Small, movement dependent perturbations substantially alter postural control strategy in healthy young adults.

Postural control is commonly investigated by observing responses to perturbations. We developed a perturbation paradigm mimicking self-generated errors in weight shifting, which are a common cause of falling among older adults. Our aim was to determine the effects of this small, but complex, perturbation on postural sway of healthy young adults and evaluate the role of vision and cognition during movement dependent perturbations. Fifteen participants stood hip-width apart with their eyes open, closed and while performing two different cognitive tasks. Participants were continuously perturbed by medial-lateral (ML) support surface translations corresponding to, and hence doubling, their own center of mass sway. We analyzed the standard deviation (SD), root mean square (RMS), range, and mean power frequency (MPF) of center of pressure displacements. ML postural sway increased due to the perturbation (SD p ≤ .001, range p < .001, RMS p ≤ .001, MPF p < .001). Cognitive load increased the ML sway range (p = .048). Lack of vision increased ML MPF (p = .001) and anterior-posterior (AP) range (p < .001), SD (p < .001), and RMS (p = .001). Significant interaction of vision with the perturbation was found for the ML range (p = .045) and AP SD (p = .018). The perturbation specifically affected ML postural sway. Increased MPF is indicative of a postural control strategy change, which was insufficient for fully controlling the increased sway. Despite being small, this type of perturbation appears to be challenging for young adults.

Staying on your feet: the effectiveness of posture and handles in counteracting balance perturbation.

Stairways, public transport and inclined walkways are often considered as sites with higher likelihood of falls due to a sudden loss of balance. Such sites are usually marked with warning signs, equipped with non-slip surfaces and handles or handrails to avert or decrease this likelihood. Especially, handles are supposed to provide additional support in cases of a sudden loss of balance. However, the mechanisms of using handles for balance at different heights are not yet fully disclosed. We simulated full body perturbations by applying an anterior force to the waist and investigated effectiveness and mechanisms of balance recovery in five different postures: step stance and normal stance with or without holding handles at different heights. Results indicate that both step stance and holding handles at different vertical positions sufficiently assist balance recovery, compared to normal stance. While there was no significant effect of handle in CoM displacement, the shoulder height handle required the lowest handle force, indicating a difference in using the handle. Practitioner summary: To investigate handle use for balance recovery, we perturbed healthy young adults in different standing positions. Even though the use of different handles had a similar effect, the lowest forces were exerted on the shoulder height handle indicating a preferred handle position for balance recovery. Abbreviation: AP: antero-posterior; CNS: Central nervous system; CoM: Center of Mass; CoMmax: Maximal displacement of the center of mass; CoP: Center of pressure; FHmax: Maximal resultant force exerted on the handle; hFHmax: Maximal horizontal force exerted on the handle; vFHmax; Maximal vertical force exerted on the handle; M1-M8: Perturbation force magnitude.

A robotic system for delivering novel real-time, movement dependent perturbations.

Perturbations are often used to study movement control and balance, especially in the context of falling. Most often, discrete perturbations defined prior to the experiment are used to mimic external disturbances to balance. However, the largest proportion of falls is due to self-generated errors in weight shifting. Inspired by self-generated weight shifting errors, we created a novel, continuous mediolateral perturbation proportional to subjects' mediolateral center of mass movement with minimal delays. This perturbation was delivered by a robotic platform controlled by a real time Matlab Simulink model using kinematic data from a marker positioned at subjects' L5 as input. Fifteen healthy young adults stood as still as possible atop the robotic platform with their eyes closed. We evaluated the performance of the perturbation in terms of accuracy and delay relative to the input signal by using cross-correlations. The perturbations were accurate (r=-0.984), with delays of 154 ms. Such systematic perturbation significantly affected mediolateral sway, increasing its range (from 5.56±3.72 to 9.58 ±4.83 mm, p=0.01), SD (from 1.08±0.74 to 1.72±0.74 mm, p = 0.02), and mean power frequency (from 0.08±0.05 to 0.25±0.17 Hz, p<0.01). These perturbation characteristics enable inducing systematic, movement-dependent perturbations and open the door for future studies investigating self-generated movement errors.

Quick foot placement adjustments during gait are less accurate in individuals with focal cerebellar lesions.

Online gait corrections are frequently used to restore gait stability and prevent falling. They require shorter response times than voluntary movements which suggests that subcortical pathways contribute to the execution of online gait corrections. To evaluate the potential role of the cerebellum in these pathways we tested the hypotheses that online gait corrections would be less accurate in individuals with focal cerebellar damage than in neurologically intact controls and that this difference would be more pronounced for shorter available response times and for short step gait corrections. We projected virtual stepping stones on an instrumented treadmill while some of the approaching stepping stones were shifted forward or backward, requiring participants to adjust their foot placement. Varying the timing of those shifts allowed us to address the effect of available response time on foot placement error. In agreement with our hypothesis, individuals with focal cerebellar lesions were less accurate in adjusting their foot placement in reaction to suddenly shifted stepping stones than neurologically intact controls. However, the cerebellar lesion group's foot placement error did not increase more with decreasing available response distance or for short step versus long step adjustments compared to the control group. Furthermore, foot placement error for the non-shifting stepping stones was also larger in the cerebellar lesion group as compared to the control group. Consequently, the reduced ability to accurately adjust foot placement during walking in individuals with focal cerebellar lesions appears to be a general movement control deficit, which could contribute to increased fall risk.

Online adjustments of leg movements in healthy young and old.

Online movement adjustments are crucial for daily life. This is especially true for leg movements in relation to gait, where failed adjustments can lead to falls, especially in elderly. However, most research has focused on reach adjustments following changes in target location. This arm research reports two categories of online adjustments (see Gaveau et al., Neuropsychologia 55:25-40, 2014 for review). Small, frequently undetected, target location shifts invoke fast, automatic adjustments, usually without awareness. In contrast, large target location shifts can lead to slow, voluntary adjustments. These fast and slow adjustments presumably rely on different neural networks, with a possible role for subcortical pathways for the fast responses. Do leg movement adjustments also fall into these two categories? We review the literature on leg movement adjustments and show that it is indeed possible to discern fast and slow adjustments. More specifically, we provide an overview of studies showing adjustments during step preparation, initiation, unobstructed, and obstructed gait. Fast adjustments were found both during stepping and gait. In the extreme case, even step adjustments appear to be further modifiable online, e.g., when avoiding obstacles during tripping. In older adults, movement adjustments are generally slower and of smaller magnitude, consistent with a greater risk of falling. However, fast responses seem less affected by aging, consistent with the idea of independent parallel mechanisms controlling movement adjustments (Gomi, Curr Opin Neurobiol 18:558-567, 2008). Finally, putative neural pathways are discussed.

Reliable estimation of inhibitory efficiency: to anticipate, choose or simply react?

Response inhibition is an important executive process studied by clinical and experimental psychologists, neurophysiologists and cognitive neuroscientists alike. Stop-signal paradigms are popular because they are grounded in a theory that provides methods to estimate the latency of an unobservable process: the stop-signal reaction time (SSRT). Critically, SSRT estimates can be biased by skew of the response time distribution and gradual slowing over the course of the experiment. Here, we present a series of experiments that directly compare three common stop-signal paradigms that differ in the distribution of response times. The results show that the widely used choice response (CR) and simple response (SR) time versions of the stop-signal paradigm are particularly susceptible to skew of the response time distribution and response slowing, and that using the anticipated response (AR) paradigm based on the Slater-Hammel task offers a viable alternative to obtain more reliable SSRT estimates.

Holding a Handle for Balance during Continuous Postural Perturbations-Immediate and Transitionary Effects on Whole Body Posture.

When balance is exposed to perturbations, hand contacts are often used to assist postural control. We investigated the immediate and the transitionary effects of supportive hand contacts during continuous anteroposterior perturbations of stance by automated waist-pulls. Ten young adults were perturbed for 5 min and required to maintain balance by holding to a stationary, shoulder-high handle and following its removal. Center of pressure (COP) displacement, hip, knee and ankle angles, leg and trunk muscle activity and handle contact forces were acquired. The analysis of results show that COP excursions are significantly smaller when the subjects utilize supportive hand contact and that the displacement of COP is strongly correlated to the perturbation force and significantly larger in the anterior than posterior direction. Regression analysis of hand forces revealed that subjects utilized the hand support significantly more during the posterior than anterior perturbations. Moreover, kinematical analysis showed that utilization of supportive hand contacts alter posture of the whole body and that postural readjustments after the release of the handle, occur at different time scales in the hip, knee and ankle joints. Overall, our findings show that supportive hand contacts are efficiently used for balance control during continuous postural perturbations and that utilization of a handle has significant immediate and transitionary effects on whole body posture.

Two-stage muscle activity responses in decisions about leg movement adjustments during trip recovery.

Studies on neural decision making mostly investigated fast corrective adjustments of arm movements. However, fast leg movement corrections deserve attention as well, since they are often required to avoid falling after balance perturbations. The present study aimed at elucidating the mechanisms behind fast corrections of tripping responses by analyzing the concomitant leg muscle activity changes. This was investigated in seven young adults who were tripped in between normal walking trials and took a recovery step by elevating the tripped leg over the obstacle. In some trials, a forbidden landing zone (FZ) was presented behind the obstacle, at the subjects' preferred foot landing position, forcing a step correction. Muscle activity of the tripped leg gastrocnemius medialis (iGM), tibialis anterior (iTA), rectus femoris (iRF), and biceps femoris (iBF) muscles was compared between normal trips presented before any FZ appearance, trips with a FZ, and normal trips presented in between trips with a FZ ("catch" trials). When faced with a real or expected (catch trials) FZ, subjects shortened their recovery steps. The underlying changes in muscle activity consisted of two stages. The first stage involved reduced iGM activity, occurring at a latency shorter than voluntary reaction, followed by reduced iTA and increased iBF and iGM activities occurring at longer latencies. The fast response was not related to step shortening, but longer latency responses clearly were functional. We suggest that the initial response possibly acts as a "pause," allowing the nervous system to integrate the necessary information and prepare the subsequent, functional movement adjustment.

Quick foot placement adjustments during gait: direction matters.

To prevent falls, adjustment of foot placement is a frequently used strategy to regulate and restore gait stability. While foot trajectory adjustments have been studied during discrete stepping, online corrections during walking are more common in daily life. Here, we studied quick foot placement adjustments during gait, using an instrumented treadmill equipped with a projector, which allowed us to project virtual stepping stones. This allowed us to shift some of the approaching stepping stones in a chosen direction at a given moment, such that participants were forced to adapt their step in that specific direction and had varying time available to do so. Thirteen healthy participants performed six experimental trials all consisting of 580 stepping stones, and 96 of those stones were shifted anterior, posterior or lateral at one out of four distances from the participant. Overall, long-step gait adjustments were performed more successfully than short-step and side-step gait adjustments. We showed that the ability to execute movement adjustments depends on the direction of the trajectory adjustment. Our findings suggest that choosing different leg movement adjustments for obstacle avoidance comes with different risks and that strategy choice does not depend exclusively on environmental constraints. The used obstacle avoidance strategy choice might be a trade-off between the environmental factors (i.e., the cost of a specific adjustment) and individuals' ability to execute a specific adjustment with success (i.e., the associated execution risk).

Effects of aging and dual tasking on step adjustments to perturbations in visually cued walking.

Making step adjustments is an essential component of walking. However, the ability to make step adjustments may be compromised when the walker's attentional capacity is limited. This study compared the effects of aging and dual tasking on step adjustments in response to stepping-target perturbations during visually cued treadmill walking. Fifteen older adults (69.4 ± 5.0 years; mean ± SD) and fifteen young adults (25.4 ± 3.0 years) walked at a speed of 3 km/h on a treadmill. Both groups performed visually cued step adjustments in response to unpredictable shifts of projected stepping targets in forward (FW), backward (BW) or sideward (SW) directions, at different levels of task difficulty [which increased as the available response distance (ARD) decreased], and with and without dual tasking (auditory Stroop task). In both groups, step adjustments were smaller than required. For FW and BW shifts, older adults undershot more under dual-task conditions. For these shifts, ARD affected the age groups differentially. For SW shifts, larger errors were found for older adults, dual tasking and the most difficult ARD. Stroop task performance did not differ between groups in all conditions. Older adults have more difficulty than young adults to make corrective step adjustments while walking, especially under dual-tasking conditions. Furthermore, they seemed to prioritize the cognitive task over the step adjustment task, a strategy that may pose aging populations at a greater fall risk. For comparable task difficulty, the older adults performed considerably worse than the young adults, indicating a decreased ability to adjust steps under time pressure.

Gait asymmetry during early split-belt walking is related to perception of belt speed difference.

Gait adaptation is essential for humans to walk according to the different demands of the environment. Although locomotor adaptation has been studied in different contexts and in various patient populations, the mechanisms behind locomotor adaptation are still not fully understood. The aim of the present study was to test two opposing hypotheses about the control of split-belt walking, one based on avoidance of limping and the other on avoiding limb excursion asymmetry. We assessed how well cerebellar patients with focal lesions and healthy control participants could sense differences between belt speeds during split-belt treadmill walking and correlated this to split-belt adaptation parameters. The ability to perceive differences between belt speeds was similar between the cerebellar patients and the healthy controls. After combining all participants, we observed a significant inverse correlation between stance time symmetry and limb excursion symmetry during the early phase of split-belt walking. Participants who were better able to perceive belt speed differences (e.g., they had a lower threshold and hence were able to detect a smaller speed difference) walked with the smallest asymmetry in stance time and the largest asymmetry in limb excursion. Our data support the hypothesis that humans aim to minimize (temporal) limping rather than (spatial) limb excursion asymmetry when using their perception of belt speed differences in the early phase of adaptation to split-belt walking.

Response inhibition and avoidance of virtual obstacles during gait in healthy young and older adults.

Adjustments of preplanned steps are essential for fall avoidance and require response inhibition. Still, inhibition is rarely tested under conditions resembling daily living. We evaluated the ability of young and older adults to modify ongoing walking movements using a novel precision step inhibition (PSI) task combined with an auditory Stroop task. Healthy young (YA, n=12) and older (OA, n=12) adults performed the PSI task at 4 individualized difficulty levels, as a single and dual task (DT). Subjects walked on a treadmill by stepping on virtual stepping stones, unless these changed color during approach, forcing the subjects to avoid them. OA made more failures (40%) on the PSI task than YA (16%), but DT did not affect their performance. In combination with increased rates of omitted Stroop task responses, this indicates a "posture first" strategy. Yet, adding obstacles to the PSI task significantly deteriorated Stroop performance in both groups (the average Stroop composite score decreased by 13% in YA and 27% in OA). Largest deficit of OA was observed in rates of incorrect responses to incongruent Stroop stimuli (OA 35% and YA 12%), which require response inhibition. We concluded that the performance of OA suffered specifically when response inhibition was required.

Fast online corrections of tripping responses.

Tripping over obstacles is one of the main causes of falls. One potential hazard to actually fall when tripped is inadequate foot landing. Adequate landing is required to control the body's angular momentum, while avoiding dangerous surfaces (slippery patch, uneven ground). To avoid such dangers, foot trajectory needs to be controlled by inhibiting and adjusting the initiated recovery foot path during a tripping reaction. We investigated whether such adjustments can be made without jeopardizing balance recovery. Sixteen healthy young adults (25.1 ± 3.2 years) walked at their comfortable speed over a walkway equipped with 14 hidden obstacles. Participants were tripped 10 times in between a random number of normal walking trials; five trips included a projection of a forbidden zone (FZ, 30 × 50 cm) at the subject's preferred landing position. Participants were instructed to land their recovery foot outside the FZ, if the FZ was presented. Responses were evaluated in terms of foot position and body angular momentum at and following recovery foot landing. Participants successfully landed their recovery foot outside the FZ in 80% of trials, using strategies of either shortening their recovery steps (84%) or side stepping (16%). Their performance improved over trials, and some participants switched strategies. Angular momenta of the adjusted steps remained small at and following recovery foot landing. Young adults can quickly change foot trajectory after tripping by using different strategies, and without detrimental consequences on balance recovery, in terms of the angular momentum. These results open possibilities for training of tripping reactions.

Response inhibition during avoidance of virtual obstacles while walking.

While walking, one often has to suppress and adjust a planned step in order to avoid a fall. Given that steps are preprogrammed this requires some form of motor inhibition. Motor inhibition is commonly tested in hand function and only recently attempts have been made to evaluate inhibition in the lower limbs, during step initiation. As adequate motor inhibition might play a role in avoiding falls a test to assess response inhibition during walking would be valuable. We developed a task in which subjects walked on a treadmill by stepping on projected patches of light, which could suddenly change color forcing the subjects to avoid it by shortening or lengthening their steps. The difficulty level was manipulated in 4 conditions by changing the distance available to respond. We hypothesized that larger demands on motor inhibition during walking would produce more failures and tested the performance of young adults (n=12) in order to establish the protocol for use in older adults. The failure rate on the walking test was analyzed. Reducing the available response distance by 150 mm from the easiest condition resulted in a significant increase in failure rates from 15.6% to 65.1%. Therefore, results indicate this novel test can be used to assess the level of motor inhibition during walking. Additionally, in comparison to previous literature on obstacle avoidance, our experiment shows that changing a precise aiming movement is considerably more challenging than changing the same movement executed automatically.

Split-second decisions on a split belt: does simulated limping affect obstacle avoidance?

During normal gait a suddenly appearing obstacle is avoided either by making a large crossing step (long-step strategy, LSS) or by interrupting the swing phase (short-step strategy, SSS) depending on the time of appearance of the obstacle in the step cycle. Limping changes the proportion of time spent in the swing phase and the question arises whether this could affect the ability to avoid obstacles. This was investigated using a split-belt treadmill that induces behavior that is similar to limping even in normal adults. Subjects walked on a split-belt treadmill with speed ratios between left and right of 2:2 up to 2:8 km/h in combination with obstacle avoidance (OA) on the slow belt. The failure rate of obstacle avoidance increased markedly as speed differences between legs increased. This increment was paralleled by augmented use of the SSS, related to an increase in time pressure. In all split-belt walking conditions, the alternative strategy (LSS) yielded less OA failures but it required much longer preparation time than the SSS. In addition, the prolonged stance phases prior to crossing in the LSS required a concomitant prolongation of the contralateral swing phase. This was difficult to achieve at times and as a result the swing phase was sometimes interrupted, giving rise to a contralateral SSS (and a 2:1 coordination pattern). It is concluded that simulated limping greatly increases the risk of failing to avoid suddenly appearing obstacles.