AM Spomer, BC Conner, MH Schwartz, ZF Lerner, KM Steele (2024) “Multi-session adaptation to audiovisual and sensorimotor biofeedback is heterogeneous among adolescents with cerebral palsy”

Journal Article in PLoS ONE

There is growing interest in the use of biofeedback-augmented gait training in cerebral palsy (CP). Audiovisual, sensorimotor, and immersive biofeedback paradigms are commonly used to elicit short-term gait improvements; however, outcomes remain variable. Because biofeedback training requires that individuals have the capacity to both adapt their gait in response to feedback and retain improvements across sessions, changes in either capacity may affect outcomes. Yet, neither has been explored extensively in CP.

Experimental protocol used to evaluate multi-session adaptation to multimodal biofeedback. Participants completed a four-day protocol using combined audiovisual and sensorimotor biofeedback. Audiovisual biofeedback on soleus activity was provided unilaterally on the more-affected limb whereas sensorimotor biofeedback was administered bilaterally using a resistive ankle exoskeleton. Each session was separated into baseline (1 minute), biofeedback (2, 10-minute bouts), and washout (1 minute) phases. The nominal torque value of the ankle exoskeleton was set at 0.1 Nm/kg during the first bout of the first session and incrementally adjusted by 0.025 Nm/kg over the subsequent bouts, according to the schedule shown. Overground walking data were collected pre- and post-intervention. A licensed physical therapist also performed a full physical examination at the pre-intervention session. Motion capture data were collected during at the pre- and post-intervention sessions and electromyography (EMG) data were collected bilaterally from the vastus lateralis, semitendinosus, soleus, and tibialis anterior across all sessions.Aim: The aim of this study was to evaluate the extent to which individuals with CP adapt gait and retain improvements during multi-session practice with a multimodal biofeedback paradigm, designed to promote plantarflexor recruitment. Secondarily, we compared overground walking performance before and after biofeedback sessions to understand if any observed in-session improvements were transferred. 

Methods: In this study, we evaluated the extent to which adolescents with CP (7M/1F; 14 years (12.5,15.26)) could adapt gait and retain improvements across four, 20-minute sessions using combined audiovisual and sensorimotor biofeedback. Both systems were designed to target plantarflexor activity. Audiovisual biofeedback displayed real-time soleus activity and sensorimotor biofeedback was provided using a bilateral resistive ankle exoskeleton. We quantified the time-course of change in muscle activity within and across sessions and overground walking function before and after the four sessions.

Results: All individuals were able to significantly increase soleus activity from baseline using multimodal biofeedback (p < 0.031) but demonstrated heterogeneous adaptation strategies. In-session soleus adaptation had a moderate positive correlation with short-term retention of the adapted gait patterns (0.40 ≤ ρ ≤ 0.81), but generally weak correlations with baseline walking function (GMFCS Level) and motor control complexity (ρ ≤ 0.43). The latter indicates that adaptation capacity may be a critical and unique metric underlying response to biofeedback. Notably, in-session gains did not correspond to significant improvements in overground walking function (p > 0.11).

Interpretation: This work suggests that individuals with CP have the capacity to adapt their gait using biofeedback, but responses are highly variable. Characterizing the factors driving adaptation to biofeedback may be a promising avenue to understand the heterogeneity of existing biofeedback training outcomes and inform future system optimization for integration into clinical care.

 

Dr. Alyssa Spomer on “Gears of Progress” Podcast

Gears of Progress Episode 7 featured Alyssa Spomer on biofeedback tech to improve motor control ankle exoskeletons, and work as a clinical scientist at Gillette Children's Hospital.“Gears of Progress” Episode Seven featured Steele Lab Alumni, Dr. Alyssa Spomer on biofeedback tech to improve motor control ankle exoskeletons, and work as a clinical scientist at Gillette Children’s Hospital.

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AM Spomer, BC Conner, MH Schwartz, ZF Lerner, KM Steele (2023) “Audiovisual biofeedback amplifies plantarflexor adaptation during walking among children with cerebral palsy”

Journal Article in Journal of NeuroEngineering and Rehabilitation

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.

Figure 1. Experimental Protocol. Audiovisual (AV) biofeedback on soleus activity was provided for the more-affected limb alongside an auto-adjusting target score. Sensorimotor (SM) biofeedback was provided for the more-affected limb using an untethered ankle exoskeleton designed to impart a resistive ankle torque through stance, proportional to baseline values. Participants completed three data collection visits (pre-acclimation, post-acclimation, and follow-up), during which they walked with both biofeedback systems independently and in combination. Trials were pseudo-randomized within and between visits to ensure that feedback modalities were presented to each participant in a different order and control for fatigue and learning effects. Each trial was 10 min long and separated into baseline, feedback, and washout phases. All data analysis was performed for early (strides 1–30), mid (strides 91–110), and late (strides 181–210) feedback phases and washout (strides 1–30). Mean soleus activity for individual strides (purple dots) was normalized to baseline activity. Between the pre-acclimation and post-acclimation visits, participants completed four, 20-min acclimation sessions where they received additional practice with both systems

Aim: The aim of this study is to evaluate how the modality of biofeedback may influence user response which has significant implications if systems are to be consistently adopted into clinical care.

Method: 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.

Interpretation: 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.

AM Spomer, RZ Yan, MH Schwartz, KM Steele (2023) “Motor control complexity can be dynamically simplified during gait pattern exploration using motor control-based biofeedback”

Journal Article in Journal of Neurophysiology

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.

Schematic of the custom biofeedback system. A) Motor control biofeedback used to encourage pattern exploration. B) Individuals significantly modified motor control complexity using biofeedback. C) Distal gait mechanics were associated with changes in control complexity.Aim: The aim of this study was to characterize the robustness of synergies to changing biomechanical constraints during walking. Specifically, we evaluated the extent to which nondisabled individuals could modulate both synergy structure and complexity while using motor control biofeedback to drive broad gait pattern exploration.

Methods: 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.

Results: 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.

Interpretation: 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.