virtual throwing task, data distributions were analyzed by the Tolerance, Noise, Covariation-method (TNC); the temporal structure was quantified by autocorrelation and detrended fluctuation analysis (DFA). We tested four hypotheses: (1) Tolerance and Covariation, not Noise, are major factors underlying long-term performance improvement. (2) Trial-to-trial dynamics in execution space exhibits preferred directions. (3) The direction-dependent organization of variability becomes more pronounced with practice. (4) The anisotropy is in directions orthogonal and parallel to the solution manifold. Results from 13 subjects practicing for 6 days revealed that performance improvement correlated with increasing Tolerance and Covariation; Noise remained relatively constant. Temporal fluctuations and their directional modulation were identified by a novel rotation method that was a priori ignorant about orthogonality. Results showed a modulation of time-dependent characteristics that became enhanced with practice. However, this directionality was not coincident with orthogonal and parallel directions of the solution manifold. A state-space model with two sources of noise replicated not only the observed temporal structure but also its deviations from orthogonality. Simulations suggested that practice-induced changes were associated with an increase in the feedback gain and a subtle weighting of the two noise sources. The directionality in the structure of variability depended on the scaling of the coordinates, a result that highlights that analysis of variability sensitively depends on the chosen coordinates.

Abnormal capacity for grip force control in patients with congenital insensitivity to pain.

Congenital insensitivity to pain (CIP), which is an extremely rare sensory neuropathy, is defined as the absence of normal responses to noxious stimuli. Although motor function is not directly impaired in CIP patients, it is likely that the sensory deficit affects the motor control system. In order to characterize motor capacity in CIP patients, we here measured grip force and acceleration of a held object in 12 patients with CIP and 12 age-matched able-bodied subjects. The results demonstrated that the grip force during the object grasp-lift-holding task was significantly greater, less reproducibility and greater fluctuation in the acceleration of the object in CIP patients than in normal subjects. Moreover, some patients showed absence of temporal coupling between the grip and load force, suggesting that anticipatory modulation of the grip force was at least partly impaired. As far as the authors know, this is the first study to characterize motor control ability in patients with CIP. The observed abnormal motor capacity can be at least partly attributed to a lack of sensory inputs mediated by Aδ and unmyelinated C-, specifically C-tactile, fibers. The present results may provide information useful for the prevention of secondary injury and education for patients during the developmental stage.

Neuromotor noise, error tolerance and velocity-dependent costs in skilled performance.

In motor tasks with redundancy neuromotor noise can lead to variations in execution while achieving relative invariance in the result. The present study examined whether humans find solutions that are tolerant to intrinsic noise. Using a throwing task in a virtual set-up where an infinite set of angle and velocity combinations at ball release yield throwing accuracy, our computational approach permitted quantitative predictions about solution strategies that are tolerant to noise. Based on a mathematical model of the task expected results were computed and provided predictions about error-tolerant strategies (Hypothesis 1). As strategies can take on a large range of velocities, a second hypothesis was that subjects select strategies that minimize velocity at release to avoid costs associated with signal- or velocity-dependent noise or higher energy demands (Hypothesis 2). Two experiments with different target constellations tested these two hypotheses. Results of Experiment 1 showed that subjects chose solutions with high error-tolerance, although these solutions also had relatively low velocity. These two benefits seemed to outweigh that for many subjects these solutions were close to a high-penalty area, i.e. they were risky. Experiment 2 dissociated the two hypotheses. Results showed that individuals were consistent with Hypothesis 1 although their solutions were distributed over a range of velocities. Additional analyses revealed that a velocity-dependent increase in variability was absent, probably due to the presence of a solution manifold that channeled variability in a task-specific manner. Hence, the general acceptance of signal-dependent noise may need some qualification. These findings have significance for the fundamental understanding of how the central nervous system deals with its inherent neuromotor noise.

Smaller sway size during quiet standing is associated with longer preceding time of motor command to body sway.

In previous studies, it was found using cross-correlation analysis that the modulation of the motor command to the calf muscles largely precedes body sway during quiet standing. The purpose of this study was to investigate whether this preceding time is correlated with an improved stabilization of the body. 26 young and 23 elderly healthy subjects were asked to stand quietly. Body sway was measured using a laser displacement sensor, and the electromyogram of the right soleus was measured as a representative of the motor command. The correlation and the time shift between motor command and body sway were estimated by means of cross-correlation analysis. We found that sway size was correlated with the identified time shift: that is, a smaller sway size was associated with a longer preceding time. The obtained results suggest that a control strategy generating a larger preceding time can stabilize the body more effectively. This result was found in both the young and elderly, suggesting that the particular control aspect associated with the time shift is a common feature in both age groups.

Temporal correlations in center of body mass fluctuations during standing and walking.

Body fluctuations during both quiet standing and walking exhibit temporal correlations that reflect mechanisms of balance control. However, knowledge about the relationship between the temporal structures observed during standing and walking is limited. The goal of the present study was (1) to investigate temporal correlations in the fluctuations of the center of body mass acceleration (ACC) in standing and walking, and (2) to test the hypothesis that the degree of the temporal correlation for the two tasks is similar and correlated across participants. Seventeen young, healthy participants stood and walked for 10 min on a treadmill equipped with two force platforms. The temporal correlations of the ACC in the anteroposterior (ACC(AP)), mediolateral (ACC(ML)), and two-dimensional (ACC(2D)) directions were evaluated using the scaling index (alpha) as calculated with Detrended Fluctuation Analysis. The scaling indices of ACC fluctuations during standing and walking were categorized as stationary signals which are temporally correlated (0.5

Shaping appropriate locomotive motor output through interlimb neural pathway within spinal cord in humans.

Direct evidence supporting the contribution of upper limb motion on the generation of locomotive motor output in humans is still limited. Here, we aimed to examine the effect of upper limb motion on locomotor-like muscle activities in the lower limb in persons with spinal cord injury (SCI). By imposing passive locomotion-like leg movements, all cervical incomplete (n = 7) and thoracic complete SCI subjects (n = 5) exhibited locomotor-like muscle activity in their paralyzed soleus muscles. Upper limb movements in thoracic complete SCI subjects did not affect the electromyographic (EMG) pattern of the muscle activities. This is quite natural since neural connections in the spinal cord between regions controlling upper and lower limbs were completely lost in these subjects. On the other hand, in cervical incomplete SCI subjects, in whom such neural connections were at least partially preserved, the locomotor-like muscle activity was significantly affected by passively imposed upper limb movements. Specifically, the upper limb movements generally increased the soleus EMG activity during the backward swing phase, which corresponds to the stance phase in normal gait. Although some subjects showed a reduction of the EMG magnitude when arm motion was imposed, this was still consistent with locomotor-like motor output because the reduction of the EMG occurred during the forward swing phase corresponding to the swing phase. The present results indicate that the neural signal induced by the upper limb movements contributes not merely to enhance but also to shape the lower limb locomotive motor output, possibly through interlimb neural pathways. Such neural interaction between upper and lower limb motions could be an underlying neural mechanism of human bipedal locomotion.

Alternate leg movement amplifies locomotor-like muscle activity in spinal cord injured persons.

It is now well recognized that muscle activity can be induced even in the paralyzed lower limb muscles of persons with spinal cord injury (SCI) by imposing locomotion-like movements on both of their legs. Although the significant role of the afferent input related to hip joint movement and body load has been emphasized considerably in previous studies, the contribution of the "alternate" leg movement pattern has not been fully investigated. This study was designed to investigate to what extent the alternate leg movement influenced this "locomotor-like" muscle activity. The knee-locked leg swing movement was imposed on 10 complete SCI subjects using a gait training apparatus. The following three different experimental conditions were adopted: 1) bilateral alternate leg movement, 2) unilateral leg movement, and 3) bilateral synchronous (in-phase) leg movement. In all experimental conditions, the passive leg movement induced EMG activity in the soleus and medial head of the gastrocnemius muscles in all SCI subjects and in the biceps femoris muscle in 8 of 10 SCI subjects. On the other hand, the EMG activity was not observed in the tibialis anterior and rectus femoris muscles. The EMG level of these activated muscles, as quantified by integrating the rectified EMG activity recorded from the right leg, was significantly larger for bilateral alternate leg movement than for unilateral and bilateral synchronous movements, although the right hip and ankle joint movements were identical in all experimental conditions. In addition, the difference in the pattern of the load applied to the leg among conditions was unable to explain the enhancement of EMG activity in the bilateral alternate leg movement condition. These results suggest that the sensory information generated by alternate leg movements plays a substantial role in amplifying the induced locomotor-like muscle activity in the lower limbs.

Modulation of elbow joint stiffness in a vertical plane during cyclic movement at lower or higher frequencies than natural frequency.

The purpose of the present study was to determine how joint stiffness during cyclic movement in a vertical plane is modulated at lower or higher frequencies than the natural frequency of the system. Five male subjects were instructed to swing their forearms rhythmically in a vertical plane under various frequency conditions (0.7-2.25 Hz). To estimate the mechanical properties of the elbow joint, external perturbations were applied by an electromagnetic torque motor system to the forearm of each subject during the movement. Joint stiffness showed a significant quadratic trend with a minimum close to the natural frequency of the apparatus-forearm system (1.09+/-0.08 Hz). The resonant frequency showed the similar tendencies to joint stiffness and was significantly different from movement frequency in the lower frequency range (0.7-0.9 Hz). In addition, the ratio of joint stiffness to the background torque (ST(ratio)) was greater in the frequency conditions below the natural frequency than in the frequency conditions above the natural frequency and was relatively constant in the latter. These results suggested that: (1) the modulation of joint stiffness for movement in a vertical plane, by which the resonant frequency of the system is kept close to the movement frequency, may be limited to the movement frequency range above the natural frequency; and (2), in the case of movement in a vertical plane, the mechanism by which joint stiffness is modulated may change according to the relation between natural frequency and movement frequency.