INTRODUCTION

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STUDIES HAVE CLEARLY DEMONSTRATED that inputs from the vestibular apparatus have effects on the sympathetic nervous system. Animal studies have shown increases in sympathetic nerve discharge during stimulation of vestibular afferents (1, 6, 9, 20) and increased orthostatic intolerance with lesions of the vestibular nerve (5).

We have reported that static head-down neck flexion elicits marked increases in muscle sympathetic nerve activity (MSNA) and calf vascular resistance (12, 14) but has no effect on skin sympathetic nerve activity (SSNA) in humans (12). Static head-down neck flexion selectively stimulates the otolith organs of the vestibular apparatus. Thus the evidence suggests that stimulation of the otolith organs elicits a sympathetic response to muscle but not to skin. The increase in MSNA appears to be related to engagement of the vestibulosympathetic reflex because other factors (e.g., baroreceptors, neck receptors, and visual inputs) that could have produced the increase in MSNA have been systematically ruled out (11, 14).

In addition to the otolith organs, the vestibular apparatus also includes the semicircular canals. The semicircular canals are involved in sensing angular acceleration of the head. Currently, no information exists regarding sympathetic nerve responses to natural stimulation of semicircular canals in humans. The purpose of this study was to determine whether sinusoidal yaw head rotation (YHR) alters MSNA and SSNA in humans. YHR (i.e., rotation of the head in the horizontal plane) is commonly used to study the semicircular canals because it stimulates the horizontal semicircular canals while not engaging the otolith organs. The results of the present study demonstrate that YHR does not affect sympathetic outflow in humans.

	METHODS

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Subjects

Experimental Design

Yaw head rotation. The subjects were oriented with the head facing forward. After 3 min in baseline position, the head was rotated from side to side (~180° in horizontal plane). Sinusoidal YHR was performed at 0.1, 0.6, and 1.0 Hz with the assistance of an auditory signal (i.e., metronome). The head was returned to the baseline position after 3 min of YHR for 3 min of recovery. During YHR performed at 0.1 Hz, an investigator manually moved the head for the subject.

Study 1. MSNA was recorded during YHR in the sitting position. YHR was performed at 0.1 (n = 8), 0.6 (n = 13), and 1.0 Hz (n = 12).

Study 2. SSNA was recorded during YHR in the sitting position. YHR was performed at 0.1 (n = 8), 0.6 (n = 8), and 1.0 Hz (n = 9). During the SSNA studies, subjects had their eyes closed.

Measurements

Continuous measurements of arterial blood pressure and heart rate were made using a Finapres blood pressure monitoring unit (Ohmeda, Englewood, CO). Changes in skin blood flow were determined by laser Doppler (ALF21D, Advance, Tokyo, Japan). The flow probe was placed on the top of the foot (dorsal aspect), where stroking of the skin elicited skin afferent fiber discharge. Skin vascular resistance was calculated as mean arterial pressure divided by skin blood flow.

All data were collected online (MacLab 8e, ADInstruments, Milford, MA) with a Macintosh computer (Quadra 840AV). The mean voltage neurograms, blood pressure tracing, and blood flows were routed to an online computer for monitoring and data collection purposes throughout the study.

Data Analysis

A one-way, within-subject, repeated-measures ANOVA was used to determine the significance of YHR on the dependent variables in each study. A significance level of P < 0.05 was used for all tests. All values are means ± SE.

	RESULTS

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YHR did not change MSNA, expressed as either burst frequency or total activity, from baseline at any frequency (Table 1 and Fig. 1). YHR responses to change in head direction (e.g., right to left) were similar at all frequencies. At 0.1 Hz, MSNA was unchanged from 30 ± 4 to 29 ± 3 bursts/90 s and from 207 ± 44 to 196 ± 43 units/90 s, burst frequency and total activity, respectively. Similarly, YHR resulted in MSNA responses of 20 ± 3 to 20 ± 3 bursts/90 s and from 237 ± 54 to 217 ± 46 units/90 s at 0.6 Hz and from 28 ± 4 to 27 ± 4 bursts/90 s and from 273 ± 55 to 246 ± 46 units/90 s at 1.0 Hz.

View larger version (19K): [in this window] [in a new window]   Fig. 1.   Muscle sympathetic nerve activity (MSNA) responses to yaw head rotation at 0.1, 0.6, and 1.0 Hz for n subjects. Right and left signify direction of head rotation. BL, baseline. Yaw rotation had no affect on MSNA.

As observed during the MSNA studies, YHR did not alter SSNA at any frequency or during change in head direction (Table 1 and Fig. 2). At the very slow frequency, 0.1 Hz, SSNA was unchanged from 27 ± 3 to 28 ± 4 bursts/90 s and from 111 ± 28 to 137 ± 40 units/90 s, burst frequency and total activity, respectively. At 0.6 Hz, SSNA was 15 ± 2 bursts/90 s and 212 ± 47 units/90 s at baseline. During YHR, SSNA was 17 ± 3 bursts/90 s and 210 ± 60 units/90 s. The SSNA response at 1.0 Hz was 18 ± 2 bursts/90 s and 139 ± 34 units/90 s at baseline and 20 ± 3 bursts/90 s and 163 ± 43 units/90 s during YHR. Similarly, there was no change in skin blood flow or skin vascular resistance during YHR at any frequency (Table 1).

View larger version (16K): [in this window] [in a new window]   Fig. 2.   Skin sympathetic nerve activity (SSNA) responses to yaw head rotation at 0.1, 0.6, and 1.0 Hz for n subjects. Right and left signify direction of head rotation. Yaw rotation had no affect on SSNA.

Heart rate and mean arterial pressure responses to YHR are presented in Table 1. YHR did not affect mean arterial pressure and heart rate at any frequency with the exception of heart rate at 1.0 Hz during the SSNA study (66 ± 5 to 69 ± 5 beats/min).

	DISCUSSION

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The purpose of this study was to determine whether natural stimulation of the horizontal semicircular canals alters MSNA and SSNA in humans. We tested this question by having subjects perform YHR. YHR failed to elicit any significant changes in sympathetic outflow to either muscle or skin. The failure of YHR to change MSNA contrasts with the increases in MSNA demonstrated with static head-down neck flexion, which stimulates the otolith organs. These findings support the concept that the otolith organs but not the horizontal semicircular canals participate in the regulation of SNA.

Studies by Yates and co-workers (18-20, 22) have failed to find any evidence that the semicircular canals modulate SNA in the cat. This is in contrast to their findings that clearly show a role for otolith organs in the regulation of SNA (18, 19, 22). Costa et al. (3) reported no change in MSNA in five subjects during caloric stimulation of the tympanic membrane by cold water. Conversely, Cui et al. (4) have reported increases in MSNA during caloric stimulation of both hot and cold water. Like YHR, caloric stimulation selectively stimulates the horizontal semicircular canals. However, unlike caloric stimulation, YHR does not elicit symptoms of dizziness and nausea, factors that could have altered sympathetic responses.

The failure of SSNA to change with YHR indicates that horizontal semicircular canals do not contribute to the regulation of sympathetic outflow to skin in humans. This finding and our previously reported finding of no change in SSNA during head-down neck flexion strongly suggest that the vestibular system does not modulate SSNA (12). Five subjects who had SSNA recorded during YHR also performed head-down neck flexion. As reported previously (12), there was no difference in the SSNA response to head-down neck flexion.

We observed that during YHR, heart rate and mean arterial pressure were not changed. These results are not surprising because YHR did not alter sympathetic outflow to either muscle or skin. These findings suggest that YHR (activation of the horizontal semicircular canals) does not powerfully influence cardiovascular responses.

Convertino et al. (2) reported that sinusoidal yaw rotation resulted in an attenuation of the carotid-cardiac baroreflex. They concluded that vestibular stimulation of the semicircular canals resulted in an inhibition of vagally mediated baroreflex control of heart rate. Although we did not specifically examine this question, our data indicate that stimulation of the horizontal semicircular canals by YHR does not significantly affect heart rate. However, the possible discrepancy between the study of Convertino et al. (2) and our study might be explained by differences in methodology. In the current study, we presumably did not alter the carotid baroreceptors, unlike Convertino et al.(2), who used neck suction.

YHR used in the present study stimulates the horizontal semicircular canals. Thus our findings are limited to the stimulation of these semicircular canals. It is possible that stimulation of the vertical (anterior and posterior) canals may produce different results. These vestibular receptors cannot be selectively stimulated in humans without concomitant stimulation of the otolith organs. However, in the cat, it has been shown that the medial and inferior vestibular nuclei are critical for the production of the vestibulosympathetic reflex (10, 17, 21, 22). This area receives afferent projections primarily from the horizontal canals but not the vertical canals (13). Thus, if human neural circuitry is similar to that of the cat, it would appear that the vertical canals would not participate in vestibular regulation of SNA. It should be noted that the medial and inferior vestibular nuclei receive significant afferent projections from the otolith organs (7, 13).

YHR activates not only the horizontal semicircular canals but also neck muscle afferents. Thus it is possible that neck afferents may be influencing SNA and obscuring the results. For example, neck afferents may be inhibiting SNA and preventing us from observing an increase in SNA. However, we do not believe this is the case. We have previously demonstrated in humans that static yaw head rotation does not elicit changes in MSNA (11). Thus, in a movement that engages the same neck muscles, no alterations in sympathetic activity occurred. In addition, in a preliminary report (15), we have shown that neck and forearm skeletal muscles evoke similar sympathetic responses. During this study, unloaded (supporting only the weight of the head) neck exercise in the prone position did not change MSNA. Only during isometric neck exercise at 10 and 30% maximum voluntary contraction of the neck extensor muscles did MSNA increase. Therefore, significant neck muscle force generation is required to elicit changes in SNA.

Because head movement was performed volitionally at 0.6 and 1.0 Hz, it is possible that sympathetic responses were blocked by central neural influences. It is known that during large voluntary head movements, the vestibular-ocular reflex is suppressed, presumably because vestibular nucleus neurons are inhibited by cortical commands (8, 16). However, there is currently no evidence to suggest that vestibular nucleus neurons that mediate vestibulosympathetic reflex are inhibited during voluntary head movements. In the current study no changes in sympathetic activity occurred during YHR at 0.1 Hz when head rotation was done manually without volitional effort. In addition, in a few subjects on whom manual head rotation was done at 0.6 Hz, no changes in sympathetic activity were observed.

In summary, we found that stimulation of the horizontal semicircular canals by sinusoidal YHR does not significantly alter sympathetic outflow to muscle and skin in humans. These findings support the concept that otolith organs but not semicircular canals contribute to sympathetic regulation in humans.

Perspectives