Effects of repeated waist-pull perturbations on gait stability in subjects with cerebellar ataxia

Abstract

Background: Damage to the cerebellum can affect neural structures involved in locomotion, causing gait and balance disorders. However, the integrity of cerebellum does not seem to be critical in managing sudden and unexpected environmental changes such as disturbances during walking. The cerebellum also plays a functional role in motor learning. Only a few effective therapies exist for individuals with cerebellar ataxia. With these in mind, we aimed at investigating: (1) corrective response of participants with cerebellar ataxia (CA) to unexpected gait perturbations; and (2) the effectiveness of a perturbation-based training to improve their dynamic stability during balance recovery responses and steady walking. Specifically, we hypothesized that: (1) CA group can show a corrective behavior similar to that of a healthy control group; (2) the exposure to a perturbation-based treatment can exploit residual learning capability, thus improving their dynamic stability during balance recovery responses and steady locomotion.

Methods: Ten participants with cerebellar ataxia and eight age-matched healthy adults were exposed to a single perturbation-based training session. The Active Tethered Pelvic Assist Device applied unexpected waist-pull perturbations while participants walked on a treadmill. Spatio-temporal parameters and dynamic stability were determined during corrective responses and steady locomotion, before and after the training. The ANalysis Of VAriance was the main statistical test used to assess the effects of group (healthy vs CA) and training (baseline vs post) on spatio-temporal parameters of the gait and margin of stability.

Results: Data analysis revealed that individuals with cerebellar ataxia behaved differently from healthy volunteers: (1) they retained a wider base of support during corrective responses and steady gait both before and after the training; (2) due to the training, patients improved their anterior-posterior margin of stability during steady walking only.

Conclusions: Our results revealed that participants with cerebellar ataxia could still rely on their learning capability to modify the gait towards a safer behavior. However, they could not take advantage from their residual learning capability while managing sudden and unexpected perturbations. Accordingly, the proposed training paradigm can be considered as a promising approach to improve balance control during steady walking in these individuals.

Keywords: Balance recovery; Cerebellar ataxia; Gait perturbations; Perturbation-based training.

Fig. 1

Experimental setup and protocol. a Schematic of the Active Tethered Pelvic Assist Device (A-TPAD). Antero-Posterior perturbations were applied using Motors 1 and 3 or Motors 2 and 4, Medio-Lateral perturbations were applied using Motors 1 and 2 or Motors 3 and 4. b Participant walks on the treadmill wearing the brace attached to the cables and the safety harness. Few reflective markers are highlighted in yellow dots. Full marker-set involves: C7 vertebrae, T10 vertebrae, clavicle, sternum and acromions, for the upper trunk; lateral and medial epicondyle of the humerus, radial and ulnar styloids, third metacarpal bones and additional markers rigidly attached to wands over the midhumerus, for both arms; anterior superior iliac spines and sacrum, for the pelvis; greater trochanters external surface, lateral and medial epicondyle of the femurs, heads of the fibula, lateral and medial malleolus, calcaneus, first and fifth metatarsal heads, toe, and additional markers rigidly attached to a wand over the midfemurs and midshaft of the tibia, for both legs; 4 markers attached to the brace. c Experiment protocol

Fig. 2

Spatio-temporal parameters during balance recovery responses. Spatio-temporal parameters (mean ± standard deviation) observed during balance recovery responses after diagonal perturbations, before (D_pre) and after (D_post) training, for subjects with cerebellar ataxia (CA; gray bars) and healthy control group (HG; black bars). Pairwise comparisons reaching significance are reported (* p < 0.05, ** p < 0.01, *** p < 0.0001); vertical and horizontal lines are related to the group (CA vs HG) and session (pre vs post) effects, respectively. a step length; b step width; c step duration; d stance_%

Fig. 3

Margin of Stability during balance recovery responses. Dynamic stability (mean ± standard deviation) observed during balance recovery responses after diagonal perturbations, before (D_pre) and after (D_post) the training, for subjects with cerebellar ataxia (CA; gray bars) and healthy control group (HG; black bars). Pairwise comparisons reaching significance are reported (* p < 0.05, ** p < 0.01, *** p < 0.0001); vertical and horizontal lines are related to the group (CA vs HG) and session (pre vs post) effects, respectively. a MoS_AP; b MoS_ML

Fig. 4

Spatio-temporal parameters during steady walking. Spatio-temporal parameters (mean ± standard deviation) observed during steady walking trials, before (baseline) and after (post-) training, for subjects with cerebellar ataxia (CA; gray bars) and healthy control group (HG; black bars). Pairwise comparisons reaching significance are reported (* p < 0.05, ** p < 0.01, *** p < 0.0001); vertical and horizontal lines are related to the group (CA vs HG) and session (pre vs post) effects, respectively. a step length; b step width; c step duration; d stance_%

Fig. 5

Margin of Stability during steady walking. Dynamic stability (mean ± standard deviation) observed during steady walking trials, before (baseline) and after (post-) training, for subjects with cerebellar ataxia (CA; gray bars) and healthy control group (HG; black bars). Pairwise comparisons reaching significance are reported (* p < 0.05, ** p < 0.01, *** p < 0.001); vertical and horizontal lines are related to the group (CA vs HG) and session (pre vs post) effects, respectively. a MoS_AP; b MoS_ML