Audiovisual biofeedback amplifies plantarflexor adaptation during walking among children with cerebral palsy.

BACKGROUND: Biofeedback is a promising noninvasive strategy to enhance gait training among individuals with cerebral palsy (CP). Commonly, biofeedback systems are designed to guide movement correction using audio, visual, or sensorimotor (i.e., tactile or proprioceptive) cues, each of which has demonstrated measurable success in CP. However, it is currently unclear how the modality of biofeedback may influence user response which has significant implications if systems are to be consistently adopted into clinical care. METHODS: In this study, we evaluated the extent to which adolescents with CP (7M/1F; 14 [12.5,15.5] years) adapted their gait patterns during treadmill walking (6 min/modality) with audiovisual (AV), sensorimotor (SM), and combined AV + SM biofeedback before and after four acclimation sessions (20 min/session) and at a two-week follow-up. Both biofeedback systems were designed to target plantarflexor activity on the more-affected limb, as these muscles are commonly impaired in CP and impact walking function. SM biofeedback was administered using a resistive ankle exoskeleton and AV biofeedback displayed soleus activity from electromyography recordings during gait. At every visit, we measured the time-course response to each biofeedback modality to understand how the rate and magnitude of gait adaptation differed between modalities and following acclimation. RESULTS: Participants significantly increased soleus activity from baseline using AV + SM (42.8% [15.1, 59.6]), AV (28.5% [19.2, 58.5]), and SM (10.3% [3.2, 15.2]) biofeedback, but the rate of soleus adaptation was faster using AV + SM biofeedback than either modality alone. Further, SM-only biofeedback produced small initial increases in plantarflexor activity, but these responses were transient within and across sessions (p > 0.11). Following multi-session acclimation and at the two-week follow-up, responses to AV and AV + SM biofeedback were maintained. CONCLUSIONS: This study demonstrated that AV biofeedback was critical to increase plantarflexor engagement during walking, but that combining AV and SM modalities further amplified the rate of gait adaptation. Beyond improving our understanding of how individuals may differentially prioritize distinct forms of afferent information, outcomes from this study may inform the design and selection of biofeedback systems for use in clinical care.

Motor control complexity can be dynamically simplified during gait pattern exploration using motor control-based biofeedback.

Understanding how the central nervous system coordinates diverse motor outputs has been a topic of extensive investigation. Although it is generally accepted that a small set of synergies underlies many common activities, such as walking, whether synergies are equally robust across a broader array of gait patterns or can be flexibly modified remains unclear. Here, we evaluated the extent to which synergies changed as nondisabled adults (n = 14) explored gait patterns using custom biofeedback. Secondarily, we used Bayesian additive regression trees to identify factors that were associated with synergy modulation. Participants explored 41.1 ± 8.0 gait patterns using biofeedback, during which synergy recruitment changed depending on the type and magnitude of gait pattern modification. Specifically, a consistent set of synergies was recruited to accommodate small deviations from baseline, but additional synergies emerged for larger gait changes. Synergy complexity was similarly modulated; complexity decreased for 82.6% of the attempted gait patterns, but distal gait mechanics were strongly associated with these changes. In particular, greater ankle dorsiflexion moments and knee flexion through stance, as well as greater knee extension moments at initial contact, corresponded to a reduction in synergy complexity. Taken together, these results suggest that the central nervous system preferentially adopts a low-dimensional, largely invariant control strategy but can modify that strategy to produce diverse gait patterns. Beyond improving understanding of how synergies are recruited during gait, study outcomes may also help identify parameters that can be targeted with interventions to alter synergies and improve motor control after neurological injury.NEW & NOTEWORTHY We used a motor control-based biofeedback system and machine learning to characterize the extent to which nondisabled adults can modulate synergies during gait pattern exploration. Results revealed that a small library of synergies underlies an array of gait patterns but that recruitment from this library changes as a function of the imposed biomechanical constraints. Our findings enhance understanding of the neural control of gait and may inform biofeedback strategies to improve synergy recruitment after neurological injury.

Factors influencing neuromuscular responses to gait training with a robotic ankle exoskeleton in cerebral palsy.

A current limitation in the development of robotic gait training interventions is understanding the factors that predict responses to treatment. The purpose of this study was to explore the application of an interpretable machine learning method, Bayesian Additive Regression Trees (BART), to identify factors influencing neuromuscular responses to a resistive ankle exoskeleton in individuals with cerebral palsy (CP). Eight individuals with CP (GMFCS levels I - III, ages 12-18 years) walked with a resistive ankle exoskeleton over seven visits while we measured soleus activation. A BART model was developed using a predictor set of kinematic, device, study, and participant metrics that were hypothesized to influence soleus activation. The model (R2 = 0.94) found that kinematics had the largest influence on soleus activation, but the magnitude of exoskeleton resistance, amount of gait training practice with the device, and participant-level parameters also had substantial effects. To optimize neuromuscular engagement during exoskeleton training in individuals with CP, our analysis highlights the importance of monitoring the user's kinematic response, in particular, peak stance phase hip flexion and ankle dorsiflexion. We demonstrate the utility of machine learning techniques for enhancing our understanding of robotic gait training outcomes, seeking to improve the efficacy of future interventions.

Soleus H-reflex modulation in cerebral palsy and its relationship with neural control complexity: a pilot study.

Individuals with cerebral palsy (CP) display motor control patterns that suggest decreased supraspinal input, but it remains unknown if they are able to modulate lower-limb reflexes in response to more complex tasks, or whether global motor control patterns relate to reflex modulation capacity in this population. Eight ambulatory individuals with CP (12-18 years old) were recruited to complete a task complexity protocol, where soleus H-reflex excitability was compared between bilateral (baseline) and unilateral (complex) standing. We also investigated the relationship between each participant's ability to modulate soleus H-reflex excitability and the complexity of their walking neural control pattern determined from muscle synergy analysis. Finally, six of the eight participants completed an exoskeleton walking protocol, where soleus H-reflexes were collected during the stance phase of walking with and without stance-phase plantar flexor resistance. Participants displayed a significant reduction in soleus H-reflex excitability (- 26 ± 25%, p = 0.04) with unilateral standing, and a strong positive relationship was observed between more refined neural control during walking and an increased ability to modulate reflex excitability (R = 0.79, p = 0.04). There was no difference in neuromuscular outcome measures with and without the ankle exoskeleton (p values all > 0.05), with variable reflex responses to walking with ankle exoskeleton resistance. These findings provide evidence that ambulatory individuals with CP retain some capacity to modulate lower-limb reflexes in response to increased task complexity, and that less refined neural control during walking appears to be related to deficits in reflex modulation.

Synergies are minimally affected during emulation of cerebral palsy gait patterns.

Muscle synergy analysis is commonly used to characterize motor control during dynamic tasks like walking. For clinical populations, such as children with cerebral palsy (CP), synergies are altered compared to nondisabled (ND) peers and have been associated with both function and treatment outcomes. However, the factors that contribute to altered synergies remain unclear. In particular, the extent to which synergies reflect altered biomechanics (e.g., changes in gait) or underlying neurologic injury is debated. To evaluate the effect that altered biomechanics have on synergies, we compared synergy complexity and structure while ND individuals (n = 14) emulated four common CP gait patterns (equinus, equinus-crouch, mild-crouch, and moderate crouch). Secondarily, we compared the similarity of ND synergies during emulation to synergies from a retrospective cohort of individuals with CP walking in similar gait patterns (n = 28 per pattern). During emulation, ND individuals recruited similar synergies as baseline walking. However, pattern-specific deviations in synergy activations and complexity emerged. In particular, equinus gait altered plantarflexor activation timing and reduced synergy complexity. Importantly, ND synergies during emulation were distinct from those observed in CP for all gait patterns. These results suggest that altered gait patterns are not primarily driving the changes in synergies observed in CP, highlighting the value of using synergies as a tool to capture patient-specific differences in motor control. However, they also highlight the sensitivity of both synergy activations and complexity to altered biomechanics, which should be considered when using these measures in clinical care.