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.

 

Introducing Dr. Charlotte DeVol Caskey!

Congratulations to Dr. Charlotte DeVol Caskey on earning her Doctorate in Mechanical Engineering! Dr. Caskey’s PhD thesis dissertation was titled Effects of Spinal Stimulation on Neuromechanics of Gait for Children with Cerebral Palsy. Congratulations and best of luck as you move forward as a Postdoc in the Human Neuromechanics Laboratory at the University of Florida in Gainesville!

EC Kuska, KM Steele (2024) “Does crouch alter the effects of neuromuscular impairments on gait? A simulation study”

Journal Article in Journal of Biomechanics

Cerebral palsy (CP) is a neurologic injury that impacts control of movement. Individuals with CP also often develop secondary impairments like weakness and contracture. Both altered motor control and secondary impairments influence how an individual walks after neurologic injury. However, understanding the complex interactions between and relative effects of these impairments makes analyzing and improving walking capacity in CP challenging.

A sagittal-plane musculoskeletal model and neuromuscular simulation framework that tracked average nondisabled (ND) kinematics and moderate and severe crouch gait. The model contains nine degrees-of-freedom (pelvic tilt and translation, and right and left hip, knee, and ankle flexion) actuated by eight Hill-type musculotendinous units per leg. The objective function minimized deviations from tracked kinematics and the sum of muscle activations squared (a2). We perturbed each gait simulation with multi-modal neuromuscular impairments—altered control, weakness, and contracture—of varying severities. Altered control was simulated by reducing the number of fixed synergies controlling each leg, and weakness and contracture were simulated by reducing a muscle’s maximum isometric force ( ) and tendon slack length ( ), respectively. A Bayesian Additive Regression Trees (BART) model then predicted resultant a2 from the simulated neuromuscular impairments for crouch and ND gait to evaluate the relative effects of each simulated neuromuscular impairment on the muscle activations required to maintain each gait pattern.Aim: The purpose of this study was to investigate the interactions between neuromuscular impairments and gait in CP.

Methods: We used a sagittal-plane musculoskeletal model and neuromuscular control framework to simulate crouch and nondisabled gait. We perturbed each simulation by varying the number of synergies controlling each leg (altered control), and imposed weakness and contracture. A Bayesian Additive Regression Trees (BART) model was also used to parse the relative effects of each impairment on the muscle activations required for each gait pattern.

Results: By using these simulations to evaluate gait-pattern specific effects of neuromuscular impairments, we identified some advantages of crouch gait. For example, crouch tolerated 13 % and 22 % more plantarflexor weakness than nondisabled gait without and with altered control, respectively. Furthermore, BART demonstrated that plantarflexor weakness had twice the effect on total muscle activity required during nondisabled gait than crouch gait. However, crouch gait was also disadvantageous in the presence of vasti weakness: crouch gait increased the effects of vasti weakness on gait without and with altered control.

Interpretation: These simulations highlight gait-pattern specific effects and interactions between neuromuscular impairments. Utilizing computational techniques to understand these effects can elicit advantages of gait deviations, providing insight into why individuals may select their gait pattern and possible interventions to improve energetics.

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.

AACPDM 2023

Two people smiling and taking a selfie while standing in front of The Shirley Ryan Ability Lab sign. Mia has blonde hair. Charlotte has brown hair and is wearing glasses.

Lab members, Charlotte Caskey and Mia Hoffman attended the 2023 American Academy for Cerebral Palsy and Developmental Medicine (AACPDM) Annual Meeting in Chicago, IL on September 10-13, 2023.

Charlotte gave a poster presentation on “Short-Burst Interval Treadmill Training Increases Step Length and Stability for Children with Cerebral Palsy.”

Mia gave a podium presentation during the Early Detection and Diagnosis session on “Quantifying the Activity Levels of Toddlers with Down Syndrome Playing in a Partial Body Weight Support System.

Great work in the Windy City!