The motor repertoire of older adult fallers may constrain their response to balance perturbations

Abstract

Older adults are at a high risk of falls, and most falls occur during locomotor activities like walking. This study aimed to improve our understanding of changes in neuromuscular control associated with increased risk of falls in older adults in the presence of dynamic balance challenges during walking. Motor module (also known as muscle synergy) analyses identified changes in the neuromuscular recruitment of leg muscles during walking with and without perturbations designed to elicit the visual perception of lateral instability. During normal walking we found that a history of falls (but not age) was associated with reduced motor module complexity and that age (but not a history of falls) was associated with increased step-to-step variability of module recruitment timing. Furthermore, motor module complexity was unaltered in the presence of optical flow perturbations. The specific effects of a history of falls on leg muscle recruitment included an absence and/or inability to independently recruit motor modules normally recruited to perform biomechanical functions important for walking balance control. These results suggest that fallers do not recruit the appropriate motor modules necessary for well-coordinated walking balance control even in the presence of perturbations. The identified changes in the modular control of walking balance in older fallers may either represent a neural deficit that leads to poor balance control or a prior history of falls that results in a compensatory motor adaptation. In either case, our study provides initial evidence that a reduced motor repertoire in older adult fallers may be a constraint on their ability to appropriately respond to balance challenges during walking. NEW & NOTEWORTHY This is the first study to demonstrate a reduced motor repertoire during walking in older adults with a history of falls but without any overt neurological deficits. Furthermore, using virtual reality during walking to elicit the visual perception of lateral instability, we provide initial evidence that a reduced motor repertoire in older adult fallers may be a constraint on their ability to appropriately respond to balance challenges during walking.

Keywords: gait; muscle synergy; stability; virtual reality; vision.

Fig. 1.

Subjects walked on a treadmill in an immersive virtual environment while watching a hallway with and without continuous mediolateral (ML) optical flow perturbations of 3 amplitudes. We recorded electromyographic activity from the following 7 leg muscles: tibialis anterior (TA), medial gastrocnemius (MG), soleus (SOL), peroneus longus (PL), vastus lateralis (VL), medial hamstrings (MH), and gluteus medius (GM). hs, Heel-strike.

Fig. 2.

Motor modules identified from a representative young adult subject (n = 1). A: variability accounted for (VAF) plot from a representative subject illustrating the 2 measures of motor module complexity: number of motor modules and VAF by 1 motor module. B: the 4 motor modules identified in the representative subject (left) and their recruitment timing (right). Step-by-step variability was quantified by averaging the root mean square error (RMSE) in the timing curves across motor modules. C: the extracted motor modules well-reconstructed the original EMG (dashed line: original EMG, solid line: reconstructed EMG). TA, tibialis anterior; MG, medial gastrocnemius; SOL, soleus; PL, peroneus longus; VL, vastus lateralis; MG, medial hamstrings; GM, gluteus medius.

Fig. 3.

Group mean hip, knee, and ankle joint angles in young (n = 12), older nonfallers (n = 11), and older fallers (n = 10) walking with and without optical flow perturbations plotted against an averaged gait cycle, from heel-strike to heel-strike. *Significant ANOVA main effect of perturbations. ¹Significant difference compared with young adults via pairwise comparisons.

Fig. 4.

Motor module outcomes for each group across perturbation conditions. A: the number of motor modules were reduced in older fallers (n = 10) compared with young adults (n = 12) and older nonfallers (n = 11). There were no ANOVA main effects of perturbation magnitude in any group. B: the variability accounted for (VAF) explained by one motor module was increased in older fallers compared with both young adults and older nonfallers. There were no ANOVA main effects of perturbation magnitude in any group. C: older adults, regardless of a history of falls, exhibited larger step-by-step variability in motor module timing. All groups increased variability as perturbation amplitude was increased. RMSE, root mean square error. **Significant ANOVA main effect of perturbations. ^1,2Significant difference from young adults and older nonfallers, respectively, via pairwise comparisons.

Fig. 5.

Motor modules recruited in each group during normal walking. In young adults (n = 12), a total of 5 motor modules were identified, with one module (module 5) only recruited in a single subject. The remaining 4 motor modules (modules 1–4) were recruited in at least 75% of young adult subjects, with qualitatively similar recruitment timing. These same four motor modules were also recruited in most of the older nonfallers (n = 11). In contrast, older fallers (n = 10) exhibited differences in motor module recruitment. Most older faller subjects recruited module 1 (plantarflexors during late stance). However, modules 2–4 were recruited in only half or fewer of older faller subjects, with module 3 [tibialis anterior (TA) during swing] recruited in only a single subject. Instead, many older faller subjects had a module with coactivation from all nonplantarflexor modules (module 6) that was active throughout much of stance. Text to the right of each module indicates the number of subjects within each group that recruited that motor module and its contribution to the overall variability accounted for (VAF) (means ± SD). MGAS, medial gastrocnemius; SOL, soleus; PERO, peroneus longus; VLAT, vastus lateralis; MH, medial hamstrings; GMED, gluteus medius.

Fig. 6.

Motor module recruitment timing across perturbation conditions. Recruitment timing was qualitatively similar across all perturbation magnitudes in each group (young: n = 12; older nonfallers: n = 11; and older fallers: n = 10).

Fig. 7.

Results of an exploratory post hoc analysis of the association between motor module complexity (i.e., # of modules) and previously published values of local dynamic instability, quantified using short-term maximum divergence exponents (λ_s, 0–1 stride) (Qiao et al. 2018b). We refer the reader to the original manuscript for a detailed description of our data reduction and analysis procedures. Briefly, in that paper, we used a state space constructed from the 3-dimensional velocity of subject’s 7th cervical vertebrae and their time-delayed copies to compute maximum rates of divergence of initially neighboring trajectories. There, larger values of λ_s signify larger local dynamic instability. We concluded there that, compared with their effects in young adults, optical flow perturbations were capable of revealing independent effects of aging and a history of falls on gait instability that are not otherwise apparent during normal, unperturbed walking. Here, we performed 2 linear regressions across our study cohort: 1 during normal, unperturbed walking (A) and 1 in the presence of the largest amplitude optical flow perturbations used in this study (B; i.e., 50 cm). Our findings reveal that individuals with less motor module complexity in this study (namely, older adults with a history of falls) had larger local dynamic instability in the presence of optical flow perturbations (r² = 0.22, P = 0.007) but not during normal, unperturbed walking (r² = 0.06, P = 0.163). This outcome provides additional evidence that a reduced motor repertoire in older adult fallers may be a constraint on their ability to appropriately respond to balance challenges during walking: the major finding of our present study.