Broken Escalator Research Articles

Dissociated cerebellar contributions to feedforward gait adaptation

The cerebellum is important for motor adaptation. Lesions to the vestibulo-cerebellum selectively cause gait ataxia. Here we investigate how such damage affects locomotor adaptation when performing the ‘broken escalator’ paradigm. Following an auditory cue, participants were required to step from the fixed surface onto a moving platform (akin to an airport travellator). The experiment included three conditions: 10 stationary (BEFORE), 15 moving (MOVING) and 10 stationary (AFTER) trials. We assessed both behavioural (gait approach velocity and trunk sway after stepping onto the moving platform) and neuromuscular outcomes (lower leg muscle activity, EMG). Unlike controls, cerebellar patients showed reduced after-effects (AFTER trials) with respect to gait approach velocity and leg EMG activity. However, patients with cerebellar damage maintain the ability to learn the trunk movement required to maximise stability after stepping onto the moving platform (i.e., reactive postural behaviours). Importantly, our findings reveal that these patients could even initiate these behaviours in a feedforward manner, leading to an after-effect. These findings reveal that the cerebellum is crucial for feedforward locomotor control, but that adaptive locomotor behaviours learned via feedback (i.e., reactive) mechanisms may be preserved following cerebellum damage.

The influence of postural threat-induced anxiety on locomotor learning and updating.

The ability to adapt our locomotion in a feedforward (i.e., "predictive") manner is crucial for safe and efficient walking behavior. Equally important is the ability to quickly deadapt and update behavior that is no longer appropriate for the given context. It has been suggested that anxiety induced via postural threat may play a fundamental role in disrupting such deadaptation. We tested this hypothesis, using the "broken escalator" phenomenon: Fifty-six healthy young adults walked onto a stationary walkway ("BEFORE" condition, 5 trials), then onto a moving walkway akin to an airport travelator ("MOVING" condition, 10 trials), and then again onto the stationary walkway ("AFTER" condition, 5 trials). Participants completed all trials while wearing a virtual reality headset, which was used to induce postural threat-related anxiety (raised clifflike drop at the end of the walkway) during different phases of the paradigm. We found that performing the locomotor adaptation phase in a state of increased threat disrupted subsequent deadaptation during AFTER trials: These participants displayed anticipatory muscular activity as if expecting the platform to move and exhibited inappropriate anticipatory forward trunk movement that persisted during multiple AFTER trials. In contrast, postural threat induced during AFTER trials did not affect behavioral or neurophysiological outcomes. These findings highlight that actions learned in the presence of postural threat-induced anxiety are strengthened, leading to difficulties in deadapting these behaviors when no longer appropriate. Given the associations between anxiety and persistent maladaptive gait behaviors (e.g., "overly cautious" gait, functional gait disorders), the findings have implications for the understanding of such conditions.NEW & NOTEWORTHY Safe and efficient locomotion frequently requires movements to be adapted in a feedforward (i.e., "predictive") manner. These adaptations are not always correct, and thus inappropriate behavior must be quickly updated. Here we showed that increased threat disrupts this process. We found that locomotor actions learned in the presence of postural threat-induced anxiety are strengthened, subsequently impairing one's ability to update (or "deadapt") these actions when they are no longer appropriate for the current context.

Persistence of the 'broken escalator' phenomenon in functional gait disorder: mechanistic insights.

This scientific commentary refers to ‘Dissociated motor learning and de-adaptation in patients with functional gait disorders’, by Lin etal. (doi:10.1093/brain/awaa190)

The "broken escalator" phenomenon: Vestibular dizziness interferes with locomotor adaptation.

Although vestibular lesions degrade postural control we do not know the relative contributions of the magnitude of the vestibular loss and subjective vestibular symptoms to locomotor adaptation. To study how dizzy symptoms interfere with adaptive locomotor learning. We examined patients with contrasting peripheral vestibular deficits, vestibular neuritis in the chronic stable phase (n = 20) and strongly symptomatic unilateral Meniere's disease (n = 15), compared to age-matched healthy controls (n = 15). We measured locomotor adaptive learning using the "broken escalator" aftereffect, simulated on a motorised moving sled. Patients with Meniere's disease had an enhanced "broken escalator" postural aftereffect. More generally, the size of the locomotor aftereffect was related to how symptomatic patients were across both groups. Contrastingly, the degree of peripheral vestibular loss was not correlated with symptom load or locomotor aftereffect size. During the MOVING trials, both patient groups had larger levels of instability (trunk sway) and reduced adaptation than normal controls. Dizziness symptoms influence locomotor adaptation and its subsequent expression through motor aftereffects. Given that the unsteadiness experienced during the "broken escalator" paradigm is internally driven, the enhanced aftereffect found represents a new type of self-generated postural challenge for vestibular/unsteady patients.

Locomotor adaptation is modulated by observing the actions of others.

Observing the motor actions of another person could facilitate compensatory motor behavior in the passive observer. Here we explored whether action observation alone can induce automatic locomotor adaptation in humans. To explore this possibility, we used the "broken escalator" paradigm. Conventionally this involves stepping upon a stationary sled after having previously experienced it actually moving (Moving trials). This history of motion produces a locomotor aftereffect when subsequently stepping onto a stationary sled. We found that viewing an actor perform the Moving trials was sufficient to generate a locomotor aftereffect in the observer, the size of which was significantly correlated with the size of the movement (postural sway) observed. Crucially, the effect is specific to watching the task being performed, as no motor adaptation occurs after simply viewing the sled move in isolation. These findings demonstrate that locomotor adaptation in humans can be driven purely by action observation, with the brain adapting motor plans in response to the size of the observed individual's motion. This mechanism may be mediated by a mirror neuron system that automatically adapts behavior to minimize movement errors and improve motor skills through social cues, although further neurophysiological studies are required to support this theory. These data suggest that merely observing the gait of another person in a challenging environment is sufficient to generate appropriate postural countermeasures, implying the existence of an automatic mechanism for adapting locomotor behavior.

Attention modulates adaptive motor learning in the ‘broken escalator’ paradigm

The physical stumble caused by stepping onto a stationary (broken) escalator represents a locomotor aftereffect (LAE) that attests to a process of adaptive motor learning. Whether such learning is primarily explicit (requiring attention resources) or implicit (independent of attention) is unknown. To address this question, we diverted attention in the adaptation (MOVING) and aftereffect (AFTER) phases of the LAE by loading these phases with a secondary cognitive task (sequential naming of a vegetable, fruit and a colour). Thirty-six healthy adults were randomly assigned to 3 equally sized groups. They performed 5 trials stepping onto a stationary sled (BEFORE), 5 with the sled moving (MOVING) and 5 with the sled stationary again (AFTER). A 'Dual-Task-MOVING (DTM)' group performed the dual-task in the MOVING phase and the 'Dual-Task-AFTEREFFECT (DTAE)' group in the AFTER phase. The 'control' group performed no dual task. We recorded trunk displacement, gait velocity and gastrocnemius muscle EMG of the left (leading) leg. The DTM, but not the DTAE group, had larger trunk displacement during the MOVING phase, and a smaller trunk displacement aftereffect compared with controls. Gait velocity was unaffected by the secondary cognitive task in either group. Thus, adaptive locomotor learning involves explicit learning, whereas the expression of the aftereffect is automatic (implicit). During rehabilitation, patients should be actively encouraged to maintain maximal attention when learning new or challenging locomotor tasks.

The effect of gait approach velocity on the broken escalator phenomenon

Walking onto a stationary surface previously experienced as moving generates an after-effect commonly known as the "broken escalator" after-effect (AE). This AE represents an inappropriate expression of the locomotor adaptation necessary to step onto the moving platform (or escalator). It is characterised by two main biomechanical components, an increased gait approach velocity (GAV) and a forward trunk overshoot on gait termination. We investigated whether the trunk overshoot and other biomechanical measures are the direct inertial consequence of the increased GAV or whether these are the result of an independent adaptive mechanism. Forty-eight healthy young adults walked onto a movable sled. They performed 5 trials with the sled stationary at their preferred walking velocity (BEFORE trials), 5 with the sled moving (MOVING or adaptation trials), and 5 with the sled stationary again (AFTER trials). For the AFTER trials, subjects were divided into four groups. One group was instructed to walk slowly ("slower"), another with cueing at the BEFORE pace ("metronome"). The third group walked without cueing at the BEFORE pace ("normal"), and the fourth, fast ("faster"). We measured trunk pitch angle, trunk linear horizontal displacement, left shank pitch angular velocity and surface EMG from lower leg and trunk muscles. In the AFTER trials, an AE was observed in these biomechanical measures for all gait speeds, but these were not strongly dependent on GAV. An AE was present even when GAV was not different from that of BEFORE trials. Therefore, we conclude that, although contributary, the trunk overshoot is not the direct consequence of the increased GAV. Instead, it appears to be generated by anticipatory motor activity "just in case" the sled moves, herewith termed a "pre-emptive" postural adjustment.

Enhanced locomotor adaptation aftereffect in the “broken escalator” phenomenon using anodal tDCS

The everyday experience of stepping onto a stationary escalator causes a stumble, despite our full awareness that the escalator is broken. In the laboratory, this "broken escalator" phenomenon is reproduced when subjects step onto an obviously stationary platform (AFTER trials) that was previously experienced as moving (MOVING trials) and attests to a process of motor adaptation. Given the critical role of M1 in upper limb motor adaptation and the potential for transcranial direct current stimulation (tDCS) to increase cortical excitability, we hypothesized that anodal tDCS over leg M1 and premotor cortices would increase the size and duration of the locomotor aftereffect. Thirty healthy volunteers received either sham or real tDCS (anodal bihemispheric tDCS; 2 mA for 15 min at rest) to induce excitatory effects over the primary motor and premotor cortex before walking onto the moving platform. The real tDCS group, compared with sham, displayed larger trunk sway and increased gait velocity in the first AFTER trial and a persistence of the trunk sway aftereffect into the second AFTER trial. We also used transcranial magnetic stimulation to probe changes in cortical leg excitability using different electrode montages and eyeblink conditioning, before and after tDCS, as well as simulating the current flow of tDCS on the human brain using a computational model of these different tDCS montages. Our data show that anodal tDCS induces excitability changes in lower limb motor cortex with resultant enhancement of locomotor adaptation aftereffects. These findings might encourage the use of tDCS over leg motor and premotor regions to improve locomotor control in patients with neurological gait disorders.

P20.18 Cortical transcranial direct current stimulation increases the duration of the ‘broken escalator’ locomotor aftereffect

P20.18 Cortical transcranial direct current stimulation increases the duration of the ‘broken escalator’ locomotor aftereffect

Locomotor Adaptation and Aftereffects in Patients With Reduced Somatosensory Input Due to Peripheral Neuropathy

We studied 12 peripheral neuropathy patients (PNP) and 13 age-matched controls with the "broken escalator" paradigm to see how somatosensory loss affects gait adaptation and the release and recovery ("braking") of the forward trunk overshoot observed during this locomotor aftereffect. Trunk displacement, foot contact signals, and leg electromyograms (EMGs) were recorded while subjects walked onto a stationary sled (BEFORE trials), onto the moving sled (MOVING or adaptation trials), and again onto the stationary sled (AFTER trials). PNP were unsteady during the MOVING trials, but this progressively improved, indicating some adaptation. During the after trials, 77% of control subjects displayed a trunk overshoot aftereffect but over half of the PNP (58%) did not. The PNP without a trunk aftereffect adapted to the MOVING trials by increasing distance traveled; subsequently this was expressed as increased distance traveled during the aftereffect rather than as a trunk overshoot. This clear separation in consequent aftereffects was not seen in the normal controls suggesting that, as a result of somatosensory loss, some PNP use distinctive strategies to negotiate the moving sled, in turn resulting in a distinct aftereffects. In addition, PNP displayed earlier than normal anticipatory leg EMG activity during the first after trial. Although proprioceptive inputs are not critical for the emergence or termination of the aftereffect, somatosensory loss induces profound changes in motor adaptation and anticipation. Our study has found individual differences in adaptive motor performance, indicative that PNP adopt different feed-forward gait compensatory strategies in response to peripheral sensory loss.

What the “Broken Escalator” Phenomenon Teaches Us about Balance

Gait adaptation is crucial for coping with varying terrain and biological needs. It is also important that any acquired adaptation is expressed only in the appropriate context. Here we review a recent series of experiments that demonstrate inappropriate expression of gait adaptation. We show that a brief period of walking onto a platform previously experienced as moving results in a large forward sway aftereffect, despite full awareness of the changing context. The adaptation mechanisms involved in this paradigm are extremely fast, just 1-2 discrete exposures to the moving platform result in the motor aftereffect. This aftereffect occurs even if subjects deliberately attempt to suppress it. However, it disappears when the location or method of gait is altered, indicating that aftereffect expression is context dependent. Conversely, making gait self-initiated increases sway during the aftereffect. This aftereffect demonstrates a profound dissociation between knowledge and action. The absence of generalization suggests a relatively simple form of motor learning, albeit involving high-level processing by cortical and cerebellar structures.

The effect of trial number on the emergence of the ‘broken escalator’ locomotor aftereffect

Walking onto a stationary platform, which had been previously experienced as moving generates a locomotor aftereffect (LAE), which resembles the 'broken escalator' phenomenon. Experimentally, this is achieved by having subjects walk initially onto a stationary sled (BEFORE condition), then onto a moving sled (MOVING condition, or adaptation trials) and then again onto the stationary sled (AFTER condition). Subjects are always appropriately warned of the change in conditions. In this paper, we ask how many adaptation trials are needed to produce such a LAE. Thus, in two experiments, the number of MOVING trials was varied between 20 and 5 (Experiment 1) and between 8 and 1 (Experiment 2). Gait velocity, trunk position, foot contact timing and EMG of the ankle flexor-extensors muscles were measured. In comparison with BEFORE trials all groups in the AFTER trials walked inappropriately fast, experienced a large overshoot of the trunk and showed increased leg EMG, indicating that all groups showed a LAE. In each experiment, and for all variables, no significant difference between the groups (i.e. 20 down to one MOVING trials) was found. The study shows that this LAE, in contrast to other motor aftereffects reported in the literature, can be generated with only one or two adaptation trials and without requiring unexpected 'catch' trials. The fast aftereffect generation observed is likely to depend on two types of mechanisms: (1) the nature of the sensorimotor adaptation process, involving multiple sensory feedbacks (visual, vestibular and proprioceptive), anticipatory control and large initial task errors and (2) the involvement of two phylogenetically old neural mechanisms, namely locomotion and fear. Fear-relevant mechanisms, which are notably resistant to cognitive control, may be recruited during the adaptation trials and contribute to the release of this LAE.