Reinforcement-based processes actively regulate motor exploration along redundant solution manifolds.

From a baby's babbling to a songbird practising a new tune, exploration is critical to motor learning. A hallmark of exploration is the emergence of random walk behaviour along solution manifolds, where successive motor actions are not independent but rather become serially dependent. Such exploratory random walk behaviour is ubiquitous across species' neural firing, gait patterns and reaching behaviour. The past work has suggested that exploratory random walk behaviour arises from an accumulation of movement variability and a lack of error-based corrections. Here, we test a fundamentally different idea-that reinforcement-based processes regulate random walk behaviour to promote continual motor exploration to maximize success. Across three human reaching experiments, we manipulated the size of both the visually displayed target and an unseen reward zone, as well as the probability of reinforcement feedback. Our empirical and modelling results parsimoniously support the notion that exploratory random walk behaviour emerges by utilizing knowledge of movement variability to update intended reach aim towards recently reinforced motor actions. This mechanism leads to active and continuous exploration of the solution manifold, currently thought by prominent theories to arise passively. The ability to continually explore muscle, joint and task redundant solution manifolds is beneficial while acting in uncertain environments, during motor development or when recovering from a neurological disorder to discover and learn new motor actions.

Effect of Increasing Obstacle Distances Task on Postural Stability Variables During Gait Initiation in Older Nonfallers and Fallers.

OBJECTIVE: To compare the scaling of the postural stability variables between older nonfallers and fallers during gait initiation (GI) while stepping over increasing obstacle distances. DESIGN: Cross-sectional study. SETTING: University research laboratory. PARTICIPANTS: A sample of participants (N=24) divided into 2 groups: older nonfallers (n=12) and older fallers (n=12). Participants had no known neurologic, musculoskeletal, or cardiovascular conditions that could have affected their walking, and all were independent walkers. All the participants had an adequate cognitive function to participate as indicated by a score of more than 24 on the Mini-Mental State Examination. INTERVENTIONS: Not applicable. MAIN OUTCOME MEASURES: The primary dependent variables were peak anterior-posterior (AP) center of mass (CoM)-center of pressure (CoP) separation during anticipatory postural adjustments (APAs), AP CoM-CoP separation at the toe-off, and peak AP CoM-CoP separation during the swing. Secondary dependent variables were AP trunk angle during GI. Within- and between-repeated measures analysis of variance was used to compare means between groups across different task conditions for all the dependent variables. RESULTS: There was a main effect of group for peak AP CoM-CoP separation during APA (P=.018), an interaction effect between group and condition for AP CoM-CoP separation at toe-off (P=.009), and a main effect of condition for peak AP CoM-CoP separation during the swing (P<.001). We also found a main effect of group for peak AP trunk angle during the swing (P=.028). CONCLUSIONS: For GI while stepping over increasing obstacle distances, older fallers adopt a more conservative strategy of AP CoM-CoP separation than nonfallers prior to toe-off and demonstrate increased peak AP trunk lean during the swing. AP CoM-CoP separation prior to toe-off during the GI task may be a critical marker to identify fallers and warrants additional investigation.

Age of First Exposure to Soccer Heading and Sensory Reweighting for Upright Stance.

US Soccer eliminated soccer heading for youth players ages 10 years and younger and limited soccer heading for children ages 11-13 years. Limited empirical evidence associates soccer heading during early adolescence with medium-to-long-term behavioral deficits. The purpose of this study was to compare sensory reweighting for upright stance between college-aged soccer players who began soccer heading ages 10 years and younger (AFE ≤ 10) and those who began soccer heading after age 10 (AFE > 10). Thirty soccer players self-reported age of first exposure (AFE) to soccer heading. Sensory reweighting was compared between AFE ≤ 10 and AFE > 10. To evaluate sensory reweighting, we simultaneously perturbed upright stance with visual, vestibular, and proprioceptive stimulation. The visual stimulus was presented at two different amplitudes to measure the change in gain to vision, an intra-modal effect; and change in gain to galvanic vestibular stimulus (GVS) and vibration, both inter-modal effects. There were no differences in gain to vision (p=0.857, η2=0.001), GVS (p=0.971, η2=0.000), or vibration (p=0.974, η2=0.000) between groups. There were no differences in sensory reweighting for upright stance between AFE ≤ 10 and AFE > 10, suggesting that soccer heading during early adolescence is not associated with balance deficits in college-aged soccer players, notwithstanding potential deficits in other markers of neurological function.

Sensory-Challenge Balance Exercises Improve Multisensory Reweighting in Fall-Prone Older Adults.

BACKGROUND AND PURPOSE: Multisensory reweighting (MSR) deficits in older adults contribute to fall risk. Sensory-challenge balance exercises may have value for addressing the MSR deficits in fall-prone older adults. The purpose of this study was to examine the effect of sensory-challenge balance exercises on MSR and clinical balance measures in fall-prone older adults. METHODS: We used a quasi-experimental, repeated-measures, within-subjects design. Older adults with a history of falls underwent an 8-week baseline (control) period. This was followed by an 8-week intervention period that included 16 sensory-challenge balance exercise sessions performed with computerized balance training equipment. Measurements, taken twice before and once after intervention, included laboratory measures of MSR (center of mass gain and phase, position, and velocity variability) and clinical tests (Activities-specific Balance Confidence Scale, Berg Balance Scale, Sensory Organization Test, Limits of Stability test, and lower extremity strength and range of motion). RESULTS: Twenty adults 70 years of age and older with a history of falls completed all 16 sessions. Significant improvements were observed in laboratory-based MSR measures of touch gain (P = 0.006) and phase (P = 0.05), Berg Balance Scale (P = 0.002), Sensory Organization Test (P = 0.002), Limits of Stability Test (P = 0.001), and lower extremity strength scores (P = 0.005). Mean values of vision gain increased more than those for touch gain, but did not reach significance. DISCUSSION AND CONCLUSIONS: A balance exercise program specifically targeting multisensory integration mechanisms improved MSR, balance, and lower extremity strength in this mechanistic study. These valuable findings provide the scientific rationale for sensory-challenge balance exercise to improve perception of body position and motion in space and potential reduction in fall risk.

A central processing sensory deficit with Parkinson's disease.

Parkinson's disease (PD) is a progressive degenerative disease manifested by tremor, rigidity, bradykinesia, and postural instability. Deficits in proprioceptive integration are prevalent in individuals with PD, even at early stages of the disease. These deficits have been demonstrated primarily during investigations of reaching. Here, we investigated how PD affects sensory fusion of multiple modalities during upright standing. We simultaneously perturbed upright stance with visual, vestibular, and proprioceptive stimulation, to understand how these modalities are reweighted so that overall feedback remains suited to stabilizing upright stance in individuals with PD. Eight individuals with PD stood in a visual cave with a moving visual scene at 0.2 Hz while an 80-Hz vibratory stimulus was applied bilaterally to their Achilles tendons (stimulus turns on-off at 0.28 Hz) and a ±1 mA bilateral monopolar galvanic stimulus was applied at 0.36 Hz. The visual stimulus was presented at different amplitudes (0.2°, 0.8° rotation about ankle axis) to measure: the change in gain (weighting) to vision, an intramodal effect; and a simultaneous change in gain to vibration and galvanic stimulation, both intermodal effects. Trunk/leg gain relative to vision decreased when visual amplitude was increased, reflecting an intramodal visual effect. In contrast, when vibration was turned on/off, leg gain relative to vision was equivalent in individuals with PD, indicating no reweighting of visual information when proprioception was disrupted through vibration (i.e., no intermodal effect). Trunk and leg angle gain relative to GVS also showed no reweighting in individuals with PD. These results are in contrast to previous results with healthy adults, who showed clear intermodal effects in the same paradigm, suggesting that individuals with PD not only have a proprioceptive deficit during standing, but also have a cross-modal sensory fusion deficit that is crucial for upright stance control.

Function dictates the phase dependence of vision during human locomotion.

In human and animal locomotion, sensory input is thought to be processed in a phase-dependent manner. Here we use full-field transient visual scene motion toward or away from subjects walking on a treadmill. Perturbations were presented at three phases of walking to test 1) whether phase dependence is observed for visual input and 2) whether the nature of phase dependence differs across body segments. Results demonstrated that trunk responses to approaching perturbations were only weakly phase dependent and instead depended primarily on the delay from the perturbation. Recording of kinematic and muscle responses from both right and left lower limb allowed the analysis of six distinct phases of perturbation effects. In contrast to the trunk, leg responses were strongly phase dependent. Leg responses during the same gait cycle as the perturbation exhibited gating, occurring only when perturbations were applied in midstance. In contrast, during the postperturbation gait cycle, leg responses occurred at similar response phases of the gait cycle over a range of perturbation phases. These distinct responses reflect modulation of trunk orientation for upright equilibrium and modulation of leg segments for both hazard accommodation/avoidance and positional maintenance on the treadmill. Overall, these results support the idea that the phase dependence of responses to visual scene motion is determined by different functional tasks during walking.

Imaging the lower limb network in Parkinson's disease.

BACKGROUND: Despite the significant impact of lower limb symptoms on everyday life activities in Parkinson's disease (PD), knowledge of the neural correlates of lower limb deficits is limited. OBJECTIVE: We ran an fMRI study to investigate the neural correlates of lower limb movements in individuals with and without PD. METHODS: Participants included 24 PD and 21 older adults who were scanned while performing a precisely controlled isometric force generation task by dorsiflexing their ankle. A novel MRI-compatible ankle dorsiflexion device that limits head motion during motor tasks was used. The PD were tested on their more affected side, whereas the side in controls was randomized. Importantly, PD were tested in the off-state, following overnight withdrawal from antiparkinsonian medication. RESULTS: The foot task revealed extensive functional brain changes in PD compared to controls, with reduced fMRI signal during ankle dorsiflexion within the contralateral putamen and M1 foot area, and ipsilateral cerebellum. The activity of M1 foot area was negatively correlated with the severity of foot symptoms based on the Movement Disorder Society-Sponsored Revision of the Unified Parkinson's Disease Rating Scale (MDS-UPDRS-III). CONCLUSION: Overall, current findings provide new evidence of brain changes underlying motor symptoms in PD. Our results suggest that pathophysiology of lower limb symptoms in PD appears to involve both the cortico-basal ganglia and cortico-cerebellar motor circuits.

Rate control deficits during pinch grip and ankle dorsiflexion in early-stage Parkinson's disease.

BACKGROUND: Much of our understanding of the deficits in force control in Parkinson's disease (PD) relies on findings in the upper extremity. Currently, there is a paucity of data pertaining to the effect of PD on lower limb force control. OBJECTIVE: The purpose of this study was to concurrently evaluate upper- and lower-limb force control in early-stage PD and a group of age- and gender-matched healthy controls. METHODS: Twenty individuals with PD and twenty-one healthy older adults participated in this study. Participants performed two visually guided, submaximal (15% of maximum voluntary contractions) isometric force tasks: a pinch grip task and an ankle dorsiflexion task. PD were tested on their more affected side and after overnight withdrawal from antiparkinsonian medication. The tested side in controls was randomized. Differences in force control capacity were assessed by manipulating speed-based and variability-based task parameters. RESULTS: Compared with controls, PD demonstrated slower rates of force development and force relaxation during the foot task, and a slower rate of relaxation during the hand task. Force variability was similar across groups but greater in the foot than in the hand in both PD and controls. Lower limb rate control deficits were greater in PD with more severe symptoms based on the Hoehn and Yahr stage. CONCLUSIONS: Together, these results provide quantitative evidence of an impaired capacity in PD to produce submaximal and rapid force across multiple effectors. Moreover, results suggest that force control deficits in the lower limb may become more severe with disease progression.

Identification of neural feedback for upright stance in humans: stabilization rather than sway minimization.

A fundamental issue in motor control is how to determine the task goals for a given behavior. Here, we address this question by separately identifying the musculoskeletal and feedback components of the human postural control loop. Eighteen subjects were perturbed by two mechanical perturbations (gentle pulling from behind at waist and shoulder levels) and one sensory perturbation (movement of a virtual visual scene). Body kinematics was described by the leg and trunk segment angles in the sagittal plane. Muscle activations were described by ankle and hip EMG signals, with each EMG signal computed as a weighted sum of rectified EMG signals from multiple muscles at the given joint. The mechanical perturbations were used to identify feedback, defined as the mapping from the two segment angles to the two EMG signals. The sensory perturbation was used to estimate parameters in a mechanistic model of the plant, defined as the mapping from the two EMG signals to the two segment angles. Using the plant model and optimal control theory, we compared identified feedback to optimal feedback for a range of cost functions. Identified feedback was similar to feedback that stabilizes upright stance with near-minimum muscle activation, but was not consistent with feedback that substantially increases muscle activation to reduce movements of the body's center of mass or center of pressure. The results suggest that the common assumption of reducing sway may not apply to musculoskeletal systems that are inherently unstable.

Dynamics of inter-modality re-weighting during human postural control.

Flexible and stable postural control requires adaptation to changing environmental conditions, a process which requires re-weighting of multisensory stimuli. Recent studies, as well as predictions from a computational model, have indicated a reciprocal re-weighting relationship between modalities when a sensory stimulus changes amplitude. As one modality is down-weighted, another is up-weighted to compensate (and vice versa). The purpose of this study was to investigate the dynamics of intra- and inter-modality re-weighting process by examining postural responses to manipulation of proprioception and visual modalities simultaneously. Twenty-two young adults were placed in a visual cave and stood on a variable-pitch platform for thirteen trials of 250 s apiece. The platform was rotated at constant frequency of 0.4 Hz and amplitudes of 0.3 (low) or 1.5 (high) degrees. Platform amplitude was manipulated in two conditions: low-to-high or high-to-low. The visual stimulus was displayed at constant frequency of 0.35 Hz and amplitude of 0.08 degrees. The results showed both fast and slow changes in center of mass (CoM) response to the switch in platform amplitude. On both timescales, CoM response changed in a reciprocal manner relative to platform amplitude. When the platform amplitude increased (low-to-high condition), CoM response decreased relative to the platform and increased relative to the visual stimulus, indicating both intra-modality and inter-modality sensory re-weighting. In the high-to-low condition, however, there was no change in CoM response relative to visual stimulus, indicating that re-weighting may also be dependent on the absolute level of gain. Sway variability at frequencies other than the stimulus frequency also showed a reciprocal relationship with CoM gain relative to platform. Overall, these results indicate that dynamics of multisensory re-weighting is clearly more complicated than the schemes proposed by current adaptive models of human postural control.