Frequency dependence of the action-perception cycle for postural control in a moving visual environment: relative phase dynamics

When standing human subjects are exposed to a moving visual environment, the induced postural sway displays varying degrees of coherence with the visual information. In our experiment we varied the frequency of an oscillatory visual display and analysed the temporal relationship between visual motion and sway. We found that subjects maintain sizeable sway amplitudes even as temporal coherence with the display is lost. Postural sway tended to phase lead (for frequencies below 0.2 Hz) or phase lag (above 0.3 Hz). However, we also observed at a fixed frequency, highly variable phase relationships in which a preferred range of phase lags is prevalent, but phase jumps occur that return the system into the preferred range after phase has begun drifting out of the preferred regime. By comparing the results quantitatively with a dynamical model (the sine-circle map), we show that this effect can be understood as a form of relative coordination and arises through an instability of the dynamics of the action-perception cycle. Because such instabilities cannot arise in passively driven systems, we conclude that postural sway in this situation is actively generated as rhythmic movement which is coupled dynamically to the visual motion. Received: 7 September 1993/Accepted in revised form: 2 May 1994     

Comparing internal models of the dynamics of the visual environment

It is well known that the human postural control system responds to motion of the visual scene, but the implicit assumptions it makes about the visual environment and what quantities, if any, it estimates about the visual environment are unknown. This study compares the behavior of four models of the human postural control system to experimental data. Three include internal models that estimate the state of the visual environment, implicitly assuming its dynamics to be that of a linear stochastic process (respectively, a random walk, a general first-order process, and a general second-order process). In each case, all of the coefficients that describe the process are estimated by an adaptive scheme based on maximum likelihood. The fourth model does not estimate the state of the visual environment. It adjusts sensory weights to minimize the mean square of the control signal without making any specific assumptions about the dynamic properties of the environmental motion.We find that both having an internal model of the visual environment and its type make a significant difference in how the postural system responds to motion of the visual scene. Notably, the second-order process model outperforms the human postural system in its response to sinusoidal stimulation. Specifically, the second-order process model can correctly identify the frequency of the stimulus and completely compensate so that the motion of the visual scene has no effect on sway. In this case the postural control system extracts the same information from the visual modality as it does when the visual scene is stationary. The fourth model that does not simulate the motion of the visual environment is the only one that reproduces the experimentally observed result that, across different frequencies of sinusoidal stimulation, the gain with respect to the stimulus drops as the amplitude of the stimulus increases but the phase remains roughly constant. Our results suggest that the human postural control system does not estimate the state of the visual environment to respond to sinusoidal stimuli.     

Relationship between Spectral Characteristics of Spontaneous Postural Sway and Motion Sickness Susceptibility

Motion sickness (MS) usually occurs for a narrow band of frequencies of the imposed oscillation. It happens that this frequency band is close to that which are spontaneously produced by postural sway during natural stance. This study examined the relationship between reported susceptibility to motion sickness and postural control. The hypothesis is that the level of MS can be inferred from the shape of the Power Spectral Density (PSD) profile of spontaneous sway, as measured by the displacement of the center of mass during stationary, upright stance. In Experiment 1, postural fluctuations while standing quietly were related to MS history for inertial motion. In Experiment 2, postural stability measures registered before the onset of a visual roll movement were related to MS symptoms following the visual stimulation. Study of spectral characteristics in postural control showed differences in the distribution of energy along the power spectrum of the antero-posterior sway signal. Participants with MS history provoked by exposure to inertial motion showed a stronger contribution of the high frequency components of the sway signal. When MS was visually triggered, sick participants showed more postural sway in the low frequency range. The results suggest that subject-specific PSD details may be a predictor of the MS level. Furthermore, the analysis of the sway frequency spectrum provided insight into the intersubject differences in the use of postural control subsystems. The relationship observed between MS susceptibility and spontaneous posture is discussed in terms of postural sensory weighting and in relation to the nature of the provocative stimulus.     

Modeling the Dynamics of Sensory Reweighting

Reweighting sensory information adaptively is considered critical for flexible postural control, but little is known of the time scale of the reweighting process. We analyzed the transient dynamics of sensory reweighting in a previously published nonlinear adaptive model of sensory integration in the human postural control system. The model’s dynamics of adaptation were tested in response to abrupt changes in the amplitude of the motion of the visual surround. In addition to qualitatively reproducing the correct asymptotic response to such changes in visual amplitude, as previously found, the model qualitatively reproduced the asymmetric transient response elucidated in recent experiments (Oie et al. in Gait Posture 2005). In particular, the model adapts at an initially rapid rate to a switch from low to high amplitude visual motion, but at an initially slower rate upon the return to low amplitude motion. The observed temporal asymmetry has potential functional value. Rapid downweighting of a visual stimulus that suddenly increases is necessary to prevent loss of upright equilibrium. A visual stimulus that decreases in amplitude does not pose a threat to upright balance, allowing for slower upweighting without functional consequence.     

Postural control in bipolar disorder: increased sway area and decreased dynamical complexity

Structural, neurochemical, and functional abnormalities have been identified in the brains of individuals with bipolar disorder, including in key brain structures implicated in postural control, i.e. the cerebellum, brainstem, and basal ganglia. Given these findings, we tested the hypothesis that postural control deficits are present in individuals with bipolar disorder. Sixteen participants with bipolar disorder (BD) and 16 age-matched non-psychiatric healthy controls were asked to stand as still as possible on a force platform for 2 minutes under 4 conditions: (1) eyes open-open base; (2) eyes closed-open base; (3) eyes open-closed base; and (4) eyes closed-closed base. Postural sway data were submitted to conventional quantitative analyses of the magnitude of sway area using the center of pressure measurement. In addition, data were submitted to detrended fluctuation analysis, a nonlinear dynamical systems analytic technique that measures complexity of a time-series, on both the anterior-posterior and medio-lateral directions. The bipolar disorder group had increased sway area, indicative of reduced postural control. Decreased complexity in the medio-lateral direction was also observed for the bipolar disorder group, suggesting both a reduction in dynamic range available to them for postural control, and that their postural corrections were primarily dominated by longer time-scales. On both of these measures, significant interactions between diagnostic group and visual condition were also observed, suggesting that the BD participants were impaired in their ability to make corrections to their sway pattern when no visual information was available. Greater sway magnitude and reduced complexity suggest that individuals with bipolar disorder have deficits in sensorimotor integration and a reduced range of timescales available on which to make postural corrections.     

Modeling human postural sway using an intermittent control and hemodynamic perturbations

Ground reaction force during human quiet stance is modulated synchronously with the cardiac cycle through hemodynamics [1]. This almost periodic hemodynamic force induces a small disturbance torque to the ankle joint, which is considered as a source of endogenous perturbation that induces postural sway. Here we consider postural sway dynamics of an inverted pendulum model with an intermittent control strategy, in comparison with the traditional continuous-time feedback controller. We examine whether each control model can exhibit human-like postural sway, characterized by its power law behavior at the low frequency band 0.1–0.7 Hz, when it is weakly perturbed by periodic and/or random forcing mimicking the hemodynamic perturbation. We show that the continuous control model with typical feedback gain parameters hardly exhibits the human-like sway pattern, in contrast with the intermittent control model. Further analyses suggest that deterministic, including chaotic, slow oscillations that characterize the intermittent control strategy, together with the small hemodynamic perturbation, could be a possible mechanism for generating the postural sway.     

Assessment of influence of breath holding and hyperventilation on human postural stability with spectral analysis of stabilographic signal

The influence of breath holding and voluntary hyperventilation on the traditional stabilometric parameters and the frequency characteristics of stabilographic signal was studied. We measured the stabilometric parameters on a force platform (“Ritm”, Russia) in the 107 healthy volunteers during quiet breath, voluntary hyperventilation (20 seconds) and maximal inspiratory breath holding (20 seconds). Respiratory frequency, respiratory amplitude and ventilation were estimated with the strain gauge. We found that antero-posterior and medio-lateral sway amplitude and velocity as well as sway surface during breath holding and during quiet breathing were the same, so breath holding didn’t influence the postural stability. However, the spectral parameters in the antero-posterior direction shifted to the high frequency range due to an alteration of the respiratory muscles’ contractions during breath holding versus quiet breath. Voluntary hyperventilation caused a significant increase of all stabilographic indices that implied an impairment of the postural stability. We also found that the spectral indices shifted toward the high-frequency range, and this shift was much greater compared to that during breath holding. Besides, amplitudes of the spectral peaks also increased. Perhaps, such change of the spectral indices was due to distortion of the proprioceptive information because of increased excitability of the nerve fibers during hyperventilation. Maximal inspiratory breath holding caused an activation of the postural control mechanisms. It was manifested as an elevation of the sway oscillations’ frequency with no postural stability changes. Hyperventilation led to the greatest strain of the postural control and to a decrease of the postural stability, which was manifested as an increase of center of pressure oscillations’ amplitude and frequency.     

Dynamic theory of action-perception patterns: the “moving room” paradigm

Action-perception patterns are studied theoretically in terms of equations of motion that capture the coordination capacity of the nervous system. We consider intrinsic dynamics in the absence of visual information that contain a single posture state as a fixed point attractor. We couple these intrinsic dynamics to visual information that stabilizes posture in the visual world. This leads to a theory of postural sway induced by an optic flow field (moving room paradigm). The optic flow is parametrized in a simplest approximation by the expansion rate of a relevant perceptual target. We show how temporal stability as the key concept of this theory can lead to prediction and serve as a measure of perceptual coupling. Finally, we discuss the relation of the present theory to biological cybernetics.     

Shannon and Renyi entropies to classify effects of Mild Traumatic Brain Injury on postural sway

Background

Mild Traumatic Brain Injury (mTBI) has been identified as a major public and military health concern both in the United States and worldwide. Characterizing the effects of mTBI on postural sway could be an important tool for assessing recovery from the injury.

Methodology/Principal Findings

We assess postural sway by motion of the center of pressure (COP). Methods for data reduction include calculation of area of COP and fractal analysis of COP motion time courses. We found that fractal scaling appears applicable to sway power above about 0.5 Hz, thus fractal characterization is only quantifying the secondary effects (a small fraction of total power) in the sway time series, and is not effective in quantifying long-term effects of mTBI on postural sway. We also found that the area of COP sensitively depends on the length of data series over which the COP is obtained. These weaknesses motivated us to use instead Shannon and Renyi entropies to assess postural instability following mTBI. These entropy measures have a number of appealing properties, including capacity for determination of the optimal length of the time series for analysis and a new interpretation of the area of COP.

Conclusions

Entropy analysis can readily detect postural instability in athletes at least 10 days post-concussion so that it appears promising as a sensitive measure of effects of mTBI on postural sway.

Availability

The programs for analyses may be obtained from the authors.     

Coupling of posture and gait: mode locking and parametric excitation

 We investigate the temporal coordination of human gait and posture and infer the nature of their coupling. Participants viewed a sinusoidally oscillating visual display which induced medial-lateral postural sway during treadmill walking, while display frequency was varied (0.075–1.025 Hz). First, postural responses exhibited the usual low-pass characteristic but with an additional resonance peak near the preferred stride frequency, although shifted downward by 0.12 Hz; this provides evidence of a coupling from gait to posture. Second, the step cycle adapted to mode lock with the visual driver and postural sway, as well as displaying instances of intermittency (slipping in and out of phase) and quasiperiodicity (phase wandering); this provides evidence of a coupling from posture to gait. We observed a spectrum of integer mode locks, including a large 1:1 trapping region about the stride frequency and superharmonic entrainment (stride frequency > driver frequency) at lower driver frequencies. A coupled-oscillator model that incorporates a novel parametric coupling from posture to the gait “stiffness” term reproduces these features of the data, including the resonance peak shift. Biological coordination patterns may thus emerge naturally as properties of a system of appropriately coupled oscillators. Received: 23 June 1999 / Accepted in revised form: 10 January 2001     

Unintentional Interpersonal Synchronization Represented as a Reciprocal Visuo-Postural Feedback System: A Multivariate Autoregressive Modeling Approach

People’s behaviors synchronize. It is difficult, however, to determine whether synchronized behaviors occur in a mutual direction—two individuals influencing one another—or in one direction—one individual leading the other, and what the underlying mechanism for synchronization is. To answer these questions, we hypothesized a non-leader-follower postural sway synchronization, caused by a reciprocal visuo-postural feedback system operating on pairs of individuals, and tested that hypothesis both experimentally and via simulation. In the behavioral experiment, 22 participant pairs stood face to face either 20 or 70 cm away from each other wearing glasses with or without vision blocking lenses. The existence and direction of visual information exchanged between pairs of participants were systematically manipulated. The time series data for the postural sway of these pairs were recorded and analyzed with cross correlation and causality. Results of cross correlation showed that postural sway of paired participants was synchronized, with a shorter time lag when participant pairs could see one another’s head motion than when one of the participants was blindfolded. In addition, there was less of a time lag in the observed synchronization when the distance between participant pairs was smaller. As for the causality analysis, noise contribution ratio (NCR), the measure of influence using a multivariate autoregressive model, was also computed to identify the degree to which one’s postural sway is explained by that of the other’s and how visual information (sighted vs. blindfolded) interacts with paired participants’ postural sway. It was found that for synchronization to take place, it is crucial that paired participants be sighted and exert equal influence on one another by simultaneously exchanging visual information. Furthermore, a simulation for the proposed system with a wider range of visual input showed a pattern of results similar to the behavioral results.     

Interaction between Depth Order and Density Affects Vection and Postural Sway

Objective

Vection, a feeling of self-motion while being physically stationary, and postural sway can be modulated by various visual factors. Moreover, vection and postural sway are often found to be closely related when modulated by such visual factors, suggesting a common neural mechanism. One well-known visual factor is the depth order of the stimulus. The density, i.e. number of objects per unit area, is proposed to interact with the depth order in the modulation of vection and postural sway, which has only been studied to a limited degree.

Methods

We therefore exposed 17 participants to 18 different stimuli containing a stationary pattern and a pattern rotating around the naso-occipital axis. The density of both patterns was varied between 10 and 90%; the densities combined always added up to 100%. The rotating pattern occluded or was occluded by the stationary pattern, suggesting foreground or background motion, respectively. During pattern rotation participants reported vection by pressing a button, and postural sway was recorded using a force plate.

Results

Participants always reported more vection and swayed significantly more when rotation was perceived in the background and when the rotating pattern increased in density. As hypothesized, we found that the perceived depth order interacted with pattern density. A pattern rotating in the background with a density between 60 and 80% caused significantly more vection and postural sway than when it was perceived to rotate in the foreground.

Conclusions

The findings suggest that the ratio between fore- and background pattern densities is an important factor in the interaction with the depth order, and it is not the density of rotating pattern per se. Moreover, the observation that vection and postural sway were modulated in a similar way points towards a common neural origin regulating both variables.     

Quality of Visual Cue Affects Visual Reweighting in Quiet Standing

Sensory reweighting is a characteristic of postural control functioning adopted to accommodate environmental changes. The use of mono or binocular cues induces visual reduction/increment of moving room influences on postural sway, suggesting a visual reweighting due to the quality of available sensory cues. Because in our previous study visual conditions were set before each trial, participants could adjust the weight of the different sensory systems in an anticipatory manner based upon the reduction in quality of the visual information. Nevertheless, in daily situations this adjustment is a dynamical process and occurs during ongoing movement. The purpose of this study was to examine the effect of visual transitions in the coupling between visual information and body sway in two different distances from the front wall of a moving room. Eleven young adults stood upright inside of a moving room in two distances (75 and 150 cm) wearing a liquid crystal lenses goggles, which allow individual lenses transition from opaque to transparent and vice-versa. Participants stood still during five minutes for each trial and the lenses status changed every one minute (no vision to binocular vision, no vision to monocular vision, binocular vision to monocular vision, and vice-versa). Results showed that farther distance and monocular vision reduced the effect of visual manipulation on postural sway. The effect of visual transition was condition dependent, with a stronger effect when transitions involved binocular vision than monocular vision. Based upon these results, we conclude that the increased distance from the front wall of the room reduced the effect of visual manipulation on postural sway and that sensory reweighting is stimulus quality dependent, with binocular vision producing a much stronger down/up-weighting than monocular vision.     

Modulation of Visually Evoked Postural Responses by Contextual Visual,Haptic and Auditory Information: A ‘Virtual Reality Check’

Externally generated visual motion signals can cause the illusion of self-motion in space (vection) and corresponding visually evoked postural responses (VEPR). These VEPRs are not simple responses to optokinetic stimulation, but are modulated by the configuration of the environment. The aim of this paper is to explore what factors modulate VEPRs in a high quality virtual reality (VR) environment where real and virtual foreground objects served as static visual, auditory and haptic reference points. Data from four experiments on visually evoked postural responses show that: 1) visually evoked postural sway in the lateral direction is modulated by the presence of static anchor points that can be haptic, visual and auditory reference signals; 2) real objects and their matching virtual reality representations as visual anchors have different effects on postural sway; 3) visual motion in the anterior-posterior plane induces robust postural responses that are not modulated by the presence of reference signals or the reality of objects that can serve as visual anchors in the scene. We conclude that automatic postural responses for laterally moving visual stimuli are strongly influenced by the configuration and interpretation of the environment and draw on multisensory representations. Different postural responses were observed for real and virtual visual reference objects. On the basis that automatic visually evoked postural responses in high fidelity virtual environments should mimic those seen in real situations we propose to use the observed effect as a robust objective test for presence and fidelity in VR.     

Motor deficits in schizophrenia quantified by nonlinear analysis of postural sway

Motor dysfunction is a consistently reported but understudied aspect of schizophrenia. Postural sway area was examined in individuals with schizophrenia under four conditions with different amounts of visual and proprioceptive feedback: eyes open or closed and feet together or shoulder width apart. The nonlinear complexity of postural sway was assessed by detrended fluctuation analysis (DFA). The schizophrenia group (n = 27) exhibited greater sway area compared to controls (n = 37). Participants with schizophrenia showed increased sway area following the removal of visual input, while this pattern was absent in controls. Examination of DFA revealed decreased complexity of postural sway and abnormal changes in complexity upon removal of visual input in individuals with schizophrenia. Additionally, less complex postural sway was associated with increased symptom severity in participants with schizophrenia. Given the critical involvement of the cerebellum and related circuits in postural stability and sensorimotor integration, these results are consistent with growing evidence of motor, cerebellar, and sensory integration dysfunction in the disorder, and with theoretical models that implicate cerebellar deficits and more general disconnection of function in schizophrenia.     

Physiological complexity and system adaptability: evidence from postural control dynamics of older adults

The degree of multiscale complexity in human behavioral regulation, such as that required for postural control, appears to decrease with advanced aging or disease. To help delineate causes and functional consequences of complexity loss, we examined the effects of visual and somatosensory impairment on the complexity of postural sway during quiet standing and its relationship to postural adaptation to cognitive dual tasking. Participants of the MOBILIZE Boston Study were classified into mutually exclusive groups: controls [intact vision and foot somatosensation, n = 299, 76 ± 5 (SD) yr old], visual impairment only (<20/40 vision, n = 81, 77 ± 4 yr old), somatosensory impairment only (inability to perceive 5.07 monofilament on plantar halluxes, n = 48, 80 ± 5 yr old), and combined impairments (n = 25, 80 ± 4 yr old). Postural sway (i.e., center-of-pressure) dynamics were assessed during quiet standing and cognitive dual tasking, and a complexity index was quantified using multiscale entropy analysis. Postural sway speed and area, which did not correlate with complexity, were also computed. During quiet standing, the complexity index (mean ± SD) was highest in controls (9.5 ± 1.2) and successively lower in the visual (9.1 ± 1.1), somatosensory (8.6 ± 1.6), and combined (7.8 ± 1.3) impairment groups (P = 0.001). Dual tasking resulted in increased sway speed and area but reduced complexity (P < 0.01). Lower complexity during quiet standing correlated with greater absolute (R = -0.34, P = 0.002) and percent (R = -0.45, P < 0.001) increases in postural sway speed from quiet standing to dual-tasking conditions. Sensory impairments contributed to decreased postural sway complexity, which reflected reduced adaptive capacity of the postural control system. Relatively low baseline complexity may, therefore, indicate control systems that are more vulnerable to cognitive and other stressors.     

Getting Your Sea Legs

Sea travel mandates changes in the control of the body. The process by which we adapt bodily control to life at sea is known as getting one''s sea legs. We conducted the first experimental study of bodily control as maritime novices adapted to motion of a ship at sea. We evaluated postural activity (stance width, stance angle, and the kinematics of body sway) before and during a sea voyage. In addition, we evaluated the role of the visible horizon in the control of body sway. Finally, we related data on postural activity to two subjective experiences that are associated with sea travel; seasickness, and mal de debarquement. Our results revealed rapid changes in postural activity among novices at sea. Before the beginning of the voyage, the temporal dynamics of body sway differed among participants as a function of their (subsequent) severity of seasickness. Body sway measured at sea differed among participants as a function of their (subsequent) experience of mal de debarquement. We discuss implications of these results for general theories of the perception and control of bodily orientation, for the etiology of motion sickness, and for general phenomena of perceptual-motor adaptation and learning.     

Ankle intrinsic stiffness changes with postural sway

In standing, the human body is inherently unstable and its stabilization requires constant regulation of ankle torque, generated by a combination of ankle intrinsic properties, peripheral reflexes, and central contributions. Ankle intrinsic stiffness, which quantifies the joint intrinsic properties, has been usually assumed constant in standing; however, there is strong evidence that it is highly dependent on the joint torque, which changes significantly with sway in stance. In this study, we examined how ankle intrinsic stiffness changes with postural sway during standing. Ten subjects stood on a standing apparatus, while subjected to pulse perturbations of ankle position. The mean torque of a short period before the start of each pulse was used as a measure of background torque. Responses with similar background torques were grouped together and used to estimate the parameters of an intrinsic stiffness model. Stiffness estimates were normalized to the critical stiffness and the background torque was transformed to the center of pressure location. We found that in most subjects, the normalized stiffness increased linearly with the movement of center of pressure towards the toes, with an average slope of 2.11 ± 0.80 1/m·rad. This modulation of ankle intrinsic stiffness seems functionally appropriate, since the intrinsic stiffness increases quickly, as the center of pressure moves toward the toes and the limits of stability. These large changes of ankle intrinsic stiffness with postural sway must be incorporated in any model of stance control.     

Specific and Nonspecific Visual Influences on the Stability of the Vertical Posture in Humans

We studied physiological mechanisms of vision-related stabilization of the vertical posture in humans using a stabilographic technique; spontaneous deviations of the projection of the center of gravity during quiet stance and magnitudes of the postural response to vibratory stimulation of proprioceptors of the lower leg muscles under varied conditions of visual control were measured. The stability of quiet stance, as estimated according to the root mean square value of the sagittal component of the stabilogram, was the best with eyes open. Vibration-induced postural responses were the smallest also under these conditions. Spontaneous postural sway and the amplitude of response to vibratory stimulation increased when only a central sector of visual field (20 ang. deg) was preserved and, especially, under conditions of closed eyes and horizontal inversion of visual perception using prismatic spectacles. Parallel changes in the quantitative stabilographic indices and amplitude of vibration-induced postural responses show that the intensity of the latter is probably determined by the background stiffness of the musculoskeletal system. We tried to estimate separately the contributions of the stiffness factor, on the one hand, and specific visual influences, on the other hand, by testing the parameters of quiet stance and postural responses under conditions of standing while lightly touching a support with the index finger. We found that the influence of the conditions of visual control on the stability of quiet stance while touching the support was eliminated. At the same time, the magnitude of postural responses to vibratory stimulation decreased but, nonetheless, changed with visual conditions in the same manner as when standing without additional support. We conclude that vision performs a dual function in the control of the vertical posture; it forms the basis for the spatial reference system and serves the source of information on the movements of one's body.     

Vestibular postural control model

Current models for physiological components and a posture control experiment conducted with three normal subjects form the basis for a model which seeks to describe quantitatively the control of body sway when only vestibular motion cues are used. Emphasis is placed on delineating the relative functional roles of the linear and the angular acceleration sensors and on modeling the functional interface between these sensors and the initiation of compensatory responses at the ankle joint.The model predicts the form of the postural response to a small sway disturbance; including initial detection of sway, characteristics of the transient correction, and maintenance of stability. The model suggests that postural stability requires a short time constant integration of semicircular canal output. Separation of semicircular canal and utricular otolith function into sway motion detector and static reference sensors respectively is demonstrated.This work was supported by NASA under Grant NGR-22-009-156.