David J. Clark

Merging of Healthy Motor Modules Predicts Reduced Locomotor Performance and Muscle Coordination Complexity Post-Stroke

Evidence suggests that the nervous system controls motor tasks using a low-dimensional modular organization of muscle activation. However, it is not clear if such an organization applies to coordination of human walking, nor how nervous system injury may alter the organization of motor modules and their biomechanical outputs. We first tested the hypothesis that muscle activation patterns during walking are produced through the variable activation of a small set of motor modules. In 20 healthy control subjects, EMG signals from eight leg muscles were measured across a range of walking speeds. Four motor modules identified through nonnegative matrix factorization were sufficient to account for variability of muscle activation from step to step and across speeds. Next, consistent with the clinical notion of abnormal limb flexion-extension synergies post-stroke, we tested the hypothesis that subjects with post-stroke hemiparesis would have altered motor modules, leading to impaired walking performance. In post-stroke subjects (n = 55), a less complex coordination pattern was shown. Fewer modules were needed to account for muscle activation during walking at preferred speed compared with controls. Fewer modules resulted from merging of the modules observed in healthy controls, suggesting reduced independence of neural control signals. The number of modules was correlated to preferred walking speed, speed modulation, step length asymmetry, and propulsive asymmetry. Our results suggest a common modular organization of muscle coordination underlying walking in both healthy and post-stroke subjects. Identification of motor modules may lead to new insight into impaired locomotor coordination and the underlying neural systems.

Impaired Voluntary Neuromuscular Activation Limits Muscle Power in Mobility-Limited Older Adults

BACKGROUND Age-related alterations of neuromuscular activation may contribute to deficits in muscle power and mobility function. This study assesses whether impaired activation of the agonist quadriceps and antagonist hamstrings, including amplitude- and velocity-dependent characteristics of activation, may explain differences in leg extension torque and power between healthy middle-aged, healthy older, and mobility-limited older adults. METHODS Torque, power, and electromyography were recorded during maximal voluntary leg extension trials across a range of velocities on an isokinetic dynamometer. RESULTS Neuromuscular activation was similar between middle-aged and older healthy groups, with differences in torque and power explained predominantly by muscle size. However, the older mobility-limited group demonstrated marked impairment of torque, power, and agonist muscle activation, with the greatest deficits occurring at the fastest movement velocities. Agonist muscle activation was found to be strongly associated with torque output. CONCLUSIONS Similar neuromuscular activation between the middle-aged and older healthy groups indicates that impaired voluntary activation is not an obligatory consequence of aging. However, the finding that the mobility-limited group exhibited impaired activation of the agonist quadriceps and concomitant deficits in torque and power output suggests that neuromuscular activation deficits may contribute to compromised mobility function in older adults.

The influence of locomotor rehabilitation on module quality and post-stroke hemiparetic walking performance

Recent studies have suggested the biomechanical subtasks of walking can be produced by a reduced set of co-excited muscles or modules. Individuals post-stroke often exhibit poor inter-muscular coordination characterized by poor timing and merging of modules that are normally independent in healthy individuals. However, whether locomotor therapy can influence module composition and timing and whether these improvements lead to improved walking performance is unclear. The goal of this study was to examine the influence of a locomotor rehabilitation therapy on module composition and timing and post-stroke hemiparetic walking performance. Twenty-seven post-stroke hemiparetic subjects participated in a 12-week locomotor intervention incorporating treadmill training with body weight support and manual trainers accompanied by training overground walking. Electromyography (EMG), kinematic and ground reaction force data were collected from subjects both pre- and post-therapy and from 19 age-matched healthy controls walking on an instrumented treadmill at their self-selected speed. Non-negative matrix factorization was used to identify the module composition and timing from the EMG data. Module timing and composition, and various measures of walking performance were compared pre- and post-therapy. In subjects with four modules pre- and post-therapy, locomotor training resulted in improved timing of the ankle plantarflexor module and a more extended paretic leg angle that allowed the subjects to walk faster and with more symmetrical propulsion. In addition, subjects with three modules pre-therapy increased their number of modules and improved walking performance post-therapy. Thus, locomotor training has the potential to influence module composition and timing, which can lead to improvements walking performance.

Neuromuscular Contributions to Age-Related Weakness

BACKGROUND Declines in skeletal muscle mass and quality are important factors contributing to age-related weakness. Neural activation of agonist and antagonist muscles may also be important contributing factors. METHODS We conducted a review of the scientific literature on older adults to determine (a) methodologies used to quantify activation, (b) the potential role of agonist and antagonist activation on weakness, and (c) some possible neurophysiological mechanisms that may underlie impaired activation. RESULTS The cumulative evidence indicates that agonist activation is impaired in some, but not all, older adults and that this impairment contributes to age-related weakness. It is possible that antagonist coactivation also plays a role in age-related weakness, though a definitive link has not been established. CONCLUSION Future research should focus on improving quantitative measurement and mechanistic understanding of impaired activation with aging.

Muscle Performance and Physical Function Are Associated With Voluntary Rate of Neuromuscular Activation in Older Adults

BACKGROUND Muscle power is related to mobility function in older adults, and effective power production requires rapid neuromuscular activation. Accordingly, this study examines the association of neuromuscular activation rate with muscle performance in persons of different age and mobility function. METHODS Participants were recruited to three experimental groups: middle-aged healthy adults (MH), older healthy adults (OH), and older adults with mobility limitations (OML). OH and OML were primarily differentiated by performance on the Short Physical Performance Battery (SPPB). Muscle performance (acceleration and power) and electromyography (EMG) were recorded during a maximal-effort leg press task at an absolute resistance (260 N) and at a relative resistance (70% of the one-repetition maximum [1 RM]). Neuromuscular activation rate was quantified as pre-movement time (duration between EMG onset and movement onset) and the rate of EMG rise. RESULTS Pre-movement time, rate of EMG rise, leg press acceleration, and leg press power were lower in OML relative to MH and OH but did not differ between OH and MH, with the exception of power at 70% 1RM. Across all older participants, rate of EMG rise was positively associated with acceleration, power, and the SPPB score. CONCLUSIONS Slowing of neuromuscular activation rate is associated with compromised dynamic muscle performance, which may contribute to mobility limitations in some older adults. Future research should identify the precise neurophysiological impairments that contribute to declines in neuromuscular activation rate and mobility function with aging.

Activation impairment alters muscle torque–velocity in the knee extensors of persons with post-stroke hemiparesis

OBJECTIVE To elucidate mechanisms of impaired force production in post-stroke hemiparesis. METHODS Knee extensor torque-velocity and activation-velocity relationships were examined in seventeen persons with post-stroke hemiparesis (age 57.5, +/-6.9) and thirteen non-disabled (age 63.0 +/-10.4) persons. RESULTS Velocity-dependent concentric torque impairment was exaggerated in subjects with hemiparesis relative to control subjects (p<.001). Muscle power was also less in the group with hemiparesis (p<.001), and plateaued at velocities > or =90deg/s (p>.05). In the control group agonist EMG during concentric actions exhibited a positive linear relationship as velocity increased (R(2)=.93, p<.05). The group with hemiparesis produced 34-60% less agonist EMG than controls (p<.02) and modulation was absent (p>.05). Antagonist EMG was either greater in the control (biceps femoris, p<.006) or similar between groups (semimembranosus, p=.95). Under eccentric testing conditions, torque normalized to peak isometric torque (p=.44) and rectus femoris activation (p=.33) were similar between groups, indicating a relative preservation of eccentric torque producing capacity post-stroke. CONCLUSIONS Certain clinical perspectives assert that weakness following central nervous system injury stems from spastic antagonist restraint. Instead, absence of an antagonist restraint strongly suggests that impaired agonist activation is the principal determinant of hemiparetic weakness. SIGNIFICANCE These findings have important implications for promoting optimal recovery of motor function in neuro-rehabilitation.

Evaluation of Abnormal Synergy Patterns Poststroke: Relationship of the Fugl-Meyer Assessment to Hemiparetic Locomotion:

Background. Assessment of poststroke motor impairment has historically focused on the ability to move within and outside of abnormal synergistic motor patterns and is typically quantified by the Fugl-Meyer Assessment (FMA). However, it is unclear if the voluntary, isolated movement tasks of the FMA are appropriate for evaluating walking task-specific motor control requirements because walking is cyclical and involves considerable sensorimotor integration. Objective. The purpose of this study is to test whether the motor impairment measured by the FMA is indicative of motor dysfunction during walking in poststroke adults. Methods. Thirty-four individuals with chronic poststroke hemiparesis and 17 healthy controls walked for 60 seconds on an instrumented treadmill while recording electromyographic activity (EMG) from 8 lower extremity muscles. EMG recordings were also obtained during the FMA for those with hemiparesis to examine muscle activation patterns. Each participant was examined with a battery of walking-specific clinical and biomechanical assessment tools and stratified based on the FMA synergy (FMS) score. To further quantify muscle activation patterns during walking, a nonnegative matrix factorization (NNMF) determined the number of independent modules required to describe 90% of the total variance in the EMG patterns. Results. Stratification poorly differentiated motor activation across FMA tasks as well as EMG patterns during walking. While FMS correlated with 2 of 6 walking assessments, the number of EMG modules significantly correlated with all 6 walking performance measures. Conclusions. Voluntary, discrete activities as performed in the FMA may be inadequate to capture the complex motor behavior in walking. Conversely, walking-specific evaluations such as NNMF appear more appropriate.

Automaticity of walking: functional significance, mechanisms, measurement and rehabilitation strategies.

Automaticity is a hallmark feature of walking in adults who are healthy and well-functioning. In the context of walking, “automaticity” refers to the ability of the nervous system to successfully control typical steady state walking with minimal use of attention-demanding executive control resources. Converging lines of evidence indicate that walking deficits and disorders are characterized in part by a shift in the locomotor control strategy from healthy automaticity to compensatory executive control. This is potentially detrimental to walking performance, as an executive control strategy is not optimized for locomotor control. Furthermore, it places excessive demands on a limited pool of executive reserves. The result is compromised ability to perform basic and complex walking tasks and heightened risk for adverse mobility outcomes including falls. Strategies for rehabilitation of automaticity are not well defined, which is due to both a lack of systematic research into the causes of impaired automaticity and to a lack of robust neurophysiological assessments by which to gauge automaticity. These gaps in knowledge are concerning given the serious functional implications of compromised automaticity. Therefore, the objective of this article is to advance the science of automaticity of walking by consolidating evidence and identifying gaps in knowledge regarding: (a) functional significance of automaticity; (b) neurophysiology of automaticity; (c) measurement of automaticity; (d) mechanistic factors that compromise automaticity; and (e) strategies for rehabilitation of automaticity.

Comparative Effects of Light or Heavy Resistance Power Training for Improving Lower Extremity Power and Physical Performance in Mobility-Limited Older Adults

BACKGROUND We compared the effects of two uniquely different lower extremity power training interventions on changes in muscle power, physical performance, neuromuscular activation, and muscle cross sectional area in mobility-limited older adults. METHODS Fifty-two subjects (78±5 years, short physical performance battery score: 8.1±1) were randomized to either 16 weeks of progressive high velocity resistance training performed at low external resistance (40% of the 1-repetition maximum [1-RM] [LO]) or high external resistance (70% of 1RM [HI]). Both groups completed three sets of leg and knee extension exercises at maximum voluntary velocity, two times per week. Neuromuscular activation was assessed using surface electromyography and muscle cross sectional area (CSA) was measured using computed tomography. RESULTS At 16 weeks, LO and HI exhibited significant and similar within-group increases of leg extensor peak power (~34% vs ~42%), strength (~13% vs ~19%), and SPPB score (1.4±0.3 vs 1.8±0.3 units), respectively (all P < .03). Improvements in neuromuscular activation occurred in LO (P = .03) while small gains in mid-thigh muscle CSA were detected in LO (1.6%, P = .35) and HI (2.1%, P = .17). No significant between-group differences were evident for any measured parameters (all P > .25). CONCLUSIONS High velocity resistance training with low external resistance yields similar improvements in muscle power and physical performance compared to training with high external resistance in mobility-limited elders. These findings may have important implications for optimizing exercise interventions for older adults with mobility limitations.

Comparison of Motor Control Deficits During Treadmill and Overground Walking Poststroke

Background. Force-sensing split-belt treadmills (TMs) provide an alternative to the conventional overground (OG) setting and allow new avenues for analyzing the biomechanics and motor control of walking. However, walking control may differ on a TM compared with walking OG. Objective. To compare spatiotemporal, kinematic, and EMG-based measures of motor control between TM and OG walking at self-selected and fastest comfortable speeds in persons with poststroke hemiparesis. Methods. Individuals with chronic hemiparesis (56) and similarly aged healthy individuals (17) walked over an instrumented walkway and on an instrumented split-belt TM; 16 channels of EMG recorded bilateral muscle activity, and a 12-camera motion capture system collected bilateral 3D kinematics. The authors applied a nonnegative matrix factorization (NNMF) algorithm to examine the underlying patterns of motor control. Results. Self-selected walking patterns differed on the TM versus OG in controls: speed decreased, stride length decreased, stance percentage increased, and double-support percentage increased. Poststroke, responses were similar, but cadence also decreased, and step length asymmetry increased. Kinematic patterns were similar except those associated with slower walking speeds. NNMF demonstrated similar EMG variance in the 2 environments. Conclusion. Persons, both healthy and poststroke, walk with different gait parameters on the TM. Although measures of motor control were mostly similar between the 2 environments, the TM induced step length asymmetry in 30% of participants (60% of whom took longer paretic steps). TM walking, therefore, is a valid method for detecting motor control deficits.