A Dynamical Systems Approach to Characterizing Brain–Body Interactions during Movement: Challenges, Interpretations, and Recommendations

Brain–body interactions (BBIs) have been the focus of intense scrutiny since the inception of the scientific method, playing a foundational role in the earliest debates over the philosophy of science. Contemporary investigations of BBIs to elucidate the neural principles of motor control have benefited from advances in neuroimaging, device engineering, and signal processing. However, these studies generally suffer from two major limitations. First, they rely on interpretations of ‘brain’ activity that are behavioral in nature, rather than neuroanatomical or biophysical. Second, they employ methodological approaches that are inconsistent with a dynamical systems approach to neuromotor control. These limitations represent a fundamental challenge to the use of BBIs for answering basic and applied research questions in neuroimaging and neurorehabilitation. Thus, this review is written as a tutorial to address both limitations for those interested in studying BBIs through a dynamical systems lens. First, we outline current best practices for acquiring, interpreting, and cleaning scalp-measured electroencephalography (EEG) acquired during whole-body movement. Second, we discuss historical and current theories for modeling EEG and kinematic data as dynamical systems. Third, we provide worked examples from both canonical model systems and from empirical EEG and kinematic data collected from two subjects during an overground walking task

A new measure of the CoP trajectory in postural sway: Dynamics of heading change

The maintenance of upright stance requires the simultaneous control of posture in both the anterior–posterior (AP) and medial–lateral (ML) dimensions. Postural sway is typically measured by quantifying the movement of the center of pressure (CoP) in the AP and ML dimensions independently. Metrics such as path length and 95% ellipse area have been developed to take into account movement in both the AP and ML directions, but these metrics only quantify the magnitude of the CoP movement. The movement of the CoP is technically a vector quantity with both magnitude and direction characteristics. The direction of displacement, or heading, of the CoP may provide further insight into the control of posture. Accordingly, we present a novel variable that describes the rate of change in direction of CoP displacement in two dimensions, the heading change (??), which is derived from the CoP heading (?). We then compared the standard deviation (SD) and the dynamic structure characterized by sample entropy (SampEn) of the heading change time series to previously examined metrics presented in the literature (SD and SampEn of the AP and ML time series, path length, SD and SampEn of the CoP resultant magnitude time series) during a 60 s single-leg stance performed by healthy participants and patients with a ruptured anterior cruciate ligament (ACL) prior to surgical intervention. Patients with an ACL rupture exhibited a different dynamic structure in ??compared to healthy controls, t(14) = 2.44, p = 0.029, whereas none of the other metrics differed between groups (all p > 0.05). The novelty and utility of ?? is that it characterizes directional changes of the CoP, whereas previously documented postural control analyses describe only changes in magnitude

Follow the leader: Visual control of speed in pedestrian following

When people walk together in groups or crowds they must coordinate their walking speed and direction with their neighbors. This paper investigates how a pedestrian visually controls speed when following a leader on a straight path (one-dimensional following). To model the behavioral dynamics of following, participants in Experiment 1 walked behind a confederate who randomly increased or decreased his walking speed. The data were used to test six models of speed control that used the leader's speed, distance, or combinations of both to regulate the follower's acceleration. To test the optical information used to control speed, participants in Experiment 2 walked behind a virtual moving pole, whose visual angle and binocular disparity were independently manipulated. The results indicate the followers match the speed of the leader, and do so using a visual control law that primarily nulls the leader's optical expansion (change in visual angle), with little influence of change in disparity. This finding has direct applications to understanding the coordination among neighbors in human crowds

Multiple timescales in postural dynamics associated with vision and a secondary task are revealed by wavelet analysis

Discrete wavelet analysis is used to resolve the center of pressure time series data into several timescale components, providing new insights into postural control. Healthy young and elderly participants stood quietly with their eyes open or closed and either performed a secondary task or stood quietly. Without vision, both younger and older participants had reduced energy in the long time-scales, supporting the concept that vision is used to control low frequency postural sway. Furthermore, energy was increased at timescales corresponding to closed-loop (somatosensory and vestibular) and open-loop mechanisms, consistent with the idea of a shift from visual control to other control mechanisms. However, a relatively greater increase was observed for older adults. With a secondary task a similar pattern was observed—increased energy at the short and moderate timescales, decreased energy at long timescales. The possibility of a common strategy—at the timescale level—in response to postural perturbations is considered

The impact of low-level blast exposure on brain function after a one-day tactile training and the ameliorating effect of a jugular vein compression neck collar device

Special Weapons and Tactics (SWAT) personnel who conduct breacher exercises are at risk for blast-related head trauma. We aimed to investigate the potential impact of low-level blast exposure during breacher training on the neural functioning of working memory and auditory network connectivity. We also aimed to evaluate the effects of a jugular vein compression collar, designed to internally mitigate slosh energy absorption, preserving neural functioning and connectivity, following blast exposure. A total of 23 SWAT personnel were recruited and randomly assigned to a non-collar (n?=?11) and collar group (n?=?12). All participants completed a 1-day breacher training with multiple blast exposure. Prior to and following training, 18 participants (non-collar, n?=?8; collar, n?=?10) completed functional magnetic resonance imaging (fMRI) of working memory using N-Back task; 20 participants (non-collar, n?=?10; collar, n?=?12) completed resting-state fMRI. Key findings from the working memory analysis include significantly increased fMRI brain activation in the right insular, right superior temporal pole, right inferior frontal gyrus, and pars orbitalis post-training for the non-collar group (p?<?0.05, threshold-free cluster enhancement corrected), but no changes were noted for the collar group. The elevation in fMRI activation in the non-collar group was found to correlate significantly (n?=?7, r?=?0.943, p?=?0.001) with average peak impulse amplitude experienced during the training. In the resting-state fMRI analysis, significant pre- to post-training increase in connectivity between the auditory network and two discrete regions (left middle frontal gyrus and left superior lateral occipital/angular gyri) was found in the non-collar group, while no change was observed in the collar group. These data provided initial evidence of the impact of low-level blast on working memory and auditory network connectivity as well as the protective effect of collar on brain function following blast exposure, and is congruent with previous collar findings in sport-related traumatic brain injury

Entrainment to a real time fractal visual stimulus modulates fractal gait dynamics

Fractal patterns characterize healthy biological systems and are considered to reflect the ability of the system to adapt to varying environmental conditions. Previous research has shown that fractal patterns in gait are altered following natural aging or disease, and this has potential negative consequences for gait adaptability that can lead to increased risk of injury. However, the flexibility of a healthy neurological system to exhibit different fractal patterns in gait has yet to be explored, and this is a necessary step toward understanding human locomotor control. Fifteen participants walked for 15 min on a treadmill, either in the absence of a visual stimulus or while they attempted to couple the timing of their gait with a visual metronome that exhibited a persistent fractal pattern (contained long-range correlations) or a random pattern (contained no long-range correlations). The stride-to-stride intervals of the participants were recorded via analog foot pressure switches and submitted to detrended fluctuation analysis (DFA) to determine if the fractal patterns during the visual metronome conditions differed from the baseline (no metronome) condition. DFA a in the baseline condition was 0.77 ± 0.09. The fractal patterns in the stride-to-stride intervals were significantly altered when walking to the fractal metronome (DFA a = 0.87 ± 0.06) and to the random metronome (DFA a = 0.61 ± 0.10) (both p < .05 when compared to the baseline condition), indicating that a global change in gait dynamics was observed. A variety of strategies were identified at the local level with a cross-correlation analysis, indicating that local behavior did not account for the consistent global changes. Collectively, the results show that a gait dynamics can be shifted in a prescribed manner using a visual stimulus and the shift appears to be a global phenomenon

Characteristics of Stride Behavior During Treadmill Walking and Stationary Stepping

Much has been learned about the characteristics of gait in overground and treadmill walking. However, there are many contexts in which overground or treadmill walking might not be possible, such as in home-based physical therapy. In those cases, a surrogate task to index gait behavior would be a valuable tool. Thus, the purpose of this study was to evaluate the stride behavior characteristics of stationary stepping compared with treadmill walking. Healthy young adults (N = 10) preformed two 15-minute tasks: (1) treadmill walking and (2) stationary stepping. Several stride behavior characteristics were recorded, including the number of strides taken, minimum and maximum knee angle, stride interval mean, stride interval standard deviation, and detrended fluctuation analysis (DFA) alpha of the stride interval time series. The results showed that stride behavior was similar between tasks when examined at the group level. However, when individual level analyses were used to examine the reliability of each metric between tasks, poor reliability was observed in most metrics, indicating that stationary stepping may not be an appropriate surrogate task for overground or treadmill walking. These results are discussed in the context of a gait dynamics framework, with attention to task constraints that may have influenced the findings

Relationship between changes in vestibular sensory reweighting & postural control complexity

Complexity measures have become increasingly prominent in the postural control literature. Several studies have found associations between clinical balance improvements and complexity, but the relationship between sensory reweighting and complexity changes has remained unobserved. The purpose of this study was to determine the relationship between sensory reweighting via Wii Fit balance training and complexity. Twenty healthy adults completed 6 weeks of training. Participants completed the sensory organization test (SOT) before and after the sessions. Complexity of postural control was analyzed through sample entropy of the center-of-pressure velocity time series in the resultant, anterior–posterior (AP), and medial–lateral directions, and compared to SOT summary score changes. Significant differences were found between pre- and post-training for the condition five (p < .001, d = .525) and vestibular summary scores (p < .001, d = .611). Similarly, changes in complexity were observed from pre- to post-training in the resultant (p = .040, d = .427) direction. While the AP velocity was not significant (p = .07, d = .355), its effect size was moderate. A moderate correlation was revealed in the posttest between AP complexity and condition 5 (r = .442, p = .05), as well as between AP complexity and the vestibular summary score (r = .351, p = .13). The results of this study show that a moderate relationship exists between postural control complexity and the vestibular system, suggesting that complexity may reflect the neurosensory organization used to maintain upright stance

Visual exteroceptive information provided during obstacle crossing did not modify the lower limb trajectory

The roles of visual exteroception (information regarding environmental characteristics) and exproprioception (the relation of body segments to the environment) during gait adaptation are not fully understood. The purpose of this study was to determine how visual exteroception regarding obstacle characteristics provided during obstacle crossing modified foot elevation and placement with and without lower limb-obstacle visual exproprioception (manipulated with goggles). Visual exteroceptive information was provided by an obstacle cue – a second obstacle identical to the obstacle that was stepped over –— which was visible during crossing. Ten subjects walked over obstacles under four visual conditions: full vision with no obstacle height cue, full vision with an obstacle height cue, goggles with no obstacle height cue and goggles with an obstacle height cue. Obstacle heights were 2, 10, 20 and 30 cm. The presence of goggles increased horizontal distance (distance between foot and obstacle at foot placement), toe clearance and toe clearance variability. The presence of the obstacle height cue did not alter horizontal distance, toe clearance or toe clearance variability. These observations strengthen the argument that it is the visual exproprioceptive information, not visual exteroceptive information, that is used on-line to fine tune the lower limb trajectory during obstacle avoidance

Gait Performance is not Influenced by Working Memory When Walking at a Self-selected Pace

Gait performance exhibits patterns within the stride-to-stride variability that can be indexed using detrended fluctuation analysis (DFA). Previous work employing DFA has shown that gait patterns can be influenced by constraints, such as natural aging or disease, and they are informative regarding a person’s functional ability. Many activities of daily living require concurrent performance in the cognitive and gait domains; specifically working memory is commonly engaged while walking, which is considered dual-tasking. It is unknown if taxing working memory while walking influences gait performance as assessed by DFA. This study used a dual-tasking paradigm to determine if performance decrements are observed in gait or working memory when performed concurrently. Healthy young participants (N = 16) performed a working memory task (automated operation span task) and a gait task (walking at a self-selected speed on a treadmill) in single- and dual-task conditions. A second dual-task condition (reading while walking) was included to control for visual attention, but also introduced a task that taxed working memory over the long term. All trials involving gait lasted at least 10 min. Performance in the working memory task was indexed using five dependent variables (absolute score, partial score, speed error, accuracy error, and math error), while gait performance was indexed by quantifying the mean, standard deviation, and DFA a of the stride interval time series. Two multivariate analyses of variance (one for gait and one for working memory) were used to examine performance in the single- and dual-task conditions. No differences were observed in any of the gait or working memory dependent variables as a function of task condition. The results suggest the locomotor system is adaptive enough to complete a working memory task without compromising gait performance when walking at a self-selected pace