Vestibular and somatosensory contributions to responses to head and body displacements in stance

The relative contribution of vestibular and somatosensory information to triggering postural responses to external body displacements may depend on the task and on the availability of sensory information in each system. To separate the contribution of vestibular and neck mechanisms to the stabilization of upright stance from that of lower body somatosensory mechanisms, responses to displacements of the head alone were compared with responses to displacements of the head and body, in both healthy subjects and in patients with profound bilateral vestibular loss. Head displacements were induced by translating two 1-kg weights suspended on either side of the head at the level of the mastoid bone, and body displacements were induced translating the support surface. Head displacements resulted in maximum forward and backward head accelerations similar to those resulting from body displacements, but were not accompanied by significant center of body mass, ankle, knee, or hip motions. We tested the effect of disrupting somatosensory information from the legs on postural responses to head or body displacements by sway-referencing the support surface. The subjects' eyes were closed during all testing to eliminate the effects of vision. Results showed that head displacements alone can trigger medium latency (48–84 ms) responses in the same leg and trunk muscles as body displacements. Nevertheless, it is unlikely that vestibular signals alone normally trigger directionally specific postural responses to support surface translations in standing humans because: (1) initial head accelerations resulting from body and head displacements were in opposite directions, but were associated with activation of the same leg and trunk postural muscles; (2) muscle responses to displacements of the head alone were only one third of the amplitude of responses to body displacements with equivalent maximum head accelerations; and (3) patients with profound bilateral vestibular loss showed patterns and latencies of leg and trunk muscle responses to body displacements similar to those of healthy subjects. Altering somatosensory information, by sway-referencing the support surface, increased the amplitude of ankle muscle activation to head displacements and reduced the amplitude of ankle muscle activation to body displacements, suggesting context-specific reweighting of vestibular and somatosensory inputs for posture. In contrast to responses to body displacements, responses to direct head displacements appear to depend upon a vestibulospinal trigger, since trunk and leg muscle responses to head displacements were absent in patients who had lost vestibular function as adults. Patients who lost vestibular function as infants, however, had near normal trunk and leg response to head displacements, suggesting a substitution of upper trunk and neck somatosensory inputs for missing vestibular inputs during development.     

Role of vestibular information in initiation of rapid postural responses

Patients with bilateral vestibular loss have difficulty maintaining balance without stepping when standing in tandem, on compliant surfaces, across narrow beams, or on one foot, especially with eyes closed. Normal individuals (with no sensory impairment) maintain balance in these tasks by employing quick, active hip rotation (a “hip strategy”). The absence of a hip strategy in vestibular patients responding to translations of a short support surface has previously been taken as evidence that the use of hip strategy requires an intact vestibular system. However, many tasks requiring hip strategy alter one or a combination of important system characteristics, such as initial state of the body (tandem stance), dynamics (compliant surfaces), or biomechanical limits of stability (narrow beams). Therefore, the balance deficit in these tasks may result from a failure to account for these support surface alterations when planning and executing sensorimotor responses. In this study, we tested the hypothesis that vestibular information is critical to trigger a hip strategy even on an unaltered support surface, which imposes no changes on the system characteristics. We recorded the postural responses of vestibular patients and control subjects with eyes closed to rearward support surface translations of varying velocity, in erect stance on a firm, flat surface. Subjects were instructed to maintain balance without stepping, if possible. Faster translation velocities (25 cm/s or more) produced a consistent pattern of early hip torque (first 400 ms) in control subjects (i.e., a hip strategy). Most of the patients with bilateral vestibular loss responded to the same translation velocities with similar torques. Contrary to our hypothesis, we conclude that vestibular function is not necessary to trigger a hip strategy. We postulate, therefore, that the balance deficit previously observed in vestibular patients during postural tasks that elicit a hip strategy may have been due to the sensorimotor consequences of the system alterations imposed by the postural tasks used in those studies. Preliminary results from two younger patients who lost vestibular function as infants indicate that age, duration of vestibular loss, and/or the timing of the loss may also be factors that can influence the use of hip strategy as a rapid postural response. Received: 20 February 1997 / Accepted: 30 April 1998     

Auditory biofeedback substitutes for loss of sensory information in maintaining stance

The importance of sensory feedback for postural control in stance is evident from the balance improvements occurring when sensory information from the vestibular, somatosensory, and visual systems is available. However, the extent to which also audio-biofeedback (ABF) information can improve balance has not been determined. It is also unknown why additional artificial sensory feedback is more effective for some subjects than others and in some environmental contexts than others. The aim of this study was to determine the relative effectiveness of an ABF system to reduce postural sway in stance in healthy control subjects and in subjects with bilateral vestibular loss, under conditions of reduced vestibular, visual, and somatosensory inputs. This ABF system used a threshold region and non-linear scaling parameters customized for each individual, to provide subjects with pitch and volume coding of their body sway. ABF had the largest effect on reducing the body sway of the subjects with bilateral vestibular loss when the environment provided limited visual and somatosensory information; it had the smallest effect on reducing the sway of subjects with bilateral vestibular loss, when the environment provided full somatosensory information. The extent that all subjects substituted ABF information for their loss of sensory information was related to the extent that each subject was visually dependent or somatosensory-dependent for their postural control. Comparison of postural sway under a variety of sensory conditions suggests that patients with profound bilateral loss of vestibular function show larger than normal information redundancy among the remaining senses and ABF of trunk sway. The results support the hypothesis that the nervous system uses augmented sensory information differently depending both on the environment and on individual proclivities to rely on vestibular, somatosensory or visual information to control sway.     

Postural adjustments in sitting humans following external perturbations: muscle activity and kinematics

There are several controversies concerning the organization and induction of postural adjustments in standing humans. Some investigators suggest the responses are triggered by somatosensory inputs (especially from the ankle in standing subjects), while others emphasize the vestibular input induced by head acceleration. We examined postural responses in sitting subjects in order to describe the muscle activation pattern during various perturbations and to test whether somatosensory or vestibular stimulation elicited the responses. The kinematics and EMG patterns in respons to perturbations caused by movements of the support surface were studied in adults. The postural muscle activation following a backward sway was mainly the same, whether it was elicited by a forward translation or a legs-up rotation. This is remarkable, since, except for pelvis rotation, the movements of all body segments including the head differed in the two conditions. Furthermore, a second experiment showed that the direction of the initial head movement could be reversed with retainment of the same postural muscle activation pattern. The results suggest that somatosensory signals derived from the backward rotation of the pelvis, and not vestibular information from the head, trigger postural responses during sitting. There was a slight but consistent difference in the muscle activation pattern, whether the backward sway was elicited by a forward translation or legs-up rotation. The difference seemed to reflect the sensory information from head and other body parts (except the pelvis). This finding allowed us to speculate in a central pattern generator for postural adjustments containing two levels. At the first level, a simple format of the muscle activation would be generated; at the second level, the centrally generated pattern could be shaped and timed by interaction from the entire somatosensory, vestibular, and visual input.     

Emergence of postural patterns as a function of vision and translation frequency.

Emergence of postural patterns as a function of vision and translation frequency. We examined the frequency characteristics of human postural coordination and the role of visual information in this coordination. Eight healthy adults maintained balance in stance during sinusoidal support surface translations (12 cm peak to peak) in the anterior-posterior direction at six different frequencies. Changes in kinematic and dynamic measures revealed that both sensory and biomechanical constraints limit postural coordination patterns as a function of translation frequency. At slow frequencies (0.1 and 0.25 Hz), subjects ride the platform (with the eyes open or closed). For fast frequencies (1.0 and 1.25 Hz) with the eyes open, subjects fix their head and upper trunk in space. With the eyes closed, large-amplitude, slow-sway motion of the head and trunk occurred for fast frequencies above 0.5 Hz. Visual information stabilized posture by reducing the variability of the head's position in space and the position of the center of mass (CoM) within the support surface defined by the feet for all but the slowest translation frequencies. When subjects rode the platform, there was little oscillatory joint motion, with muscle activity limited mostly to the ankles. To support the head fixed in space and slow-sway postural patterns, subjects produced stable interjoint hip and ankle joint coordination patterns. This increase in joint motion of the lower body dissipated the energy input by fast translation frequencies and facilitated the control of upper body motion. CoM amplitude decreased with increasing translation frequency, whereas the center of pressure amplitude increased with increasing translation frequency. Our results suggest that visual information was important to maintaining a fixed position of the head and trunk in space, whereas proprioceptive information was sufficient to produce stable coordinative patterns between the support surface and legs. The CNS organizes postural patterns in this balance task as a function of available sensory information, biomechanical constraints, and translation frequency.     

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.     

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.     

Temporal facilitation of gaze in the presence of postural reactions triggered by sudden surface perturbations

Saccadic reaction times can be shortened by an additional sensory modality (e.g. auditory, tactile) presented in temporal proximity to the triggering cue. Whereas somatosensory cues given by sudden perturbations of the support surface can trigger appropriate postural adjustments to maintain upright stance, it is not known how gaze executions are affected by the dual task of maintaining upright balance while redirecting gaze. It was hypothesized that the onset latency of gaze movements toward visual targets will be shortened by sudden surface perturbations following visual target shifts to prompt a stable visual anchor for postural stabilization. Eight subjects stood on a movable platform with gaze fixated on a central target 2 m directly in front, and were instructed to shift their gaze to lateral targets located along a 63 degrees arc to the right and left. The trials began with the central target lit followed randomly by either the right, left or center target. Fifty or 250 ms following this target shift, balance was perturbed by a sudden yaw movement of the support surface (15.5 degrees over 210 ms at 130 degrees /s), with no stepping or large arm reactions observed. The latency of the gaze shifts was significantly shortened (by approximately 72 ms) when executed simultaneously with a surface perturbation. A decrease in excitation latency was also observed in the cervical paraspinals and sternocleidomastoid muscles. Postural responses in the ankle and knee muscles were not affected by gaze shifts. Pelvic horizontal angular motion closely followed surface motion whereas head motion was influenced by gaze shifts. During the combined gaze shift and surface motion conditions, thorax movement excursion was larger and not correlated with either the surface motion or visual target shift. In conclusion, postural adjustments in response to sudden surface yaws facilitate voluntary gaze shift execution and this enhancement may result from the sensory fusion of somatosensory and visual information.     

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.     

Human standing posture control system depending on adopted strategies

Control of the standing posture of humans involves at least two distinct modes of operation to restore the body balance in the sagittal plane: the ankle strategy and the hip strategy. The objective of the study was to estimate the contribution of vestibular, visual and somatosensory feedbacks to these distinct strategies. The body dynamics was described as the motion of two linked rigid segments that represented the legs and the rest of the body. The posture controller received the inclination angles of the two body segments as inputs and regulated the moments around the ankle and hip joints. The controller had four feedback paths that were characterised by transfer functions connecting the two inputs and the two outputs. To evoke the distinct strategies, the floor conditions were varied by narrowing the support surface under the feet. A continuous pseudo-random external disturbing force was applied to the waist and the thigh independently. The inclination angles of the body segments and the ground reaction force were measured, and the transfer functions of the controller were estimated with the maximum-likelihood system identification procedure. Six healthy male adult subjects participated in the experiment. When the hip strategy became evident under the narrow support surface conditions, the transfer function relating the leg inclination angle and the ankle joint moment decreased its DC gain (16%), whereas the other three transfer functions increased the gains (20–140%) (ANOVA, p<0.05). Based on a criterion for simplicity in the modification of the posture controller, these changes suggest a new hypothesis that, when posture control becomes difficult, the central nervous system selectively activates the somatosensory feedback paths from the hip joint angle to the moments around the ankle and hip joints.     

Somatosensory loss increases vestibulospinal sensitivity

To determine whether subjects with somatosensory loss show a compensatory increase in sensitivity to vestibular stimulation, we compared the amplitude of postural lean in response to four different intensities of bipolar galvanic stimulation in subjects with diabetic peripheral neuropathy (PNP) and age-matched control subjects. To determine whether healthy and neuropathic subjects show similar increases in sensitivity to galvanic vestibular stimulation when standing on unstable surfaces, both groups were exposed to galvanic stimulation while standing on a compliant foam surface. In these experiments, a 3-s pulse of galvanic current was administered to subjects standing with eyes closed and their heads turned toward one shoulder (anodal current on the forward mastoid). Anterior body tilt, as measured by center of foot pressure (CoP), increased proportionately with increasing galvanic vestibular stimulation intensity for all subjects. Subjects with peripheral neuropathy showed larger forward CoP displacement in response to galvanic stimulation than control subjects. The largest differences between neuropathy and control subjects were at the highest galvanic intensities, indicating an increased sensitivity to vestibular stimulation. Neuropathy subjects showed a larger increase in sensitivity to vestibular stimulation when standing on compliant foam than control subjects. The effect of galvanic stimulation was larger on the movement of the trunk segment in space than on the body's center of mass (CoM) angle, suggesting that the vestibular system acts to control trunk orientation rather than to control whole body posture. This study provides evidence for an increase in the sensitivity of the postural control system to vestibular stimulation when somatosensory information from the surface is disrupted either by peripheral neuropathy or by standing on an unstable surface. Simulations from a simple model of postural orientation incorporating feedback from the vestibular and somatosensory systems suggest that the increase in body lean in response to galvanic current in subjects with neuropathy could be reproduced only if central vestibular gain was increased when peripheral somatosensory gain was decreased. The larger effects of galvanic vestibular stimulation on the trunk than on the body's CoM suggest that the vestibular system may act to control postural orientation via control of the trunk in space.     

Head position-based electrotactile tongue biofeedback affects postural responses to Achilles tendon vibration in humans

The purpose of the present experiment was to investigate whether postural responses to ankle proprioceptive perturbation Achilles tendon vibration were affected by the availability of augmented sensory information about head orientation/motion with respect to gravitational vertical, i.e., normally provided by the vestibular system. To achieve this goal, ten standing subjects were exposed to Achilles tendon vibration in two No Biofeedback and Biofeedback conditions. The No Biofeedback condition served as a control condition. In the Biofeedback condition, subjects performed the postural task using a head position-based electrotactile tongue-placed biofeedback system. Center of foot pressure (CoP) displacements were recorded using a force platform. Results showed that (1) Achilles tendon vibration increased CoP displacements in the No Biofeedback condition and (2) this destabilizing effect was less accentuated in the Biofeedback condition. These results are consistent with and discussed in terms of sensory re-weighting mechanisms involved in postural control. In the condition of Achilles tendon vibration, which renders ankle proprioceptive information less reliable for controlling posture, the central nervous system was able to integrate alternatively available augmented sensory information suitable and usable in upright postural control to reduce the destabilizing effect of the ankle proprioceptive perturbation.     

The importance of somatosensory information in triggering and scaling automatic postural responses in humans

To clarify the role of somatosensory information from the lower limbs of humans in triggering and scaling the magnitude of automatic postural responses, patients with diabetic peripheral neuropathy and agematched normal controls were exposed to posterior horizontal translations of their support surface. Translation velocity and amplitude were varied to test the patients' ability to scale their postural responses to the magnitude of the translation. Postural response timing was quantified by measuring the onset latencies of three shank, thigh, and trunk muscles and response magnitude was quantified by measuring torque at the support surface. Neuropathy patients showed the same distalto-proximal muscle activation pattern as normal subjects, but the electromyogram (EMG) onsets in patients were delayed by 20–30 ms at all segments, suggesting an important role for somatosensory information from the lower limb in triggering centrally organized postural synergies. Patients showed an impaired ability to scale torque magnitude to both the velocity and amplitude of surface translations, suggesting that somatosensory information from the legs may be utilized for both direct sensory feedback and use of prior experience in scaling the magnitude of automatic postural responses.     

Interactions between vestibular and proprioceptive inputs triggering and modulating human balance-correcting responses differ across muscles

Interactions between proprioceptive and vestibular inputs contributing to the generation of balance corrections may vary across muscles depending on the availability of sensory information at centres initiating and modulating muscle synergies, and the efficacy with which the muscle action can prevent a fall. Information which is not available from one sensory system may be obtained by switching to another. Alternatively, interactions between sensory systems and the muscle to which this interaction is targeted may be fixed during neural development and not switchable. To investigate these different concepts, balance corrections with three different sets of proprioceptive trigger signals were examined under eyes-open and eyes-closed conditions in the muscles of normal subjects and compared with those of subjects with bilateral peripheral vestibular loss. The different sets of early proprioceptive inputs were obtained by employing three combinations of support surface rotation and translation, for which ankle inputs were nulled, normal or enhanced, the knees were either locked or in flexion, and the trunk was either in flexion or extension. Three types of proprioceptive and vestibulospinal interactions were identified in muscles responses. These interactions were typified by the responses of triceps surae, quadriceps, and paraspinal muscles. The amplitudes of stretch responses at 50 ms after the onset of ankle flexion in triceps surae muscles were related to the velocity of ankle stretch. The amplitude of balance-correcting responses at 100 ms corresponded more with stretch of the biarticular gastrocnemius when the knee was re-extended at 60 ms. Absent stretch reflexes at 50 ms in triceps surae with nulled ankle inputs caused a minor, 12-ms delay in the onset of balance-correcting responses in triceps surae muscles. Vestibular loss caused no change in the amplitude of balance-correcting responses, but a negligible decrease in onset latency in triceps surae even with nulled ankle inputs. Stretch responses in quadriceps at 80 ms increased with the velocity of knee flexion but were overall lower in amplitude in vestibular loss subjects. Balance-correcting responses in quadriceps had amplitudes which were related to the directions of initial trunk movements, were still present when knee inputs were negligible and were also altered after vestibular loss. Stretch and unloading responses in paraspinals at 80 ms were consistent with the direction of initial trunk flexion and extension. Subsequent balance-correcting responses in paraspinals were delayed 20 ms in onset and altered in amplitude by vestibular loss. The changes in the amplitudes of ankle (tibialis anterior), knee (quadriceps) and trunk (paraspinal) muscle responses with vestibular loss affected the amplitudes and timing of trunk angular velocities, requiring increased stabilizing tibialis anterior, paraspinal and trapezius responses post 240 ms as these subjects attempted to remain upright. The results suggest that trunk inputs provide an ideal candidate for triggering balance corrections as these would still be present when vestibular, ankle and knee inputs are absent. The disparity between the amplitudes of stretch reflex and automatic balance-correcting responses in triceps surae and the insignificant alteration in the timing of balance-correcting responses in these muscles with nulled ankle inputs indicates that ankle inputs do not trigger balance corrections. Furthermore, modulation of balance corrections normally performed by vestibular inputs in some but not all muscles is not achieved by switching to another sensory system on vestibular loss. We postulate that a confluence of trunk and upper-leg proprioceptive input establishes the basic timing of automatic, triggered balance corrections which is then preferentially weighted by vestibular modulation in muscles that prevent falling. The organisation of balance corrections around trunk inputs portrayed here would have considerable advantage for the infant learning balance control, but forces balance control centres to rely on limited sensory information related to this most unstable body segment, the trunk, when triggering balance corrections. Received: 13 October 1997 / Accepted: 30 March 1998     

Multisensory information for human postural control: integrating touch and vision

Despite extensive research on the influence of visual, vestibular and somatosensory information on human postural control, it remains unclear how these sensory channels are fused for self-orientation. The focus of the present study was to test whether a linear additive model could account for the fusion of touch and vision for postural control. We simultaneously manipulated visual and somatosensory (touch) stimuli in five conditions of single- and multisensory stimulation. The visual stimulus was a display of random dots projected onto a screen in front of the standing subject. The somatosensory stimulus was a rigid plate which subjects contacted lightly (<1 N of force) with their right index fingertip. In each condition, one sensory stimulus oscillated (dynamic) in the medial-lateral direction while the other stimulus was either dynamic, static or absent. The results qualitatively supported five predictions of the linear additive model in that the patterns of gain and variability across conditions were consistent with model predictions. However, a strict quantitative comparison revealed significant deviations from model predictions, indicating that the sensory fusion process clearly has nonlinear aspects. We suggest that the sensory fusion process behaved in an approximately linear fashion because the experimental paradigm tested postural control very close to the equilibrium point of vertical upright.     

Sensory supplementation system based on electrotactile tongue biofeedback of head position for balance control

The present study aimed at investigating the effects of an artificial head position-based tongue-placed electrotactile biofeedback on postural control during quiet standing under different somatosensory conditions from the support surface. Eight young healthy adults were asked to stand as immobile as possible with their eyes closed on two Firm and Foam support surface conditions executed in two conditions of No-biofeedback and Biofeedback. In the Foam condition, a 6-cm thick foam support surface was placed under the subjects’ feet to alter the quality and/or quantity of somatosensory information at the plantar sole and the ankle. The underlying principle of the biofeedback consisted of providing supplementary information about the head orientation with respect to gravitational vertical through electrical stimulation of the tongue. Centre of foot pressure (CoP) displacements were recorded using a force platform. Larger CoP displacements were observed in the Foam than Firm conditions in the two conditions of No-biofeedback and Biofeedback. Interestingly, this destabilizing effect was less accentuated in the Biofeedback than No-biofeedback condition. In accordance with the sensory re-weighting hypothesis for balance control, the present findings evidence that the availability of the central nervous system to integrate an artificial head orientation information delivered through electrical stimulation of the tongue to limit the postural perturbation induced by alteration of somatosensory input from the support surface.     

Sensory supplementation system based on electrotactile tongue biofeedback of head position for balance control

The present study aimed at investigating the effects of an artificial head position-based tongue-placed electrotactile biofeedback on postural control during quiet standing under different somatosensory conditions from the support surface. Eight young healthy adults were asked to stand as immobile as possible with their eyes closed on two Firm and Foam support surface conditions executed in two conditions of No-biofeedback and Biofeedback. In the Foam condition, a 6-cm thick foam support surface was placed under the subjects' feet to alter the quality and/or quantity of somatosensory information at the plantar sole and the ankle. The underlying principle of the biofeedback consisted of providing supplementary information about the head orientation with respect to gravitational vertical through electrical stimulation of the tongue. Centre of foot pressure (CoP) displacements were recorded using a force platform. Larger CoP displacements were observed in the Foam than Firm conditions in the two conditions of No-biofeedback and Biofeedback. Interestingly, this destabilizing effect was less accentuated in the Biofeedback than No-biofeedback condition. In accordance with the sensory re-weighting hypothesis for balance control, the present findings evidence that the availability of the central nervous system to integrate an artificial head orientation information delivered through electrical stimulation of the tongue to limit the postural perturbation induced by alteration of somatosensory input from the support surface.     

Human postural responses to motion of real and virtual visual environments under different support base conditions

The role of visual orientation cues for human control of upright stance is still not well understood. We, therefore, investigated stance control during motion of a visual scene as stimulus, varying the stimulus parameters and the contribution from other senses (vestibular and leg proprioceptive cues present or absent). Eight normal subjects and three patients with chronic bilateral loss of vestibular function participated. They stood on a motion platform inside a cabin with an optokinetic pattern on its interior walls. The cabin was sinusoidally rotated in anterior-posterior (a-p) direction with the horizontal rotation axis through the ankle joints (f=0.05-0.4 Hz; A (max)=0.25 degrees -4 degrees ; v (max)=0.08-10 degrees /s). The subjects' centre of mass (COM) angular position was calculated from opto-electronically measured body sway parameters. The platform was either kept stationary or moved by coupling its position 1:1 to a-p hip position ('body sway referenced', BSR, platform condition), by which proprioceptive feedback of ankle joint angle became inactivated. The visual stimulus evoked in-phase COM excursions (visual responses) in all subjects. (1) In normal subjects on a stationary platform, the visual responses showed saturation with both increasing velocity and displacement of the visual stimulus. The saturation showed up abruptly when visually evoked COM velocity and displacement reached approximately 0.1 degrees /s and 0.1 degrees , respectively. (2) In normal subjects on a BSR platform (proprioceptive feedback disabled), the visual responses showed similar saturation characteristics, but at clearly higher COM velocity and displacement values ( approximately 1 degrees /s and 1 degrees , respectively). (3) In patients on a stationary platform (no vestibular cues), the visual responses were basically similar to those of the normal subjects, apart from somewhat higher gain values and less-pronounced saturation effects. (4) In patients on a BSR platform (no vestibular and proprioceptive cues, presumably only somatosensory graviceptive and visual cues), the visual responses showed an abnormal increase in gain with increasing stimulus frequency in addition to a displacement saturation. On the normal subjects we performed additional experiments in which we varied the gain of the visual response by using a 'virtual reality' visual stimulus or by applying small lateral platform tilts. This did not affect the saturation characteristics of the visual response to a considerable degree. We compared the present results to previous psychophysical findings on motion perception, noting similarities of the saturation characteristics in (1) with leg proprioceptive detection thresholds of approximately 0.1 degrees /s and 0.1 degrees and those in (2) with vestibular detection thresholds of 1 degrees /s and 1 degrees , respectively. From the psychophysical data one might hypothesise that a proprioceptive postural mechanism limits the visually evoked body excursions if these excursions exceed 0.1 degrees /s and 0.1 degrees in condition (1) and that a vestibular mechanism is doing so at 1 degrees /s and 1 degrees in (2). To better understand this, we performed computer simulations using a posture control model with multiple sensory feedbacks. We had recently designed the model to describe postural responses to body pull and platform tilt stimuli. Here, we added a visual input and adjusted its gain to fit the simulated data to the experimental data. The saturation characteristics of the visual responses of the normals were well mimicked by the simulations. They were caused by central thresholds of proprioceptive, vestibular and somatosensory signals in the model, which, however, differed from the psychophysical thresholds. Yet, we demonstrate in a theoretical approach that for condition (1) the model can be made monomodal proprioceptive with the psychophysical 0.1 degrees /s and 0.1 degrees thresholds, and for (2) monomodal vestibular with the psychophysical 1 degrees /s and 1 degrees thresholds, and still shows the corresponding saturation characteristics (whereas our original model covers both conditions without adjustments). The model simulations also predicted the almost normal visual responses of patients on a stationary platform and their clearly abnormal responses on a BSR platform.     

Dynamics, Stability, and Control of Stepping

The dynamics, stability, and control of stepping are considered. The role of internal models is elaborated. The main objective of the paper is to provide a better understanding of the machinery and processing in the central nervous system (CNS) that relates to stepping. The role of the vestibular system in balance and balance recovery is described. Balance and balance recovery are essential in stepping, and guarantee the stability of the system before, during, and after stepping. In sagittal standing, humans use two distinct sets of control strategies to maintain their postural stability in response to external disturbance. In one set of strategies, the configuration of the base of support, namely, the position of the feet, remains unchanged. The ankle and hip strategies are examples of postural adjustments where the feet do not move. When the disturbances are large, and move the center of mass or pressure outside the support boundaries, stepping strategies are required. A simple control strategy is proposed for illustrative purposes. Its effectiveness is verified by computer simulation of a seven-link two-dimensional sagittal biped. The applications of the model in assessing trauma and injury are discussed.