The Throw-and-Catch Model of Human Gait: Evidence from Coupling of Pre-Step Postural Activity and Step Location

Postural activity normally precedes the lift of a foot from the ground when taking a step, but its function is unclear. The throw-and-catch hypothesis of human gait proposes that the pre-step activity is organized to generate momentum for the body to fall ballistically along a specific trajectory during the step. The trajectory is appropriate for the stepping foot to land at its intended location while at the same time being optimally placed to catch the body and regain balance. The hypothesis therefore predicts a strong coupling between the pre-step activity and step location. Here we examine this coupling when stepping to visually-presented targets at different locations. Ten healthy, young subjects were instructed to step as accurately as possible onto targets placed in five locations that required either different step directions or different step lengths. In 75% of trials, the target location remained constant throughout the step. In the remaining 25% of trials, the intended step location was changed by making the target jump to a new location 96 ms ± 43 ms after initiation of the pre-step activity, long before foot lift. As predicted by the throw-and-catch hypothesis, when the target location remained constant, the pre-step activity led to body momentum at foot lift that was coupled to the intended step location. When the target location jumped, the pre-step activity was adjusted (median latency 223 ms) and prolonged (on average by 69 ms), which altered the body’s momentum at foot lift according to where the target had moved. We conclude that whenever possible the coupling between the pre-step activity and the step location is maintained. This provides further support for the throw-and-catch hypothesis of human gait

Sensorimotor processing for balance in spinocerebellar ataxia type 6.

We investigated whether balance impairments caused by cerebellar disease are associated with specific sensorimotor processing deficits that generalize across all sensory modalities. Experiments focused on the putative cerebellar functions of scaling and coordinate transformation of balance responses evoked by stimulation of single sensory channels. Vestibular, visual, and proprioceptive sensory channels were stimulated in isolation using galvanic vestibular stimulation, moving visual scenery, and muscle vibration, respectively, in 16 subjects with spinocerebellar ataxia type 6 (SCA6) and 16 matched healthy controls. Two polarities of each stimulus type evoked postural responses of similar form in the forward and backward directions. Disease severity was assessed using the Scale for Assessment and Rating of Ataxia. Impaired balance of SCA6 subjects during unperturbed stance was reflected in faster than normal body sway (P = 0.009), which correlated with disease severity (r = 0.705, P < 0.001). Sensory perturbations revealed a sensorimotor processing abnormality that was specific to response scaling for the visual channel. This manifested as visually evoked postural responses that were approximately three times larger than normal (backward, P < 0.001; forward P = 0.005) and correlated with disease severity (r = 0.543, P = 0.03). Response direction and habituation properties were no different from controls for all three sensory modalities. Cerebellar degeneration disturbs the scaling of postural responses evoked by visual motion, possibly through disinhibition of extracerebellar visuomotor centers. The excessively high gain of the visuomotor channel without compensatory decreases in gains of other sensorimotor channels provides a potential mechanism for instability of the balance control system in cerebellar disease. © 2015 International Parkinson and Movement Disorder Society

Asymmetry of balance responses to monaural galvanic vestibular stimulation in subjects with vestibular schwannoma

OBJECTIVE: We investigated the potential of galvanic vestibular stimulation (GVS) to quantify lateralised asymmetry of the vestibulospinal pathways by measuring balance responses to monaural GVS in 10 subjects with vestibular schwannoma and 22 healthy control subjects. METHODS: Subjects standing without vision were stimulated with 3s, 1mA direct current stimuli delivered monaurally. The mean magnitude and direction of the evoked balance responses in the horizontal plane were measured from ground-reaction forces and from displacement and velocity of the trunk. Vestibular-evoked myogenic potentials (VEMPs) to 500Hz air and bone-conducted tones were also recorded. RESULTS: In healthy subjects, the magnitudes of the force, velocity and displacement responses were not significantly different for left compared to right ear stimulation. Their individual asymmetry ratios were always <30%. Subjects with vestibular schwannoma had significantly smaller force, velocity and displacement responses to stimulation of the affected compared with non-affected ear. Their mean asymmetry ratios were significantly elevated for all three measures (41.2±10.3%, 40.3±15.1% and 21.9±14.6%). CONCLUSIONS: Asymmetry ratios of balance responses to monaural GVS provide a quantitative and clinically applicable lateralising test of the vestibulospinal pathways. SIGNIFICANCE: This method offers a more clinically relevant measure of standing balance than existing vestibular function tests which assess only vestibuloocular and vestibulocollic pathways

Violation of the Craniocentricity Principle for Vestibularly Evoked Balance Responses under Conditions of Anisotropic Stability.

The balance response direction to electrically evoked vestibular perturbation is closely tied to head orientation. Such craniocentric response organization is expected of a simple error correction process. Here we ask whether this is maintained when the body is made more stable, but with the stability being greater in one direction than another. Since it is known that vestibularly evoked balance responses become smaller as body stability increases, the following two outcomes are possible: (1) response magnitude is attenuated, but with craniocentricity maintained; and (2) anisotropy of stability is considered such that components of the response are differentially attenuated, which would violate a craniocentric organizing principle. We tested these alternatives by measuring the direction of balance responses to electrical vestibular stimulation across a range of head orientations and stance widths in healthy humans. With feet together, the response was highly craniocentric. However, when stance width was increased so that the body was more stable in the frontal plane, response direction became biased toward the sagittal direction. This resulted in a nonlinear relationship between head orientation and response direction. While stance width changes the mechanical state of the body, the effect was also present when lateral light touch was used to produce anisotropy in stability, demonstrating that a significantly altered mechanical state was not crucial. We conclude that the balance system does not simply act according to the direction of vestibular input. Instead, it appears to assign greater relevance to components of vestibular input acting in the plane of lesser body stability than the plane of greater body stability, and acts accordingly

Altered visual and haptic verticality perception in posterior cortical atrophy and Alzheimer's disease

There is increasing theoretical and empirical support for the brain combining multisensory information to determine the direction of gravity and hence uprightness. A fundamental part of the process is the spatial transformation of sensory signals between reference frames: eye-centred, head-centred, body-centred, etc. The question ‘Am I the right way up?’ posed by a patient with posterior cortical atrophy (PCA) suggests disturbances in upright perception, subsequently investigated in PCA and typical Alzheimer's disease (tAD) based on what looks or feels upright. Participants repeatedly aligned to vertical a rod presented either visually (visual-vertical) or haptically (haptic-vertical). Visual-vertical involved orienting a projected rod presented without or with a visual orientation cue (circle, tilted square (±18°)). Haptic-vertical involved orientating a grasped rod with eyes closed using a combination of side (left, right) and hand (unimanual, bimanual) configurations. Intraindividual uncertainty and bias defined verticality perception. Uncertainty was consistently greater in both patient groups than in control groups, and greater in PCA than tAD. Bias in the frontal plane was strongly directionally affected by visual cue tilt (visual-vertical) and grip side (haptic-vertical). A model was developed that assumed verticality information from multiple sources is combined in a statistically optimal way to produce observed uncertainties and biases. Model results suggest the mechanism that spatially transforms graviceptive information between body parts is disturbed in both patient groups. Despite visual dysfunction being typically considered the primary feature of PCA, disturbances were greater in PCA than tAD particularly for haptic-vertical, and are considered in light of posterior parietal vulnerability

Modifying one’s hand’s trajectory when a moving target’s orientation changes

The path that the hand takes to intercept an elongated moving target depends on the target’s orientation. How quickly do people respond to changes in the moving target’s orientation? In the present study, participants were asked to intercept moving targets that sometimes abruptly changed orientation shortly after they started moving. It took the participants slightly more than 150 ms to adjust their hands’ paths to a change in target orientation. This is about 50 ms longer than it took them to respond to a 5-mm jump in the moving target’s position. It is only slightly shorter than it took them to initiate the movement. We propose that responses to changes in visually perceived orientation are not exceptionally fast, because there is no relationship between target orientation and direction of hand movement that is sufficiently general in everyday life for one to risk making an inappropriate response in order to respond faster