Maintaining balance during human movement typically involves sensorimotor integration of multiple sensory feedback modalities. Humans rely on visual, proprioceptive, vestibular, and cutaneous feedback to update their internal cognitive model about body dynamics (Peterka, 2018). These modalities help us balance when we stand, walk, and run. When stability of movement is challenged, the central nervous system uses all these sensory modalities to prevent a loss of balance and avoid a fall. When feedback from one of the modalities is inhibited or removed, the central nervous system relies more heavily on the other modalities.
Narrow beam walking is a good test of balance function. Performance while walking on a narrow beam can discriminate balance abilities between experts, novices, and transtibial amputees (Sawers & Ting, 2015). Many additional studies assessed the validity, reliability, and feasibility of using narrow beam walking as a clinical balance assessment (Sawers & Hafner, 2018a, 2018b, 2018c, 2020; da Silva Costa et al., 2020; Sawers et al., 2020). Sawers et al. (2015) examined whether long-term training altered muscle coordination patterns during beam walking by studying professional ballet dancers and novices. Muscle activity analysis revealed that experts had greater similarity between overground walking and beam walking than the novice participants. Experts also had less coactivity in muscle activity patterns during beam walking compared with the novices. The pool of motor modules shared between overground and beam walking was also greater in experts than novices which suggests motor module function is more generalized across different motor behaviors in trained individuals. Beam walking performance depends on many factors, such as the level of physical guidance (Domingo & Ferris, 2009), footwear (Huber et al., 2020), arm position (da Silva Costa et al., 2022), and beam width (Domingo & Ferris, 2009; da Silva Costa et al., 2022). Studies using high-density electroencephalography on individuals walking on a balance beam indicate that many brain areas are engaged during beam walking, including sensorimotor cortex, anterior cingulate, and posterior parietal cortex (Sipp et al., 2013; Symeonidou & Ferris, in press). This last area, the posterior parietal cortex, is critical for sensory integration of multiple sensory modalities (Drew & Marigold, 2015; Freedman & Ibos, 2018; Medendorp & Heed, 2019). The left sensorimotor cortex showed large changes in electrocortical power about a second before participants made contact with the ground after stepping off the beam.
In addition to being a good test of balance function, beam walking has also been used for balance training (Milani et al., 2022; Peterson, Rios, & Ferris, 2018; Symeonidou & Ferris, 2022). A 3-day training intervention was shown to improve dynamic balance control in older adults (Milani et al., 2022). Although it is unclear whether this type of task would transfer to overground walking, with its wider stance, it is important to find effective balance training methods for populations that suffer from stability decrements, such as older adults and individuals with Down syndrome, cerebral palsy, Parkinson’s disease, and other neurological disorders.
Brief, intermittent visual perturbations during beam walking practice increases beam walking performance in subsequent posttests without visual perturbations. Peterson, Rios, and Ferris (2018) found that 0.5-s visual field rotations introduced approximately every 10 s led to large gains in beam walking performance, characterized by fewer step-offs per minute, compared to a control group that practiced without intermittent visual rotations. In a subsequent study, Symeonidou and Ferris (2022) found that brief intermittent visual occlusions (duration of 1.5 s) while beam walking practice also led to large increases in subsequent beam walking performance in a posttest without visual perturbations compared with a control group without visual perturbations. Both studies had participants practice beam walking for 30 min at a constant speed on a treadmill-mounted balance beam prior to taking the posttest. The results indicated that the quality of the visual information during beam walking practice influenced the learning of dynamic balance, with intermittent visual disruptions increasing motor learning.
Interfering in visual feedback while participants learn a beam walking balance task likely prioritizes the weighting of proprioceptive, cutaneous, and vestibular information (Assländer & Peterka, 2014; Peterka, 2018). This might improve the learning of the task by making participants more attuned to proprioceptive, cutaneous, and vestibular information, making the task easier when they have reliable vision again. Balance training interventions with stroke patients similarly demonstrated that removing visual feedback during balance training led to greater balance improvements than training with full vision (Bonan et al., 2004; Paul, 2014). However, different effects of vision removal were found for a beam walking task (Robertson et al., 1994; Robertson & Elliott, 1996a, 1996b). Robertson and colleagues examined participants as they crossed an overground balance beam as fast as possible both with and without vision (Robertson et al., 1994; Robertson & Elliott, 1996a, 1996b). Novice participants walked more slowly, took more steps, and made more errors without vision compared to with vision, whereas experts showed similar time and steps between vision and no vision and only increased in form errors indicating a reliance on proprioceptive and/or vestibular inputs during no vision balance beam walking.
Due to the contradictory findings in the literature on the effect of complete visual occlusion on balance training, the goal of this study was to investigate the influence of full vision removal during practice walking on a treadmill-mounted balance beam. Distinctly from the Robertson experiments (Robertson et al., 1994; Robertson & Elliott, 1996a, 1996b), we kept walking speed constant across participants to control for walking speed. We studied healthy, neurologically intact participants walking on a treadmill-mounted balance beam at a constant speed (0.22 m/s) for 30 min. One group of participants practiced with normal vision and the second group practiced with eyes open but wearing a headset that blocked all light and vision. Both groups performed a 3-min pre- and posttraining evaluation with normal vision. Although intermittent visual disruptions have been found to improve beam walking performance (Peterson, Rios, & Ferris, 2018; Symeonidou & Ferris, 2022), we hypothesized that completely removing visual feedback would lead to less balance improvements than training with normal vision. Specifically, we hypothesized that training with vision would lead to a larger percentage decrease in step-offs per minute between pre- and posttraining than training without vision. Our secondary hypothesis was that training without vision would lead to a greater number of step-offs during training than training with vision. We anticipated these results based on the specificity of practice hypothesis which suggests that adding sensory information that was unavailable during practice leads to decrements in motor learning (Proteau et al., 1992).
Materials and Methods
Participants
Twenty healthy young adults participated in this experiment (10 males, 10 females; age 23 ± 5 years, mean ± SD; all right hand and foot dominant). They were free from orthopedic, cardiac, or neurological conditions, and injuries. The research was approved by the University of Michigan Health Sciences and Behavioral Sciences Institutional Review Board (HUM00100932), and all participants provided written informed consent before their participation in the study.
We performed a sample size calculation using prior results of beam walking with normal vision versus virtual reality vision (Peterson, Rios, & Ferris, 2018). Ten participants per group provided us with >0.9 power for detecting a difference with an alpha of .05, based on the means and standard deviations of those two groups from the prior study.
Experimental Setup
Participants walked on a 2.5 cm wide × 2.5 cm tall treadmill-mounted balance beam (Domingo & Ferris, 2009; Sipp et al., 2013; Peterson & Ferris, 2018; Peterson, Furuichi, & Ferris, 2018, Peterson, Rios, & Ferris, 2018; Symeonidou & Ferris, 2022) while equipped with a safety harness that did not impede mediolateral movements (Figure 1). All participants walked at the fixed speed of 0.22 m/s. As illustrated in Figure 1, they were instructed to cross their arms and walk heel-to-toe, with their feet along the direction of the beam, and to look straight ahead and avoid looking at their feet. This protocol is a replication of previous experiments (Domingo & Ferris, 2009; Sipp et al., 2013; Peterson & Ferris, 2018; Peterson, Furuichi, & Ferris, 2018, Peterson, Rios, & Ferris, 2018; Symeonidou & Ferris, 2022). Participants were asked to cross their arms because, in pilot testing, we found that participants using their arms to avoid a fall increased variability across participants. In addition, crossing their arms made the task more difficult. Participants would only release their arms when they made contact with the ground. If they stepped off the beam, they were told to step off with both feet and walk on the treadmill for about 5 s before returning to the balance beam. Participants who had no visual feedback felt the beam with their foot before returning to the beam. They were also instructed to move their hips side to side in case of a loss of balance, instead of turning sideways to change the direction they were facing.
—Experimental setup. Participant walking on a 2.5 cm wide × 2.5 cm tall treadmill-mounted balance beam while equipped with a safety harness. Participants were instructed to cross their arms, walk heel-to-toe with their feet along the direction of the beam, and look straight ahead.
Citation: Motor Control 28, 4; 10.1123/mc.2023-0145
Participants performed a 3-min pretraining walking interval, followed by 30 min of training separated into three 10-min trials, then took a 5-min break before completing a 3-min posttraining walking interval. All subjects took a break between each 10-min trial. The pre- and posttraining intervals consisted of beam walking with unaltered vision. We randomly assigned participants to two groups during training: (a) normal vision and (b) no vision. Each group had 10 participants and an equal number of males and females. Both groups performed the same physical beam walking task. Participants in the no vision group wore a headset that blocked all visual feedback. They were asked to keep their eyes open, even though they were blinded.
Data and Statistical Analyses
An experimenter manually recorded the number of times each participant stepped off the beam and cumulated the total time that each participant spent on the beam. We divided the number of step-offs by the total time (in minutes) spent on the beam to measure step-offs per minute (Domingo & Ferris, 2009, 2010; Peterson, Rios, & Ferris, 2018). We calculated this for pre- and posttraining as well as for the three 10-min training intervals. We calculated the percentage change in step-offs per minute by subtracting the step-offs per minute in posttraining from those in pretraining, divided by the pretraining value, and multiplied by 100. A negative value indicated an improvement in balance performance after training.
We performed a repeated measures analysis of variance on Group (vision vs. no vision) × Time (pretraining vs. posttraining) with repeated measures on Time for the number of step-offs per minute. We also performed a repeated measures analysis of variance on Group (vision vs. no vision) × Training interval (first, second, and third interval) with repeated measures on Training Interval for step-offs per minute. Finally, we performed an independent samples Student’s t test on the percentage change in step-offs per minute for the normal vision versus no vision groups. We used Jamovi software (www.jamovi.org) to conduct the analyses and set the level of significance to α = .05.
Results
The average time on the beam and number of step-offs for each training interval for the normal vision and no vision groups are presented in Table 1.
Average ± SD Time Spent on the Beam, in Minutes, and Number of Step-Offs for Each Training Interval for the Normal Vision and No Vision Groups
| Pretraining | Training interval 1 | Training interval 2 | Training interval 3 | Posttraining | ||||||
|---|---|---|---|---|---|---|---|---|---|---|
| Time on beam (min) | Step-offs | Time on beam (min) | Step-offs | Time on beam (min) | Step-offs | Time on beam (min) | Step-offs | Time on beam (min) | Step-offs | |
| Normal vision | 1.09 ± 0.20 | 22.00 ± 3.30 | 4.30 ± 1.10 | 63.80 ± 13.24 | 4.47 ± 0.99 | 61.30 ± 13.13 | 4.58 ± 1.20 | 59.10 ± 15.01 | 1.66 ± 0.35 | 18.80 ± 5.51 |
| No vision | 1.17 ± 0.23 | 22.70 ± 4.42 | 2.41 ± 0.60 | 78.80 ± 15.45 | 2.56 ± 0.68 | 72.40 ± 17.63 | 2.81 ± 0.93 | 71.20 ± 17.09 | 1.69 ± 0.60 | 19.00 ± 5.68 |
Both groups showed improvements throughout the session. During the 30-min training, there was a significant effect of training interval, F(2, 18) = 14.25, p < .001,
—Number of step-offs per minute in pretraining, three 10-min training intervals, and posttraining for the normal vision and no vision groups. The first interval of training had significantly more step-offs, for both groups, than the second and third intervals (*p = .005). On average, the no vision group had twice as many step-offs per minute during training (30 step-offs per minute) as the normal vision group (15 step-offs per minute; **p = .002). The groups had similar number of step-offs per minute in the pre- and posttest (p = .67), and both showed improvements in the posttest compared to the pretest (***p < .001).
Citation: Motor Control 28, 4; 10.1123/mc.2023-0145
Both groups improved in beam walking performance from pre- to posttraining. The groups had similar number of step-offs per minute in pre- and posttraining, F(1, 9) = 0.19, p = .67,
—Percentage change in step-offs per minute (%) from pre- to posttraining in the normal vision and no vision groups. Both groups performed the pre- and posttraining with normal vision. Negative values represent an improvement in balance performance after training. While both groups reduced their step-offs per minute by ∼40%, there was no significant difference in improvement between the two groups (p = .41).
Citation: Motor Control 28, 4; 10.1123/mc.2023-0145
Discussion
It has been shown that interfering with visual feedback during balance training can improve the effectiveness of balance training; however, certain experiments using complete visual occlusion have shown opposite effects. To better understand the effect of vision on balance training, our objective was to investigate the influence of full vision removal during practice walking on a treadmill-mounted balance beam. Contrary to our hypothesis, we found that both training groups improved beam walking ability, as seen with a similar percentage change in step-offs per minute between pre- and posttraining, and there was no statistically significant difference between groups (Figures 2 and 3).
Our findings may be considered surprising as the specificity of practice hypothesis suggests that adding sensory information that was unavailable during training led to decrements in performance (Proteau et al., 1992). Our results are in line with previous experiments that found that removing vision during balance training improved the effectiveness of training (Bonan et al., 2004; Paul, 2014). They are also somewhat in line with the findings from Robertson et al., who found that beam walking without vision led to slower walking, more steps, and more errors compared with full vision in novice balance beam walkers (Robertson et al., 1994; Robertson & Elliott, 1996a, 1996b). The Robertson group without vision likely reduced speed to offset accuracy given the trade-off between speed and accuracy (Fitts, 1954). Our findings are similar because our no vision group also experienced more errors during training compared with the normal vision group. However, in the Robertson experiments, participants were asked to cross the beam as fast as possible, and they adapted to the lack of vision by walking more slowly and taking more steps. A slowing of walking speed has been shown to result in greater lateral instability (Bauby & Kuo, 2000; Den Otter et al., 2004), which is an important factor in balance beam walking. Therefore, the slower speed in the participants without visual feedback could explain the detrimental effect of vision removal observed in these experiments. By keeping the walking speed constant, we isolated balance errors (i.e., step-offs) from changes in walking speed.
A possible explanation for the lack of difference between our groups could be the sensory reweighting that occurred in our no vision group. Humans use a combination of visual, proprioceptive, cutaneous, and vestibular feedback to sense their current body state and make corrective muscle actions to prevent loss of balance. Without vision, participants had to rely completely on proprioceptive, cutaneous, and vestibular feedback to sense their current body state. This might facilitate later performance of the task by making participants more attuned to proprioceptive, cutaneous, and vestibular information.
Experiments investigating the electrocortical activity in a beam walking task demonstrated evidence of sensory reweighting during sensorimotor perturbations. They showed changes in spectral power in occipitoparietal areas (Peterson & Ferris, 2018) and decreased connectivity between the occipital and parietal areas during visual perturbations (Peterson & Ferris, 2019), which differed from physical perturbations to balance (Peterson & Ferris, 2018, 2019). Similar electrocortical changes were observed in gait adaptation studies to changing sensory stimuli (Wagner et al., 2016; Malcolm et al., 2018). Previous work studying electrocortical activity in healthy young adults walking on a treadmill without vision increased electrocortical power fluctuations in their somatosensory cortex (Oliveira et al., 2017). The increased somatosensory cortex fluctuations could have indicated increased reliance on somatosensory feedback when denied visual feedback. Beam walking is not the same as normal treadmill walking. The reduced width of the surface for foot–ground contact means that the no vision participants in our study had to rely on estimates of foot position from proprioceptive feedback during swing and cutaneous feedback when the foot made contact with the beam surface. Although the number of errors during training increased by twofold (Figure 2), there were still considerable balance improvements with practice without visual feedback.
The effects from removal of all vision were very different than previous results involving brief, intermittent visual perturbations. Experiments with 1.5-s intermittent visual occlusions (Symeonidou & Ferris, 2022) and 0.5-s intermittent visual rotations (Peterson, Rios, & Ferris, 2018) during beam walking practice both led to large enhancements of training effectiveness. Completely removing vision did not improve balance training effectiveness relative to normal vision in our participants. The difference provides insight into the neural mechanism likely responsible for the improved effectiveness in the first two studies. It seems plausible that intermittently perturbing vision leads to intermittent increased focus on proprioceptive, cutaneous, and vestibular feedback. If vision is deemed to be not trustworthy when it is intermittently perturbed, then the nervous system may cyclically alter the sensory gains in sensorimotor integration (Peterka, 2018). The consistent ebb and wane of sensory weighting may have a greater effect on the cortical processes involved in balance performance. The results from the current study also suggest that visual perturbation by itself may not be the main reason that brief, intermittent visual perturbations enhance balance training effectiveness with practice beam walking. Future experiments with high-density electroencephalography might provide more insight into the neural changes that occur with different types of visual perturbations during balance training.
Limitations
There were some inherent limitations to our study. We did not test individuals with inherent balance problems, such as those with neurological or physical disabilities. We should not extrapolate the results from the healthy, young, neurologically intact participants we tested to individuals with spinal cord injury, poststroke hemiparesis, multiple sclerosis, vestibular problems, or aging-induced balance deficits. Future studies should confirm the results from this and the other visual perturbation studies (Peterson, Rios, & Ferris, 2018; Symeonidou & Ferris, 2022) on a wider selection of participants. We only studied participants completing a single 30-min training session to examine balance training efficacy, without examining long-term training effects or retention of improvements. It may be that completing multiple sessions over many weeks leads to a clear differentiation between motor learning in individuals using normal vision during beam walking practice compared to no vision. It is also possible that the pretraining interval generated a learning effect, although both groups underwent the same pretraining therefore would have experienced the same effect. Future studies could include a control group who does not receive the 30-min intervention. We did not measure any changes in kinematics, kinetics, electromyography, or electroencephalography of the participants. This was an initial behavioral study to determine if there were clear differences in balance training efficacy from beam training with and without vision. A recent comparison of kinematic measures on healthy young participants practicing beam walking found that kinematic parameters are not very sensitive to improvements in dynamic balance with beam walking practice (Symeonidou et al., 2023). Electromyography and electroencephalography would both likely increase understanding of the neuromuscular mechanisms involved in improved dynamic balance related to practicing beam walking with visual perturbations (Peterson & Ferris, 2018, 2019; Symeonidou & Ferris, in press). In addition, the headset was only worn by the no vision group, which could have affected posture or created a difference between groups that may have influenced the results.
Conclusions
This work investigated the influence of full vision removal during practice walking on a treadmill-mounted balance beam. Although previous experiments show that intermittent visual perturbations increased training effectiveness of beam walking, we hypothesized that completely removing visual feedback would lead to less balance improvements than training with normal vision due to the specificity of practice. Our results show, instead, that both groups improved to a similar extent, although the no vision group did make more errors during training. These results suggest that the enhanced balance training that accompanies visual perturbations during beam walking practice is not simply a result of less visual feedback. Complete removal of visual feedback during beam walking practice led to no improvement in balance training effectiveness compared to the normal vision group. Further investigations of the neural mechanisms involved in beam walking with visual perturbations are warranted.
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