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1 Departments of Biological Sciences and Biomedical Engineering, Michigan Technological University, Houghton, Michigan 49931; and 2 Departments of Medicine and Cellular & Molecular Physiology, Pennsylvania State University College of Medicine, Hershey, Pennsylvania 17033
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ABSTRACT |
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 TOP
 ABSTRACT
 INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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Increases in sympathetic neural activity occur independently with either vestibular or mental stimulation, but it is unknown whether sympathetic activation is additive or inhibitive when both stressors are combined. The purpose of the present study was to investigate the combined effects of vestibular and mental stimulation on sympathetic neural activation and arterial pressure in humans. Muscle sympathetic nerve activity (MSNA), arterial pressure, and heart rate were recorded in 10 healthy volunteers in the prone position during 1) head-down rotation (HDR), 2) mental stress (MS; using arithmetic), and 3) combined HDR and MS. HDR significantly (P < 0.05) increased MSNA (9 ± 2 to 13 ± 2 bursts/min). MS significantly increased MSNA (8 ± 2 to 13 ± 2 bursts/min) and mean arterial pressure (87 ± 2 to 101 ± 2 mmHg). Combined HDR and MS significantly increased MSNA (9 ± 1 to 16 ± 2 bursts/min) and mean arterial pressure (89 ± 2 to 100 ± 3 mmHg). Increases in MSNA (7 ± 1 bursts/min) during the combination trial were not different from the algebraic sum of each trial performed alone (8 ± 2 bursts/min). We conclude that the interaction for MSNA and arterial pressure is additive during combined vestibular and mental stimulation. Therefore, vestibular- and stress-mediated increases of MSNA appear to occur independently in humans.
otolith stimulation; sympathetic nerve activity; orthostatic tolerance; arterial pressure control
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INTRODUCTION |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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MAINTENANCE OF ARTERIAL PRESSURE and cerebral perfusion during an orthostatic challenge depends critically on sympathetic neural activation. Muscle sympathetic nerve activity (MSNA) increases linearly as a function of the sine of the tilt angle during passive head-up tilt (7, 17) and disappears at the onset of presyncope in patients with vasovagal syncope (24, 25). Astronauts who experience postflight orthostatic intolerance have lower peripheral resistance (4) and plasma norepinephrine levels (13) during standing compared with astronauts who do not. These findings suggest that factors affecting sympathetic activity influence orthostatic tolerance.
Studies have shown that the vestibular system participates importantly in maintaining arterial pressure by activating sympathetic nerve activity. Doba and Reis (9) found that arterial pressure oscillations increase during tilt after transection of the vestibular nerve in cats. Subsequent animal studies demonstrated increases in sympathetic outflow during electrical stimulation (6, 16, 20, 36) and nose-up tilt (38). In humans, head-down rotation (HDR) in the prone position activates the otolith organs of the vestibule. Using this model, Shortt and Ray (35) found that HDR increases MSNA but does not change arterial pressure or heart rate. Ray and co-workers (15, 30-32, 35) have confirmed that sympathetic activation with HDR is related directly to otolith stimulation and is not confounded by other sympathetic activators.
Only recently have interactive effects between the vestibulosympathetic reflex and other sympathetic activators been investigated, and understanding these interactions may be of prime importance to understanding orthostatic intolerance in astronauts and clinical patients. Astronauts return from space with blunted arterial baroreflex responsiveness (12) and skeletal muscle function (3), but the vestibulosympathetic reflex occurs independent of arterial baroreceptor unloading (28) or skeletal muscle afferent feedback (22, 29). Specifically, interactions among the vestibulosympathetic reflexes, baroreflexes, and skeletal muscle reflexes appear to be additive. However, astronauts also return from space with increased resting MSNA (19), plasma norepinephrine spillover and clearance (10), and circulating leukocytes (21), which suggests, in part, that astronauts experience high levels of stress on reentry. Because the vestibular system also adapts to microgravity (8), it is feasible that the stresses of reentry combined with vestibular adaptations could impact postflight orthostatic tolerance, but changes in MSNA during the combination of mental stress and vestibular stimulation have not been studied.
Therefore, the purpose of this study was to investigate the neural interaction between the vestibulosympathetic reflex and mental stress by examining MSNA during HDR, mental arithmetic, and the simultaneous performance of HDR and mental arithmetic. Because mental stress is reported to increase MSNA in the leg (2), but not in the arm (2, 14), it is possible that mental stimulation during HDR will either increase or decrease the vestibulosympathetic reflex. On the basis of other vestibulosympathetic interactive studies (22, 28, 29), we hypothesize an additive interaction for MSNA output between mental stress and the vestibulosympathetic reflex.
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METHODS |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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Subjects. Ten healthy volunteers (7 men and 3 women; age 22 ± 0.3 yr, height 176 ± 2 cm, weight 78 ± 5 kg) participated in this study. Both men and women were studied because gender does not affect the vestibulosympathetic reflex (27). All subjects were nonsmokers and had no history of autonomic dysfunction. Subjects arrived at the laboratory after abstaining from caffeine and exercise for at least 12 h. The experimental protocol was approved by the Human Research Committee of Michigan Technological University, and all subjects gave written, informed consent before participating.
Experimental design. Each subject performed three experimental trials in the prone position. We examined sympathetic and cardiovascular responses during 1) HDR to activate the vestibulosympathetic reflex, 2) mental arithmetic to induce mental stress, and 3) the simultaneous performance of mental arithmetic and HDR. Each trial was 2 min in length. The order of the three trials was randomized, with 3-min rest periods interspersed between trials. Each trial began and ended with a 2-min baseline and recovery period with the head upright, the neck extended, and the chin supported. This position approximates the gravitational orientation of the head for an individual standing upright. During HDR, the head was passively lowered in the vertical plane over the edge of the table by an investigator supporting the head. During mental arithmetic, subjects continuously subtracted the number four or six from a two or three digit number. The subtraction number (four or six) was randomized for the two trials involving mental arithmetic. Subjects answered verbally and were encouraged by an investigator to subtract as fast as possible. An investigator provided a new number to subtract from every 5-10 s. Subjects were asked to rate perceived stress using a standard five-point scale of 0 (not stressful), 1 (somewhat stressful), 2 (stressful), 3 (very stressful), and 4 (very, very stressful) (5).
Measurements. MSNA was directly measured by inserting a tungsten microelectrode (Frederick Haer, Bowdoinham, ME) into the peroneal nerve in the popliteal region behind the left knee. A reference electrode was inserted subcutaneously 2-3 cm from the recording electrode. Both electrodes were connected to a differential preamplifier and then to an amplifier (total gain of 70,000) where the nerve signal was band-pass filtered (700-2,000 Hz) and integrated (time constant 0.1 s) to obtain a mean voltage display of the nerve activity. Satisfactory recordings of MSNA were defined by spontaneous, pulse-synchronous bursts that increased during Valsalva straining or end-expiratory apnea and did not change during auditory stimulation (yell) or stroking of the skin. Continuous heart rate was measured with a three-lead electrocardiogram. Systolic (SAP) and diastolic (DAP) arterial pressures were measured at 1-min intervals throughout the experiment by use of an automated sphygmomanometer (Arterial Tonometry, Colin Medical Instruments, San Antonio, TX). Mean arterial pressure (MAP) was calculated as MAP = (2 × DAP + SAP)/3. Data were sampled at 500 Hz and stored on a computer (WINDAQ, Dataq Instruments, Akron, OH).
Data analysis. Data were imported into a customized software program for analysis (WinCPRS, Absolute Aliens, Turku, Finland). R-waves were detected and marked in the time series. Muscle sympathetic bursts were automatically detected on the basis of amplitude by use of a signal-to-noise ratio of ~3:1, within a 0.5-s search window centered on a 1.3-s expected burst peak latency from the previous R-wave (11). A revised burst peak latency was entered on the basis of the first iteration of computerized burst detection. The procedure was repeated until further latency corrections failed to detect additional bursts or change the average latency. Potential bursts were then displayed and edited by one of the investigators. The computer program calculated the integral of all sympathetic bursts occurring during the initial baseline period and divided that total by the number of bursts to derive an average control burst area that could be compared across time. With this technique, subsequent bursts that were equal to average bursts occurring during baseline were assigned a value of 1.0. MSNA was expressed as bursts per minute and total activity (total activity = total number of bursts multiplied by the average normalized burst area for each experimental condition, expressed in arbitrary units).
All data were analyzed with commercial software (SAS Institute, Cary, NC). Dependent variables during each trial were evaluated by use of a repeated-measures ANOVA. The changes in MSNA, MAP, and heart rate from baseline for each of the three trials were calculated. The algebraic sum of the changes during HDR and mental arithmetic performed separately was compared with the change when HDR and mental arithmetic were performed together by use of a paired t-test. Perceived stress levels were compared by use of a Wilcoxon rank test. Means were considered to be significantly different when P < 0.05. Results are expressed as means ± SE.| |
RESULTS |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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Mean values for MSNA (burst frequency and total activity), MAP,
and heart rate during the three experimental trials are presented in
Table 1. Baseline values for all
variables were not different across the three trials. MSNA
significantly increased during HDR, mental stress, and simultaneous
performance of HDR and mental stress. MAP and heart rate did not change
during the HDR trial. Both mental stress alone and the simultaneous
performance of HDR and mental stress elicited increases in MAP and
heart rate. During simultaneous performance of HDR and mental stress,
MAP and heart rate increased by 11 ± 2 mmHg and 22 ± 3 beats/min, respectively. These changes during the combination trial
were not significantly different from the algebraic sum of HDR and
mental stress trials performed alone (11 ± 1 mmHg and 18 ± 2 beats/min).
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Figure 1 shows representative neurograms
from one subject during all three trials. Figure
2 shows changes in MSNA during the three
trials. HDR elicited a 4 ± 1 bursts/min and 8 ± 2 unit
increase in MSNA. Mental stress increased MSNA by 4 ± 1 bursts/min and 11 ± 3 units. During simultaneous performance of
HDR and mental stress, MSNA increased by 7 ± 1 bursts/min and
17 ± 6 units. These changes during the combination trial were not
significantly different from the algebraic sum of HDR and mental stress
trials performed alone (8 ± 2 bursts/min and 18 ± 4 units).
The perceived stress levels during the mental stress alone (2.4 ± 0.3 units) and mental stress during HDR (2.6 ± 0.2 units) trials
were not different (P > 0.05).
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DISCUSSION |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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The primary finding from this study is that the neural interaction between mental stress and the vestibulosympathetic reflex is additive. This finding indicates that vestibular- and stress-mediated increases of MSNA are independent in humans. Previous studies have also reported additive interactions among the vestibulosympathetic reflex and the baroreflex (28), skeletal muscle reflex (29), and arterial chemoreflex (22). These previous findings, taken together with results from the present study, suggest that muscle sympathetic nerve activation by the vestibular system is a robust reflex, in which its effector response appears independent.
Mental stress. Mental stress, a complex motor command signal that originates in the cerebral cortex, has been shown to evoke increases in heart rate and arterial pressure, but MSNA responses are dependent on the recording site (2, 14). Anderson and co-workers (2) reported that mental stress increased sympathetic outflow and peripheral vascular resistance to the legs, but not to the arm. In contrast, Halliwill et al. (14) demonstrated a significant decrease of MSNA and peripheral vascular resistance in the arm. Vasoconstriction in one vascular bed with vasodilation in another highlights the capacity of the central nervous system to locally control regional vascular responses to mental stress, but the physiological significance of this control strategy remains unclear. Recently, sympathetic and vascular responses during mental stress were examined before and after head-down bed rest. Kamiya et al. (18) reported that head-down bed rest augmented increases of MSNA to the leg but attenuated vasodilation of the calf muscle in response to mental stress.
Our data confirm previous studies showing a significant increase in leg MSNA, heart rate, and arterial pressure during mental arithmetic (1, 2, 5, 18). Concurrent increases of both arterial pressure and MSNA demonstrate that mental stress overrides baroreflex inhibition of MSNA and is therefore a powerful sympathetic activator. Our results are in agreement with those of Anderson et al. (1), who showed increases of MSNA during mental stress and infusion of phenylephrine. Because mental stress is capable of overriding the arterial baroreflex, it is reasonable to speculate that mental stress may be capable of overriding other neural cardiovascular reflexes, particularly the vestibulosympathetic reflex. Because stimulation of MSNA in the leg during mental stress is primarily dependent on perceived stress, we asked our subjects to rate the perceived stress during each trial involving mental stress by using a standard five-point scale (5). Ratings of perceived stress were not different during mental stress alone and mental stress during HDR. Concerned that the second mental stress trial could be easier than the first (learning effect), we randomly assigned the subtraction number four or six during the mental stress trial. Callister et al. (5) demonstrated that stimulation of MSNA during stress is dependent on perception of stress and not on the type of task. Therefore, our results suggest that similar levels of stress were applied during each mental stress trial.Vestibulosympathetic reflex. Recent studies have confirmed that the vestibular system regulates arterial pressure through activation of the sympathetic nervous system. Yates and Miller (38) reported increases in sympathetic nerve activity during vestibular stimulation in cats. It has been hypothesized that vestibular stimulation evokes sympathetic discharges even before arterial pressure changes are detected, suggesting a sensitive feed-forward mechanism that may help regulate blood pressure and prevent orthostatic hypotension (37). In humans, lowering the head while in the prone position activates the otolith organs, increases MSNA in the leg (15, 28-30, 32, 33, 35) and arm (23), and decreases limb blood flow in the leg and arm (23). Ray and co-workers have conducted a series of investigations indicating that increases of MSNA during HDR are mediated through otolith organ activation by excluding nonvestibular mechanisms that could potentially activate MSNA during HDR, including baroreflexes (35), visual input (35), central command (30-32), neck afferents (30), and nonspecific receptors in the head (15). In the present study, we confirm that HDR activates the vestibulosympathetic reflex without changing arterial pressure, suggesting that arterial baroreceptor unloading does not cause increases in MSNA during HDR.
Although autonomic responses to both mental arithmetic and vestibular stimulation appear to be integrated and processed in the same region of the brain (26), the actual responses are quite different. Monahan and Ray (23) found that vestibular stimulation increases MSNA and decreases blood flow in both the leg and arm. However, mental stress does not induce parallel increases in MSNA and blood flow as seen during vestibular stimulation; mental stress increases MSNA and decreases blood flow in the leg (1, 2, 5) but decreases MSNA and increases blood flow in the arm (14). Therefore, it is possible that one stimulus may override or otherwise affect responses to the second stimulus when both are performed simultaneously. The interactive influences of such a combination could differentially affect the output variable (MSNA). Our results show that MSNA responses during mental stress and vestibular stimulation are additive, suggesting these two reflexes do not centrally integrate to modify sympathetic outflow. Previous interactive studies between the vestibulosympathetic reflex and other cardiovascular reflexes also indicate an additive interaction (22, 28, 29). Baroreceptor unloading (using lower body negative pressure) and HDR performed together increases MSNA equal to the sum of each trial performed individually (28). Interactions between the vestibulosympathetic and skeletal muscle reflex (29) and arterial chemoreflex (22) have also been shown to be additive. Therefore, results from interactive studies between the vestibulosympathetic reflex and other sympathetic activators, along with results from the present study, collectively suggest that the vestibulosympathetic reflex is a powerful and independent reflex, capable of stimulating MSNA in the presence of other sympathetic activators. It is possible that vestibular stimulation may override regional MSNA responses during mental stress, but this speculation can only be tested by measuring both arm and leg MSNA during vestibular and mental stimulation. On Earth, the interaction between mental stress and the vestibulosympathetic reflex is additive, but this reflex interaction may undergo important adaptations in microgravity. Spaceflight has been shown to dramatically affect otolith hair cells in rats (34). Because depolarization of otolith hair cells requires gravitational input, it is reasonable to speculate that the vestibulosympathetic reflex is impaired during spaceflight because of otolith organ inactivation. Head-down bed rest appears to augment MSNA increases during mental stress, but this response has not been examined after spaceflight (18). The interaction between stress and the vestibulosympathetic reflex may be of prime importance to astronauts who return from space exhibiting signs of significant stress (10, 19, 21). An additive interaction would indicate that stresses associated with landing may increase sympathetic activity to help prevent orthostatic hypotension. An inhibitive interaction would suggest that stresses associated with reentry may contribute to orthostatic hypotension by blunting the vestibulosympathetic reflex. It remains to be determined what effects, if any, simulated microgravity has on the vestibulosympathetic reflex and orthostatic stability. Future studies should examine the vestibulosympathetic reflex after both simulated and actual spaceflight. In summary, our results show that mental stress and HDR performed together increase MSNA and arterial pressure equal to the sum of each trial performed individually. These findings indicate an additive neural interaction between mental stress and the vestibulosympathetic reflex. Therefore, neural independence exists between these two sympathetic reflexes with regard to MSNA output in humans.| |
ACKNOWLEDGEMENTS |
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We thank Olga Kovolenko, Guy Pellegrini, and Mark Jentoft for assisting us in this project.
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FOOTNOTES |
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This study was supported by a grant from the National Aeronautics and Space Administration through the Michigan Space Grant Consortium (to J. R. Carter); a Scientist Development Grant from the American Heart Association (0030203N to W. H. Cooke); National Heart, Lung, and Blood Institute Grants (HL-67787 to W.H. Cooke; HL-58503 to C. A. Ray); a National Space Biomedical Research Institute Grant (NCC 9-58-168 to C. A. Ray); and an Established Investigator Grant from the American Heart Association (to C. A. Ray).
Address for reprint requests and other correspondence: J. R. Carter, Dept. of Biological Sciences, Michigan Technological Univ., 1400 Townsend Dr., Houghton, MI 49931 (E-mail: jcarter{at}mtu.edu).
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.
June 14, 2002;10.1152/japplphysiol.00331.2002
Received 12 April 2002; accepted in final form 4 June 2002.
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METHODS
RESULTS
DISCUSSION
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 J. R. Carter, W. H. Cooke, and C. A. Ray Forearm neurovascular responses during mental stress and vestibular activation Am J Physiol Heart Circ Physiol, February 1, 2005; 288(2): H904 - H907. [Abstract] [Full Text] [PDF]
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 I. Bonyhay and R. Freeman Sympathetic Nerve Activity in Response to Hypotensive Stress in the Postural Tachycardia Syndrome Circulation, November 16, 2004; 110(20): 3193 - 3198. [Abstract] [Full Text] [PDF]
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T. E. Wilson and C. A. Ray Effect of thermal stress on the vestibulosympathetic reflexes in humans J Appl Physiol, October 1, 2004; 97(4): 1367 - 1370. [Abstract] [Full Text] [PDF]
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W. H. Cooke, J. R. Carter, and T. A. Kuusela Human cerebrovascular and autonomic rhythms during vestibular activation Am J Physiol Regulatory Integrative Comp Physiol, May 1, 2004; 286(5): R838 - R843. [Abstract] [Full Text] [PDF]
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) in MSNA during HDR and MS performed alone, the
algebraic sum of changes during HDR and mental stress performed
independently (Sum), and the change when HDR and MS were performed
simultaneously. *Significantly different from corresponding baseline
values; n = 10; P < 0.05. NS, not
significant.