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Effects of a Perturbation-Based Balance Training on Compensatory Postural Responses to Backward Loss of Balance in Patients with Cerebellar Disease: A Case Study

OBJECTIVES The damage to the cerebellum primarily results in balance-related abnormalities that may affect performance of locomotion and postural adjustments, eventually contributing to an increased risk of fall and fear of falling in patients with cerebellar disease. The purpose of the present study was to investigate the effect of a perturbation-based training that induced backward loss of balance on compensatory postural responses in patients with cerebellar disease. METHODS The participant was a 51-year-old female diagnosed with spinocerebellar ataxia and had the disease for 19 years. The perturbation-based backward balance training was performed over 8 weeks (a total of 24 training sessions) in order to facilitate the perception of postural perturbation onset and execution of rapid compensatory responses. RESULTS The patient demonstrated a noticeable reduction in the number of steps required to recover body balance after postural disturbances. The reduction of multi-step reactions in recovering balance could be attributed to improvements in the body center-of-mass displacement and trunk control during the landing of step. Besides, there were also improvements in subjective measures of functional mobility and psychological well-being after the balance training. CONCLUSION Although current research evidence of balance rehabilitation for cerebellar patients is lacking, this study offers the feasibility of adaptive training to improve postural stability through task-specific training intervention.


Introduction
The cerebellum is a neural structure that plays a crucial role in regulating gait, postural stability, and coordination of movements. Particularly, the medial region of the cerebellum (i.e., vermis) is known to be greatly involved in maintenance of upright balance and stance [1]. Neurophysiological studies revealed that the medial cerebellar zone integrates spinal and vestibular inputs, and affects the neural pathways for balance control [2]. Accordingly, damage or lesions to this region primarily result in balance-related abnormalities that may influence performance of postural adjustments. These motor dysfunctions are known to significantly contribute to an increased risk of fall and fear of falling in patients with cerebellar disease [3]. In fact, it has been reported that cerebellar patients are more likely to experience more than Asian J Kinesiol 2021; 23 (1): 53-61 · DOI: https://doi.org /10.15758/ajk.2021.23.1.53 Case Study 54 | The Asian Journal of Kinesiology Asian J Kinesiol 2021; 23 (1): 53-61 . DOI: https://doi.org /10.15758/ajk.2021.23.1.53 one fall annually [4]. These falls frequently led to injuries or immobility in physical activity causing reduced quality of life in patients with cerebellar disease [5].
A fall is essentially a failure to regain balance from a postural instability [6]. Many studies have attempted to develop effective fall prevention programs, and it is suggested that exercise-based programs with balance training appear to be optimal rehabilitation interventions in preventing falls in older adults [7]. Particularly, task-specific balance training based on the objective analysis of key components in recovering balance could have more positive influence on fall prevention [8].
Although there are many factors that contribute to balance recovery from falls, it has been shown that execution of rapid and effective stepping responses upon postural disturbances is critical to prevent falls. Particularly, the characteristics of the first step movement after loss of balance, such as stepping time and length, are associated with successful recovery of body stability [9]. In addition, another key factor is the control of trunk movement following perturbation. Sufficient flexion of trunk motion in the opposite direction to the perturbation is also required to arrest the body center of mass (COM) for recovering stability [10]. Therefore, it is evident that exercise training programs that aimed to improving both capabilities of executing rapid stepping reactions and controlling trunk motion would produce greater reduction in fall rates.
It is reported that the most common causes of fall incidence in elderly population in daily life are associated with tripping or slipping [11]. In case of slipping that mostly induces a posterior fall, rapid compensatory responses are necessary to avoid a fall. Backward loss of balance is more dangerous than other directions of falls because the limit of foot stability is shorter than anterior direction and direct vision of environment is not available. Thus, adequate sensation of the posterior instability and subsequent execution of backward reactive stepping are important to prevent posterior falls [12].
Previous studies have demonstrated that repeated exposure to slipping conditions resulted in a reduction in step reaction time and an increase in step distance, and perturbationbased training that induces backward balance loss enhanced the capability to recover from posterior instability and subsequently reduced the likelihood of fall incidence in older adults [13]. The positive effects of training of the perturbation responses on adaptive control of postural balance were also observed in people with stoke and Parkinson's disease [14,15].
Although previous research has provided convincing evidence of the improved reactive responses upon backward postural disturbances, there is little research investigating such training effects in patients with cerebellar disease who suffer primarily from postural imbalance and coordination deficits. The reasons for the lack of study on the effectiveness of interventions for patients with cerebellar disease could be due to the facts that the number of cerebellar patient population is relatively small and the underlying causes of disease and symptoms are diverse as compared with other neurological diseases [16]. Although there is some debate about the effects of rehabilitation training for balance improvement in cerebellar dysfunction, recent studies showed that intensive balance training could enhance functional recovery of balance in cerebellar patients, and these changes were medicated by the neural plasticity in the remaining intact parts of the cerebellum and remote brain areas such as premotor cortex [17,18]. These promising results suggest that patients with

Participant
The patient was a 51-year-old, right-handed female

Experimental design and procedure
This case study used an A-B-A type design with a single subject of cerebellar patient. The outcome measures were conducted three times; pre-test (A) one week before the intervention, post-test (B) one week after the end of the intervention, and follow-up test (A) 4 weeks after the completion of the intervention. We assessed clinical and kinematic outcomes in each testing period. We measured the compensatory recovery responses with using a backwarddirected lean-and-release test. A horizontal cable was connected to the participant and she kept her body inclined in a backward direction. Then, the cable was released after a random time delay, and she was instructed to recover balance from a posterior fall in a natural way. The perturbation magnitude of backward lean was selected between 1 and 5% of her body weight. The magnitude was monitored using a load cell connected to the cable. She wore a suspended safety harness attached to the ceiling to protect from a fall to the floor. External assistance by a researcher was provided if she was unable to recover balance alone. No practice trials were allowed, and 4 trials for each magnitude were presented randomly to minimize anticipatory actions. In order to measure compensatory stepping responses and trunk motion, we analyzed the outcomes only from the two largest lean magnitudes (i.e., 4 and 5% BW), from which the participant took at least one step on average to recover balance from the perturbation.

Outcome measures
Balance recovery performance data were collected using an OPTITRACK 3D camera system (NaturalPoint Inc., Oregon, USA) at sampling frequency with 120 Hz. A 14-body segment

Results
The patient attended all 24 training sessions over an   Our results showed that the balance training employed in this study led to a substantial improvement in reducing the number of steps required to restore balance from perturbation.
It is known that rapid perception of the perturbation onset and execution of appropriate stepping actions are crucial to avoid falls when responding to the postural instability [14]. Although there were improvements in spatiotemporal characteristics of step execution following the balance intervention, we found less gains in stepping-related outcomes as compared to those of trunk-related movements. These small changes may result from the nature of movement task adopted and executed by the patient in the current study.
Previous studies reported that reactive stepping movement in response to a sudden external perturbation is mostly governed by lower lever of neural control (e.g., brainstem or spinal cord) [29]. Thus, upper neural centers including cerebellum are not significantly involved in producing reactive stepping movements. In support of this report, it has been shown that cerebellar patients virtually preserve the capability to execute rapid compensatory stepping reactions when responding to postural perturbations [30]. Therefore, the reason for the The observed finding could be explained by the fact that cerebellar diseases commonly affect coordination of multijoint movements such as limb and trunk movements [31], which may the cause for the poor control of torso motion and consequent failure of successful recovery of balance. However, the task-specific intervention targeting such coordination and balance impairments due to cerebellar disease could lead to promotion of the patient's capacity to control trunk motion and subsequently reduce the number of steps to recover balance. This description is consistent with previous studies reporting that therapeutic training strategies relevant to the specific functional goals or outcomes can have more beneficial effects on motor recovery than nonspecific rehabilitation training [32].
The potential mechanisms underlying functional improvement after the training have not been extensively documented in patients with cerebellar disease. Recent studies revealed that perturbation-based training induces an improved intersegmental coordination strategy that may promote dynamic stability and specifically the ability of controlling foot movement during balance recovery responses in order to compensate for the impaired cerebellar functions [33,34].
In addition, studies on neural rehabilitation have suggested that although cerebellar damages can induce poor recovery or low benefit of rehabilitation training, it has been shown that cerebellar patients still able to adapt or relearn motor coordination [17]. Burciu and colleagues [18] exhibited the neural changes associated with improvements of motor function after two weeks of sensorimotor balance training in patients with cerebellar disease. They found that the learning impairments because of cerebellar dysfunction are compensated by other part of the brain and also by remaining cerebellar areas less affected by the disease. Moreover, a recent study using fMRI demonstrated that not only motor and sensory brain areas, but prefrontal area was also greatly engaged in improved reactive balance control, which indicates that higher-level processing such as planning and modulating reactive responses is associated with adaptation to external perturbations [35]. Taken together, it can be speculated that these proposed compensatory neural mechanisms might be attributed to the observed gains in reactive balance functions after perturbation training in the cerebellar patient.
Our findings also demonstrated that the 8-week balance intervention also had a positive effect on the patients' depression and QOL level. In general, cerebellar patients are frequently accompanied by depressive symptoms. Nonetheless, the use of motor rehabilitation approaches such as the postural balance training in the current study diminished the symptoms of depression and perceived qualify of life. It is possible that these improvements may be due to increased confidence toward balance and mobility in everyday activities, and social and supportive relationships with experimenters during her visit for the training. The training effects on psychological well-being were even evident 1 month later at the follow-up test. However, it should be noted that the motor and functional improvements were not sustained over the follow-up period, which emphasizes the importance of continuous rehabilitative training for long-term maintenance of therapeutic benefits in patients with cerebellar disease.

Conclusions
The present study demonstrated that the perturbationbased balance training may be helpful for improving compensatory postural responses following backward loss of balance in patients with cerebellar disease. Although current research evidence of balance rehabilitation for cerebellar patients is lacking, this study offers the feasibility of adaptive training to improve postural stability through task-specific training intervention. The major limitation of the study is that general inferences cannot be drawn from a report of one patient's case. Thus, future research should attempt to investigate the effectiveness of this rehabilitation training with a larger sample of patients to provide further confirmation. In addition, future work also needs to examine neural substrates the for insight into pathophysiological mechanisms underlying the beneficial effects of perturbation-based balance training.