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Uneven substrates constrain walking speed in ants through modulation of stride frequency more than stride length.

ABSTRACT: Natural terrain is rarely flat. Substrate irregularities challenge walking animals to maintain stability, yet we lack quantitative assessments of walking performance and limb kinematics on naturally uneven ground. We measured how continually uneven 3D-printed substrates influence walking performance of Argentine ants by measuring walking speeds of workers from laboratory colonies and by testing colony-wide substrate preference in field experiments. Tracking limb motion in over 8000 videos, we used statistical models that associate walking speed with limb kinematic parameters to compare movement over flat versus uneven ground of controlled dimensions. We found that uneven substrates reduced preferred and peak walking speeds by up to 42% and that ants actively avoided uneven terrain in the field. Observed speed reductions were modulated primarily by shifts in stride frequency instead of stride length (flat R 2: 0.91 versus 0.50), a pattern consistent across flat and uneven substrates. Mixed effect modelling revealed that walking speeds on uneven substrates were accurately predicted based on flat walking data for over 89% of strides. Those strides that were not well modelled primarily involved limb perturbations, including missteps, active foot repositioning and slipping. Together these findings relate kinematic mechanisms underlying walking performance on uneven terrain to ecologically relevant measures under field conditions.

SUBMITTER: Clifton GT

PROVIDER: S-EPMC7137955 | biostudies-literature | 2020 Mar

REPOSITORIES: biostudies-literature

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Uneven substrates constrain walking speed in ants through modulation of stride frequency more than stride length.

Clifton G T GT Holway D D Gravish N N

Royal Society open science 20200325 3

Natural terrain is rarely flat. Substrate irregularities challenge walking animals to maintain stability, yet we lack quantitative assessments of walking performance and limb kinematics on naturally uneven ground. We measured how continually uneven 3D-printed substrates influence walking performance of Argentine ants by measuring walking speeds of workers from laboratory colonies and by testing colony-wide substrate preference in field experiments. Tracking limb motion in over 8000 videos, we us ...[more]

PMID: 32269814

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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: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.

Dataset Information

Uneven substrates constrain walking speed in ants through modulation of stride frequency more than stride length.

Publications

Uneven substrates constrain walking speed in ants through modulation of stride frequency more than stride length.

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