Persistent fluctuations in stride intervals under fractal auditory stimulation

Copyright @ 2014 Marmelat et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.Stride sequences of healthy gait are characterized by persistent long-range correlations, which become anti-persistent in the presence of an isochronous metronome. The latter phenomenon is of particular interest because auditory cueing is generally considered to reduce stride variability and may hence be beneficial for stabilizing gait. Complex systems tend to match their correlation structure when synchronizing. In gait training, can one capitalize on this tendency by using a fractal metronome rather than an isochronous one? We examined whether auditory cues with fractal variations in inter-beat intervals yield similar fractal inter-stride interval variability as isochronous auditory cueing in two complementary experiments. In Experiment 1, participants walked on a treadmill while being paced by either an isochronous or a fractal metronome with different variation strengths between beats in order to test whether participants managed to synchronize with a fractal metronome and to determine the necessary amount of variability for participants to switch from anti-persistent to persistent inter-stride intervals. Participants did synchronize with the metronome despite its fractal randomness. The corresponding coefficient of variation of inter-beat intervals was fixed in Experiment 2, in which participants walked on a treadmill while being paced by non-isochronous metronomes with different scaling exponents. As expected, inter-stride intervals showed persistent correlations similar to self-paced walking only when cueing contained persistent correlations. Our results open up a new window to optimize rhythmic auditory cueing for gait stabilization by integrating fractal fluctuations in the inter-beat intervals.Commission of the European Community and the Netherlands Organisation for Scientific Research

Walking Is Not Like Reaching: Evidence from Periodic Mechanical Perturbations

The control architecture underlying human reaching has been established, at least in broad outline. However, despite extensive research, the control architecture underlying human locomotion remains unclear. Some studies show evidence of high-level control focused on lower-limb trajectories; others suggest that nonlinear oscillators such as lower-level rhythmic central pattern generators (CPGs) play a significant role. To resolve this ambiguity, we reasoned that if a nonlinear oscillator contributes to locomotor control, human walking should exhibit dynamic entrainment to periodic mechanical perturbation; entrainment is a distinctive behavior of nonlinear oscillators. Here we present the first behavioral evidence that nonlinear neuro-mechanical oscillators contribute to the production of human walking, albeit weakly. As unimpaired human subjects walked at constant speed, we applied periodic torque pulses to the ankle at periods different from their preferred cadence. The gait period of 18 out of 19 subjects entrained to this mechanical perturbation, converging to match that of the perturbation. Significantly, entrainment occurred only if the perturbation period was close to subjects' preferred walking cadence: it exhibited a narrow basin of entrainment. Further, regardless of the phase within the walking cycle at which perturbation was initiated, subjects' gait synchronized or phase-locked with the mechanical perturbation at a phase of gait where it assisted propulsion. These results were affected neither by auditory feedback nor by a distractor task. However, the convergence to phase-locking was slow. These characteristics indicate that nonlinear neuro-mechanical oscillators make at most a modest contribution to human walking. Our results suggest that human locomotor control is not organized as in reaching to meet a predominantly kinematic specification, but is hierarchically organized with a semi-autonomous peripheral oscillator operating under episodic supervisory control.New York State Spinal Cord Injury Center of Research Excellence (contract CO19772)Massachusetts Institute of Technology. Eric P. and Evelyn E. Newman Laboratory for Biomechanics and Human RehabilitationSamsung Scholarship Foundatio

From locomotion to dance and back : exploring rhythmic sensorimotor synchronization

Le rythme est un aspect important du mouvement et de la perception de l’environnement. Lorsque l’on danse, la pulsation musicale induit une activité neurale oscillatoire qui permet au système nerveux d’anticiper les évènements musicaux à venir. Le système moteur peut alors s’y synchroniser. Cette thèse développe de nouvelles techniques d’investigation des rythmes neuraux non strictement périodiques, tels que ceux qui régulent le tempo naturellement variable de la marche ou la perception rythmes musicaux. Elle étudie des réponses neurales reflétant la discordance entre ce que le système nerveux anticipe et ce qu’il perçoit, et qui sont nécessaire pour adapter la synchronisation de mouvements à un environnement variable. Elle montre aussi comment l’activité neurale évoquée par un rythme musical complexe est renforcée par les mouvements qui y sont synchronisés. Enfin, elle s’intéresse à ces rythmes neuraux chez des patients ayant des troubles de la marche ou de la conscience.Rhythms are central in human behaviours spanning from locomotion to music performance. In dance, self-sustaining and dynamically adapting neural oscillations entrain to the regular auditory inputs that is the musical beat. This entrainment leads to anticipation of forthcoming sensory events, which in turn allows synchronization of movements to the perceived environment. This dissertation develops novel technical approaches to investigate neural rhythms that are not strictly periodic, such as naturally tempo-varying locomotion movements and rhythms of music. It studies neural responses reflecting the discordance between what the nervous system anticipates and the actual timing of events, and that are critical for synchronizing movements to a changing environment. It also shows how the neural activity elicited by a musical rhythm is shaped by how we move. Finally, it investigates such neural rhythms in patient with gait or consciousness disorders

An Analysis of the Relationship Between Complexity and Gait Adaptability

The presented sequence of studies considers theoretical applications from Complexity Science and Chaos Theory for gait time-series analysis. The main goal of this research is to build on insights from a previous body of knowledge, which have identified measures derived from Complexity Science and Chaos Theory as critical markers of gait control. Specifically, the studies presented in this dissertation attempt to directly test whether characterizing gait complexity relates to an ability to flexibly adjust gait. The broader impact of this research is utilizing measures of complexity to characterize gait control, and as a tool for rehabilitation which have both gained momentum in fall prevention research. Through a series of four studies, this dissertation was designed to test the theoretical viewpoint that complexity is related to gait control, particularly gait adaptability. Firstly, I sought to develop a paradigm for reliably entraining gait complexity with the use of several auditory fluctuating timing imperatives which, differed based on specified fractal characteristics. I also sought to quantify the duration of the retention of gait complexity, following entrainment. Thirdly, I assessed whether attentional demands required during entrainment were affected by the fractal characteristics of a fluctuating timing imperative. Lastly, I applied the developed paradigm to evaluate the theoretical relationship between gait complexity and stepping performance. The findings from this dissertation have developed a framework for assessing gait control. This series of projects has determined that a fluctuating timing imperative can reliably prescribe the gait pattern of healthy individuals towards a particular complexity. The use of a fluctuating timing imperative leads to entrainment of the stimulus complexity. Furthermore, once the timing imperative has ceased, there is a brief period of complexity retention in the walking pattern. This dissertation has also confirmed that entraining complexity to a fluctuating timing imperative does not alter the attentional demands associated with entrainment. However, entraining gait to fluctuating timing imperatives of different complexities alters the stepping strategy that is adopted. Lastly, this dissertation has shown that synchronizing gait to a fixed-interval stimulus following entrainment, depends on the complexities of the gait pattern

Gait variablility is altered in older adults when listening to auditory stimuli with differing temporal structures

Gait variability in the context of a deterministic dynamical system may be quantified using nonlinear time series analyses that characterize the complexity of the system. Pathological gait exhibits altered gait variability. It can be either too periodic and predictable, or too random and disordered, as it is the case with aging. While gait therapies often focus on restoration of linear measures such as gait speed or stride length, we propose that the goal of gait therapy should be to restore optimal gait variability, which exhibits chaotic fluctuations and is the balance between predictability and complexity. In this context, our purpose was to investigate how listening to different auditory stimuli affects gait variability. Twenty-seven young and 27 elderly subjects walked on a treadmill for 5 minutes while listening to white noise, a chaotic rhythm, a metronome, and with no auditory stimulus. Stride length, step width, and stride intervals were calculated for all conditions. Detrended Fluctuation Analysis was then performed on these time series. A quadratic trend analysis determined that an idealized inverted-U shape described the relationship between gait variability and the structure of the auditory stimuli for the elderly group, but not for the young group. This proof-of-concept study shows that the gait of older adults may be manipulated using auditory stimuli. Future work will investigate which structures of auditory stimuli lead to improvements in functional status in older adults

Using feedback enhanced visual metronomes to manipulate gait dynamics

Recent literature suggests that gait dynamics plays a role in establishing healthy, adaptive gait behavior, and that illness or injury can alter the dynamic patterns of gait (termed fractal patterns). So called “dynamical diseases” change the fractal patterns in gait, hereby reducing adaptive gait ability and increasing fall-risk. Previous research has shown that fractal patterns in gait can be strengthened through the use of a fractal metronome stimulus. However, in previous research participants have consistently presented weaker fractal patterns than prescribed by the metronome, despite improvements from their baseline. One postulate is that this gap between the stimulus and the participants’ response is due to the prescriptive nature of the stimulus – that is, the metronome is presented with no interaction with the user. If so, the introduction of real-time feedback regarding synchrony with the stimulus may be beneficial to strengthening fractal patterns. The purpose of this study was to examine the role of feedback in increasing synchrony with a fractal metronome stimulus, and in entraining fractal gait patterns. There were three hypotheses: First, feedback would elicit a stronger coupling between participants’ gait dynamics and the dynamics of the stimulus relative to a non-feedback condition. Second, the addition of feedback to the visual metronome would lead to a stronger fractal pattern during the training and post-training (retention) phases. Third, participants with the strongest coupling during training would exhibit the strongest fractal patterns during training and post training. Results showed no difference in coupling between feedback and non-feedback conditions. The addition of feedback to the fractal metronome lead to no significant difference in fractal strength from baseline to training and baseline to retention. While greater coupling was correlated to stronger fractal patterns during training, there was no relationship between coupling and retention. This study provided further evidence supporting the use of metronomes to alter gait dynamics, and was one of the first to examine feedback in conjunction with fractal gait training

Entrainment and synchronization to auditory stimuli during walking in healthy and neurological populations : a methodological systematic review

Background: Interdisciplinary work is needed for scientific progress, and with this review, our interest is in the scientific progress toward understanding the underlying mechanisms of auditory-motor coupling, and how this can be applied to gait rehabilitation. Specifically we look into the process of entrainment and synchronization; where entrainment is the process that governs the dynamic alignments of the auditory and motor domains based on error-prediction correction, whereas synchronization is the stable maintenance of timing during auditory-motor alignment. Methodology: A systematic literature search in databases PubMed and Web of Science were searched up to 9th of August 2017. The selection criteria for the included studies were adult populations, with a minimum of five participants, investigating walking to an auditory stimulus, with an outcome measure of entrainment, and synchronization. The review was registered in PROSPERO as CRD42017080325. Objectives: The objective of the review is to systematically describe the metrics which measure entrainment and synchronization to auditory stimuli during walking in healthy and neurological populations. Results: Sixteen articles were included. Fifty percent of the included articles had healthy controls as participants (N = 167), 19% had neurological diseases such as Huntington's and Stroke (N = 76), and 31% included both healthy and neurological [Parkinson's disease (PD) and Stroke] participants (N = 101). In the included studies, six parameters were found to capture the interaction between the human movement and the auditory stimuli, these were: cadence, relative phase angle, resultant vector length, interval between the beat and the foot contact, period matching performance, and detrended fluctuation analysis. Conclusion: In this systematic review, several metrics have been identified, which measure the timing aspect of auditory-motor coupling and synchronization of auditory stimuli in healthy and neurological populations during walking. The application of these metrics may enhance the current state of the art and practice across the neurological gait rehabilitation. These metrics also have current shortcomings. Of particular pertinence is our recommendation to consider variability in data from a time-series rather than time-windowed viewpoint. We need it in view of the promising practical applications from which the studied populations may highly benefit in view of personalized medical care

An investigation into the relationship between locomotor dynamics and adaptability

Over the last 40 years, a new paradigm has been posited where the variability observed in physiological systems is a consequence of the interactions occurring between the various components that affect the system. While quantifying the magnitude of variability can be useful, analyses that measure how the structure of the variability (dynamics) changes over time have been posited to reflect the health of the system. Many researchers interpret the results of these analyses to be indicative of the system’s adaptive capacity. While there is ample indirect evidence to support this notion, a lack of direct findings has left the literature lacking a definitive foundation to move forward with this interpretation. While many physiological systems are too invasive to safely perturb, the movement-based systems are routinely perturbed in real-world environments without dire consequences. Of particular interest is the locomotor system, which is constantly challenged in real-world environments via slips and trips. Furthermore, the locomotor system can be safely and validly perturbed in the laboratory. A range of locomotor dynamics-based measures have been used to describe differences between various clinical populations, but none have been directly associated with a person’s ability to remain upright when perturbed. The objectives of this study are to (1) examine the relationship between locomotor dynamics/stability to overall fall-risk prior, (2) examine how locomotor dynamics relate to the ability to recover from a trip via global stability, and (3) determine the extent to which an acute trip-training session alters locomotor dynamics and global stability. Forty healthy, older adults (75.2±4.9 yrs) were recruited by convenience from the local community. The participants completed a variety of clinical assessments in order to determine overall fall-risk. Afterwards, they participated in three walking trials consisting of: 1) a 15-minute unperturbed walking session, 2) a 10-minute unperturbed walking session (control) or a 10-minute trip-training session (intervention), and 3) a 15-minute unperturbed walking session. Various measurements of locomotor dynamics and adaptability were calculated from full-body 3-D kinematics collected at 100Hz. Multiple regression and repeated measure analysis of variance models were calculated to determine to what extent locomotor dynamics and adaptability relate to one another and how an acute trip-training session affects their relationship. The results from our first experiment suggested that locomotor dynamics and stability during steady state do not significantly relate to overall fall-risk. However, the second experiment showed that locomotor dynamics are predictive of an individual’s ability to recover from a trip. Our last experiment showed the feasibility of using an acute trip-training session to alter locomotor dynamics and stability. These data represent the first direct evidence of physiological variability being indicative of adaptive capacity in the locomotor system. Further investigation will be necessary to determine the robustness of the analyses to indicate adaptive capacity across perturbations and populations