HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS		QUICK SEARCH:   [advanced] Author: Keyword(s): Year:  Vol:  Page:

This Article Abstract Full Text (PDF) All Versions of this Article: 286/1/R25    most recent 00458.2003v1 Alert me when this article is cited Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in Web of Science Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via HighWire Citing Articles via Web of Science (26) Citing Articles via Google Scholar Google Scholar Articles by Gotoh, T. M. Articles by Morita, H. Search for Related Content PubMed PubMed Citation Articles by Gotoh, T. M. Articles by Morita, H.

NEUROHUMORAL CONTROL OF CIRCULATION AND HYPERTENSION

Roles of baroreflex and vestibulosympathetic reflex in controlling arterial blood pressure during gravitational stress in conscious rats

Department of Physiology, Gifu University School of Medicine, Gifu 500-8705, Japan

Submitted 13 August 2003 ; accepted in final form 10 September 2003

	ABSTRACT

TOP ABSTRACT METHODS RESULTS DISCUSSION GRANTS REFERENCES

 
Gravity acts on the circulatory system to decrease arterial blood pressure (AP) by causing blood redistribution and reduced venous return. To evaluate roles of the baroreflex and vestibulosympathetic reflex (VSR) in maintaining AP during gravitational stress, we measured AP, heart rate (HR), and renal sympathetic nerve activity (RSNA) in four groups of conscious rats, which were either intact or had vestibular lesions (VL), sinoaortic denervation (SAD), or VL plus SAD (VL + SAD). The rats were exposed to 3 G in dorsoventral axis by centrifugation for 3 min. In rats in which neither reflex was functional (VL + SAD group), RSNA did not change, but the AP showed a significant decrease (-8 ± 1 mmHg vs. baseline). In rats with a functional baroreflex, but no VSR (VL group), the AP did not change and there was a slight increase in RSNA (25 ± 10% vs. baseline). In rats with a functional VSR, but no baroreflex (SAD group), marked increases in both AP and RSNA were observed (AP 31 ± 6 mmHg and RSNA 87 ± 10% vs. baseline), showing that the VSR causes an increase in AP in response to gravitational stress; these marked increases were significantly attenuated by the baroreflex in the intact group (AP 9 ± 2 mmHg and RSNA 38 ± 7% vs. baseline). In conclusion, AP is controlled by the combination of the baroreflex and VSR. The VSR elicits a huge pressor response during gravitational stress, preventing hypotension due to blood redistribution. In intact rats, this AP increase is compensated by the baroreflex, resulting in only a slight increase in AP.

centrifuge; renal sympathetic nerve; feedback control; feedforward control; predictive control

Several candidates have been proposed as compensatory mechanisms that maintain arterial blood pressure (AP) during gravitational stress, namely, the baroreflex, vestibulosympathetic reflex (VSR), somatosympathetic reflex, and central command (9). Of these, the baroreflex is a well-known feedback control system for AP, playing a role in maintaining AP during bleeding, postural changes, and exercise (3, 10, 25). Vestibular receptors are also considered to be involved in maintaining AP through the VSR (27). In cats, moving the head up without changing the overall body position ("nose-up" vestibular stimulation) elicits an increase in AP, which is eliminated by vestibular lesions (26). Furthermore, hypotension induced by head-up tilting is augmented by vestibular lesions, showing that vestibular input plays an important role in maintaining AP during postural change (4, 8). Accordingly, the baroreflex and VSR may cooperate to maintain AP during gravitational stress. Ray (17) showed in humans an additive effect of baroreflex and VSR on muscle sympathetic nerve activity during head-down vestibular stimulation and lower body negative pressure.

The goal of the present study was to clarify the role of the vestibular and baroreflex systems in maintaining AP during gravitational stress. For this purpose, we measured AP, heart rate (HR), and renal sympathetic nerve activity (RSNA) in conscious rats during a gravitational stress of 3 G induced by centrifugation. Experiments were performed on rats with intact reflexes (intact), bilateral vestibular lesions (VL), bilateral sinoaortic denervation (SAD), and VL plus SAD (VL + SAD).

	METHODS

TOP ABSTRACT METHODS RESULTS DISCUSSION GRANTS REFERENCES

 
Male Sprague-Dawley rats weighing 320-360 g (12-14 wk old) were used (n = 23) and were maintained in accordance with the "Guiding Principles for Care and Use of Animals in the Field of Physiological Science" of the Physiological Society of Japan. The experiments were approved by the Animal Research Committee of Gifu University.

Two to three weeks before the start of the experiment, surgical intervention to induce SAD was performed on the SAD and VL + SAD groups. The rats were anesthetized with pentobarbital sodium (50 mg/kg body wt ip). Under a surgical microscope, the aortic depressor nerve was isolated and dissected by a midcervical incision, and the carotid sinus was isolated from the surrounding connective tissues. After surgery, an antibiotic (cefpimizole sodium, 0.3 g/kg body wt im) was administered for 3 days to prevent infection.

One day before the experiment, another surgical intervention was performed on all four groups. The rats were anesthetized using pentobarbital sodium (50 mg/kg body wt ip); then a polyethylene catheter (PE-50, Becton Dickinson, Sparks) for AP measurement was inserted into the abdominal aorta at a level immediately below the diaphragm through the femoral artery, and another for drug administration was inserted into the inferior vena cava through the femoral vein. These catheters were exteriorized at the back of the neck. For RSNA recordings, the postganglionic renal sympathetic nerve was isolated by a right flank incision, and two stainless steel electrodes (AS633, Cooner Wire, Chatworth) were placed around it (13). The nerve and electrodes were covered and fixed with silicone gel (Semicosil 932 A and B, Wacker Chemie, Munich, Germany), and the electrodes were exteriorized at the back of the neck. To avoid accidental damage, the electrodes and catheters were covered with a flexible spring (OD 3.0 mm) that was sutured to the neck skin using a plastic connector. Due to the flexibility of the spring, rats could move almost freely inside the cage. In the VL and VL + SAD groups, vestibular lesions were produced by injection of sodium arsanilate solution into the bilateral middle ear cavities (100 mg/ml, 50 µl/ear) (5, 6). Each rat was placed in a custom-made aluminum cage (35 x 25 x 17 cm), which was placed inside the rotating box of the centrifuge immediately after surgery to allow the rats to become accustomed to the environment of the experimental room. The temperature in the experimental room was maintained at 24°C.

One day later, gravitational stress in the dorsoventral direction was applied to the rats in the prone posture by centrifugation using a custom-made gondola-type rotating box (Shimadzu, Kyoto, Japan; Fig. 1). The AP catheter was connected to a pressure transducer (MP5200, Baxter). It was vital for the transducer probe to be fixed at the same level as the catheter tip, since a difference in level between the two would result in a hydrostatic pressure difference on a change in gravity. The signal from the AP transducer was transmitted to an amplifier (AP-621G, Nihon Kohden, Tokyo). The electrodes for RSNA recording were connected to another amplifier (AP-651J, Nihon Kohden) equipped with a 50- to 2,000-Hz band-pass filter. A gravity sensor (MTS-050, Mitec, Hiroshima, Japan) was placed on the cage floor to measure gravity. All signals were recorded using a DAT data recorder (RD-145T, TEAC, Tokyo). Each experiment consisted of three 3-min periods: a control period at 1 G, a 3-G period, and a recovery period at 1 G. The centrifuge automatically controlled its speed to maintain gravity at the set point.

View larger version (8K): [in this window] [in a new window]   Fig. 1. Schematic illustration of the centrifuge. The arm turns around the vertical axis. Since the rotating box is suspended to move freely at the end of the arm, the direction of the resultant force generated by centrifugal force and natural gravity is always from the top of the rotating box to the bottom.

After completion of the experiment, SAD was confirmed by the absence of an HR response to an increase in AP caused by injection of an ₁-receptor-selective agonist (phenylephrine hydrochloride, 3 µg/kg body wt iv) (23). VL was confirmed by a swimming test, in which rats were gently put into the small tub filled with warm water (5, 6). When the lesion was complete, the rat was not able to recognize the direction of the water surface and continued to turn around inside the water. In contrast, when the lesion was incomplete, the rat was able to float on the water. Although we did not confirm VL by the histological means, it is known that the injection of sodium arsanilate solution into middle ear cavity elicits a degeneration of the vestibular nerve (1).

The data were played back and sampled using an analog-to-digital converter (PowerLab, ADinstruments, Castle Hill, Australia) at a rate of 1,000 samples/s. The HR was calculated using the AP signal. To eliminate the variability in AP or HR between rats, the results were expressed as the change from the baseline levels (AP and HR). The amplified RSNA signal was rectified and the moving average calculated (mean RSNA; MRSNA). For comparisons between rats, the MRSNA was expressed as the percent change from the baseline level.

To examine the detailed time course of the change, the data for the first minute of gravitational stress were averaged over 0-10, 10-20, 20-30, and 30-60 s after onset of the gravitational stress, and the remainder was averaged over 1 min. To analyze the time course of changes, repeated-measures two-way ANOVA was used, followed by Fisher's protected least significant difference test. For comparisons between the four groups, the differences between the levels during the first 30 s of gravitational stress and the baseline levels were calculated and compared using ANOVA followed by the Scheffé's test. The significance level was set at P < 0.05.

	RESULTS

TOP ABSTRACT METHODS RESULTS DISCUSSION GRANTS REFERENCES

 
Table 1 shows the baseline levels for each group before application of gravitational stress. Although the AP was not significantly different between the four groups, the HR was significantly higher in the VL group than in the intact group.

Figure 2 shows typical AP, HR, RSNA, and MRSNA responses during the first 30 s of gravitational stress. A rapid increase in gravity from 1 to 3 G was induced by centrifugation. In the intact rat, the AP started to increase at the onset of gravitational stress and then remained above the baseline level, while the HR gradually decreased and RSNA increased. These responses were modified by VL and/or SAD. In the VL rat, the RSNA increase was attenuated, and the pressor and bradycardial responses were completely abolished. In contrast, in the SAD rat, the AP and RSNA increases were markedly augmented, while the HR decrease was reduced compared with in intact rats. In the VL + SAD rat, the AP decreased, while the HR and RSNA did not change.

View larger version (27K): [in this window] [in a new window]   Fig. 2. Original recordings of gravity, arterial blood pressure (AP), heart rate (HR), renal sympathetic nerve activity (RSNA), and mean RSNA (MRSNA) responses to centrifugation in conscious rats with intact reflexes (Intact, A), vestibular lesions (VL, B), sinoaortic denervation (SAD, C) and VL + SAD (D). Note that the scale of the y-axis for the MRSNA is different in the different panels. bpm, Beats/min.

The averaged data for the whole experimental period (1-G, 3-G, and 1-G recovery period) are presented in Fig. 3. In the intact group, the AP increased during the initial 30 s of gravitational stress and then returned to the baseline level. In the SAD group, the AP increased markedly and peaked at 20 s of gravitational stress and then gradually returned toward the baseline level. In the VL group, the AP was stable throughout gravitational stress, whereas in the VL + SAD group, it showed a significant decrease. It is interesting to note that the increase in AP in the intact and SAD groups occurred immediately after the onset of gravitational stress, whereas the AP decrease in the VL + SAD group was delayed. A marked bradycardia was seen in the intact and SAD groups, but not in the VL and VL + SAD groups, showing that it was caused by vestibular input. Bradycardia continued even after cessation of gravitational stress. RSNA increased in the intact, VL, and SAD groups but was unaffected in the VL + SAD group.

View larger version (24K): [in this window] [in a new window]   Fig. 3. Changes in AP (A), RSNA (B), and HR (C) from baseline levels in conscious rats with intact reflexes, VL, SAD, or VL + SAD. Each data point represents the mean ± SE for 5 (VL + SAD group) or 6 (other groups) animals. The horizontal bar represents the period of gravitational stress induced by centrifugation. *P < 0.05 vs. baseline (repeated-measures 2-way ANOVA followed by Fisher's protected least significant difference test).

Because an increase in AP was observed only during the initial 30 s of gravitational stress in the intact group, we compared changes during this period between the four groups (Fig. 4). The increase in AP was significantly larger in the SAD group than in the intact group, showing that the baroreflex suppressed the AP increase in the intact group. Moreover, the decrease in HR seen in the intact group was augmented by SAD. The RSNA increase observed in the intact group was augmented by SAD and attenuated by VL, suggesting that the VSR augmented, and the baroreflex attenuated, RSNA in the intact group.

View larger version (14K): [in this window] [in a new window]   Fig. 4. Averaged changes in AP (A), HR (B), and RSNA (C) from baseline levels during the first 30 s of gravitational stress induced by centrifugation in conscious rats with intact reflexes, VL, SAD, or VL + SAD. Means ± SE for 5 (VL + SAD group) or 6 (other groups) animals. *P < 0.05 (ANOVA followed by Scheffé's test).

	DISCUSSION

TOP ABSTRACT METHODS RESULTS DISCUSSION GRANTS REFERENCES

 
The present study demonstrates the importance of the vestibular and baroreflex systems in controlling AP during gravitational stress. The major findings of the present study are that 1) the AP increase observed in the intact group was completely abolished by VL and augmented by SAD; 2) although the AP did not change in the VL group, it was decreased in the VL + SAD group; 3) vestibular input was essential for eliciting bradycardia; and 4) the RSNA increase observed in the intact group was augmented by SAD, attenuated by VL, and completely abolished by VL + SAD.

There have been few reports that evaluated the vestibular effect on HR change during gravitational stress (2, 17, 28). In the present study, a marked bradycardia was observed in the intact and SAD groups but not in the VL and VL + SAD groups, indicating that this response was elicited by vestibular inputs. This finding is consistent with the report of Yates et al. (28) that gravitational stress induced by linear acceleration in humans elicits an AP increase and an HR decrease and that these responses are attenuated in the patients with vestibular dysfunction. In contrast, HR change was not reported in the experiment using caloric stimulation, suggesting that signal from otolith organs may be the afferent input eliciting this response (2).

In the present study, the roles of the baroreflex and VSR on RSNA during gravitational stress were assessed by lesion experiments. Afferent signals that can modify sympathetic nerve activity are from the eyes, baroreceptors, vestibular receptors, nonspecific receptors in the head, muscle proprioceptors, mechanoreceptors in the skin, and central command (7, 18-20, 24, 27). Because RSNA did not change in response to gravitational stress in rats lacking functional baroreceptor and vestibular receptors (i.e., the VL + SAD group), these receptors can be considered the two major components affecting RSNA under the conditions of our present study. The RSNA response observed in rats with functional vestibular receptors, but no baroreceptor activity (i.e., the SAD group), indicates that vestibular input elicited a marked RSNA increase in response to gravitational stress. In contrast, the role of the baroreflex in controlling RSNA is complex. In the intact group, gravitational stress elicited an increase in RSNA, which was significantly augmented by SAD, suggesting that the baroreflex suppressed the RSNA increase in the intact group. In the VL + SAD group, RSNA was not affected by gravitational stress, but in the VL group, i.e., rats with a functional baroreflex, but no functional vestibular receptors, RSNA increased in response to gravitational stress, suggesting that the baroreflex augmented RSNA. These opposing effects of the baroreflex on RSNA may be due to the bidirectional input to baroreceptors. The baroreceptor is loaded in rats with a functioning VSR (i.e., the intact and SAD groups) due to the pressor effect of the VSR but is unloaded in rats lacking a functioning VSR (i.e., the VL and VL + SAD groups)

As mentioned above, in the intact group, the VSR and baroreflex had opposing effects on RSNA, i.e., the VSR augmented, and the baroreflex suppressed, RSNA. This result contrasts with the findings of Ray (17), who demonstrated that the baroreflex and VSR in humans have an additive effect on muscle sympathetic nerve activity. The discrepancy can be explained if the direction of the input to the baroreceptor is considered. In the present study, we demonstrated that the baroreceptor was loaded due to the pressor response induced by the VSR, whereas in Ray's study, the baroreceptor was probably unloaded because of the lower body negative pressure. Thus the baroreflex and VSR might function cooperatively or competitively, depending on the direction of the input to the baroreceptor.

While it is well known that AP, as well as many other variables in a living body, is maintained at a constant level by the feedback control system, some variables are controlled by a feedforward control system (12, 14, 21). In the present study, we demonstrated that the vestibular system is involved in maintaining AP. If gravitational stress occurs, it is detected by the vestibular receptors, which reflexively (i.e., VSR) control the AP before it decreases due to blood redistribution. Thus the vestibular system acts as a feedforward AP controller against gravitational stress. However, the AP increase observed in the intact group indicates that the AP was overcompensated rather than compensated, and this effect was more readily seen in the SAD group lacking the baroreflex. While feedforward control has the advantage of a short response delay, the major disadvantages are the instability of the response and the overcorrect error (16). Comparison of the AP response in the intact and SAD groups showed that the overcompensated AP was compensated by the baroreflex. It is interesting to note that such overcompensation is also observed in other feedforward control systems in the living body, i.e., K⁺ excretion by the kidney and the body temperature control (12, 21). Thus the AP control system during gravitational stress is a combination of the vestibular feedforward system and the baroreflex feedback system (Fig. 5).

View larger version (10K): [in this window] [in a new window]   Fig. 5. Schematic illustration showing that the control system protecting the AP against gravitational stress is composed of the baroreflex and vestibulosympathetic reflex (VSR). Gravitational stress acts on cardiovascular organs, resulting in a decrease in AP due to blood redistribution, and on vestibular receptors, resulting in a marked increase in sympathetic nerve activity (SNA). Consequently, the AP does not remain constant but increases (overcompensation). The overcorrect error by the VSR feedforward control system is compensated by the baroreflex feedback control system.

This overcompensation by the VSR feedforward control system can be quantified. Because a step input of gravity was applied to the rats, the gain (input-to-output ratio) can be calculated. The important issue is that, because the baroreflex loop was open and the VSR eliminated in the VL + SAD group (Fig. 6A), the AP response in this group is caused only by the effect of gravitational stress on AP via blood redistribution. The estimated gain between the AP change and gravitational stress due to blood redistribution (Gd) was -3.2 mmHg/G. Similarly, the gain between the AP change and gravitational stress due to the VSR (Gv) was 6.8 mmHg/G (Fig. 6B). In the case of Gd + Gv = 0, the AP decrease due to blood redistribution matches the AP increase due to VSR, resulting in no change in AP. However, because Gd + Gv > 0 in the present study, the AP increased in the SAD group.

View larger version (17K): [in this window] [in a new window]   Fig. 6. Illustration of the gain (input/output ratio) calculation. In the VL + SAD group (A), the baroreflex and VSR do not function. Because gravitational stress elicits only blood redistribution, the gain between the AP change and gravitational stress due to blood redistribution (Gd; a negative value in case of AP decrease) equals the AP change (AP) divided by the gravity change (G). In the SAD group (B), only the baroreflex does not function. Since the gravitational stress elicits blood redistribution and VSR, the gain between the AP change and gravitational stress due to the VSR (Gv) can be calculated as (AP/G) - Gd. Gb, the gain of baroreflex.

Because only one input, i.e., the 3-G step input, was used in the present study, we could not determine whether the AP response to gravity was linear. Furthermore, in the present study, the gravitational stress was applied in the dorsoventral axis, whereas in the previous animal experiments, VSR was examined during the gravitational stress in the head-to-foot axis by head-up tilting (4, 8). Because blood pooling by gravity depends on the height difference between the hydrostatic indifferent point and the pooling site, it can be supposed that blood pooling is more prominent when the gravity acts in head-to-foot axis than in dorsoventral axis. Thus the Gd would be greater if the rats were set in head-up tilting position in the present study. Further study is necessary to elucidate the relationship between the Gd and direction of the gravitational stress.

In conclusion, the control system for protecting the AP from gravitational stress is composed of two subsystems, i.e., the baroreflex feedback control system and the vestibular feedforward control system. Vestibular inputs elicit rapid and marked sympathetic outflow before the change in AP, thus preventing the development of hypotension. Thus the AP is controlled by the VSR in a predictive manner. The overcorrect error caused by the VSR is compensated by the baroreflex.

	GRANTS

TOP ABSTRACT METHODS RESULTS DISCUSSION GRANTS REFERENCES

 
This study was supported by a grant-in-aid for Scientific Research from the Ministry of Education, Culture, Sports, Science, and Technology of Japan, and a Ground Research for Space Utilization research grant from the National Space Development Agency of Japan and the Japan Space Forum.

	FOOTNOTES

 

Address for reprint requests and other correspondence: T. M. Gotoh, Dept. of Physiology, Gifu Univ. School of Medicine, 40 Tsukasa-Machi, Gifu 500-8705, Japan (E-mail: a2001072{at}hotmail.com).

The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

	REFERENCES

TOP ABSTRACT METHODS RESULTS DISCUSSION GRANTS REFERENCES

 

1. Chen YC, Pellis SM, Sirkin DW, Potegal M, and Teitelbaum P. Bandage backfall: labyrinthine and non-labyrinthine components. Physiol Behav 37: 805-14, 1986.[CrossRef][Medline]
2. Cui J, Iwase S, Mano T, and Kitazawa H. Responses of sympathetic outflow to skin during caloric stimulation in humans. Am J Physiol Regul Integr Comp Physiol 276: R738-R744, 1999.[Abstract/Free Full Text]
3. DiCarlo SE and Bishop VS. Onset of exercise shifts operating point of arterial baroreflex to higher pressures. Am J Physiol Heart Circ Physiol 262: H303-H307, 1992.[Abstract/Free Full Text]
4. Doba N and Reis DJ. Role of the cerebellum and the vestibular apparatus in regulation of orthostatic reflexes in the cat. Circ Res 40: 9-18, 1974.[Medline]
5. Fujiki N, Hagiike M, Tanaka K, Tsuchiya Y, Miyahara T, and Morita H. Role of the vestibular system in sudden shutdown of renal sympathetic nerve activity during microgravity in rats. Neurosci Lett 286: 61-65, 2000.[CrossRef][Web of Science][Medline]
6. Horn KM, DeWitt JR, and Nielson HC. Behavioral assessment of sodium arsanilate induced vestibular dysfunction in rats. Physiol Psychol 9: 371-378, 1981.
7. Hume KM and Ray CA. Sympathetic responses to head-down rotations in humans. J Appl Physiol 86: 1971-1976, 1999.[Abstract/Free Full Text]
8. Jian BJ, Cotter LA, Emanuel BA, Cass SP, and Yates BJ. Effects of bilateral vestibular lesions on orthostatic tolerance in awake cats. J Appl Physiol 86: 1552-1560, 1999.[Abstract/Free Full Text]
9. Kerman IA, McAllen RM, and Yates BJ. Patterning of sympathetic nerve activity in response to vestibular stimulation. Brain Res Bull 53: 11-16, 2000.[CrossRef][Web of Science][Medline]
10. Mano T and Iwase S. Sympathetic nerve activity in hypotension and orthostatic intolerance. Acta Physiol Scand 177: 359-365, 2003.[CrossRef][Web of Science][Medline]
11. Monahan KD and Ray CA. Vestibulosympathetic reflex during orthostatic challenge in aging humans. Am J Physiol Regul Integr Comp Physiol 283: R1027-R1032, 2002.[Abstract/Free Full Text]
12. Morita H, Fujiki N, Miyahara T, Lee K, and Tanaka K. Hepatoportal bumetanide-sensitive K⁺-sensor mechanism controls urinary K⁺ excretion. Am J Physiol Regul Integr Comp Physiol 278: R1134-R1139, 2000.[Abstract/Free Full Text]
13. Morita H, Tanaka K, Tsuchiya Y, Miyahara T, and Fujiki N. Response of renal sympathetic nerve activity to parabolic flight-induced gravitational change in conscious rats. Neurosci Lett 310: 129-132, 2001.[CrossRef][Web of Science][Medline]
14. Morita H, Tsunooka K, Hagiike M, Yamaguchi O, and Lee K. Role of the liver in long-term control of drinking behavior, Na⁺ balance, and arterial pressure in Dahl rats. Am J Physiol Regul Integr Comp Physiol 274: R1111-R1118, 1998.[Abstract/Free Full Text]
15. Nicogossian EA and Robbins ED. Characteristics of the space environment. In: Space Physiology and Medicine (3rd ed.), edited by Nicogossian EA, Huntoon LC, and Pool SL. Philadelphia, PA: Lea and Febiger, 1994.
16. Ogata K. Introduction to control systems. In: Modern Control Engineering (4th ed.), edited by Horton JM. Upper Saddle River, NJ: Prentice-Hall, 2002.
17. Ray CA. Interaction of the vestibular system and baroreflexes on sympathetic nerve activity in humans. Am J Physiol Heart Circ Physiol 279: H2399-H2404, 2000.[Abstract/Free Full Text]
18. Ray CA and Hume KM. Neck afferents and muscle sympathetic activity in humans: implications for the vestibulosympathetic reflex. J Appl Physiol 84: 450-453, 1998.[Abstract/Free Full Text]
19. Ray CA, Hume KM, and Shortt TL. Skin sympathetic outflow during head-down neck flexion in humans. Am J Physiol Regul Integr Comp Physiol 273: R1142-R1146, 1997.[Abstract/Free Full Text]
20. Sato T, Kawada T, Inagaki M, Shishido T, Sugimachi M, and Sunagawa K. Dynamics of sympathetic baroreflex control of arterial pressure in rats. Am J Physiol Regul Integr Comp Physiol 285: R262-R270, 2003.[Abstract/Free Full Text]
21. Savage MV and Brengelmann GL. Control of skin blood flow in the neutral zone of human body temperature regulation. J Appl Physiol 80: 1249-1257, 1996.[Abstract/Free Full Text]
22. Schondorf R, Benoit J, and Stein R. Cerebral autoregulation in orthostatic intolerance. Ann NY Acad Sci 940: 514-26, 2001.[Web of Science][Medline]
23. Sei H, Morita Y, Tsunooka K, and Morita H. Sino-aortic denervation augments the increase in blood pressure seen during paradoxical sleep in the rat. J Sleep Res 8: 45-50, 1999.[CrossRef][Web of Science][Medline]
24. Shortt TL and Ray CA. Sympathetic and vascular responses to head-down neck flexion in humans. Am J Physiol Heart Circ Physiol 272: H1780-H1784, 1997.[Abstract/Free Full Text]
25. Thrasher TN and Keil LC. Arterial baroreceptors control blood pressure and vasopressin responses to hemorrhage in conscious dogs. Am J Physiol Regul Integr Comp Physiol 275: R1843-R1857, 1998.[Abstract/Free Full Text]
26. Woodring SF, Rossiter CD, and Yates BJ. Pressor response elicited by nose-up vestibular stimulation in cats. Exp Brain Res 113: 165-168, 1997.[CrossRef][Web of Science][Medline]
27. Yates BJ. Vestibular influences on the sympathetic nervous system. Brain Res Brain Res Rev 17: 51-59, 1992.[CrossRef][Medline]
28. Yates BJ, Aoki M, Burchill P, Bronstein AM, and Gresty MA. Cardiovascular responses elicited by linear acceleration in humans. Exp Brain Res 125: 476-484, 1999.[CrossRef][Web of Science][Medline]

This article has been cited by other articles:

				K. J. Yavorcik, D. A. Reighard, S. P. Misra, L. A. Cotter, S. P. Cass, T. D. Wilson, and B. J. Yates Effects of postural changes and removal of vestibular inputs on blood flow to and from the hindlimb of conscious felines Am J Physiol Regulatory Integrative Comp Physiol, December 1, 2009; 297(6): R1777 - R1784. [Abstract] [Full Text] [PDF]

				C. Abe, K. Tanaka, C. Awazu, and H. Morita Galvanic vestibular stimulation counteracts hypergravity-induced plastic alteration of vestibulo-cardiovascular reflex in rats J Appl Physiol, October 1, 2009; 107(4): 1089 - 1094. [Abstract] [Full Text] [PDF]

				C. Abe, K. Tanaka, C. Awazu, and H. Morita Impairment of vestibular-mediated cardiovascular response and motor coordination in rats born and reared under hypergravity Am J Physiol Regulatory Integrative Comp Physiol, July 1, 2008; 295(1): R173 - R180. [Abstract] [Full Text] [PDF]

				C. Abe, K. Tanaka, C. Awazu, and H. Morita Strong galvanic vestibular stimulation obscures arterial pressure response to gravitational change in conscious rats J Appl Physiol, January 1, 2008; 104(1): 34 - 40. [Abstract] [Full Text] [PDF]

				D. J. Dyckman, K. D. Monahan, and C. A. Ray Effect of baroreflex loading on the responsiveness of the vestibulosympathetic reflex in humans J Appl Physiol, September 1, 2007; 103(3): 1001 - 1006. [Abstract] [Full Text] [PDF]

				H. Zhu, J. R. Jordan, S. P. G. Hardy, B. Fulcher, C. Childress, C. Varner, B. Windham, B. Jeffcoat, R. W. Rockhold, and W. Zhou Linear acceleration-evoked cardiovascular responses in awake rats J Appl Physiol, August 1, 2007; 103(2): 646 - 654. [Abstract] [Full Text] [PDF]

				T. D. Wilson, L. A. Cotter, J. A. Draper, S. P. Misra, C. D. Rice, S. P. Cass, and B. J. Yates Vestibular inputs elicit patterned changes in limb blood flow in conscious cats J. Physiol., September 1, 2006; 575(2): 671 - 684. [Abstract] [Full Text] [PDF]

				T. D. Wilson, L. A. Cotter, J. A. Draper, S. P. Misra, C. D. Rice, S. P. Cass, and B. J. Yates Effects of postural changes and removal of vestibular inputs on blood flow to the head of conscious felines J Appl Physiol, May 1, 2006; 100(5): 1475 - 1482. [Abstract] [Full Text] [PDF]

				A. Kamiya, T. Kawada, K. Yamamoto, D. Michikami, H. Ariumi, K. Uemura, C. Zheng, S. Shimizu, T. Aiba, T. Miyamoto, et al. Resetting of the arterial baroreflex increases orthostatic sympathetic activation and prevents postural hypotension in rabbits J. Physiol., July 1, 2005; 566(1): 237 - 246. [Abstract] [Full Text] [PDF]

				R. L. Mori, L. A. Cotter, H. E. Arendt, C. J. Olsheski, and B. J. Yates Effects of bilateral vestibular nucleus lesions on cardiovascular regulation in conscious cats J Appl Physiol, February 1, 2005; 98(2): 526 - 533. [Abstract] [Full Text] [PDF]

				B. Xue, K. Skala, T. A. Jones, and M. Hay Diminished baroreflex control of heart rate responses in otoconia-deficient C57BL/6JEi head tilt mice Am J Physiol Heart Circ Physiol, August 1, 2004; 287(2): H741 - H747. [Abstract] [Full Text] [PDF]

				T. M. Gotoh, N. Fujiki, K. Tanaka, T. Matsuda, S. Gao, and H. Morita Acute hemodynamic responses in the head during microgravity induced by free drop in anesthetized rats Am J Physiol Regulatory Integrative Comp Physiol, June 1, 2004; 286(6): R1063 - R1068. [Abstract] [Full Text] [PDF]

				B. J. Yates The vestibular system and cardiovascular responses to altered gravity Am J Physiol Regulatory Integrative Comp Physiol, January 1, 2004; 286(1): R22 - R22. [Full Text] [PDF]

This Article Abstract Full Text (PDF) All Versions of this Article: 286/1/R25    most recent 00458.2003v1 Alert me when this article is cited Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in Web of Science Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via HighWire Citing Articles via Web of Science (26) Citing Articles via Google Scholar Google Scholar Articles by Gotoh, T. M. Articles by Morita, H. Search for Related Content PubMed PubMed Citation Articles by Gotoh, T. M. Articles by Morita, H.