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Temporal organization of stride-to-stride variations contradicts predictive models for sensorimotor control of footfalls during walking.

ABSTRACT: Walking exhibits stride-to-stride variations. Given ongoing perturbations, these variations critically support continuous adaptations between the goal-directed organism and its surroundings. Here, we report that stride-to-stride variations during self-paced overground walking show cascade-like intermittency-stride intervals become uneven because stride intervals of different sizes interact and do not simply balance each other. Moreover, even when synchronizing footfalls with visual cues with variable timing of presentation, asynchrony in the timings of the cue and footfall shows cascade-like intermittency. This evidence conflicts with theories about the sensorimotor control of walking, according to which internal predictive models correct asynchrony in the timings of the cue and footfall from one stride to the next on crossing thresholds leading to the risk of falling. Hence, models of the sensorimotor control of walking must account for stride-to-stride variations beyond the constraints of threshold-dependent predictive internal models.

SUBMITTER: Mangalam M

PROVIDER: S-EPMC10449478 | biostudies-literature | 2023

REPOSITORIES: biostudies-literature

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Temporal organization of stride-to-stride variations contradicts predictive models for sensorimotor control of footfalls during walking.

Mangalam Madhur M Kelty-Stephen Damian G DG Sommerfeld Joel H JH Stergiou Nick N Likens Aaron D AD

PloS one 20230824 8

Walking exhibits stride-to-stride variations. Given ongoing perturbations, these variations critically support continuous adaptations between the goal-directed organism and its surroundings. Here, we report that stride-to-stride variations during self-paced overground walking show cascade-like intermittency-stride intervals become uneven because stride intervals of different sizes interact and do not simply balance each other. Moreover, even when synchronizing footfalls with visual cues with var ...[more]

PMID: 37616227

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Project description:Variability is ubiquitous in human movement, arising from internal and external noise, inherent biological redundancy, and from the neurophysiological control actions that help regulate movement fluctuations. Increased walking variability can lead to increased energetic cost and/or increased fall risk. Conversely, biological noise may be beneficial, even necessary, to enhance motor performance. Indeed, encouraging more variability actually facilitates greater improvements in some forms of locomotor rehabilitation. Thus, it is critical to identify the fundamental principles humans use to regulate stride-to-stride fluctuations in walking. This study sought to determine how humans regulate stride-to-stride fluctuations in stepping movements during treadmill walking. We developed computational models based on pre-defined goal functions to compare if subjects, from each stride to the next, tried to maintain the same speed as the treadmill, or instead stay in the same position on the treadmill. Both strategies predicted average behaviors empirically indistinguishable from each other and from that of humans. These strategies, however, predicted very different stride-to-stride fluctuation dynamics. Comparisons to experimental data showed that human stepping movements were generally well-predicted by the speed-control model, but not by the position-control model. Human subjects also exhibited no indications they corrected deviations in absolute position only intermittently: i.e., closer to the boundaries of the treadmill. Thus, humans clearly do not adopt a control strategy whose primary goal is to maintain some constant absolute position on the treadmill. Instead, humans appear to regulate their stepping movements in a way most consistent with a strategy whose primary goal is to try to maintain the same speed as the treadmill at each consecutive stride. These findings have important implications both for understanding how biological systems regulate walking in general and for being able to harness these mechanisms to develop more effective rehabilitation interventions to improve locomotor performance.

Project description:Introduction: The seemingly periodic human gait exhibits stride-to-stride variations as it adapts to the changing task constraints. The optimal movement variability hypothesis (OMVH) states that healthy stride-to-stride variations exhibit "fractality"-a specific temporal structure in consecutive strides that are ordered, stable but also variable, and adaptable. Previous research has primarily focused on a single fractality measure, "monofractality." However, this measure can vary across time; strideto-stride variations can show "multifractality." Greater multifractality in stride-tostride variations would highlight the ability to tune and adjust movements more. Methods: We investigated monofractality and multifractality in a cohort of eight healthy adults during self-paced walking and running trials, both on a treadmill and overground. Footfall data were collected through force-sensitive sensors positioned on their heels and feet. We examined the effects of self-paced walking vs. running and treadmill vs. overground locomotion on the measure of monofractality, α-DFA, in addition to the multifractal spectrum width, W, and the asymmetry in the multifractal spectrum, WAsym, of stride interval time series. Results: While the α-DFA was larger than 0.50 for almost all conditions, α-DFA was higher in running and locomoting overground than walking and locomoting on a treadmill. Similarly, W was greater while locomoting overground than on a treadmill, but an opposite trend indicated that W was greater in walking than running. Larger WAsym values in the negative direction suggest that walking exhibits more variation in the persistence of shorter stride intervals than running. However, the ability to tune and adjust movements does not differ between treadmill and overground, although both exhibit more variation in the persistence of shorter stride intervals. Discussion: Hence, greater heterogeneity in shorter than longer stride intervals contributed to greater multifractality in walking compared to running, indicated by larger negative WAsym values. Our results highlight the need to incorporate multifractal methods to test the predictions of the OMVH.

Project description:BackgroundGait disorders of Parkinson's disease (PD) are characterized by the breakdown of the temporal organization of stride duration variability that was tightly associated to dynamic instability in PD. Activating the upper body during walking, Nordic Walking (NW) may be used as an external cueing to improve spatiotemporal parameters of gait, such as stride length or gait variability, in PD. The aim of this study was to evaluate the beneficial effects of NW on temporal organization of gait variability and spatiotemporal gait variables in PD.MethodsFourteen mild to moderate PD participants and ten age-matched healthy subjects performed 2 × 12 min overground walking sessions (with and without pole in a randomized order) at a comfortable speed. Gait speed, cadence, step length and temporal organization (i.e. long-range autocorrelations; LRA) of stride duration variability were studied on 512 consecutive gait cycles using a unidimensional accelerometer placed on the malleola of the most affected side in PD patients and of the dominant side in healthy controls. The presence of LRA was determined using the Rescaled Range Analysis (Hurst exponent) and the Power Spectral Density (α exponent). To assess NW and disease influences on gait, paired t-tests, Z-score and a two-way (pathological condition x walking condition) ANOVA repeated measure were used.ResultsLeading to significant improvement of LRA, NW enhances step length and reduces gait cadence without any change in gait speed in PD. Interestingly, LRA and step length collected from the NW session are similar to that of the healthy population.ConclusionThis cross-sectional controlled study demonstrates that NW may constitute a powerful way to struggle against the randomness of PD gait and the typical gait hypokinesia. Involving a voluntary intersegmental coordination, such improvement could also be due to the upper body rhythmic movements acting as rhythmical external cue to bypass their defective basal ganglia circuitries.Ethics committee's reference numberB403201318916 TRIAL REGISTRATION: NCT02419768.

Dataset Information

Temporal organization of stride-to-stride variations contradicts predictive models for sensorimotor control of footfalls during walking.

Publications

Temporal organization of stride-to-stride variations contradicts predictive models for sensorimotor control of footfalls during walking.

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