Pronounced overestimation of support surface tilt during stance

A veridical internal notion of the kinematic state of the foot support is essential for postural control. The means by which this is obtained is still a matter of debate. We therefore measured the conscious perception of support tilt during transient anterior-posterior rotations of a motion platform in six healthy subjects, using a psychophysical matching procedure. Furthermore, we evaluated subjects' postural responses (in terms of displacement of subjects' center of mass, COM, and their ankle torque, as represented by the center of foot pressure, COP). The platform tilts were applied in absence of visual and auditory orientation cues. The platform rotations consisted of smoothed position ramps with different dominant frequencies (0.025, 0.05, 0.1, 0.2, 0.4, and 0.8 Hz) and different amplitudes (0.125 degrees, 0.25 degrees, 0.5 degrees, 1 degree, 2 degrees, 4 degrees, and 8 degrees) for the forward and backward directions, which yielded a 6x14 stimulus matrix. The stimuli were repeated five times in a random order. For the matching procedure, subjects tried to maintain an upright body orientation, while trying to orient a light-weight rod, which was attached to a belt around their waists, parallel to the perceived platform surface. We measured the stimulus-evoked angular excursions of the rod and of the subjects' COM as well as the COP shift. We found that the subjects' rod indications overestimated the platform tilts, particularly with small stimulus amplitudes. To characterize the overestimation, we compared the rod indications obtained while subjects stood on the tilting platform, to rod indications in a situation in which they stood next to the platform and tried to match the rod angle to the now visually perceived platform angle. From this comparison, we inferred that the subjects' kinesthetically derived notion of platform tilt overestimates the actual tilt by a factor of approximately 4. The estimates were linearly related to the angle between body (COM) and platform, i.e., to approximately the angle of the ankle joint, a finding which suggests a proprioceptive source of the overestimation. Further analyses supported this view; they showed that the onset latencies of the rod indications could be approximated by a theoretical indication mechanism with a reaction time of about 0.31 s, a velocity threshold of 0.099 degrees/s, and a displacement threshold of 0.12 degrees. These threshold values are well in line with previous work on the leg proprioceptive detection threshold of conscious perception of body sway. We therefore assume that the phenomenon of support tilt overestimation reflects a still unknown mechanism of leg proprioception in postural control.     

Multisensory control of human upright stance

The interaction of different orientation senses contributing to posture control is not well understood. We therefore performed experiments in which we measured the postural responses of normal subjects and vestibular loss patients during perturbation of their stance. Subjects stood on a motion platform with their eyes closed and auditory cues masked. The perturbing stimuli consisted of either platform tilts or external torque produced by force-controlled pull of the subjects' body on a stationary platform. Furthermore, we presented trials in which these two stimuli were applied when the platform was body-sway referenced (i.e., coupled 1:1 to body position, by which ankle joint proprioceptive feedback is essentially removed). We analyzed subjects' postural responses, i.e., the excursions of their center of mass (COM) and center of pressure (COP), using a systems analysis approach. We found gain and phase of the responses to vary as a function of stimulus frequency and in relation to the absence versus presence of vestibular and proprioceptive cues. In addition, gain depended on stimulus amplitude, reflecting a non-linearity in the control. The experimental results were compared to simulation results obtained from an 'inverted pendulum' model of posture control. In the model, sensor fusion mechanisms yield internal estimates of the external stimuli, i.e., of the external torque (pull), the platform tilt and gravity. These estimates are derived from three sensor systems: ankle proprioceptors, vestibular sensors and plantar pressure sensors (somatosensory graviceptors). They are fed as global set point signals into a local control loop of the ankle joints, which is based on proprioceptive negative feedback. This local loop stabilizes the body-on-foot support, while the set point signals upgrade the loop into a body-in-space control. Amplitude non-linearity was implemented in the model in the form of central threshold mechanisms. In model simulations that combined sensor fusion and thresholds, an automatic context-specific sensory re-weighting across stimulus conditions occurred. Model parameters were identified using an optimization procedure. Results suggested that in the sway-referenced condition normal subjects altered their postural strategy by strongly weighting feedback from plantar somatosensory force sensors. Taking this strategy change into account, the model's simulation results well paralleled all experimental results across all conditions tested.     

Role of somatosensory and vestibular cues in attenuating visually induced human postural sway

The purpose of this study was to determine the contribution of visual, vestibular, and somatosensory cues to the maintenance of stance in humans. Postural sway was induced by full-field, sinusoidal visual surround rotations about an axis at the level of the ankle joints. The influences of vestibular and somatosensory cues were characterized by comparing postural sway in normal and bilateral vestibular absent subjects in conditions that provided either accurate or inaccurate somatosensory orientation information. In normal subjects, the amplitude of visually induced sway reached a saturation level as stimulus amplitude increased. The saturation amplitude decreased with increasing stimulus frequency. No saturation phenomena were observed in subjects with vestibular loss, implying that vestibular cues were responsible for the saturation phenomenon. For visually induced sways below the saturation level, the stimulus-response curves for both normal subjects and subjects experiencing vestibular loss were nearly identical, implying (1) that normal subjects were not using vestibular information to attenuate their visually induced sway, possibly because sway was below a vestibular-related threshold level, and (2) that subjects with vestibular loss did not utilize visual cues to a greater extent than normal subjects; that is, a fundamental change in visual system gain was not used to compensate for a vestibular deficit. An unexpected finding was that the amplitude of body sway induced by visual surround motion could be almost 3 times greater than the amplitude of the visual stimulus in normal subjects and subjects with vestibular loss. This occurred in conditions where somatosensory cues were inaccurate and at low stimulus amplitudes. A control system model of visually induced postural sway was developed to explain this finding. For both subject groups, the amplitude of visually induced sway was smaller by a factor of about 4 in tests where somatosensory cues provided accurate versus inaccurate orientation information. This implied (1) that the subjects experiencing vestibular loss did not utilize somatosensory cues to a greater extent than normal subjects; that is, changes in somatosensory system gain were not used to compensate for a vestibular deficit, and (2) that the threshold for the use of vestibular cues in normal subjects was apparently lower in test conditions where somatosensory cues were providing accurate orientation information.     

Vestibular, visual, and somatosensory contributions to human control of upright stance

We investigated the changes of human posture control of upright stance which occur when vestibular cues (VEST) are absent and visual and somatosensory orientation cues (VIS, SOM) are removed. Postural responses to sinusoidal tilts of a motion platform in the sagittal plane (+/-2 degrees, f=0.05, 0.1, 0.2 and 0.4 Hz) were studied in normal subjects (Ns) and patients with bilateral vestibular loss (Ps). We found that absence of VEST (Ps, visual reference) and removal of VIS (Ns, no visual reference) had little effect on stabilization of upright body posture in space. In the absence of both VEST and VIS (Ps, no visual reference) somatosensory graviception still provided some information on body orientation in space at 0.05 and 0.1 Hz. However, at the higher frequencies Ps qualitatively changed their behavior; they then tended to actively align their bodies with respect to the motion platform. The findings confirm predictions of a novel postural control model.     

A functional link between area MSTd and heading perception based on vestibular signals

Recent findings of vestibular responses in part of the visual cortex--the dorsal medial superior temporal area (MSTd)--indicate that vestibular signals might contribute to cortical processes that mediate the perception of self-motion. We tested this hypothesis in monkeys trained to perform a fine heading discrimination task solely on the basis of inertial motion cues. The sensitivity of the neuronal responses was typically lower than that of psychophysical performance, and only the most sensitive neurons rivaled behavioral performance. Responses recorded in MSTd were significantly correlated with perceptual decisions, and the correlations were strongest for the most sensitive neurons. These results support a functional link between MSTd and heading perception based on inertial motion cues. These cues seem mainly to be of vestibular origin, as labyrinthectomy produced a marked elevation of psychophysical thresholds and abolished MSTd responses. This study provides evidence that links single-unit activity to spatial perception mediated by vestibular signals, and supports the idea that the role of MSTd in self-motion perception extends beyond optic flow processing.     

Neck proprioception compensates for age-related deterioration of vestibular self-motion perception

Vestibular functions are known to show some deterioration with age. Vestibular deterioration is often thought to be compensated for by an increase in neck proprioceptive gain. We studied this presumed compensatory mechanism by measuring psychophysical responses to vestibular (horizontal canal), neck and combined stimuli in 50 healthy human subjects as a function of age (range 15–76 years). After passive horizontal rotations of head and/or trunk (torso) in complete darkness (dominant frequencies 0.05, 0.1, and 0.4 Hz), subjects readjusted a visual target to its remembered prerotational location in space. (1) Vestibular-only stimulus (whole-body rotation); subjects' responses were shifted towards postrotatory body position, this only slightly at 0.4 Hz and pronounced at 0.1 and 0.05 Hz. These errors reflect the known physiological drop of vestibular gain at low rotational frequency. They exhibited a slight but significant increase with age. (2) Neck-only stimulus (trunk rotated, head stationary); the responses showed errors similar to those upon vestibular stimulation (with offset towards postrotatory trunk position) and this again slightly more with increasing age. (3) Vestibular-neck stimulus combination during head rotation on stationary trunk; the errors were close to zero, independent of stimulus frequency and the subjects' age. (4) Opposite stimulus combination (trunk rotated in the same direction as the head, but with double amplitude); the errors were clearly enhanced, essentially reflecting the sum of those with vestibular-only and neck-only stimulation. Taken together, we find a parallel increase in neck- and vestibular-related errors with age, in seeming contrast to previous studies. We explain our and the previous findings by a vestibular-neck interaction model in which two different neck signals are involved. One neck signal is used, in combination with the vestibular signal, for estimating trunk-in-space rotation. It is internally shaped to always match the vestibular signal, so that these two signals cancel each other out when summed during head rotation on stationary trunk. Because of this matching, perceived trunk stationariness during head rotation on the stationary trunk is independent of vestibular deterioration (related to stimulus frequency, age, ototoxic medication, etc.). The other neck proprioceptive signal, coding head-on-trunk rotation, is superimposed on the estimate of trunk-in-space rotation, thereby yielding a notion of head-in-space. This neck signal remains essentially unchanged with vestibular deterioration. Generally, we hold that the transformation of the vestibular signal from the head down to the trunk proceeds further to include the hip and the legs as well as the haptically perceived body support surface; by this, subjects yield a notion of support kinematics in space. As a consequence, spatial orientation is impaired by chronic vestibular deterioration only to the extent that the body support is moving in space, while it is unimpaired (determined by proprioception alone) during body motion with respect to a stationary support. Electronic Publication     

A cognitive intersensory interaction mechanism in human postural control

Human control of upright body posture involves inputs from several senses (visual, vestibular, proprioceptive, somatosensory) and their central interactions. We recently studied visual effects on posture control and their intersensory interactions and found evidence for the existence of an indirect and presumably cognitive mode of interaction, in addition to a direct interaction (we found, e.g., that a 'virtual reality' visual stimulus has a weaker postural effect than a 'real world' scene, because of its illusory character). Here we focus on the presumed cognitive interaction mechanism. We report experiments in healthy subjects and vestibular loss patients. We investigated to what extent a postural response to lateral platform tilt is modulated by tilt of a visual scene in an orthogonal rotational plane (anterior-posterior, a-p, direction). The a-p visual stimulus did not evoke a lateral postural response on its own. But it enhanced the response to the lateral platform tilt (i.e., it increased the evoked body excursion). The effect was related to the velocity of the visual stimulus, showed a threshold at 0.31 degrees /s, and increased monotonically with increasing velocity. These characteristics were similar in normals and patients, but body excursions were larger in patients. In conclusion, the orthogonal stimulus arrangement in our experiments allowed us to selectively assess a cognitive intersensory interaction that upon co-planar stimulation tends to be merged with direct interaction. The observed threshold corresponds to the conscious perceptual detection threshold of the visual motion, which is clearly higher than the visual postural response threshold. This finding is in line with our notion of a cognitive phenomenon. We postulate that the cognitive mechanism in normals interferes with a central visual-vestibular interaction mechanism. This appears to be similar in vestibular loss patients, but patients use less effective somatosensory instead of vestibular anti-gravity mechanisms.     

Contribution of visual velocity and displacement cues to human balancing of support surface tilt

Vision helps humans in controlling bipedal stance, interacting mainly with vestibular and proprioceptive cues. This study investigates how postural compensation of support surface tilt is compromised by selectively reducing visual velocity cues by stroboscopic illumination of a stationary visual scene. Healthy adult subjects were presented with pseudorandom tilt sequences in the sagittal plane (tilt frequency range 0.017–2.2 Hz; velocity amplitude spectrum constant up to a frequency of 0.6 Hz, angular displacement amplitude spectrum increasing with decreasing frequencies). Center of mass (COM) sway responses were recorded for stroboscopic illuminations at 48, 32, 16, 8, and 4 Hz, as well as under continuous illumination and with eyes closed. With strobe duration (5 ms) and mean luminance (1 lx) kept constant, visual acuity and perceived brightness remained constant and the visual scene was perceived as stationary. Yet, tilt-evoked COM excursions increased with decreasing strobe frequency in a graded way, with largest effects occurring at tilt frequencies where large tilt velocities coincided with small displacements. In addition, COM excursions were reduced at the lowest strobe frequency compared to eyes closed, with the largest effect occurring at tilt frequencies where tilt displacements were large. We conclude that two mechanisms exist, a velocity mechanism that deals with tilt compensation and is foremost affected by the stroboscopic illumination and a displacement mechanism. This compares favorably to previous findings that, transferred to a stance control model, suggest a velocity mechanism for tilt compensation and a position mechanism for gravity compensation.     

Sensorimotor integration in human postural control

It is generally accepted that human bipedal upright stance is achieved by feedback mechanisms that generate an appropriate corrective torque based on body-sway motion detected primarily by visual, vestibular, and proprioceptive sensory systems. Because orientation information from the various senses is not always available (eyes closed) or accurate (compliant support surface), the postural control system must somehow adjust to maintain stance in a wide variety of environmental conditions. This is the sensorimotor integration problem that we investigated by evoking anterior-posterior (AP) body sway using pseudorandom rotation of the visual surround and/or support surface (amplitudes 0.5-8 degrees ) in both normal subjects and subjects with severe bilateral vestibular loss (VL). AP rotation of body center-of-mass (COM) was measured in response to six conditions offering different combinations of available sensory information. Stimulus-response data were analyzed using spectral analysis to compute transfer functions and coherence functions over a frequency range from 0.017 to 2.23 Hz. Stimulus-response data were quite linear for any given condition and amplitude. However, overall behavior in normal subjects was nonlinear because gain decreased and phase functions sometimes changed with increasing stimulus amplitude. "Sensory channel reweighting" could account for this nonlinear behavior with subjects showing increasing reliance on vestibular cues as stimulus amplitudes increased. VL subjects could not perform this reweighting, and their stimulus-response behavior remained quite linear. Transfer function curve fits based on a simple feedback control model provided estimates of postural stiffness, damping, and feedback time delay. There were only small changes in these parameters with increasing visual stimulus amplitude. However, stiffness increased as much as 60% with increasing support surface amplitude. To maintain postural stability and avoid resonant behavior, an increase in stiffness should be accompanied by a corresponding increase in damping. Increased damping was achieved primarily by decreasing the apparent time delay of feedback control rather than by changing the damping coefficient (i.e., corrective torque related to body-sway velocity). In normal subjects, stiffness and damping were highly correlated with body mass and moment of inertia, with stiffness always about 1/3 larger than necessary to resist the destabilizing torque due to gravity. The stiffness parameter in some VL subjects was larger compared with normal subjects, suggesting that they may use increased stiffness to help compensate for their loss. Overall results show that the simple act of standing quietly depends on a remarkably complex sensorimotor control system.     

Visuomotor sensitivity to visual information about surface orientation

We measured human visuomotor sensitivity to visual information about three-dimensional surface orientation by analyzing movements made to place an object on a slanted surface. We applied linear discriminant analysis to the kinematics of subjects' movements to surfaces with differing slants (angle away form the fronto-parallel) to derive visuomotor d's for discriminating surfaces differing in slant by 5 degrees. Subjects' visuomotor sensitivity to information about surface orientation was very high, with discrimination "thresholds" ranging from 2 to 3 degrees. In a first experiment, we found that subjects performed only slightly better using binocular cues alone than monocular texture cues and that they showed only weak evidence for combining the cues when both were available, suggesting that monocular cues can be just as effective in guiding motor behavior in depth as binocular cues. In a second experiment, we measured subjects' perceptual discrimination and visuomotor thresholds in equivalent stimulus conditions to decompose visuomotor sensitivity into perceptual and motor components. Subjects' visuomotor thresholds were found to be slightly greater than their perceptual thresholds for a range of memory delays, from 1 to 3 s. The data were consistent with a model in which perceptual noise increases with increasing delay between stimulus presentation and movement initiation, but motor noise remains constant. This result suggests that visuomotor and perceptual systems rely on the same visual estimates of surface slant for memory delays ranging from 1 to 3 s.     

Multisensory integration in the estimation of walked distances

When walking through space, both dynamic visual information (optic flow) and body-based information (proprioceptive and vestibular) jointly specify the magnitude of distance travelled. While recent evidence has demonstrated the extent to which each of these cues can be used independently, less is known about how they are integrated when simultaneously present. Many studies have shown that sensory information is integrated using a weighted linear sum, yet little is known about whether this holds true for the integration of visual and body-based cues for travelled distance perception. In this study using Virtual Reality technologies, participants first travelled a predefined distance and subsequently matched this distance by adjusting an egocentric, in-depth target. The visual stimulus consisted of a long hallway and was presented in stereo via a head-mounted display. Body-based cues were provided either by walking in a fully tracked free-walking space (Exp. 1) or by being passively moved in a wheelchair (Exp. 2). Travelled distances were provided either through optic flow alone, body-based cues alone or through both cues combined. In the combined condition, visually specified distances were either congruent (1.0×) or incongruent (0.7× or 1.4×) with distances specified by body-based cues. Responses reflect a consistent combined effect of both visual and body-based information, with an overall higher influence of body-based cues when walking and a higher influence of visual cues during passive movement. When comparing the results of Experiments 1 and 2, it is clear that both proprioceptive and vestibular cues contribute to travelled distance estimates during walking. These observed results were effectively described using a basic linear weighting model.     

Phobic postural vertigo

Patients with phobic postural vertigo (PPV) often report a particularly increased unsteadiness when looking at moving visual scenes. Therefore, the differential effects of large-field visual motion stimulation in roll plane on body sway during upright stance were analyzed in 23 patients with PPV, who had been selected for the integrity of their vestibular and balance systems, and in 17 healthy subjects. Visual motion stimulation induced a sensation of apparent body motion (roll vection) in all patients and normal subjects. Normal subjects showed an increased lateral sway path with a lateral shift of the center of pressure (COP) in stimulus direction (mean 1.67 cm, SD 1.63). The patients also exhibited an increase in sway path during visual motion stimulation; however, their body sway differed from that of normals in that there was no lateral displacement of COP (mean 0.19 cm, SD 0.73). The lateral displacement of COP and the increase in RMS of body sway during visual motion stimulation were significantly greater in normals than in the patients ( p<0.05). The patients' increased body sway without COP deviation does not imply an increased risk of falling. Two explanations are conceivable for this increased body sway without body deviation in patients with PPV: (a) the patients rely more on proprioceptive and vestibular rather than on visual cues to regulate upright stance; or (b) they depend on visual, vestibular, and proprioceptive information, but the threshold at which they initiate a compensatory body sway opposite in direction to a perceived body deviation is lower than in normal subjects. The data support the second explanation.     

Multisensory integration in the estimation of relative path length

One of the fundamental requirements for successful navigation through an environment is the continuous monitoring of distance travelled. To do so, humans normally use one or a combination of visual, proprioceptive/efferent, vestibular, and temporal cues. In the real world, information from one sensory modality is normally congruent with information from other modalities; hence, studying the nature of sensory interactions is often difficult. In order to decouple the natural covariation between different sensory cues, we used virtual reality technology to vary the relation between the information generated from visual sources and the information generated from proprioceptive/efferent sources. When we manipulated the stimuli such that the visual information was coupled in various ways to the proprioceptive/efferent information, human subjects predominantly used visual information to estimate the ratio of two traversed path lengths. Although proprioceptive/efferent information was not used directly, the mere availability of proprioceptive information increased the accuracy of relative path length estimation based on visual cues, even though the proprioceptive/efferent information was inconsistent with the visual information. These results convincingly demonstrated that active movement (locomotion) facilitates visual perception of path length travelled.     

Contributions of visual and proprioceptive information to travelled distance estimation during changing sensory congruencies

Recent research has provided evidence that visual and body-based cues (vestibular, proprioceptive and efference copy) are integrated using a weighted linear sum during walking and passive transport. However, little is known about the specific weighting of visual information when combined with proprioceptive inputs alone, in the absence of vestibular information about forward self-motion. Therefore, in this study, participants walked in place on a stationary treadmill while dynamic visual information was updated in real time via a head-mounted display. The task required participants to travel a predefined distance and subsequently match this distance by adjusting an egocentric, in-depth target using a game controller. Travelled distance information was provided either through visual cues alone, proprioceptive cues alone or both cues combined. In the combined cue condition, the relationship between the two cues was manipulated by either changing the visual gain across trials (0.7×, 1.0×, 1.4×; Exp. 1) or the proprioceptive gain across trials (0.7×, 1.0×, 1.4×; Exp. 2). Results demonstrated an overall higher weighting of proprioception over vision. These weights were scaled, however, as a function of which sensory input provided more stable information across trials. Specifically, when visual gain was constantly manipulated, proprioceptive weights were higher than when proprioceptive gain was constantly manipulated. These results therefore reveal interesting characteristics of cue-weighting within the context of unfolding spatio-temporal cue dynamics.     

Human discrimination of translational accelerations

Human perception of self-motion is the result of combining information from many sensory systems such as visual, vestibular, and proprioceptive systems. Research on vestibular thresholds has mainly focused on estimating absolute thresholds for translational and rotational motions and estimating difference thresholds for rotational velocities. In this study, psychophysical methods are used to determine the ability of normal subjects to discriminate among sinusoidal accelerations in the horizontal plane. Difference thresholds were estimated using four different acceleration amplitudes ranging from peak amplitude of 0.5–2.0 m/s² and three different frequencies ranging from 0.25 to 0.6 Hz. Difference thresholds ranged from 0.05 m/s² for a sinusoidal acceleration with peak amplitude of 0.5 to 0.13 m/s² for a sinusoidal acceleration with peak amplitude of 2.0 m/s². The relationship between difference threshold estimates and peak accelerations is found to compare favorably to Weber’s law, which is often used to represent changes in threshold values in other sensory systems. Moreover, the threshold estimates tend to decrease as frequency increases. The effect of visual condition on thresholds was also investigated. It was shown that when the visual scene is stationary with respect to the subject, there are no significant differences between threshold estimates based on closed-eye and open-eye scenarios.     

Differences in coding provided by proprioceptive and vestibular sensory signals may contribute to lateral instability in vestibular loss subjects

One of the signatures of balance deficits observed in vestibular loss subjects is the greater instability in the roll compared to pitch planes. Directional differences in the timing and strengths of vestibular and proprioceptive sensory signals between roll and pitch may lead to a greater miscalculation of roll than pitch motion of the body in space when vestibular input is absent. For this reason, we compared the timing and amplitude of vestibular information, (observable in stimulus-induced head accelerations when subjects are tilted in different directions), with that of proprioceptive information caused by stimulus induced rotations of ankle and hip joints [observable as short latency (SL) stretch responses in leg and trunk muscle EMG activity]. We attempted to link the possible mode of sensory interaction with the deficits in balance control. Six subjects with bilaterally absent vestibular function and 12 age-matched controls were perturbed, while standing, in 8 directions of pitch and roll support surface rotation in random order. Body segment movements were recorded with a motion analysis system, head accelerations with accelerometers, and muscle activity with surface EMG. Information on stimulus pitch motion was available sequentially. Pitch movements of the support surface were best coded in amplitude by ankle rotation velocity, and by head vertical linear acceleration, which started at 13 ms after the onset of ankle rotation. EMG SL reflex responses in soleus with onsets at 46 ms provided a distal proprioceptive correlate to the pitch motion. Roll information on the stimulus was available simultaneously. Hip adduction and lumbo-sacral angular velocity were represented neurally as directionally specific short latency stretch and unloading reflexes in the bilateral gluteus medius muscles and paraspinal muscles with onsets at 28 ms. Roll angular accelerations of the head coded roll amplitude and direction at the same time (31 ms). Significant differences in amplitude coding between vestibular loss subjects and controls were only observed as a weaker coding between stimulus motion and head roll and head lateral linear accelerations. The absence of vestibular inputs in vestibular loss subjects led to characteristic larger trunk in motion in roll in the direction of tilt compared to pitch with respect to controls. This was preceded by less uphill flexion and no downhill extension of the legs in vestibular loss subjects. Downhill arm abduction responses were also greater. These results suggest that in man vestibular inputs provide critical information necessary for the appropriate modulation of roll balance-correcting responses in the form of stabilising knee and arm movements. The simultaneous arrival of roll sensory information in controls may indicate that proprioceptive and vestibular signals can only be interpreted correctly when both are present. Thus, roll proprioceptive information may be interpreted inaccurately in vestibular loss subjects, leading to an incorrect perception of body tilt and insufficient uphill knee flexion, especially as cervico-collic signals appear less reliable in these subjects as an alternative sensory input.     

Influence of expectation on postural disturbance evoked by proprioceptive stimulation

Recent experiments have shown that the vestibular channel of balance control differs fundamentally from the visual channel. Whereas the response to a visual perturbation can be suppressed if the subject has awareness that an upcoming disturbance is likely to be caused by an external agent rather than by self-motion, a similar assumption cannot be made concerning the vestibular system. The present experiment investigated whether postural responses evoked by a proprioceptive perturbation (vibration of the Achilles’ tendon at 90 Hz for 2.2 s) are either automatic and immune to expectation (similarly to vestibular responses) or cognitively penetrable (similarly to visual responses). Subjects (n = 12) stood on a force platform while stimuli were delivered either by the subject himself (self-triggered condition) or by the experimenter. For the latter condition, the stimulus was delivered either without warning (unpredictable condition) or at a fixed interval (500 ms) following an auditory cue (precue condition). Results showed that the backward CoP displacement induced by vibration was delayed by approximately 500 ms in the expected and self-triggered conditions compared to the unexpected condition. However, once initiated, the velocity of the backward displacement was higher in the self-triggered condition as compared to the unexpected condition. After a period of 2.2 s of vibration, the amplitude of this backward CoP displacement was similar in the three experimental conditions. Therefore, although expectation appears to delay the upcoming of the main backward body sway, it does not appear to be able to weight the impact of the proprioceptive stimulation. This suggested that afferents provided by the different sensory channels involved in postural control are not similarly susceptible to high level processes such as expectation.     

Sensorimotor integration for multisegmental frontal plane balance control in humans

To quantify the contribution of sensory information to multisegmental frontal plane balance control in humans, we developed a feedback control model to account for experimental data. Subjects stood with feet close together on a surface that rotated according to a pseudorandom waveform at three different amplitudes. Experimental frequency-response functions and impulse-response functions were measured to characterize lower body (LB) and upper body (UB) motion evoked during surface rotations while subjects stood with eyes open or closed. The model assumed that corrective torques in LB and UB segments were generated with no time delay from intrinsic musculoskeletal mechanisms and with time delay from sensory feedback mechanisms. It was found that subjects' LB control was primarily based on sensory feedback. Changes in the LB control mechanisms across stimulus amplitude were consistent with the hypothesis that sensory reweighting contributed to amplitude-dependent changes in balance responses whereby subjects decreased reliance on proprioceptive cues that oriented the LB toward the surface and increased reliance on vestibular/visual cues that oriented the LB upright toward earth vertical as stimulus amplitude increased in both eyes open and closed conditions. Sensory reweighting in the LB control system also accounted for most of the amplitude-dependent changes observed in UB responses. In contrast to the LB system, sensory reweighting was not a dominant mechanism of UB control, and UB control was more influenced by intrinsic musculoskeletal mechanisms. The proposed model refines our understanding of sensorimotor integration during balance control by including multisegmental motion and explaining how intersegmental interactions influence frontal plane balance responses.     

Eye movements evoked by proprioceptive stimulation along the body axis in humans

Proprioceptive input arising from torsional body movements elicits small reflexive eye movements. The functional relevance of these eye movements is still unknown so far. We evaluated their slow components as a function of stimulus frequency and velocity. The horizontal eye movements of seven adult subjects were recorded using an infrared device, while horizontal rotations were applied at three segmental levels of the body [i.e., between head and shoulders (neck stimulus), shoulders and pelvis (trunk stimulus), and pelvis and feet (leg stimulus)]. The following results were obtained: (1) Sinusoidal leg stimulation evoked an eye response with the slow component in the direction of the movement of the feet, while the response to trunk and neck stimulation was oriented in the opposite direction (i.e., in that of the head). (2) In contrast, the gain behavior of all three responses was similar, with very low gain at mid- to high frequencies (tested up to 0.4 Hz) but increasing gain at low frequencies (down to 0.0125 Hz). We show that this gain behavior is mainly due to a gain nonlinearity for low angular velocities. (3) The responses were compatible with linear summation when an interaction series was tested in which the leg stimulus was combined with a vestibular stimulus. (4) There was good correspondence of the median gain curves when eye responses were compared with psychophysical responses (perceived body rotation in space; additionally recorded in the interaction series). However, correlation of gain values on a single-trial basis was poor. (5) During transient neck stimulation (smoothed position ramp), the neck response noticeably consisted of two components – an initial head-directed eye shift (phasic component) followed by a shift in the opposite direction (compensatory tonic component). Both leg and neck responses can be described by one simple, dynamic model. In the model the proprioceptive input is fed into the gaze network via two pathways which differ in their dynamics and directional sign. The model simulates either leg or neck responses by selecting an appropriate weight for the gain of one of the pathways (phasic component). The interaction results can also be simulated when a vestibular path is added. This model has similarities to one we recently proposed for human self-motion perception and postural control. A major difference, though, is that the proprioceptive input to the gaze-stabilizing network is weak (restricted to low velocities), unlike that used for perception and postural control. We hold that the former undergoes involution during ontogenesis, as subjects depend on the functionally more appropriate vestibulo-ocular reflex. Yet, the weak proprioceptive eye responses that remain may have some functional relevance. Their tonic component tends to stabilize the eyes by slowly shifting them toward the primary head position relative to the body support. This applies solely to the earth-horizontal plane in which the vestibular signal has no static sensitivity. Received: 10 October 1997 / Accepted: 22 January 1998     

Visual object localisation in space

Perceptual updating of the location of visual targets in space after intervening eye, head or trunk movements requires an interaction between several afferent signals (visual, oculomotor efference copy, vestibular, proprioceptive). The nature of the interaction is still a matter of debate. To address this problem, we presented subjects (n=6) in the dark with a target (light spot) at various horizontal eccentricities (up to +/-20 degrees ) relative to the initially determined subjective straight-ahead direction (SSA). After a memory period of 12 s in complete darkness, the target reappeared at a random position and subjects were to reproduce its previous location in space using a remote control. For both the presentation and the reproduction of the target's location, subjects either kept their gaze in the SSA (retinal viewing condition) or fixated the eccentric target (visuo-oculomotor). Three experimental series were performed: A, "visual-only series": reproduction of the target's location in space was found to be close to ideal, independently of viewing condition; estimation curves (reproduced vs presented positions) showed intercepts approximately 0 degrees and slopes approximately 1; B, "visual-vestibular series": during the memory period, subjects were horizontally rotated to the right or left by 10 degrees or 18 degrees at 0.8-Hz or 0.1-Hz dominant frequency. Following the 0.8-Hz body rotation, reproduction was close to ideal, while at 0.1 Hz it was partially shifted along with the body, in line with the known vestibular high-pass characteristics. Additionally, eccentricity of target presentation reduced the slopes of the estimation curves (less than 1); C, "visual-vestibular-neck series": a shift toward the trunk also occurred after low-frequency neck stimulation (trunk rotated about stationary head). When vestibular and neck stimuli were combined (independent head and trunk rotations), their effects summed linearly, such that the errors cancelled each other during head rotation on the stationary trunk. Variability of responses was always lowest for targets presented at SSA, irrespective of intervening eye, head or trunk rotations. We conclude that: (1) subjects referenced "space" to pre-rotatory SSA and that the memory trace of the target's location in space was not altered during the memory period; and that (2) they used internal estimates of eye, head and trunk displacements with respect to space to match current target position with the memory trace during reproduction; these estimates would be obtained by inverting the physical coordinate transformations produced by these displacements. We present a model which is able to describe these operations and whose predictions closely parallel the experimental results. In this model the estimate of head rotation in space is not obtained directly from the vestibular head-in-space signal, but from a vestibular estimate of the kinematic state of the body support.