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Chapter 22 On the role of vestibular, visual and somatosensory information for dynamic postural control in humans
0.Pompcinno and J.H.J. Allurn (Eds.) Prupws m Bruin Research, Vol. 76 0 19XX Elsevier Science Publishers B.V. (Biorncdical Division)
253 CHAPTER 22
On the role of vestibular, visual and somatosensory information for dynamic postural control in humans H.-C. Diener and J. Dichgans Neurologische Klinik, Eberhard- Karls Universitat, Tubingen, Liebermeisterstrasse 18-20,0-7400 Tubingen, F.R.G.
Postural stabilization in altered visual, vestibular, and somatosensory conditions was investigated in humans subjected to either a fast unidirectional displacement or to a continuous sinusoidal movement of the standing support. Visual inputs were varied in four ways: (1) stroboscopic illumination, (2) stabilizing the visual surround with respect to head movements, (3) inducing apparent body movement in pitch using stripe patterns which moved continuously up or down in front of the subject, (4) eye closure. Static vestibular (and neck) input was modified by bending the head forwards or backwards, or to the right or left shoulder with the eyes closed. Somatosensory input from both feet was reduced by an ischaemic block at a level just above the ankle joints. With fast, transient, toe-up platform displacements (high-frequency test) neither the biomechanical parameters as measured by the displacement of the centre of foot pressure nor the early EMG responses of the anterior tibia1 and triceps surae muscles were modified by a manipulation of visual, vestibular or somatosensory feedback conditions. Sudden disturbances are obviously compensated by an early set of reflex-like muscle responses that, depending on the starting position, are stereotypically released without feedback control to save time at the expence of accuracy (emergency reaction). Continuous regulation of upright stance during sinusoidal displacement at 1 or 0.3 Hz (low-frequency test), however, clearly depends on visual, vestibular, and somatosensory feedback. Studies in patients should contain both tests, since each examines different functions of the very complex posture stabilizing network. Manipulations of sensory feedback, however, are only recommended in the low-frequency test. The experimental suppression
or disturbance by disease of two of the three feedback loops invariably causes a conspicuous postural instability.
Introduction The stabilization of human stance after external disturbances depends on the integrative evaluation of afferent information from proprioceptive, visual, and vestibular inputs. Nashner [ I , 21 indicated that each of the three sensory systems, although with some overlap, is specialized to work within a certain domain of frequencies and amplitudes and that in this respect the three systems are not entirely redundant. Up to now, it is not entirely clear whether the selection of a certain sensory input for postural control is performed in a hierarchical way giving, for example, vestibular priority over visual input or whether all three inputs are used in parallel. Most experiments performed so far dealt with the influence of the visual system on postural control [3]. Results from experiments in which subjects were exposed to large moving visual scenes in order to induce a visual disturbance of posture and selfmotion perception [4-61 indicated that visual stabilization of posture operates mainly in the low frequency range at and below 0.1 Hz. The importance of visual information for dynamic posture control was earlier evaluated by applying sinusoidal platform oscillations in pitch with eyes open and
Abbreviations: CFP, centre of foot pressure; EMG, electromyogram; RMS, root mean square.
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closed. Stabilization of posture by vision in this experiment was best within the frequency range between 0.03 and 0.3 Hz [7]. The unexpected exposure to conflicting information from different sensory channels may extend the frequency range of the visual channel. In the case of a mismatch between visual and vestibular motion inputs, e.g. when the subject is linearly displaced and the visual scene moves together with the head, thus indicating a stable visual surround, postural EMG responses as early as 100 ms after the beginning of the linear displacement are significantly attenuated [8]. The working range of the vestibular system for posture control in humans can only be estimated. A model of vestibular motor control by Nashner [9] predicted that the semicircular channels best sense the rate of sway above 0.1 Hz and the otoliths sense sway below this frequency. The working range of somatosensory inputs like pressure receptors, joint receptors, and tendon organs in humans is largely unknown. Proprioception involving muscle spindles includes high frequencies above 1 Hz [lo, 111. The present study was undertaken to investigate the influence of different visual, vestibular, and somatosensory inputs on two experimental tasks testing postural stabilization after sudden or slow displacements of a supporting platform. Sudden disturbances of upright stance are compensated by a set of rapid, mostly automatic motor responses in the stretched muscles and their antagonists of the lower leg [12-141 as well as trunk and neck muscles [ 151. Sinusoidal displacements of the support surface also require continuous regulation of postural balance [7]. It was investigated whether both tasks require visual, vestibular, and somatosensory feedback and if so whether this feedback provides information about motion and/or orientation. The question of conflict solution and corroborative action in the case of corresponding or contradictory sensory information was also addressed. The entire study was performed with the goal of not only understanding the postural control system but also exploring the potential clinical usefulness of these tests.
Material and methods
Apparatus Subjects stood on a movable force-measuring platform (Tonnies Inc.) with their feet 4 cm apart. Strain gauges at the four corners of the platform measured the forces perpendicular to the platform and allowed calculation of the displacement of the CFP in anterior-posterior and lateral directions. EMGs from both legs were recorded with surface electrodes from the anterior tibia1 and triceps surae muscles. EMG signals were fullwave rectified, band-pass filtered, and amplified.
Changes in visualfeedback The contribution of vision to postural stabilization was measured in the following way: (1) To assess visual stabilization of the quiet stance, sway parameters were compared while standing with the eyes open and closed respectively. (2) To investigate whether the important parameter for visual stabilization was the orientation of contours or whether it was motion, the earlier experimental set up by Amblard and Crkmieux [26] was applied to our displacement conditions. We used a 4 Hz stroboscopic illumination of the surrounding laboratory. (3) Conflicting information from the different visual feedback loops were tested using two paradigms: (a) To study the effect of large field visual motion that contradicts the gravitational input of stationarity, subjects stood in front of a curved projection screen which fully covered the visual field in its vertical extension. The remaining lateral parts of the visual field were covered by flat white projection surfaces. An optokinetic pattern projector above the head of the subject produced a pattern of horizontally oriented black-and-white stripes. These stripes could be moved either up- or downwards with an angular velocity of 65"/s or kept stationary. (b) To study the reverse conflict, i.e. veridical vestibular feedback about spontaneous sway but visu-
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a1 perception of stationarity, the visual scene was stabilized with respect to head movements. Subjects wore a very light paper dome that surrounded the head entirely and moved with it like a hat. Its inner surface was covered with black and white stripes. Changes in vestibular conditions
To investigate the vestibular contribution to postural sway, static vestibular input was modified by changing the head position prior to platform displacement. This manoeuvre puts the utricles (and saccules) into in an anomalous position away from the optimal working range. The following conditions were compared: head in its normal position (eyes closed), head tilted forward (30"), head extended as far as posible backwards (45"), or bent to the left or right shoulder (45") respectively. Changes in somatosensory input
In order to assess the contribution of somatosensory information from foot and ankle joint receptors, we applied ischaemia. Ischaemia is known to affect the fast-conducting Ia fibres from small foot muscles first. Thus this technique allows for selective (early) measurements of the effects of sensory deprivation [ 161. After recording with platform tilts and sinusoidal platform movements under normal physiological conditions, two blood-pressure cuffs were applied above the level of the ankle joints on both sides. The pressure of the two cuffs was increased to 300 mmHg. The effect of ischaemia on motor neurons and somatosensory input was tested every 5 minutes between single trials by manually determining the force of maximal voluntary dorsiflection and plantarflection of the big toe and the foot. The sensitivity for vibration or tactile stimulation and position sense of the big toe and the ankle joint were also tested. Platform displacements
The equilibrium was perturbed with sudden toe-up ramp rotations of the platform by 4" with a velocity
of 80°/s in a sequence with random intervals of eight runs each. The initial body position was monitored by the experimenter (for details see [14, 193). Sinusoidal toe-up and -down platform displacements around the ankle joint were performed with a frequency of 1 or 0.3 Hz and with an amplitude of f. 4". Data analysis
Onset latencies of EMG activity after sudden tilt as well as durations and integrals were calculated after visual identification of the onset and termination of each EMG component in each of eight consecutive single trials. EMG and CFP recordings were then averaged over eight runs and plotted. The anteriorposterior displacements of the CFP during sinusoidal platform movements were fed into a computer for on-line Fourier analysis. The total duration of sampling was 44.1 s. We calculated the RMSs of the power spectrum for the whole frequency range between 0 and 12.5 Hz. Angular displacements of the head and hip in the anterior-posterior direction were recorded by means of goniometers rigidly attached to head and hip belts. These data also were subjected to a Fourier analysis. Subjects
Ten healthy subjects aged between 18 and 33 years participated in the experiments with altered visual and vestibular conditions and four healthy men aged between 28 and 32 years in the experiment with altered somatosensory input.
Results Standing on a stable surface
Postural sway increases by about 50% with closed eyes as compared to open eyes. The anterior-posterior sway is invariably greater than sway in the lateral dimension with and without the visual contribution to postural stabilization [ 171.
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Sinusoidal displacements
60
The sinusoidal movement of the platform provoked a continuous anterior-posterior regulation of upright posture. The Fourier spectra revealed that the greatest power of CFP displacement was at the frequency of the imposed displacement (Fig. 1). Additionally, there were lower- and higher-frequency components of body sway besides the one at the stimulus frequency which contributed to postural control. The total amount of anterior-posterior body sway as measured by the RMSs of Fourier spectra was significantly influenced by the seven dif-
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m
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Fig. 2. RMS of body sway from the Fourier power spectra during 1 Hz sinusoidal platform movements (means and standard deviations from 10 subjects). The visual conditions from left to right were: normal visual surround, viewing a stationary stripe pattern, stroboscopic illumination, stabilized vision, eyes closed, stripe movement upwards, and stripe movement downwards.
8
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Fig. I . (1) Original recording of the anterior-posterior body sway during sinusoidal platform movements at I Hz over a time period of 40 s. (2) Fourier power spectra of sway with a linear scale for the ordinate with eyes open (A) or eyes closed (B). Note the increased power of body sway around the stimulus frequency (1 Hz) and between 2 and 3 Hz when the eyes are closed.
ferent visual and five different vestibular conditions (for details see [14]). RMSs increased from the eyesopen condition to stroboscopic illumination, stabilized visual surround, and eyes closed. Stripe patterns moving upwards created less postural instability than stripe patterns moving downwards (Fig. 2). The RMSs of anterior-posterior body sway with the eyes closed were identical for normal head position and head flexed forwards. Body sway was increased with the head bent to the right and left shoulder and was further increased when the head was extended to the neck (Fig. 3). Body sway as measured by the RMSs of the power spectrum as well as head and hip sway increased with increasing time of ischaemia at the level of the ankle. The biggest effect could be observed after 45 minutes of ischaemia [19]. The mean RMSs increased from 121 to 196 after 45 minutes of ischaemia, the peak amplitude in the Fourier spectrum increased from 39 to 138 mV. The results indicate that visual, vestibular, and somatosensory feedback are essential for the compensation of continuously applied low-frequency disturbances to the upright standing human. Dis-
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Changing the visual, vestibular, or somatosensory experimental conditions had no significant influence on latency, duration, and integral of each of the three EMG responses or the displacement of the CFP during the first 500 ms (Figs. 4 and 5). Thus phasic EMG responses to rapid ankle rotation and related torque changes reflected through the CFP remained unchanged despite very different visual, vestibular, and somatosensory inputs. In addition,
5
10 5
P 3
Fig. 3 . Original recordings of the platform stimulus at 1.0 and 0.3 Hz and displacements of the anterior-posterior component of the CFP under different static vestibular conditions with the eyes closed. Note the increase of body sway when the head is extended backwards or bent to the right or left shoulder.
turbed somatosensory and vestibular information obviously can be compensated by visual input. Transient ramp displacements
With the eyes open or closed, sudden tilt of the platform toe-up with a velocity of 8Oo/s and an amplitude of 4" evokes a short-latency response with the mean latency between 37 and 50 ms and a medium latency response after between 75 and 110 ms in the triceps surae muscle. The long-latency response, with a latency of between 110 and 124 ms, appears in the antagonist, the anterior tibial muscle.
0
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ms Fig. 4. Averaged recordings (eight trials) of rectified EMGs from the anterior tibial (TA) and triceps surae (TS) after a rapid tilt of the platform toe-up (80"/s, 4"; see upper trace) under different conditions of static vestibular input. SL = short latency; ML =medium latency; LL = long latency response. Note the unchanged EMG recordings under different vestibular conditions.
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Fig. 5. Averaged recordings (eight runs) of the displacements of the CFP, head angle and hip angle after sudden tilts of the platform toe-up (vertical dotted line) with increasing time after the beginning of ischaemia above the ankle. Upward deflections or the recordings imply an anterior shift of the body or a forward inclination of head and hip. Despite considerable interindividual differences between the four subjects (rows 1 4 ) , there is a close similarity of the induced sway within one subject throughout the entire experiment between minutes 0 and 43.
we observed no side differences between the EMG responses from the right and left legs when the head was tilted to the right or left side respectively. Experiments in patients
In order to get more insight into the role of the vestibular input for posture control, we performed platform tilts in three patients with a total bilateral loss of vestibular function. In two cases this was due to bilateral surgery of a neurinoma of the VIIIth nerve. In one case, it was due to inherited degeneration of the VIIIth nerve. The missing vestibular function was in all cases proved by absent ca-
lorics, and absent vestibulo-ocular reflexes in horizontal and vertical direction with low- and highfrequency stimulation. In the two operated cases, acoustically evoked responses were absent. Lesions outside the vestibular system were excluded by neurological examination, electrophysiological testing, somatosensory evoked potentials, visual evoked potentials, by computed tomography, and nuclear magnetic resonance imaging. The latencies of short- and medium-latency EMG responses in triceps surae and the long-latency response in anterior tibia1 muscle were not different in patients with bilateral vestibular deficit than in normals (Fig. 6). The size of the long-latency
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Bilateral vestibular deficit
Normal subject Stimulus
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Fig. 6 . Rectified averaged EMG recordings after platform tilt toe-up in a normal subject and a patient with bilateral vestibular deficit with eyes open and eyes closed. Short-, medium-, and long-latency reflexes can be observed with normal latency in the patient with bilateral vestibular deficit. The size of the long-latency response, however, is decreased. For abbreviations see Fig. 4.
EMG response, which stabilizes posture, however, was decreased. The number of subjects was too small to perform a statistical analysis. In some of the trials, the patients were not able to keep upright after platform tilt when the eyes were closed. These results confirm that the size of the long-latency EMG response is modulated by vestibulospinal influences [20]. Discussion
The present study confirms that visual, vestibular, and somatosensory feedback contribute to the compensation of a low-frequency disturbance continuously applied to the upright standing human, whereas, provided that proprioceptive feedback
through spindle afferents from leg muscles is intact, these additional feedback loops seem to be insignificant for the compensation 'of transient high-frequency postural disturbances. Visual input can compensate for the deficiency of somatosensory and vestibular input [19]. Our results with stabilized visual conditions are in contrast with those of Nashner and Berthoz [8] and Vidal et al. [21]. In their experiments with linear displacements, EMG responses as early as 100 ms were significantly attenuated when the visual surround moved together with the head, whereas no such attenuation was seen in our experiments. This is most probably due to different stimulus conditions. The angular velocity of displacement around the ankle joint was around 6"/s in their stu-
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dy compared to 80°/s in our experiments. Another explanation could be that visual input is much more important in cases of linear translation (as in Nashner and Vidal's experiment) than with tilt around the ankle joint, as in our experiments. A third alternative could be that our subjects were continuously provided with stabilized visual surrounding even between platform tilts whereas visual stabilization started in Nashner and Berthoz' [8] conditions at the moment of linear surface displacements. Our results by no means indicate that afferent information is not used for rapid postural control, but that after exclusion or malfunction of one of the three systems the other two are able to compensate completely. At least two of the three senses must be out of order to provoke falling after a sudden disturbance. This was also shown in the experiments with bilaterally labyrinthectomized patients who have normal EMG responses and perfect postural stabilization with rapid tilt as long as the eyes are open but may fall with the eyes closed. The same is true in patients with severe demyelinating polyneuropathy and missing position sense as well as in patients with Friedreich's ataxia who are quite stable with their eyes open but fall backwards with the eyes closed [22, 231. Considering the possible modulation of stretch reflex amplitudes with head tilt, our results are in disagreement with those obtained in humans who were tilted on a tilting table in pitch with their neck fixed [24, 251. We were unable to find a significant modulation of stretch reflex amplitudes by alteration of static vestibular input. This can possibly be ascribed to the compensatory effect of neck afferents on tonic labyrinthine reflexes. Visual, vestibular, and somatosensory afferent information clearly influences the compensation of sinusoidally applied disturbances. Stroboscopic illumination resulted in increased body sway. The importance of visual movement perception as opposed to perception of contour orientation was already evaluated by Amblard and Crkmieux [26], who were able to induce postural destabilization in quietly standing humans by stroboscopic illumina-
tion. The fact that postural instability was greater with eyes closed than with stroboscopic illumination may indicate that the intermittent presentation of stationary contours also contributes to postural stability [27]. The most dramatic destabilizing effect was seen when moving patterns induced the perception of being tilted in pitch. The movement pattern induced perceived motion of the body in pitch in the direction opposite to that of the moving stripes. This leads to the perception of falling backwards in the case of stripes moving down. The asymmetry between the two conditions is explained by the fact that normal subjects feel much more uncomfortable and unsafe when tilted backwards than when tilted forwards. The result with changed afferent input from somatosensory receptors fits well with the assumption that spindle afferents have their working range above I Hz, whereas pressure, joint, and skin receptors are more important in the low frequency range. Vision has its working range below 1 Hz [3, 71 and therefore is able to compensate for the deficiency of somatosensory information under ischaemia with low-frequency sinusoidal stimulation. In summary, the comparison of the results obtained in this study with fast transient ramp and slow continuous sinusoidal platform displacement indicates that there are at least two different modes of postural stabilization. (1) One mode acts through reflex-like responses that are not immediately modified and possibly not even accessible to modifying inputs from the visual, vestibular, or somatosensory system but are organized in advance according to prior experience about functional objectives. Afferent information from spindle receptors is only used to trigger spinal and transcortical reflexes. Within the system, there is a certain amount of flexibility in both the time and amplitude domains [I 3,221 but this, although functionally adaptive, acts through preset modifications of the response pattern and not via feedback. Postural stabilization is performed normally as long as at least two of the three afferent systems contain congruent information. This mode subserves only fast corrections to fast (transient) disturbances.
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(2) A continuous mode, highly dependent on visual, vestibular, and proprioceptive feedback that subserves the compensation of low-frequency disturbances on the one side and of continuous displacements on the other. This mode is more subjected to adaptive changes [28]. The results indicate that postural studies in patients with deficits in vestibular, visual, or somatosensory and proprioceptive input should either be performed with low-frequency testing or during conflicting afferent input conditions or excluding at least two of the three afferent systems. Acknowledgements This paper has been supported by the Deutsche Forschungsgemeinschaft, SFB 307 A3.
References Nashner. L.M. (1970) Sensory feedback in human posture control. Massachusetts Institute of Technology Report, MVT 70-3. Nashner, L.M. (1981) Analysis of stance posture in humans. In A.L. Towe and E.S. Luschei (Eds.), Handbook of Behavioural Neurobiology, Vol. 5 , Plenum, New York, pp. 527-561. Dichgans, J. and Brandt, Th. (1978) Visual-vestibular interaction. In H.W. Leibowitz and H.L. Teubner (Eds.), Handbook of Sensory Physiology, Springer, Berlin, pp. 755-804. Dichgans, J., Mauritz, K.H., Allum, J.H.J. and Brandt, Th. (1 976) Postural sway in normals and ataxic patients: analysis of the stabilizing and destabilizing effects of vision. Agqressologie, 17C: 15-24. Lestienne, F., Soechting, J. and Berthoz, A. (1977) Postural readjustments induced by linear motion of visual scenes. Exp. Brain Res., 28: 363-384. Mauritz, K.H., Dichgans, J. and Hufschmidt, A. (1977) The angle of visual roll motion determines the displacement of subjective visual vertical. Percept. Psychophys., 22: 557562. Diener, H.C., Dichgans, J., Bruzek, W. and Selinka, H. (1982) Stabilization of human posture during induced oscillations of the body. Exp. Bruin Res., 45: 12&132. Nashner, L.M. and Berthoz, A. (1978) Visual contribution to rapid motor responses during postural control. Bruin Res.. 150: 403407. Nashner, L.M. (1972) Vestibular posture control model. Kybrrnetik, 10: 1 0 6 1 10.
[lo] Goodwin, G.M., Hulliger, M. and Matthews, W.B. (1976) Studies on muscle spindle primary endings with sinusoidal stretching. In S. Homma (Ed.), Understanding the Stretch Refex. Progress in Brain Research, Vol. 44, Elsevier, Amsterdam, pp. 89-98. [I I] Poppele, R.E. and Kennedy, W.R. (1974) Comparison between behaviour of human and cat muscle spindles recorded in vitro. Brain Res., 75: 316-319. [I21 Diener, H.C., Dichgans, J. and Bruzek, W. (1983) Variability of postural ‘reflexes’ in humans. Exp. Brain Res., 52: 423428. [I31 Diener, H.C., Dichgans, J., Bootz, F. and Bacher, M. (1984) Early stabilization of human posture after a sudden disturbance: Influence of rate and amplitude of displacement. Exp. Brain Res., 56: 126-134. [I41 Diener, H.C., Dichgans, J., Guschlbauer, B. and Bacher, M. (1986) Role of vestibular and static vestibular influences on dynamic posture control. Human Neurohiol., 5: 105-1 13. [I51 Keshner, E.A. and Woollacott, M.H. (1987) Neck and trunk muscle response during postural perturbations in humans. In press. Mauritz, K.H. and Dietz, V. (1980) Characteristics of postural instability induced by ischemic blocking of leg afferents. Exp. Brain Res., 38: 117-1 19. Diener, H.C., Dichgans, J., Bacher, M. and Gompf, B. (1984) Quantification of postural sway in normals and patients with cerebellar diseases. EEG Clin. Neurophysiol., 57: 134-142. Berthoz, A,, Lacour, M., Soechting, J.F. and Vidal, P.P. (1979) The role of vision in the control of posture during linear motion. In R. Granit and 0. Pompeiano (Eds.), Reflex Control of Posture and Movement. Progress in Brain Research, Vol. 50, Elsevier, Amsterdam, pp. 197-209. Diener, H.C., Dichgans, J . , Guschlbauer, B. and Mau, H. (1 984) The significance of proprioception on postural stabilization as assessed by ischemia. Exp. Brain Res., 296: 103109. Allum, J.H.J. and Pfaltz, C.R. (1985) Visual and vestibular contributions to pitch sway stabilization in the ankle muscles of normals and patients with bilateral peripheral vestibular deficits. Exp. Brain Res., 58: 82-94. Vidal, P.P., Gouny, M. and Berthoz, A. (1979) R61e de la vision dans le declenchement de rtactions posturales rapides. Arch. Ital. Biol., 116: 281-291. Diener, H.C. and Dichgans, J . (1986) Long loop reflexes and posture. In W. Bles and Th. Brandt (Eds.), Disorders ofPostwe and Gait, Elsevier, Amsterdam, pp. 41-5 1. Friedemann, H.H., Noth, J., Diener, H.C. and Bacher, M. (1987) Long latency EMG responses in hand and leg muscles: cerebellar disorders. J . Neurol. Neurosurg. Psychiatr., 50: 71-77. Chan, C.W.Y. and Kearney, R.E. (1982) Influence of static tilt on soleus motoneuron excitability in man. Neurosci. Lett., 33: 333- 338.
262 [25] Aiello, I., Rosati, G., Serra, G., Jugnoli, V. and Manca, M.
(1983) Static vestibular spinal influences in relation to different body tilts in man. Exp. Brain Res., 79: 18-26. [26] Amblard, B. and Cremieux, J. (1976) Role of visual information in the maintenance of postural equilibrium in man. Aggressologie, 17C: 25-36.
[27] Paulus, W.M., Straube, A. and Brandt, Th. (1984) Visual stabilization of posture. Brain, 107: 1143-1 163. [28] Black, F.O. and Nashner, L.M. (1984) Vestibulo-spinal control differs in patients with reduced versus distorted vestibular function. Acta Otolaryngol. Stockholm, Suppl., 406: 110-114.
253 CHAPTER 22
On the role of vestibular, visual and somatosensory information for dynamic postural control in humans H.-C. Diener and J. Dichgans Neurologische Klinik, Eberhard- Karls Universitat, Tubingen, Liebermeisterstrasse 18-20,0-7400 Tubingen, F.R.G.
Postural stabilization in altered visual, vestibular, and somatosensory conditions was investigated in humans subjected to either a fast unidirectional displacement or to a continuous sinusoidal movement of the standing support. Visual inputs were varied in four ways: (1) stroboscopic illumination, (2) stabilizing the visual surround with respect to head movements, (3) inducing apparent body movement in pitch using stripe patterns which moved continuously up or down in front of the subject, (4) eye closure. Static vestibular (and neck) input was modified by bending the head forwards or backwards, or to the right or left shoulder with the eyes closed. Somatosensory input from both feet was reduced by an ischaemic block at a level just above the ankle joints. With fast, transient, toe-up platform displacements (high-frequency test) neither the biomechanical parameters as measured by the displacement of the centre of foot pressure nor the early EMG responses of the anterior tibia1 and triceps surae muscles were modified by a manipulation of visual, vestibular or somatosensory feedback conditions. Sudden disturbances are obviously compensated by an early set of reflex-like muscle responses that, depending on the starting position, are stereotypically released without feedback control to save time at the expence of accuracy (emergency reaction). Continuous regulation of upright stance during sinusoidal displacement at 1 or 0.3 Hz (low-frequency test), however, clearly depends on visual, vestibular, and somatosensory feedback. Studies in patients should contain both tests, since each examines different functions of the very complex posture stabilizing network. Manipulations of sensory feedback, however, are only recommended in the low-frequency test. The experimental suppression
or disturbance by disease of two of the three feedback loops invariably causes a conspicuous postural instability.
Introduction The stabilization of human stance after external disturbances depends on the integrative evaluation of afferent information from proprioceptive, visual, and vestibular inputs. Nashner [ I , 21 indicated that each of the three sensory systems, although with some overlap, is specialized to work within a certain domain of frequencies and amplitudes and that in this respect the three systems are not entirely redundant. Up to now, it is not entirely clear whether the selection of a certain sensory input for postural control is performed in a hierarchical way giving, for example, vestibular priority over visual input or whether all three inputs are used in parallel. Most experiments performed so far dealt with the influence of the visual system on postural control [3]. Results from experiments in which subjects were exposed to large moving visual scenes in order to induce a visual disturbance of posture and selfmotion perception [4-61 indicated that visual stabilization of posture operates mainly in the low frequency range at and below 0.1 Hz. The importance of visual information for dynamic posture control was earlier evaluated by applying sinusoidal platform oscillations in pitch with eyes open and
Abbreviations: CFP, centre of foot pressure; EMG, electromyogram; RMS, root mean square.
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closed. Stabilization of posture by vision in this experiment was best within the frequency range between 0.03 and 0.3 Hz [7]. The unexpected exposure to conflicting information from different sensory channels may extend the frequency range of the visual channel. In the case of a mismatch between visual and vestibular motion inputs, e.g. when the subject is linearly displaced and the visual scene moves together with the head, thus indicating a stable visual surround, postural EMG responses as early as 100 ms after the beginning of the linear displacement are significantly attenuated [8]. The working range of the vestibular system for posture control in humans can only be estimated. A model of vestibular motor control by Nashner [9] predicted that the semicircular channels best sense the rate of sway above 0.1 Hz and the otoliths sense sway below this frequency. The working range of somatosensory inputs like pressure receptors, joint receptors, and tendon organs in humans is largely unknown. Proprioception involving muscle spindles includes high frequencies above 1 Hz [lo, 111. The present study was undertaken to investigate the influence of different visual, vestibular, and somatosensory inputs on two experimental tasks testing postural stabilization after sudden or slow displacements of a supporting platform. Sudden disturbances of upright stance are compensated by a set of rapid, mostly automatic motor responses in the stretched muscles and their antagonists of the lower leg [12-141 as well as trunk and neck muscles [ 151. Sinusoidal displacements of the support surface also require continuous regulation of postural balance [7]. It was investigated whether both tasks require visual, vestibular, and somatosensory feedback and if so whether this feedback provides information about motion and/or orientation. The question of conflict solution and corroborative action in the case of corresponding or contradictory sensory information was also addressed. The entire study was performed with the goal of not only understanding the postural control system but also exploring the potential clinical usefulness of these tests.
Material and methods
Apparatus Subjects stood on a movable force-measuring platform (Tonnies Inc.) with their feet 4 cm apart. Strain gauges at the four corners of the platform measured the forces perpendicular to the platform and allowed calculation of the displacement of the CFP in anterior-posterior and lateral directions. EMGs from both legs were recorded with surface electrodes from the anterior tibia1 and triceps surae muscles. EMG signals were fullwave rectified, band-pass filtered, and amplified.
Changes in visualfeedback The contribution of vision to postural stabilization was measured in the following way: (1) To assess visual stabilization of the quiet stance, sway parameters were compared while standing with the eyes open and closed respectively. (2) To investigate whether the important parameter for visual stabilization was the orientation of contours or whether it was motion, the earlier experimental set up by Amblard and Crkmieux [26] was applied to our displacement conditions. We used a 4 Hz stroboscopic illumination of the surrounding laboratory. (3) Conflicting information from the different visual feedback loops were tested using two paradigms: (a) To study the effect of large field visual motion that contradicts the gravitational input of stationarity, subjects stood in front of a curved projection screen which fully covered the visual field in its vertical extension. The remaining lateral parts of the visual field were covered by flat white projection surfaces. An optokinetic pattern projector above the head of the subject produced a pattern of horizontally oriented black-and-white stripes. These stripes could be moved either up- or downwards with an angular velocity of 65"/s or kept stationary. (b) To study the reverse conflict, i.e. veridical vestibular feedback about spontaneous sway but visu-
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a1 perception of stationarity, the visual scene was stabilized with respect to head movements. Subjects wore a very light paper dome that surrounded the head entirely and moved with it like a hat. Its inner surface was covered with black and white stripes. Changes in vestibular conditions
To investigate the vestibular contribution to postural sway, static vestibular input was modified by changing the head position prior to platform displacement. This manoeuvre puts the utricles (and saccules) into in an anomalous position away from the optimal working range. The following conditions were compared: head in its normal position (eyes closed), head tilted forward (30"), head extended as far as posible backwards (45"), or bent to the left or right shoulder (45") respectively. Changes in somatosensory input
In order to assess the contribution of somatosensory information from foot and ankle joint receptors, we applied ischaemia. Ischaemia is known to affect the fast-conducting Ia fibres from small foot muscles first. Thus this technique allows for selective (early) measurements of the effects of sensory deprivation [ 161. After recording with platform tilts and sinusoidal platform movements under normal physiological conditions, two blood-pressure cuffs were applied above the level of the ankle joints on both sides. The pressure of the two cuffs was increased to 300 mmHg. The effect of ischaemia on motor neurons and somatosensory input was tested every 5 minutes between single trials by manually determining the force of maximal voluntary dorsiflection and plantarflection of the big toe and the foot. The sensitivity for vibration or tactile stimulation and position sense of the big toe and the ankle joint were also tested. Platform displacements
The equilibrium was perturbed with sudden toe-up ramp rotations of the platform by 4" with a velocity
of 80°/s in a sequence with random intervals of eight runs each. The initial body position was monitored by the experimenter (for details see [14, 193). Sinusoidal toe-up and -down platform displacements around the ankle joint were performed with a frequency of 1 or 0.3 Hz and with an amplitude of f. 4". Data analysis
Onset latencies of EMG activity after sudden tilt as well as durations and integrals were calculated after visual identification of the onset and termination of each EMG component in each of eight consecutive single trials. EMG and CFP recordings were then averaged over eight runs and plotted. The anteriorposterior displacements of the CFP during sinusoidal platform movements were fed into a computer for on-line Fourier analysis. The total duration of sampling was 44.1 s. We calculated the RMSs of the power spectrum for the whole frequency range between 0 and 12.5 Hz. Angular displacements of the head and hip in the anterior-posterior direction were recorded by means of goniometers rigidly attached to head and hip belts. These data also were subjected to a Fourier analysis. Subjects
Ten healthy subjects aged between 18 and 33 years participated in the experiments with altered visual and vestibular conditions and four healthy men aged between 28 and 32 years in the experiment with altered somatosensory input.
Results Standing on a stable surface
Postural sway increases by about 50% with closed eyes as compared to open eyes. The anterior-posterior sway is invariably greater than sway in the lateral dimension with and without the visual contribution to postural stabilization [ 171.
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Sinusoidal displacements
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The sinusoidal movement of the platform provoked a continuous anterior-posterior regulation of upright posture. The Fourier spectra revealed that the greatest power of CFP displacement was at the frequency of the imposed displacement (Fig. 1). Additionally, there were lower- and higher-frequency components of body sway besides the one at the stimulus frequency which contributed to postural control. The total amount of anterior-posterior body sway as measured by the RMSs of Fourier spectra was significantly influenced by the seven dif-
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Fig. 2. RMS of body sway from the Fourier power spectra during 1 Hz sinusoidal platform movements (means and standard deviations from 10 subjects). The visual conditions from left to right were: normal visual surround, viewing a stationary stripe pattern, stroboscopic illumination, stabilized vision, eyes closed, stripe movement upwards, and stripe movement downwards.
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Fig. I . (1) Original recording of the anterior-posterior body sway during sinusoidal platform movements at I Hz over a time period of 40 s. (2) Fourier power spectra of sway with a linear scale for the ordinate with eyes open (A) or eyes closed (B). Note the increased power of body sway around the stimulus frequency (1 Hz) and between 2 and 3 Hz when the eyes are closed.
ferent visual and five different vestibular conditions (for details see [14]). RMSs increased from the eyesopen condition to stroboscopic illumination, stabilized visual surround, and eyes closed. Stripe patterns moving upwards created less postural instability than stripe patterns moving downwards (Fig. 2). The RMSs of anterior-posterior body sway with the eyes closed were identical for normal head position and head flexed forwards. Body sway was increased with the head bent to the right and left shoulder and was further increased when the head was extended to the neck (Fig. 3). Body sway as measured by the RMSs of the power spectrum as well as head and hip sway increased with increasing time of ischaemia at the level of the ankle. The biggest effect could be observed after 45 minutes of ischaemia [19]. The mean RMSs increased from 121 to 196 after 45 minutes of ischaemia, the peak amplitude in the Fourier spectrum increased from 39 to 138 mV. The results indicate that visual, vestibular, and somatosensory feedback are essential for the compensation of continuously applied low-frequency disturbances to the upright standing human. Dis-
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Changing the visual, vestibular, or somatosensory experimental conditions had no significant influence on latency, duration, and integral of each of the three EMG responses or the displacement of the CFP during the first 500 ms (Figs. 4 and 5). Thus phasic EMG responses to rapid ankle rotation and related torque changes reflected through the CFP remained unchanged despite very different visual, vestibular, and somatosensory inputs. In addition,
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Fig. 3 . Original recordings of the platform stimulus at 1.0 and 0.3 Hz and displacements of the anterior-posterior component of the CFP under different static vestibular conditions with the eyes closed. Note the increase of body sway when the head is extended backwards or bent to the right or left shoulder.
turbed somatosensory and vestibular information obviously can be compensated by visual input. Transient ramp displacements
With the eyes open or closed, sudden tilt of the platform toe-up with a velocity of 8Oo/s and an amplitude of 4" evokes a short-latency response with the mean latency between 37 and 50 ms and a medium latency response after between 75 and 110 ms in the triceps surae muscle. The long-latency response, with a latency of between 110 and 124 ms, appears in the antagonist, the anterior tibial muscle.
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ms Fig. 4. Averaged recordings (eight trials) of rectified EMGs from the anterior tibial (TA) and triceps surae (TS) after a rapid tilt of the platform toe-up (80"/s, 4"; see upper trace) under different conditions of static vestibular input. SL = short latency; ML =medium latency; LL = long latency response. Note the unchanged EMG recordings under different vestibular conditions.
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Fig. 5. Averaged recordings (eight runs) of the displacements of the CFP, head angle and hip angle after sudden tilts of the platform toe-up (vertical dotted line) with increasing time after the beginning of ischaemia above the ankle. Upward deflections or the recordings imply an anterior shift of the body or a forward inclination of head and hip. Despite considerable interindividual differences between the four subjects (rows 1 4 ) , there is a close similarity of the induced sway within one subject throughout the entire experiment between minutes 0 and 43.
we observed no side differences between the EMG responses from the right and left legs when the head was tilted to the right or left side respectively. Experiments in patients
In order to get more insight into the role of the vestibular input for posture control, we performed platform tilts in three patients with a total bilateral loss of vestibular function. In two cases this was due to bilateral surgery of a neurinoma of the VIIIth nerve. In one case, it was due to inherited degeneration of the VIIIth nerve. The missing vestibular function was in all cases proved by absent ca-
lorics, and absent vestibulo-ocular reflexes in horizontal and vertical direction with low- and highfrequency stimulation. In the two operated cases, acoustically evoked responses were absent. Lesions outside the vestibular system were excluded by neurological examination, electrophysiological testing, somatosensory evoked potentials, visual evoked potentials, by computed tomography, and nuclear magnetic resonance imaging. The latencies of short- and medium-latency EMG responses in triceps surae and the long-latency response in anterior tibia1 muscle were not different in patients with bilateral vestibular deficit than in normals (Fig. 6). The size of the long-latency
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Bilateral vestibular deficit
Normal subject Stimulus
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Fig. 6 . Rectified averaged EMG recordings after platform tilt toe-up in a normal subject and a patient with bilateral vestibular deficit with eyes open and eyes closed. Short-, medium-, and long-latency reflexes can be observed with normal latency in the patient with bilateral vestibular deficit. The size of the long-latency response, however, is decreased. For abbreviations see Fig. 4.
EMG response, which stabilizes posture, however, was decreased. The number of subjects was too small to perform a statistical analysis. In some of the trials, the patients were not able to keep upright after platform tilt when the eyes were closed. These results confirm that the size of the long-latency EMG response is modulated by vestibulospinal influences [20]. Discussion
The present study confirms that visual, vestibular, and somatosensory feedback contribute to the compensation of a low-frequency disturbance continuously applied to the upright standing human, whereas, provided that proprioceptive feedback
through spindle afferents from leg muscles is intact, these additional feedback loops seem to be insignificant for the compensation 'of transient high-frequency postural disturbances. Visual input can compensate for the deficiency of somatosensory and vestibular input [19]. Our results with stabilized visual conditions are in contrast with those of Nashner and Berthoz [8] and Vidal et al. [21]. In their experiments with linear displacements, EMG responses as early as 100 ms were significantly attenuated when the visual surround moved together with the head, whereas no such attenuation was seen in our experiments. This is most probably due to different stimulus conditions. The angular velocity of displacement around the ankle joint was around 6"/s in their stu-
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dy compared to 80°/s in our experiments. Another explanation could be that visual input is much more important in cases of linear translation (as in Nashner and Vidal's experiment) than with tilt around the ankle joint, as in our experiments. A third alternative could be that our subjects were continuously provided with stabilized visual surrounding even between platform tilts whereas visual stabilization started in Nashner and Berthoz' [8] conditions at the moment of linear surface displacements. Our results by no means indicate that afferent information is not used for rapid postural control, but that after exclusion or malfunction of one of the three systems the other two are able to compensate completely. At least two of the three senses must be out of order to provoke falling after a sudden disturbance. This was also shown in the experiments with bilaterally labyrinthectomized patients who have normal EMG responses and perfect postural stabilization with rapid tilt as long as the eyes are open but may fall with the eyes closed. The same is true in patients with severe demyelinating polyneuropathy and missing position sense as well as in patients with Friedreich's ataxia who are quite stable with their eyes open but fall backwards with the eyes closed [22, 231. Considering the possible modulation of stretch reflex amplitudes with head tilt, our results are in disagreement with those obtained in humans who were tilted on a tilting table in pitch with their neck fixed [24, 251. We were unable to find a significant modulation of stretch reflex amplitudes by alteration of static vestibular input. This can possibly be ascribed to the compensatory effect of neck afferents on tonic labyrinthine reflexes. Visual, vestibular, and somatosensory afferent information clearly influences the compensation of sinusoidally applied disturbances. Stroboscopic illumination resulted in increased body sway. The importance of visual movement perception as opposed to perception of contour orientation was already evaluated by Amblard and Crkmieux [26], who were able to induce postural destabilization in quietly standing humans by stroboscopic illumina-
tion. The fact that postural instability was greater with eyes closed than with stroboscopic illumination may indicate that the intermittent presentation of stationary contours also contributes to postural stability [27]. The most dramatic destabilizing effect was seen when moving patterns induced the perception of being tilted in pitch. The movement pattern induced perceived motion of the body in pitch in the direction opposite to that of the moving stripes. This leads to the perception of falling backwards in the case of stripes moving down. The asymmetry between the two conditions is explained by the fact that normal subjects feel much more uncomfortable and unsafe when tilted backwards than when tilted forwards. The result with changed afferent input from somatosensory receptors fits well with the assumption that spindle afferents have their working range above I Hz, whereas pressure, joint, and skin receptors are more important in the low frequency range. Vision has its working range below 1 Hz [3, 71 and therefore is able to compensate for the deficiency of somatosensory information under ischaemia with low-frequency sinusoidal stimulation. In summary, the comparison of the results obtained in this study with fast transient ramp and slow continuous sinusoidal platform displacement indicates that there are at least two different modes of postural stabilization. (1) One mode acts through reflex-like responses that are not immediately modified and possibly not even accessible to modifying inputs from the visual, vestibular, or somatosensory system but are organized in advance according to prior experience about functional objectives. Afferent information from spindle receptors is only used to trigger spinal and transcortical reflexes. Within the system, there is a certain amount of flexibility in both the time and amplitude domains [I 3,221 but this, although functionally adaptive, acts through preset modifications of the response pattern and not via feedback. Postural stabilization is performed normally as long as at least two of the three afferent systems contain congruent information. This mode subserves only fast corrections to fast (transient) disturbances.
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(2) A continuous mode, highly dependent on visual, vestibular, and proprioceptive feedback that subserves the compensation of low-frequency disturbances on the one side and of continuous displacements on the other. This mode is more subjected to adaptive changes [28]. The results indicate that postural studies in patients with deficits in vestibular, visual, or somatosensory and proprioceptive input should either be performed with low-frequency testing or during conflicting afferent input conditions or excluding at least two of the three afferent systems. Acknowledgements This paper has been supported by the Deutsche Forschungsgemeinschaft, SFB 307 A3.
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