Older adults exhibit variable responses in stepping behaviour following unexpected forward perturbations during gait initiation

With the socioeconomic burden associated with falls expected to rise as the average age of the Canadian population increases, research is needed to elucidate the nature of postural responses generated by older adults (OA) following a posture-destabilizing event. This knowledge is even more imperative for novel and difficult tasks, such as gait initiation (GI), a task known to pose a postural threat to stability for OA. A common technique to regain stability following an unexpected perturbation is reactive stepping. A deficiency in the execution of a reactive control strategy following a destabilizing event may be the cause of many unexpected falls in OA. The purpose of this study is to explore age related changes in the nature of these responses during a challenging GI task combined with an unexpected forward perturbation of the support surface. A total of 18 young adults (YA) and 16 OA performed 36 trials containing 20 unexpected perturbations. We calculated step width, length, time and COM velocity in the first unperturbed step and the second perturbed step. Results revealed that, during unperturbed GI, OA had a reduced forward velocity and took shorter, faster steps. Following forward perturbations, OA altered stepping patterns, perhaps to reduce single support duration, via reduced base of support and shorter step length compared to YA. Additionally, OA executed both forward and backwards directed steps however YA only generated forward steps. Regression analyses revealed that reduced forward velocity was predictive of step direction; which is possibly an unfavorable motor control strategy as OA who walk slower generated a posterior directed step immediately following the perturbation. This strategy is of concern as rapid responses by the trail limb are required to recover successfully, and these alterations may be associated with an elevated risk of falls.     

Specificity and variability of trunk kinematics on a mechanical horse

As perturbation training is gaining popularity, it is important to better understand postural control during complex three-dimensional stimuli. One clinically relevant and commonly used three-dimensional stimulus is found in hippotherapy and simulated hippotherapy on a mechanical horse. We tested nine healthy participants on a horse simulator, measured head and trunk kinematics, and characterized data in time (root-mean-square and variability) and frequency (amplitude spectra, gains, and phases) domains. We addressed three fundamental questions: 1) What is the specificity of postural responses to the simulator? 2) Which plane of motion is associated with the most and least variability (repeatable movements across repeated stimuli and across participants)? 3) To what extent are postural responses influenced by different degrees of stability (addition of pelvis straps and trunk support)? We found head and trunk responses were highly specific to the three-dimensional simulator perturbation direction and frequency. Frontal plane responses had the least variability across repetitions and participants whereas transverse motion was most variable. Head motion was more variable than the trunk at low frequencies and exhibited a marked decrease in tilt in the sagittal plane. Finally, the inclusion of pelvis straps had minimal effect on kinematics at low frequencies but altered higher frequencies; whereas added trunk support reduced head and trunk responses to perturbations and altered timing characteristics in all three planes. In conclusion, the present study suggests that frontal plane motion was under a high level of control, and results support the idea that specific head and trunk postural responses can be elicited from a complex three-dimensional stimuli, such as those found in hippotherapy. Researchers and clinicians can use results from this study to help interpret variability, implement mechanical adjustments to stability, and assess responses in pathological populations.     

Repeated Exposure to Forward Support-Surface Perturbation During Overground Walking Alters Upper-Body Kinematics and Step Parameters

Locomotion requires both proactive and reactive control strategies to maintain balance. The current study aimed to: (i) ascertain upper body postural responses following first exposure to a forward (slip) support-surface perturbation; (ii) investigate effects of repeated perturbation exposure; (iii) establish relationships between arms and other response components (trunk; center of mass control). Young adults (N = 11) completed 14 walking trials on a robotic platform; six elicited a slip response. Kinematic analyses were focused on extrapolated center of mass position (xCoM), bilateral upper- and forearm elevation velocity, trunk angular velocity, and step parameters. Results demonstrated that postural responses evoked in the first slip exposure were the largest in magnitude (e.g., reduced backward stability, altered reactive stepping, etc.) and preceded by anticipatory anterior adjustments of xCoM. In relation to the perturbed leg, the large contra- and ipsilateral arm responses observed (in first exposure) were characteristically asymmetric and scaled to the degree of peak trunk extension. With repeated exposure, xCoM anticipatory adjustments were altered and in turn, reduced posterior xCoM motion occurred following a slip (changes plateaued at second exposure). The few components of the slip response that persisted across multiple exposures did so at a lesser magnitude (e.g., step length and arms).     

Stepping Responses in Young and Older Adults Following a Perturbation to the Support Surface During Gait

The objective of this work was to investigate the influence perturbation direction has on postural responses during overground gait, and whether these responses are age related. Differences in stepping patterns following perturbations of the support surface were examined in the frontal and sagittal planes during forward walking. Eleven young and 10 older adults completed Mini BESTest, hip strength tests, and 45 perturbed walking trials, triggered on heel contact. Lateral perturbations were more challenging to postural stability for both groups. Step length measures showed young adults recovered in the step proceeding the perturbation, while older adults needed additional steps to regain balance. Young adults arrested center of mass movement by producing larger step widths than older adults following the support surface perturbation.     

Examination of reactive motor responses to Achilles tendon vibrations during an inhibitory stepping reaction time task

Inhibition is known to influence balance, step initiation and gait control. A specific subcomponent of inhibition, the perceptual inhibition process, has been suggested to be specifically involved in the integration of proprioceptive information that is necessary for efficient postural responses. This study aimed to investigate the inhibition requirements of planning and executing a choice step initiation task in young adults following experimental perturbation of proprioceptive information using Achilles tendon vibrations. We developed an inhibitory stepping reaction time task in which participants had to step in response to visual arrows that manipulated specific perceptual or motor inhibition according to two proprioceptive configurations: without or with application of vibrations. Performance of twenty-eight participants (mean age 21 years) showed that Achilles tendon vibrations induced an increase in attentional demands (higher reaction time and longer motor responses). Further, this increase in attentional demands did not affect specifically the different inhibitory processes tested in this reactive stepping task. It suggests that attentional demands associated with the vibratory perturbation to postural control do not lead to a shift from automatic to more attentional inhibition processes, at least in young adults.     

Posture-movement responses to stance perturbations and upper limb fatigue during a repetitive pointing task

Localized muscle fatigue and postural perturbation have separately been shown to alter whole-body movement but little is known about how humans respond when subjected to both factors combined. Here we sought to quantify the kinematics of postural control and repetitive upper limb movement during standing surface perturbations and in the presence of fatigue. Subjects stood on a motion-based platform and repetitively reached between two shoulder-height targets until noticeably fatigued (rating of perceived exertion = 8/10). Every minute, subjects experienced a posterior and an anterior platform translation while reaching to the distal target. Outcomes were compared prior to and with fatigue (first vs. final minute data). When fatigued, regardless of the perturbation condition, subjects decreased their shoulder abduction and increased contralateral trunk flexion, a strategy that may relieve the load on the fatiguing upper limb musculature. During perturbations, kinematic adaptations emerged across the trunk and arm to preserve task performance. In contrast to our expectation, the kinematic response to the perturbations did not alter in the presence of fatigue. Kinematic adaptations in response to the perturbation predominantly occurred in the direction of the reach whereas fatigue adaptations occurred orthogonal to the reach. These findings suggest that during repetitive reaching, fatigue and postural perturbation compensations organize so as to minimize interaction with each other and preserve the global task characteristics of endpoint motion.     

Postural muscle responses following changing balance threats in young, stable older, and unstable older adults

The authors determined the postural muscle response to support surface perturbations, in relation to aging and level of stability of 16 young adults and 32 older adults who were classified into stable (SOA) and unstable (UOA) groups on the basis of their functional balance abilities. Forward and backward support surface translations of various amplitudes and velocities were used so that postural responses of the standing adults could be elicited. The thigh and leg postural muscle responses were recorded with surface electromyography (EMG). The older groups had significantly longer onset latency in the anterior postural muscles, smaller integrated EMG in the posterior muscles, and greater extent of integrated EMG attenuation over time. The UOA showed longer onset latency in the gastrocnemius following slow backward perturbation and used a greater percentage of the functional capacity of the gastrocnemius muscle than the SOA did. Those findings indicate that the SOA and UOA had limited ability to adapt to changing balance threats; the UOA were more limited than the SOA. When designing balance training programs, therefore, therapists should consider the adult's level of functional stability.     

Phase-dependent compensatory responses to perturbation applied during walking in humans

The interaction between the peripheral and the central regulation of locomotion was studied by examining the dependency of the response to unexpected perturbation on the phase of the step cycle. The changes in the latency and magnitude of various muscle responses to electrical stimulation of the toe and applied unexpectedly at different phases of the locomotor cycle in humans are described. The results show that response to perturbation is gated and modulated in both ipsi- and contralateral limb muscles. These muscle responses, when present, were always excitatory in nature. They were not correlated with the normal locomotor activity, thus suggesting a more complex organization of the response. Except for one muscle in the contralateral limb, the latency of the other muscle responses did not vary across the step cycle. in response to the perturbation, the appropriate phase of the step cycle was shortened. The results from this study suggest that the perturbation applied elicits a phase-independent, normal ipsilateral flexor response in the tibialis anterior muscle, while the gating and modulation of other ipsi- and contralateral muscles provide appropriate phase-dependent adaptive response to maintain postural stability and continue with the ongoing task of locomotion.     

Phase-Dependent Compensatory Responses to Perturbation Applied During Walking in Humans

The interaction between the peripheral and the central regulation of locomotion was studied by examining the dependency of the response to unexpected perturbation on the phase of the step cycle. The changes in the latency and magnitude of various muscle responses to electrical stimulation of the toe applied unexpectedly at different phases of the locomotor cycle in humans are described. The results show that response to perturbation is gated and modulated in both ipsi-and contralateral limb muscles. These muscle responses, when present, were always excitatory in nature. They were not correlated with the normal locomotor activity, thus suggesting a more complex organization of the response. Except for one muscle in the contralateral limb, the latency of the other muscle responses did not vary across the step cycle. In response to the perturbation, the appropriate phase of the step cycle was shortened. The results from this study suggest that the perturbation applied elicits a phase-independent, normal ipsilateral flexor response in the tibialis anterior muscle, while the gating and modulation of other ipsi-and contralateral muscles provide appropriate phase-dependent adaptive response to maintain postural stability and continue with the ongoing task of locomotion.     

Oscillations in Motor Priming: Positive Rebound Follows the Inhibitory Phase in the Masked Prime Paradigm

From among the diverse meanings of stability, the one the author adopts here is that the effects of a perturbation are opposed, and therefore small effects remain small. Except in linear systems, however, instability need not lead to unbounded motion and may actually be desirable when maneuverability is important. Moreover, properties of nerves, muscles, and tendons present serious challenges to stabilization. A review of observations from the motor control literature reveals that responses to perturbations in many common situations assist rather than resist the perturbation and are therefore presumably destabilizing. The observations encompass situations of position maintenance as well as impending or ongoing movement. The author proposes that the motor control system responds to a sudden perturbation by a pattern of muscle activity that mimics an accustomed voluntary movement, oblivious of stability considerations. What prevents runaway motion in the face of short-term instability appears to be voluntary intervention.     

The human motor control system's response to mechanical perturbation: should it, can it, and does it ensure stability?

From among the diverse meanings of stability, the one the author adopts here is that the effects of a perturbation are opposed, and therefore small effects remain small. Except in linear systems, however, instability need not lead to unbounded motion and may actually be desirable when maneuverability is important. Moreover, properties of nerves, muscles, and tendons present serious challenges to stabilization. A review of observations from the motor control literature reveals that responses to perturbations in many common situations assist rather than resist the perturbation and are therefore presumably destabilizing. The observations encompass situations of position maintenance as well as impending or ongoing movement. The author proposes that the motor control system responds to a sudden perturbation by a pattern of muscle activity that mimics an accustomed voluntary movement, oblivious of stability considerations. What prevents runaway motion in the face of short-term instability appears to be voluntary intervention.     

The effects of sub-threshold vibratory noise on visuomotor entrainment during human walking and standing in a virtual reality environment

Humans will naturally synchronize their posture to the motion of a visual surround, but it is unclear if this visuomotor entrainment can be attenuated with an increased sensitivity to somatosensory information. Sub-threshold vibratory noise applied to the Achilles tendons has proven to enhance ankle proprioception through the phenomenon of stochastic resonance. Our purpose was to compare visuomotor entrainment during walking and standing, and to understand how this entrainment might be attenuated by applying sub-threshold vibratory noise over the Achilles tendons. We induced visuomotor entrainment during standing and treadmill walking for ten subjects (24.5 ± 2.9 years) using a speed-matched virtual hallway with continuous mediolateral perturbations at three different frequencies. Vibrotactile motors over the Achilles tendons provided noise (0–400 Hz) with an amplitude set to 90% of each participant’s sensory threshold. Mediolateral sacrum, C7, and head motion was greatly amplified (4–8× on average) at the perturbation frequencies during walking, but was much less pronounced during standing. During walking, individuals with greater mediolateral head motion at the fastest perturbation frequency saw the greatest attenuation of that motion with applied noise. Similarly, during standing, individuals who exhibited greater postural sway (as measured by the center of pressure) also saw the greatest reductions in sway with sub-threshold noise applied in three of our summary metrics. Our results suggest that, at least for healthy young adults, sub-threshold vibratory noise over the Achilles tendons can slightly improve postural control during disruptive mediolateral visual perturbations, but the applied noise does not substantially attenuate visuomotor entrainment during walking or standing.     

Task-dependent compensatory responses to perturbations applied during rhythmic movements in humans

Modulation of the responses to perturbation applied during different phases of three rhythmic movements in humans-running, cycling, and hopping-was studied. The perturbation was an electrical stimulus. The results showed gating and modulation of the responses in both ipsi- and contralateral limb muscles. The responses during running and cycling were only excitatory in nature, while during hopping an inhibitory response was observed. These responses were not correlated with the normal activity during the movement. The latency of the response in general was not altered for different stimulation phases. The alterations in the step cycle demonstrated overt behavioral changes due to the responses. There were differences between the responses observed during these movements and walking. In running, the major adaptation to perturbations appears to be in the contralateral side as seen in the changes in the step cycle. During cycling (except for one phase) and hopping, the same set of muscles was activated in response to perturbation. This represents a simplifying strategy in response organization. The dependency of the response on the task characteristics, postural stability requirement, and external constraints imposed on the subject is discussed. These studies provide insights into task-dependent strategies adopted by the nervous system to meet unexpected perturbation during rhythmic movements in humans.     

Task-Dependent Compensatory Responses to Perturbations Applied During Rhythmic Movements in Humans

Modulation of the responses to perturbation applied during different phases of three rhythmic movements in humans—running, cycling, and hopping—was studied. The perturbation was an electrical stimulus. The results showed gating and modulation of the responses in both ipsi-and contralateral limb muscles. The responses during running and cycling were only excitatory in nature, while during hopping an inhibitory response was observed. These responses were not correlated with the normal activity during the movement. The latency of the response in general was not altered for different stimulation phases. The alterations in the step cycle demonstrated overt behavioral changes due to the responses. There were differences between the responses observed during these movements and walking. In running, the major adaptation to perturbations appears to be in the contralateral side as seen in the changes in the step cycle. During cycling (except for one phase) and hopping, the same set of muscles was activated in response to perturbation. This represents a simplifying strategy in response organization. The dependency of the response on the task characteristics, postural stability requirement, and external constraints imposed on the subject is discussed. These studies provide insights into task-dependent strategies adopted by the nervous system to meet unexpected perturbation during rhythmic movement in humans.     

Higher order balance control: Distinct effects between cognitive task and manual steadiness constraint on automatic postural responses

In the present experiment, we aimed to evaluate the interactive effect of performing a cognitive task simultaneously with a manual task requiring either high or low steadiness on APRs. Young volunteers performed the task of recovering upright balance following a mechanical perturbation provoked by unanticipatedly releasing a load pulling the participant’s body backwards. The postural task was performed while holding a cylinder steadily on a tray. One group performed that task under high (cylinder’ round side down) and another one under low (cylinder’ flat side down) manual steadiness constraint. Those tasks were evaluated in the conditions of performing concurrently a cognitive numeric subtraction task and under no cognitive task. Analysis showed that performance of the cognitive task led to increased body and tray displacement, associated with higher displacement at the hip and upper trunk, and lower magnitude of activation of the GM muscle in response to the perturbation. Conversely, high manual steadiness constraint led to reduced tray velocity in association with lower values of trunk displacement, and decreased rotation amplitude at the ankle and hip joints. We found no interactions between the effects of the cognitive and manual tasks on APRs, suggesting that they were processed in parallel in the generation of responses for balance recovery. Modulation of postural responses from the manual and cognitive tasks indicates participation of higher order neural structures in the generation of APRs, with postural responses being affected by multiple mental processes occurring in parallel.     

A concurrent attention-demanding task did not interfere with balance recovery function in standing and walking among young adults – An explorative laboratory study

This study aimed to explore the ability to overcome unannounced surface perturbations of different magnitudes during standing and walking under single-task and dual-task conditions. Balance recovery abilities during perturbed walking and concurrently performing cognitive tasks has rarely been investigated although it provides more ecological information in regard to real-life situations than perturbations during single-task conditions (i.e., just walking). Thirteen young adults were asked to perform: 1) a cognitive task while sitting; 2) perturbed standing; 3) a concurrent cognitive task during perturbed standing; 4) perturbed walking; and 5) a concurrent cognitive task during perturbed walking. The cognitive task was to perform number subtractions by seven. The participants were instructed to “try to avoid a fall” during the perturbation trials. Step threshold, cognitive task performance, and 3D kinematic analysis of the first recovery step, i.e., the spatiotemporal characteristics, were compared between all conditions. Step threshold and the spatiotemporal parameters of the first recovery stepping responses were similar between all task conditions. Cognitive performance was also unaffected by the postural challenges in all task conditions. These results suggest that the first balance recovery stepping response among young adults is automatic. Furthermore, young adults seem to have sufficient motor-cognitive resources to perform concurrently both balance recovery and cognitive tasks with no interference effects.     

Harnessing the Power of a Novel Program for Dynamic Balance Perturbation with Supported Body Weight

Abstract

Self-initiated postural adjustments commonly occur in daily life. To accessibly measure this type of dynamic balance, we developed a simple computer program to induce virtual perturbations and combined it with a commercially available balance board and portable EMG system to measure resulting self-initiated postural adjustments. When performing perturbed balance tests, safety harness with body weight support (BWS) is often used. However, influences of these harnesses on postural reactions are not well known. This study investigated the sensitivity of our assessment tool under different BWS conditions and muscle responses during postural adjustments following perturbation at different directions. Fifteen neurologically intact participants performed self-initiated postural adjustments under conditions with: (1) no harness; (2) harness with no BWS; and (3) harness with 10% BWS. Postural adjustment time and muscle activities of the lower leg were measured. We observed significant increases in postural adjustment time in the harness with no BWS condition and differneces in lower leg muscles response to virtual perturbation. Our findings suggest that the combination of our customized program with EMG is a sensitive and convenient tool to measure postural adjustments that approximate real-world scenarios. This method can be used with light body weight support to ensure safety without influencing muscle synergies.     

Older adults exhibit altered motor coordination during an upper limb object transport task requiring a lateral change in support

Investigating an ecologically relevant upper limb task, such as manually transporting an object with a concurrent lateral change in support (sidestepping alongside a kitchen counter), may provide greater insight into potential deficits in postural stability, variability and motor coordination in older adults. Nine healthy young and eleven older, community dwelling adults executed an upper limb object transport task requiring a lateral change in support in two directions at two self-selected speeds, self-paced and fast-paced. Dynamic postural stability and movement variability was quantified via whole-body center of mass motion. The onset of lead lower limb movement in relation to object movement onset was quantified as a measure of motor coordination. Older adults demonstrated similar levels of stability and variability as their younger counterparts, but at slower peak movement velocity and increased task duration. Furthermore, older adults demonstrated asymmetrical motor coordination between left and right task directions, while younger adults remained consistent regardless of task direction. Thus, older adults significantly modulated movement speed and motor coordination to maintain similar levels of stability and variability compared to their younger counterparts.     

The effects of initial movement dynamics on human responses to postural perturbations

Falls are a major cause of injury, and often occur while turning, reaching, or bending. Yet, we have little understanding of how an ongoing feet-in place activity at the onset of imbalance, and its associated cognitive and biomechanical demands, influence our ability to recover balance. In the current study, we used an ankle-rocking paradigm to determine how the nature of the baseline task influences the balance recovery response to a backward support surface translation. Fourteen participants were instructed to “recover balance without stepping” and were perturbed at vertical while standing quietly (“S”), while ankle rocking and moving forward (“A_f”), or while ankle rocking and moving backward (“A_b”). The results showed that changes in rocking velocity at the time of the perturbation elicited changes in the incidence of stepping, magnitude of trunk angular displacements (p < .01), and the onset latencies of distal muscles (gastrocnemius and soleus, both p < .01) used to recover balance. In addition, plots of onset latencies across all muscles showed that onset latencies appeared to occur earlier in many muscles when participants held a static position compared to when they performed a dynamic task at the onset of the perturbation. The results suggest that muscle activities used to recover balance are tailored to the nature of the perturbation and the ongoing task, and that onset latencies are later when participants are performing a dynamic as opposed to static task at the time of a perturbation. These findings support previous research suggesting that automatic postural responses are highly adaptable to environmental, situational, and task demands.     

Review of first trial responses in balance control: influence of vestibular loss and Parkinson's disease

The reaction to an unexpected balance disturbance is unpractised, often startling and frequently associated with falls. This everyday situation can be reproduced in an experimental setting by exposing standing humans to sudden, unexpected and controlled movements of a support surface. In this review, we focus on the responses to the very first balance perturbation, the so-called first trial reactions (FTRs). Detailed analysis of FTRs may have important implications, both for clinical practice (providing new insights into the pathophysiological mechanisms underlying accidental falls in real life) and for understanding human physiology (what triggers and mediates these FTRs, and what is the relation to startle responses?). Several aspects of the FTRs have become clear. FTRs are characterized by an exaggerated postural reaction, with large EMG responses and co-contracting muscles in multiple body segments. This balance reaction is associated with marked postural instability (greater body sway to the perturbation). When the same perturbation is repeated, the size of the postural response habituates and the instability disappears. Other issues about FTRs remain largely unresolved, and these are addressed here. First, the functional role of FTRs is discussed. It appears that FTRs produce primarily increased trunk flexion during the multi-segmental response to postural perturbations, thus producing instability. Second, we consider which sensory signals trigger and modulate FTRs, placing specific emphasis on the role of vestibular signals. Surprisingly, vestibular signals appear to have no triggering role, but vestibular loss leads to excessive upper body FTRs due to loss of the normal modulatory influence. Third, we address the question whether startle-like responses are contributing to FTRs triggered by proprioceptive signals. We explain why this issue is still unresolved, mainly because of methodological difficulties involved in separating FTRs from ‘pure’ startle responses. Fourth, we review new work about the influence of perturbation direction on FTRs. Recent work from our group shows that the largest FTRs are obtained for toe-up support surface rotations which perturb the COM in the posterior direction. This direction corresponds to the directional preponderance for falls seen both in the balance laboratory and in daily life. Finally, we briefly touch upon clinical diagnostic issues, addressing whether FTRs (as opposed to habituated responses) could provide a more ecologically valid perspective of postural instability in patients compared to healthy subjects. We conclude that FTRs are an important source of information about human balance performance, both in health and disease. Future studies should no longer discard FTRs, but routinely include these in their analyses. Particular emphasis should be placed on the link between FTRs and everyday balance performance (including falls), and on the possible role played by startle reactions in triggering or modulating FTRs.