Effect of Galvanic Vestibular Stimulation on Human ...

RAPID

JOURNALOFNEUROPHYSIOLOGY Vol. 73, No. 2, February 1995. Printed in U.S.A.

PUBLICATION

Effect of Galvanic Vestibular Stimulation on Human Postural Responses During Support Surface Translations J. TIMOTHY INGLIS, CHARLOTTE L. SHUPERT, FRANTISEK HLAVACKA, AND FAY B. HORAK R. S. Dow Neurological Sciences Institute, Portland, Oregon 97209; Department of Physical Therapy, Faculty of Applied Sciences, University of Western Ontario, London, Ontario N6G lH1, Canada; and Slovak Academy of Sciences, Institute of Normal and Pathological Physiology, Bratislava, Slovakia SUMMARY

AND

CONCLUSIONS

1. We investigated the role of the vestibular system in postural control by combining galvanic vestibular stimulation (0.2-0.5 mA) with platform translations in standing subjects. Vestibular stimulation delivered 500 ms before and continuously during the platform translation produced little change in the earliest center of pressure (COP) and center of mass (COM) movements in response to platform translations, but resulted in large changes during the execution of the postural movement and in the final equilibrium position. 2. Vestibular stimulation produced anterior or posterior shifts in the position of COP and COM, depending on the polarity of the galvanic current. These shifts were larger during platform translations than during quiet stance. The peak of these shifts in COP and COM occurred at 1S-2.5 s after the onset of platform translation, and increased in magnitude with increasing platform velocity. The final equilibrium positions of COP and COM were also shifted, but these shifts were smaller and not dependent on platform velocity. 3. These results imply that a tonic step of galvanic current to the vestibular system can change the final equilibrium position for an automatic postural response. Furthermore, these results indicate that the vestibular system may play a larger role in interpreting sensory reafference during postural movements, and especially during fast postural movements, than in controlling quiet stance. Finally, these results indicate that the vestibular system does not play a critical role in triggering the earliest postural responses, but it may be critical in establishing an internal reference for verticality.

INTRODUCTION

The role of vestibular signals in automatic postural responses to externally imposed displacements in stance is debated. The vestibular system is sensitive to a wide range of head motions, including those typically observed during quiet stance (Benson et al. 1986; Grossman et al. 1988), and vestibulospinal pathways to the trunk and limbs are well known (Boyle et al. 1992; Shinoda et al. 1986, 1992; Wilson and Peterson 198 1) . The vestibular system could therefore serve any of several important functions in postural control. First, vestibular signals indicating head motion could trigger the onset of automatic postural responses (Horak et al. 1994; Melvill Jones and Watt 197 1) . Second, vestibular signals concerning the velocity of head motion could also be important for modulating the amplitude of automatic postural responses and scaling their magnitude to the magnitude of the postural disturbance (Allum et al. 1994; Horak et al. 1990; Keshner et al. 1987; Macpherson and Inglis 1993). 896

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Third, the vestibular system could contribute to developing the CNS’s internal representation of the direction of gravity (Borah et al. 1988; Fitzpatrick et al. 1994; Popov et al. 1986). Finally, the vestibular system may play a critical role in providing the sensory reafference (von Holst and Mittelstaedt 1973) during postural movements that would permit the CNS to determine whether an automatic postural response is appropriate and effective, i.e., whether the currently ongoing postural movement is appropriately matched to the intended movement and whether the body’s final position is properly aligned with the internal perception of verticality after an automatic postural response. The role of the vestibular system in postural control has been explored previously using galvanic vestibular current, but these studies have been limited to effects on body sway in quiet stance. Galvanic current delivered to the mastoid bones activates the peripheral vestibular afferents (Goldberg et al. 1984; Minor and Goldberg 199 1) and causes standing subjects to lean in different directions depending on the polarity of the current (B&ton et al. 1993; Hlavacka and Njiokiktjien 1985; Iles and Pisini 1992), suggesting that vestibular signals can trigger short-latency postural responses and that vestibular information about the direction of gravity determines body alignment. However, the interpretation of vestibular information depends on the configuration of somatosensory information about body alignment. Galvanic current delivered to subjects with the head facing forward causes them to lean laterally, but when the head alone or the trunk and head are turned to the side, the subjects lean forward or backward (Lund and Broberg 1983; Nashner and Wolfson 1974). Also, subjects who are externally supported show absent or altered responses to galvanic vestibular stimulation, suggesting that the CNS interprets vestibular signals differently depending on somatosensory cues (B&ton et al. 1993; Fitzpatrick et al. 1994; Popov et al. 1986; Storper and Honrubia 1992). To determine how vestibular sensory information contributes to the formulation and execution of responses to sudden perturbations in stance, we combined platform translations with low-level (0.2-0.5 mA) steps of galvanic vestibular stimulation. If the vestibular system contributes to the triggering or the amplitude modulation of the automatic postural responses, disruption of normal vestibular signals by galvanic stimulation should affect the onset or the amplitude of the earliest responses. If the role of the vestibular system is to provide sensory reafference during the postural move-

0 1995 The American

Physiological

Society

EFFECT OF GALVANIC

STIMULATION

ON POSTURAL

RESPONSES

897

form translation. Because some previous studies have indicated that the vestibular system is more heavily involved in responses to faster or larger perturbations (Horak et al. 1990; Peterka and Benolken 1992), we compared three different platform velocities: 1.4 cm/s, which is near the threshold of the vestibular system for linear movements; and 3X and 10X this threshold (Benson et al. 1986).

A 81

METHODS

Vestibular

Subjects

posterior

Subjects were seven healthy volunteers (4 males and 3 females, aged 24-38 yr). The experimental protocols described here complied with federal and institutional guidelines for protection of human subjects.

Vestibular I Platform

Experimental apparatus and procedure 1

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Time (s) B 81

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Vestibular Platform t

+ 0

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Time (s) FIG. 1. A: position of the center of pressure (COP) as a function of time for a 14-cm/s translation only, and for anterior and posterior vestibular stimulation paired with the 14-cm/s translation. Arrows on abscissa: onset times for vestibular stimulation and platform movement. For anterior stimulation the anode was on the forward ear, which resulted in anterior sway, and for posterior the cathode was on the forward ear, resulting in posterior sway. In this and all following figures, group means are displayed and positive numbers indicate anterior movement. B: position of COP as a function of time for 14-cm/s translation paired with anterior and posterior vestibular stimulation and for anterior and posterior vestibular stimulation during quiet stance ( ‘ ‘Vestibular stimulation only’ ’ )

ment or to signal body alignment with respect to gravity, vestibular stimulation should have a greater effect on later components of the automatic postural response, rather than the earliest components, which are programmed and executed before feedback from the active postural movement is available (Horak et al. 1989). To examine the interaction of vestibular and somatosensory information for postural control, the galvanic vestibular stimulation in these experiments was either congruent with or opposed to the direction of somatosensory sway signals generated by backward plat-

Subjects stood on two computer-controlled hydraulically driven force platforms. Postural responses were quantified by measuring the position of the center of pressure (COP) on the platform surface and the position of the whole body center of mass (COM). Active postural responses result in ankle torques that shift the position of COP and subsequently the position of the body’s COM. COP was calculated from vertical forces (250-Hz sampling). The position of COM was calculated using a multisegment model of the body (Koozekanani et al. 1980) from the positions of markers placed at the joint centers of the ankle, knee, hip, shoulder, and earlobe (Watsmart system, Northern Digital, 125Hz sampling). For galvanic trials, a constant-current isolation unit (A-M Systems, Model 2200) was used to deliver current to 9-cm2 pieces of carbon-rubber placed over the subjects’ mastoid processes. The current intensity was chosen for each subject and was the lowest at which the subject both reported a slight feeling of disorientation with the eyes closed and demonstrated a slight increase in body sway (range 0.2-0.5 mA). Subjects began each trial with the eyes closed and the head turned to the right. The experiment consisted of 60 trials (5 trials in each of 12 conditions), and each trial was 8 s in duration. The 12 conditions consisted of 3 galvanic conditions ( anode on left ear with rightward head turn, causing anterior sway; anode on right ear, causing posterior sway; and no galvanic current) combined with 4 platform conditions (quiet stance; 9-cm backward translations at 1.4,4.2, or 14 cm/s). Conditions were presented in random order by dividing the 60 trials into five blocks of 12 trials and presenting 1 trial from each condition in random order within each block. Each trial began with a lOO-ms baseline period. For trials involving both galvanic vestibular stimulation and platform movement, vestibular stimulation was applied after the baseline period and the current was ramped up to the chosen intensity over a 52-ms period and maintained for the duration of the trial (8 s). Vestibular stimulation was initiated 500 ms before the onset of platform movement. A 500-ms lead of vestibular stimulation with respect to the onset of platform movement was shown during pilot studies to produce the largest effects on postural responses. Control trials consisted of vestibular stimulation or platform movement alone.

Data analysis COP (filtered at 30 Hz) and COM (filtered at 5 Hz) were averaged for like trials within subjects. All subjects were required to realign COP and COM to initial positions between trials; therefore these initial values were arbitrarily assigned to a value of 0, and positive numbers indicate anterior movement. To clearly display the effect of vestibular stimulation on postural responses without the component of the response due to the translation alone, the “net” effect of vestibular stimulation on COP and COM was calculated

898

J. T. INGLIS, C. L. SHUPERT, F. HLAVACKA,

the grand means for all seven subjects. The results for different experimental conditions were compared using a repeated-measures multiple analysis of variance; post-hoc analyses were performed using Newman-Keuls procedures (a! = 0.05).

A n E ,o

1

14cmls 4.2 cm/s 1.4 cm/s Vestibular only

AND F. B. HORAK

m RESULTS --......Bo~g~ The effect of galvanic vestibular stimulation on the earliest

components of the responses to platform movement was small, but the effects on later components were larger. Figure 1A shows that large COP position differences due to continuous vestibular stimulation before and during platform translations do not appear until 1 - 1.5 s after the onset of platform translation, long after the initial postural response (Horak et al. 1990). These differences persist throughout the trial and result in different final equilibrium positions for responses to displacement during anterior and posterior vestibular stimulation compared with responses to platform translation only ( compare ‘ ‘Vestibular anterior’ ’ and ‘ ‘Vestibular posterior’ ’ 2 4 6 to “Platform only” ) . Figure 1B shows that the effect of Time (s) vestibular stimulation on the final COP position is larger when vestibular stimulation is paired with a translation than B when it is presented during quiet stance ( “Vestibular Stimulation only” ) . The very small COP position shifts due to vestibular stimulation before platform movement observed E 14cmls *WIOIW(OOOOOWO -0 1 here have been previously shown to have no effect on re4.2 cm/s sponses to translations and therefore do not account for the 1.4 cm/s --effect of pairing vestibular stimulation with platform translaVestibular only .SDSS.SS..I tions (Horak and Moore 1993). Figure 2, A and B, shows that the net effect of the vestibular stimulation paired with any platform velocity was larger than the effect of vestibular stimulation applied during quiet stance. If the effect of pairing galvanic vestibular stimulation with platform translation were an algebraic summation of the effects of platform translation and galvanic stimulation alone, the curves for galvanic stimulation alone and the curves for galvanic stimulation for the three platform velocities would be superimposed, because the component of the response due to the platform only has been subtracted from these curves (see Data analysis above). The largest effect 0 2 4 6 of vestibular stimulation occurred at 1.5-2.5 s after the onset Time (s) of the translation, which is during the execution of the posFIG. 2. A : net effect of vestibular stimulation on COP as a function of tural movement, and the magnitude of this effect increased time for 14-, 4.2-, and 1.4-cm/s translations paired with vestibular stimulawith increasing velocity ( see Table 1) . The differences in the tion and for vestibular stimulation during quiet stance ( ‘ ‘Vestibular only” ) . peak net COP for the different velocities were statistically Curves are formed by subtracting the results for conditions with posterior significant (all P values < 0.04, with 1 exception; 1.4 vs. vestibular stimulation from the corresponding results for conditions with 0

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anterior vestibular stimulation. Zero on abscissa: onset of platform movement. B: net effect of vestibular stimulation on center of mass (COM) . by subtracting responses to posterior vestibular stimulation (negative values) from the corresponding responses to anterior vestibular stimulation (positive values) and dividing the result by 2. This procedure removes the effect of the platform translation on COP and COM, which is common to both vestibular stimulation polarities, and averages the effect of posterior and anterior vestibular stimulation. The timing and amplitude of peak net COP and COM position changes and the final equilibrium position of COP and COM at the end of each trial were determined. The rate of change of the unsubtracted COP and COM was also calculated for 60-ms bins between 0.76 and 1 s (initial COP slope), and the timing and amplitude of the peak slope were determined. Analyses were performed on individual trials and then averaged to produce mean results for individual subjects, which were used for statistical comparisons. Figures show

TABLE

1.

COP and COM related to platform

COP Peak position, cm Final position, cm COM Peak position, cm Final position, cm Values are means

velocity

Quiet Stance

1.4 cm/s

4.2 cm/s

14 cm/s

0.9 5 0.5

1.7 Ifi 0.7

2.2 5 1.0

2.9 + 0.9

0.8 + 0.5

1.6 t 0.8

1.5 -+ 0.4

1.6 t 0.7

0.8 + 0.5

1.4 5 0.5

2.1 + 0.8

2.1 5 0.3

0.8 + 0.6

1.3 + 0.8

1.5 2 0.4

1.5 5 0.5

SD. COP, center of pressure; COM, center of mass.

EFFECT OF GALVANIC 10 8

1I

STIMULATION

Vestibular anterior Platform only

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14

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........

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RESPONSES

899

DISCUSSION

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200

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400

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600

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800

Time (ms) FIG. 3. COP in response to translations alone and translations with anterior and posterior vestibular stimulation for 14-, 4.2-, and 1.4-cm/s translations plotted over the 1st 800 ms. Note change in time scale from Figs. 1 and 2. Vertical dashed line: onset of platform movement. Initial peak slopes are indicated by slope lines superimposed on the data.

4.2 cm/s, P < 0.08). The net COM change due to vestibular stimulation was also larger for larger velocities, with one exception (see Fig. 2B): the difference between 14 and 4.2 cm/s was not statistically significant (P < 0.9; all others P < 0.05). In contrast to the peak position change for net COP and COM, the final net COP and COM positions were not different for different platform velocities. However, the effect of vestibular stimulation during a platform translation was always larger than the effect of vestibular stimulation during quiet stance (see Table 1). For COP, the shifts in final position for the different velocities were all significantly larger than the shift for vestibular stimulation alone (all P values < 0.007), but they were not different from each other. The pattern of results was similar for COM (see Table 1); the final positions for all velocities were different from vestibular stimulation only (all P values < O.OS), but not from each other. Galvanic vestibular stimulation had a small effect on the earliest part of the response to platform movement. Figure 3 shows COP in response to translations alone and translations with anterior and posterior vestibular stimulation for 14-, 4.2-, and 1.4-cm/s translations plotted over the first 800 ms. The peak rate of change for COP occurred at -200 ms after the onset of platform movement, and the time was not significantly different across conditions (P > 0.2; see Table 2). The amplitude of the peak rate of change- of COP for anterior and posterior vestibular stimulation combined with the platform movement was not significantly different from the peak COP rate of change for platform translation only. The peak rate of change of COP for posterior vestibular stimulation was slightly smaller than that for anterior stimulation, but the difference was quite small (roughly 3 cm/s for all 3 velocities) and did not achieve statistical significance (P < 0.08).

These findings support the hypothesis that the vestibular system plays a larger role in controlling the magnitude of postural movements and determining the final equilibrium position than in triggering the earliest postural responses to displacements. Stimulating the vestibular system with very small currents before and during postural responses resulted in only very small changes in initial peak COP velocity, but significant late changes in COP position and in the final equilibrium position. The tonic vestibular asymmetry induced by bipolar galvanic current in these experiments appears to set the internal estimate of verticality to a new position, and subjects appear to alter the magnitude of their automatic postural responses to realign their COM and COP with the newly established equilibrium position. When bipolar galvanic current was applied with the anode on the forward ear 0.5 s before and during unexpected support surface translations, subjects altered their postural responses to platform translations by increasing plantarflexion torque against the surface, which increases the anterior COP and shifts the final position of COM forward. Backward shifts in COM and COP responses to platform translations and final positions resulted when the cathode was at the forward ear. The shifts of COM and COP observed here are, however, not direct effects of galvanic stimulation on vestibulospinal reflex pathways. The timing of these changes suggests that they are corrections in body position initiated by the CNS when sensory reafference from the postural movement itself indicated that the initial automatic postural response would not bring the body into alignment with the changed internal estimate of upright. The largest change in COP responses to platform translations alone and responses to platform translations paired with galvanic stimulation did not occur in the earliest part of the automatic postural response, but rather occurred at 1.5-2.5 s after the onset of platform movement; that is, during the postural movement itself. Previous studies of changes in perceived body alignment resulting from galvanic stimulation are also consistent with the hypothesis of a change in the internal representation of the direction of gravity. Freely standing subjects lean in TABLE

galvanic

2.

Initial peak COP slope and time COP related vestibular stimulation and platform velocity

to

Platform Velocity, cm/s

Initial peak COP slope, cm/s Vestibular anterior stimulation No stimulation Vestibular posterior stimulation Initial peak COP time, ms Vestibular anterior stimulation No stimulation Vestibular posterior stimulation

1.4

4.2

14

6.5 t 2.2 5.5 2 2.2

19.5 + 5.8 16.0 + 5.8

51.5 2 11.9 49.7 !I 15.4

3.7 t 2.5

16.8 + 7.6

47.9 2 14.4

209 + 16 207 + 12

192 2 15 197 t 17

198 _+ 32 201 t 31

210 5 13

206 _+ 22

209 + 30

Values are means t SD. For abbreviations see Table 1.

900

J. T. INGLIS,

C. L.

SHUPERT,

F. HLAVACKA,

response to galvanic stimulation but perceive themselves to be aligned with gravity. When subjects are prevented from leaning during galvanic stimulation, however, they perceive themselves to be tilted in the opposite direction to the leaning posture they adopt when allowed to move; that is, they perceive themselves to be tilted away from their changed estimate of verticality (Fitzpatrick et al. 1994; Popov et al. 1986). Thus the results of both the present and previous findings are consistent with the hypothesis that a step change in galvanic current produces a step change in the estimate of the direction of gravity. This estimate is most likely derived from tonic otolith signals from pathways separate from those involved in vestibuloocular reflexes (VORs) . Tonic galvanic currents do not affect the yaw and pitch VOR, which suggests that tonic galvanic currents may preferentially affect pathways involved in perceived vertical and postural alignment (Minor and Goldberg 199 1) . The change in final equilibrium position due to vestibular stimulation was larger after a surface displacement than during quiet stance, and the change in final equilibrium position was more than the simple algebraic sum of the effect of platform translation and galvanic stimulation separately. These results are consistent with previous findings showing that the effect of a galvanic stimulus was greater when it was applied during an ongoing voluntary movement than during quiet stance (Popov et al. 1986; Smetanin et al. 1988). Consistent with this notion, Peterka and Benolken ( 1992) found that when accurate somatosensory cues about body motion are available, vestibular signals contribute to stabilization of COM at lower rotational velocities of the body than when somatosensory cues are unreliable. The somatosensory motion cues available during body motion may aid in the interpretation of vestibular signals that result from motion of both the body and the head. This integration of somatosensory and vestibular signals may improve the sensitivity of the CNS’s estimate of body motion. The magnitude of the effect of vestibular stimulation increased with platform velocity, suggesting that the vestibular system may also play a larger role in higher-velocity postural movements. Patients with bilateral loss of vestibular function also differ most from normal control subjects in making large or fast postural movements in response to support surface displacements (Horak et al. 1990). Although the vestibular system is sensitive to the range of head accelerations present during quiet stance (Benson et al. 1986), it has been hypothesized that vestibular signals do not contribute significantly to the control of posture until body movements exceed a higher threshold (Nashner et al. 1989). Peterka and Benolken ( 1992) found that somatosensorv signals dominate in the controlof posture in response to movini visual surrounds rotating at low velocities, despite the fact that the velocity of body sway often exceeded vestibular thresholds in these test conditions. Taken together, these previous findings and the results of the present study are all consistent with the idea that somatosensory signals trigger and shape initial postural responses to platform translations, whereas vestibular signals modulate the amplitude of postural responses. contribute to the interpretation of sensory reafference, and’signal the direction of upright to permit accurate realignment of the body after a disturbance in stance.

AND

F. B. HORAK

We thank M. Cohen and J. Knop for technical assistance. Dr. Inglis was supported by a Postdoctoral Fellowship from the Medical Research Council of Canada. Drs. Shupert and Horak were supported by National Institute of Deafness and Other Communications Disorders Grants DC-O 1104 and DC-O 1849. Address for reprint requests: F. B. Horak, R. S. Dow Neurological Sciences Institute, 1120 NW 20th Ave., Portland, OR 97209. Received

1 August

1994; accepted

in final form

3 November

1994.

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