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Department of Integrative Physiology, University of North Texas Health Science Center, Fort Worth, Texas 76107
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ABSTRACT |
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Physiological responses to mental tasks and physical exercise were studied independently and combined. We hypothesized that combined mental and physical stresses produce a synergistic interaction. We studied cardiovascular responses to 5 min of static handgrip, mental arithmetic, and the combined stimuli in random order in 12 healthy subjects. Muscle sympathetic nerve activity (SNA) and mean arterial blood pressure (MAP) responses to handgrip and the combined stimuli exceeded responses to mental arithmetic, yet no significant difference existed between responses to handgrip and the combined stimuli. Peak changes in SNA (in %) were greatest during handgrip (188 ± 41), followed by the combined stimuli (166 ± 31) and mental arithmetic (51 ± 9). Peak changes in MAP (in mmHg) were also greatest during handgrip (26 ± 4), followed by the combined stimuli (23 ± 3) and then mental arithmetic (8 ± 2). Peak changes in heart rate (in beats/min) followed the same trend: handgrip (15 ± 2), combined (13 ± 2), and mental arithmetic (10 ± 2). Mental stimulation did not synergistically interact with or add to the responses elicited by handgrip exercise; in fact, a trend existed for math during handgrip to reduce responses relative to handgrip alone.
human; arithmetic; static handgrip; sympathetic nerve activity; hemodynamics
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INTRODUCTION |
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THE COMBINATION OF PHYSICAL and mental activity is something we all do every day. For some of us, it involves typing a paper, whereas others may perform spacewalks with simultaneous physical and mental activities. Physical and mental stress each elicits physiological responses that are mediated through the autonomic nervous system and endocrine system (17, 19). These responses include increases in blood pressure (BP), heart rate (HR), cardiac output, and skeletal muscle blood flow and decreases in renal and splanchnic blood flow (4, 12, 39). For example, Brod et al. (4) found that renal vascular resistance increased, whereas forearm vascular resistance (FVR) decreased, during mental arithmetic. These responses act to restrict blood flow to visceral capillary beds and to redirect blood to systems of the body that respond to stressful stimuli, such as the heart, brain, and skeletal muscle. Hormonal changes are also seen during the stress response. An increase in epinephrine exerts tissue-specific effects, such as vasoconstriction in the splanchnic region (14) and vasodilation in skeletal muscle (25, 28). These actions also aid in redirecting blood flow to systems of the body responding to stressful stimuli. Activation of the cortisol system via corticotropin-releasing hormone aids in mobilizing energy stores. The actions of the renin-angiotensin-aldosterone system and vasopressin both contribute to the maintenance of elevated BP (17, 41).
Physiological responses to physical and mental stresses are
controversial. Some previous studies have suggested that these two
stressors elicit similar responses (30), whereas others have found them to be quite different depending on where the responses were measured and what physical and mental stresses were used (1,
15, 27). For example, most investigators agree that static
handgrip increases muscle sympathetic nerve activity (SNA) and vascular
resistance (21). Mental stress also increases muscle SNA
in the leg but not in the forearm (1). In fact, mental stress decreases FVR (increases forearm blood flow) via sympathetic withdrawal and
-adrenergic vasodilation (15). Also,
work by Eklund and others (7, 8) reveals transient
-adrenergic vasodilation in resting skeletal muscle at the onset of
isometric handgrip.
The purpose of this study was to determine the nature of interaction that occurs between specific mental and physical stimuli by comparing muscle SNA and cardiovascular responses during combined and individual stressors. We hypothesized that the combined imposition of mental and physical stress would elicit a synergistic response of leg SNA, HR, and arterial BP relative to the response seen to either stress by itself. We employed oral arithmetic as the mental stress and static handgrip as the physical stress.
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METHODS |
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Subjects. Twelve subjects (4 women and 8 men) between 24 and 29 yr of age were studied. Women were not tested during menses to avoid hormonal fluctuations that might affect the results (10, 33). All procedures were approved by the University of North Texas Health Science Center Institutional Review Board, and each subject gave written, informed consent to participate in the study. Subjects were asked to refrain from consuming alcoholic and caffeinated beverages for 12 h before the experiment.
Measurements. HR was obtained from an electrocardiogram and cardiotachometer. Arterial BP was measured noninvasively with a Finapres photoplethysmographic monitor placed around the middle finger (Finapres model 2300, Ohmeda, Englewood, CO). The Finapres finger cuff was adjusted to match diastolic arterial pressure determined by conventional arm auscultation. Mean arterial BP (MAP) was calculated as diastolic pressure plus one-third of the pulse pressure, and rate pressure product (RPP) equals MAP × HR.
Muscle SNA was measured directly in the peroneal nerve at the popliteal fossa (the posterior and lateral aspect of the knee) by standard microneurographic techniques, as described previously (32, 37, 42). Briefly, the course of the nerve was determined by electrical stimulation through the skin. Once the nerve was located, a sterile tungsten reference microelectrode was inserted through the skin near the nerve. A similar recording microelectrode was then inserted into the nerve. The position of the recording electrode was adjusted to find a muscle sympathetic nerve signal. SNA was normalized within subjects to allow comparisons within and between subjects, as described previously (37, 42). Noninvasive pulsed Doppler blood flow velocity measured at the brachial artery of the right (resting) arm was used with two-dimensional, ultrasonically measured artery cross-sectional area to calculate forearm blood flow (Interspec XL, Conshohocken, PA, presently owned by ATL, Bothell, WA). This technique has been utilized in previous studies and validated against occlusion plethysmography (5, 16, 35). Brachial arterial blood flow velocity was quantified for 10 cardiac cycles during each measurement time period. Brachial artery cross-sectional area was measured at the probe site and quantified for each measurement time by built-in software. Forearm blood flow was then calculated as the product of velocity and vessel area. FVR was calculated as MAP divided by forearm blood flow; FVR provided an independent and functional index of SNA.Protocol. Before data collection, a practice session allowed determination of the subjects' maximal left handgrip strengths and familiarized subjects with the protocol. For data collection, subjects were instrumented in the supine position. They then underwent 5 min of each experimental stimulus (static handgrip, mental arithmetic, or combined) in random order. Two minutes of baseline data collection preceded each 5-min stimulus, and 1 min of recovery data collection followed each stimulus. A 15-min break occurred between each stimulus to ensure that subjects fully recovered to baseline conditions. Room temperature was held at ~22°C throughout the protocol.
Handgrip. Subjects performed 5 min of static left handgrip exercise at 25-30% of their maximal left handgrip force. For a given subject, the same handgrip exercise force was used for the handgrip and handgrip plus mental arithmetic experimental conditions. The subject was verbally coached to maintain handgrip level within 1 kg of their target level. One 5-s break occurred after 2.5 min of exercise to avoid palm discomfort of the gripping hand. We wanted to emphasize handgrip muscle fatigue in this study. An electronic handgrip dynamometer (model 76618, Lafayette Instruments, IN) provided grip-force input to our data acquisition system. All subjects used their left hands for the static handgrip exercise.
Mental arithmetic. Subjects performed 5 min of mental arithmetic aloud, consisting of sequential subtraction of one- to two-digit integers from four- to five-digit integers as fast as possible. Previous studies have demonstrated that this task produces cardiovascular responses (20). Subjects underwent repeated practice sessions before data collection to ensure their familiarization with this vocal math task. A metronome was set at 30 beats/min to help impose a sense of time urgency on the subject. Subjects were made aware of any mistakes with a buzzer. Also, subjects were buzzed and given a new starting number if more than five consecutive correct answers were given.
Handgrip plus mental arithmetic. Subjects simultaneously performed both of the challenges described above. Mental arithmetic started as soon as static handgrip force stabilized at a subject's target level.
Data analyses.
Two-factor repeated-measures ANOVA (factors: condition and time) and
post hoc paired t-tests determined whether dependent variables changed significantly across time and between stressors (
= 0.05). Also, changes from baseline to peak response levels of a dependent variable were analyzed with paired t-tests.
All data are expressed as means ± SE. Excel (Microsoft, Bothell,
WA) and Sigmastat (SPSS, Chicago, IL) software performed statistical analyses.
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RESULTS |
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A comparison of baseline SNA, FVR, MAP, and HR indicated no
significant differences before the three experimental conditions (Table
1 ). Figure 1
presents raw SNA, BP, and HR data
before and during the perturbations for one subject. In this example, greater SNA burst frequency was seen with handgrip and combined stressors relative to math. BP increased during each of the three stresses (Fig. 1).
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SNA significantly exceeded baseline at minutes
3-5 for the static handgrip and combined conditions
(P < 0.05). SNA did not increase significantly during
mental arithmetic nor did SNA decrease significantly after cessation of
mental arithmetic (Fig. 2). Figure 3
illustrates that peak increases in SNA
were significantly less during mental arithmetic than during static
handgrip and combined conditions (P < 0.05). To assess
whether peak responses to the combined stimulus differed significantly
from the sum of the peak responses to the two isolated stimuli, we
compared them statistically by using paired t-tests. In the
case of SNA, the sum of peak handgrip and math responses tended to
exceed but was not significantly greater than the peak response to the
combined stimulus (P = 0.052; Fig. 3). Burst frequency
results were similar to total SNA results.
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There were no significant differences between conditions for FVR across time (Fig. 2). There was a more consistent trend toward increased FVR during handgrip and combined stimuli than during mental arithmetic. The peak increase in FVR for math was significantly less than the peak increase for the combined stimuli (Fig. 3).
MAP increased significantly from baseline at and after minute 1 for all three stimuli (Fig. 2; P < 0.05). At minutes 4 and 5, MAP rose significantly higher in response to static handgrip and combined stimuli than in response to mental arithmetic (P < 0.05). All variables returned to baseline levels within 1 min after the end of the stimulus. There was no significant difference in peak increases in MAP between static handgrip and combined stimuli (Fig. 3; P = 0.33). However, both static handgrip and combined stimuli increased peak MAP more than mental arithmetic (P < 0.05). The sum of peak MAP responses to math and handgrip was significantly greater than the peak MAP response to the combined stimuli.
HR increased significantly from baseline by minute 1 for all three conditions (P < 0.05). At minute 1, the mental arithmetic and combined stimuli elicited significantly greater HR elevation than handgrip, whereas at minute 5 handgrip and combined stimuli evoked greater increases in HR of the three stimuli (Fig. 2). The sum of peak changes in HR for the handgrip and mental arithmetic was significantly greater than peak changes during the combined stimulus (Fig. 3).
Figure 4 presents the responses of RPP
during 5 min of mental arithmetic or static handgrip and the combined
stresses. RPP was significantly higher during the mental arithmetic and
combined perturbations than during the static handgrip stimulus at
minute 1 of the protocol. However, at minute 5,
RPP was significantly higher during the static handgrip and combined
stimuli than during the mental arithmetic stimulus. As with all other
measurements, RPP returned to baseline within 1 min of recovery. Peak
RPP was significantly higher during static handgrip and combined
stimuli than during mental arithmetic. The calculated sum of peak
changes in RPP for individual stimuli (static handgrip + mental
arithmetic) exceeded peak RPP during the combined (static handgrip and
mental arithmetic) stimulus.
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DISCUSSION |
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Our data refute the hypothesis that physical and mental stresses interact in a synergistic manner to produce greater SNA and MAP responses. The response to the combined stimuli approximately equaled the response to handgrip alone. Responses of HR and RPP were somewhat more complicated, but again no physical-mental synergism was seen.
Not surprisingly, responses were time dependent. For example, during the first 3 min, mental, handgrip, and the combined stimuli resulted in similar increases in MAP. By minute 4, however, static handgrip and the combined stimuli produced greater increases in MAP than mental arithmetic. For the combined stimulus, it appeared that math-induced HR elevation contributed importantly to early, modest MAP elevation, whereas handgrip-induced muscle SNA elevation generated the later and more dramatic hypertension. A cortical "activation" response probably produced the early HR response to math, whereas the well-established muscle metaboreceptors drove the later hypertensive response to handgrip (38).
In contrast to observations by Halliwill et al. (15), we did not observe reduction of resting FVR during math alone or math combined with handgrip. However, no significant increase in FVR occurred in our study with math alone; FVR increased only when the stimulus included static handgrip exercise. In contrast to prior works by Eklund and others (7, 8, 22), we saw no transient vasodilation in resting FVR at the onset of contralateral handgrip. However, in no case did leg SNA or FVR increase before minute 2 of a stimulus. (FVR increased significantly at minute 2 of handgrip alone; see Fig. 2.) Therefore, we do not believe our findings importantly contradict these earlier works. We did not exclude the hand in our blood flow measurements, so it is possible that changes in hand circulation affected our forearm blood flow measurements.
RPP indexes cardiac work (26) such that those findings suggest cardiac work initially increases more during mental arithmetic and the combined stimuli than during handgrip alone. At the 5-min mark, cardiac work is increased during handgrip and combined more than during the mental stimuli. During minute 1 of the protocol, cardiac work elevation was due to an increase in HR for the mental and combined stimuli, whereas the increase in cardiac work during minute 5 is due to an increase in BP for the handgrip and combined stimuli.
An interesting trend appeared for peak responses to the combined stimulus to be less than peak responses to handgrip alone. Although not statistically significant, this trend appeared for all variables studied. Fatiguing exercise causes discomfort and pain, and such sensations may contribute to cardiovascular responses to fatiguing exercise (3, 6). We speculate that mental activity during physical stress may mask the discomfort associated with muscle fatigue and thereby attenuate some cardiovascular responses to muscle fatigue. A related but unquantified observation from our study also supports this idea. We noted that subjects often required less coaching to maintain their target handgrip force when they were simultaneously engaged in arithmetic vs. when they performed static handgrip exercise by itself.
Our findings disagree with those from some previous studies. For example, Rousselle et al. (27) studied responses to mental arithmetic and seated cycling at 50 W and found that combined physical and mental stresses exert a synergistic impact on cardiac output. Also, Myrtek and Spital (23) and Siconolfi et al. (36) reported that the combination of physical and mental stress elicits greater cardiovascular responses than either physical or mental stress alone. Myrtek and Spital (23) employed nonvocal mental arithmetic and supine cycling at 25 W as stresses. Siconolfi et al. (36) employed treadmill walking at 3 miles/h with grade increases of 4% every 2 min until a target HR of 60% of peak was reached. The mental stress used was the Stroop-Color-Word Test. This stress was added 1 min after subjects reached steady-state exercise. With the addition of the mental task, Siconolfi et al. saw significant increases in HR, systolic BP, diastolic BP, RPP, and oxygen consumption above those seen when exercise continued without mental stress.
Differences in relative exercise intensity probably explain at least part of the difference between our study and the above works. In our study, 25-30% of isometric handgrip MVC for 5 min brought subjects very near their grip fatigue tolerance limit. We designed this handgrip protocol for that purpose on the basis of pilot studies. In contrast, dynamic exercise at 25-50 W (23, 27) or 60% peak HR (36), as used in the studies discussed above, are easily tolerated for many minutes by even unfit subjects (13). Therefore, the exercise stimulus we employed probably elicited substantially greater fatigue-related stress than that used by the other groups.
Static handgrip exercise is fundamentally different than large muscle group dynamic exercise (18). Constantly elevated intramuscular pressure during static (isometric) exercise impedes blood flow through the exercising muscle; during dynamic exercise, low intramuscular pressure during the relaxation phase of exercise permits muscle perfusion (2). This reduced perfusion during static exercise relative to dynamic exercise at similar energy expenditures leads to greater metabolite accumulation, fatigue, and thus cardiovascular responses during static exercise (18, 29). Furthermore, cardiovascular responses increase depending on the mass of the exercising muscle (31, 34). It has also been shown that upper body cycling exercise is more stressful than lower body cycling exercise at comparable workloads (24, 40), perhaps in part due to the static handgrip component of upper body cycling exercise.
At the brainstem level, there are possible differences in how signals traveling from the cortex, in response to mental stress, interact with other central and peripheral signals associated with exercise. Motor cortical signals to exercise ("central command") may contribute to neurocirculatory responses (29). Mental stress from a math task or from central perception of fatigue could possibly modify central command influences in the brain stem. However, our study design does not isolate such influences. Central command may actually enhance muscle perfusion during fatiguing exercise (11). The static exercise used in our study generates a strong metaboreceptor signal that may be unchanged or possibly attenuated by mental stress, whereas dynamic exercise used in previous studies sends somewhat different signals to the brain stem that are augmented by mental stress. Dynamic exercise also elicits nonreflex responses, such as activation of the skeletal muscle pump, that are not influenced by mental stress, whereas any exercise signal that travels through the brain stem will possibly be modified by the addition of mental stress. The collective findings demonstrate the importance of exercise mode and relative exercise intensity on the interactive effects of mental and physical stress on cardiovascular control.
Limitations. We studied responses to only 5 min of each perturbation. By decreasing handgrip contraction force and increasing the duration of the stimuli, one could detect changes over a longer period of time. Again, we did not exclude the hand in our blood flow measurements, so it is possible that changes in hand circulation affected our forearm blood flow measurements. Another limitation is that we only studied one type of mental stress and one type of physical stress and the combination of the two. Other types of mental and physical stress may combine differently, as indicated by the literature above (23, 36).
This study was conducted in a laboratory. Of course, this is a strength in that experimental conditions were carefully controlled. However, it is also a limitation in that we cannot necessarily extrapolate our results to field or occupational situations. For example, subjects in such situations may be highly motivated to perform and thus experience greater mental stress and cardiovascular responses than in laboratory conditions. In conclusion, our data indicate that handgrip and mental arithmetic stimuli do not interact in a synergistic or additive manner in generating cardiovascular and autonomic responses. In fact, the results suggest that combining a mental task with physical activity may act to dampen physiological responses of the body to physical stress. On the basis of the present work and prior related literature, we conclude that potential interactions between mental and physical stress responses probably depend importantly on the type and intensity of exercise.| |
ACKNOWLEDGEMENTS |
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We sincerely thank the subjects for participation. We also heartily thank Judy Smith and Debbie Castillo for contributions to this project.
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FOOTNOTES |
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Address for reprint requests and other correspondence: M. L. Smith, Dept. of Integrative Physiology, Univ. of North Texas Health Science Center, 3500 Camp Bowie Blvd., Fort Worth, TX 76107 (E-mail:msmith{at}hsc.unt.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.
10.1152/japplphysiol.00019.2001
Received 9 January 2001; accepted in final form 8 January 2002.
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J. R. Carter and J. E. Lawrence Effects of the menstrual cycle on sympathetic neural responses to mental stress in humans J. Physiol., December 1, 2007; 585(2): 635 - 641. [Abstract] [Full Text] [PDF] |
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H. J. Bell, W. Feenstra, and J. Duffin The initial phase of exercise hyperpnoea in humans is depressed during a cognitive task Exp Physiol, May 1, 2005; 90(3): 357 - 365. [Abstract] [Full Text] [PDF] |
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N. Hjortskov, J. Skotte, C. Hye-Knudsen, and N. Fallentin Sympathetic outflow enhances the stretch reflex response in the relaxed soleus muscle in humans J Appl Physiol, April 1, 2005; 98(4): 1366 - 1370. [Abstract] [Full Text] [PDF] |
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