Different responses in skin and muscle sympathetic nerve activity to static muscle contraction MITSURU SAITO, MAR1 NAITO, AND TADAAKI MAN0 Department of Aerospace Psychology, Research Institute of Environmental Medicine, Nagoya University, Nugoyu 404-01; Toyota Technological Institute, Nagoya 468; and Department of Public Health, School of Medicine, Kunuzuwu University, Kunuxuwu 920, Japan SAITO,
MITSURU,
MARI
NAITO,
AND TADAAKI
MANO.
oiffer-
ent responses in skin and musclesympathetic nerve activity to static musclecontraction. J. Appl. Physiol. 69(6): 2085-2090, 1990.-We microneurographically recorded the traffic of sympathetic nerves leading to foot volar skin activity (SSA) and leg skeletal muscleactivity (MSA) during isometric handgrip and simultaneously determined sweat rate by the ventilated capsulemethod and skin blood flow by laser-Dopplerflowmetry in the innervating area of SSA. SSA increasedabruptly and was almost constant during handgrip, accompaniedby an increasein sweatrate, whereasskin blood flow showedno significant changeduring the handgrip. MSA showeda time-dependent increase during the course of handgrip. During arterial occlusionof the working forearm after handgrip, SSA decayed to the precontraction control level, whereasMSA remained at a higher level than during control. During involuntary biceps musclecontraction inducedby electrical stimulation, both SSA and MSA increased.The resultssuggestthat the SSA response during voluntary handgrip, which was demonstratedto contain mainly sudomotor activity, might be influenced by central commandand input from peripheral mechanoreceptorsbut be influenced little by input from musclechemoreceptors.
predominantly vasoconstrictor nerves, were shown to have arteriovenous anastomoses. Thermal sweating, which is seen in the forearm skin, is absent in the palm of the hand and the sole of the foot. In addition, stronger responses to muscle work as well as to mental and emotional stress are seen on the volar aspect of the hand (hairless region) compared with the forearm (hairy region) (16, 17). Such results suggest that the sympathetic nerves innervating nonhairy skin may be activated during voluntary static contraction. This study aimed to examine whether SSA led to nonhairy skin increases during static voluntary muscle contraction and to compare the response patterns of SSA and MSA to muscle contraction. A preliminary report of the experiments has been presented (22). METHODS
Subjects. Eight healthy males, aged 21-27 yr, were engaged as subjects. They were informed of the purpose and procedures of this study and gave their consent to central command; reflex control; sudomotor and vasomotor participate in the experiment. All subjects previously nerves; hairlessskin and hairy skin sympathetic nerves; non- participated in studies using microneurography and were thermoregulatory sweating very familiar with this kind of protocol. The approval of this study was given by the Ethical Committee of the Research Institute of Environmental Medicine, Nagoya ALTHOUGH muscle sympathetic nerve activity (MSA) is University. known to increase during muscle work (14, 21, 23,26), it Recordings of sympathetic nerve activity. The subject is unclear whether skin sympathetic nerve activity (SSA) lay on a special bed with an opening that allowed access increases during muscle work. Delius et al. (5) demonof the recording electrode. Sympathetic nerve discharges strated that, during static muscle contraction, one-half were recorded by the microneurographic technique. A of the subjects showed an increase in SSA but the other tungsten microelectrode with a shaft diameter of 0.1 mm and an impedance of l-5 MQ was inserted manually by half did not show any apparent alteration in SSA. Bini et al. (2) reported that, during muscle contraction, the an experimenter into the tibia1 nerve at the popliteal activity of sympathetic nerves innervating the forearm fossa through the opening from under the bed (21). At skin increased but that there was no change in the first, traffic of sympathetic nerves leading to triceps activity of nerves innervating the palm of the hand. surae in the right leg was recorded; the second electrode Recently, Richardson et al. (18) observed finger vasoconwas then impaled into the skin fasicular nerve, of which striction during static muscle contraction, but no de- the innervating area was on the volar aspect of the left crease in forearm skin blood flow has been demonstrated foot. The sympathetic nerve activity supplying skeletal by Taylor et al. (24). Such inconsistency in response to muscle and nonhairy skin of the foot was judged as muscle work in SSA in the different regions may be follows: MSA showed 1) an appearance of afferent disattributed to the functional difference in the skin vessels charges with tapping or stretching of calf muscle but not between hairy and nonhairy regions. Forearm skin is with light touch on the calf skin, 2) spontaneously supplied by both vasoconstrictor and vasodilator nerves grouped burst discharges in synchrony with heartbeat, (3,20), but arteriovenous anastomoses have not yet been and 3) rhythmic discharges not altered by applying arousal or weak electrical stimulation (4, 25); the volar found (19), although the hand vessels, which contain 0161-7567/90 $1.50 Copyright
0 1990 the American
Physiological
Society
2085
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2086
SKIN
SYMPATHETIC
ACTIVITY
SSA, after the fascicular receptive field was confirmed from the appearance of mechanoreceptive afferent discharges arising in response to touch stimuli on the volar aspect of the foot, showed spontaneous and/or evoked sympathetic activity induced by emotional or electrical stimuli, with discharges independent of the heartbeat (1, 7, 8). MSA was represented quantitatively as total sympathetic nerve activity expressed as burst number multiplied by the peak of the mean voltage neurogram (Fig.
1A ). It is easy to distinguish
MSA burst
discharges
and
to determine
the number of bursts and amplitude, but it is slightly difficult to determine SSA burst number and amplitude (Fig. lA). Therefore the total SSA was represented as total voltage, which was calculated from the tracing of the full-wave rectified and integrated (bin width 1 s) neurogram (Fig. 1B). Total MSA and total SSA were calculated every 30 s and represented as percentages of the control value. Determination of sweat rate and skin blood flow. Sweat rate and skin blood flow were monitored along with the recording of SSA in six of eight subjects who took part in the experiment
under the same protocol
with the same
physiological measurements as on the previous day. The ventilation capsule method (Hidrograph AMU 3, Fourtion) was employed for the determination of sweat rate (9). A plastic capsule possessing an open surface area of 1 cm2 was fixed on the receptive field of the foot volar skin. Dry nitrogen gas was allowed to flow into this capsule at a rate of 0.2 l/min and drained. This humidified gas was then led to a highly sensitive capacitance hydrometer. The skin blood flow was determined by a laser-Doppler flow device (wavelength 780 nm; AFL210, Advance), and the probe was tightly fixed to the volar surface of the foot 0.5 cm from the capsule. Every 15 s, the sweat rate was represented by a relative change in
A
a.u.
Mean Voltage Neurogram
5s
B
AND
STATIC
EXERCISE
humidity calculated from the tracing of the hydrometer, and skin blood flow was determined from the flowmeter. Heart rate and blood pressure. Heart rate was determined from the electrocardiogram recorded from the chest. Systolic and diastolic blood pressures were recorded from the resting upper arm by a semiautomatic sphygmomanometer (Nippon Colin BP-203Y). Mean blood pressure was calculated as one-third of pulse pressure plus diastolic pressure. Skin vascular resistance was calculated as mean blood pressure divided by laser-Doppler flow. Static muscle contraction. The static handgrip was performed in the supine position for 2 min in each subject using an electrodynamometer. The subject was asked to exert constant force corresponding to the trace on the oscilloscope set before the test at a tension of 30% of maximal voluntary contraction, determined before the experiment. Observation of the subject was made throughout the investigation to ensure that he did not contract any muscle other than those of his exercising forearm and that he did not hold his breath. In the second handgrip trial, arterial occlusion of the exercising arm was performed starting 5 s before the handgrip
ceased at a cuff pressure of 260 mmHg and maintained for 2 min. The handgrip exercise was performed once on each side. The first exercise was on the left hand, and
after a 15min rest period the second handgrip exercise was exerted on the right hand. Arterial occlusion was applied arbitrarily on either side. The subject was made to hold the grip very lightly and to be completely alert 4-5 min before commencement of the muscle contraction, For the third experiment, involuntary biceps muscle contraction for 2 min was performed after a 2-min control period. The muscle contraction was induced by electrical stimulation to stimulate the peripheral receptors in the arm without the effect of central motor command. Two surface electrodes (5 mm diam) were set on the musculocutaneous nerve at the proximal site of the medial upper arm, and square pulses of 1-ps duration with 70- to 80-V intensity at a 20-Hz frequency were delivered. This stimulus strength did not produce any discomfort or pain. The contraction force induced by this electrical stimulation was on average 11% of the tension needed for maximum voluntary elbow flexion. Throughout the experiment, uncontrolled external in1 mln
a.u. 20
2oy*
Yean
Yottrga MSA a 1. 2ctl;y’
Mean Voltage Neurogram
Man Voltrgo SSA
I
0 x
0t
10 Swart
Rata
01 IV lkln Blood
integrated Neurogram
Twwton
Ffow
0 CL*
of
r
HmdQrip I
5s
FIG. 1. Mean voltage neurograms (time constant 0.1 s) of MSA (A) and SSA (B) and integrated neurogram of SSA (bin width 1 s). au, arbitrary unit.
salore
FIG. 2. neurograms),
Simultaneous
maximum
voluntary
’
.
Handwip
[SO% MVCI
’
Racovwy
recordings of MSA and SSA (mean voltage and skin blood flow in the foot volar aspect and of tension of handgrip before, during, and after handgrip. MVC, sweat
rate,
contraction.
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1
SKIN SYMPATHETIC
ACTIVITY
fluences, such as sudden loud noise, as well as visual and tactile stimuli were avoided as carefully as possible. The ambient temperature was maintained at 23 t l*C, and the basal noise level in the room was ~20 dB. S&&&s. The control value of each variable was shown as the average during the time between 3 and 1 min before commencement of handgrip. The significance of change among tested periods was checked with repeated measurements by a one-way multivariable analysis of variance. Only results with P 5 0.05 were considered significant. After this, the possibility of a difference between the variables and the control values was investigated by a paired Student’s t test. Values were represented as means t SE. RESULTS
Voluntary muscle ccmtruction. For 1 min just before static muscle contraction, there was no significant difference from the control value in SSA and MSA, whereas both SSA and MSA increased during muscle contraction (Figs. 2 and 3). However, the response patterns in SSA ---
AND STATIC
2087
EXERCISE
and MSA were apparently different. SSA showed an abrupt increase with commencement of the contraction and thereafter was constant at ~35% higher than the control value during the contraction. MSA increased gradually in a time-dependent pattern until the end of the handgrip. During the last 30 s of the contraction, the magnitude of MSA was -2OO-300% of the control value. A marked increase in sweat rate was seen immediately after commencement of muscle contraction, and the high rate remained during handgrip, which corresponded with the change in SSA (Figs. 2 and 4). Blood flow in the foot volar skin and skin vascular resistance showed no significant change during handgrip compared with the control value. During the recovery period after the handgrip, SSA, sweat rate, and skin blood flow returned quickly to control levels. Posthandgrip arterial occlusion of the exercising arm did not produce high SSA, whereas MSA remained as high as during muscle contraction. SSA and sweat rate decayed gradually during the ischemia and during the recovery, resulting in no significant difference from the control value during and after the occlusion (Figs. 5 and 6) ‘Heart rate and MBP increased by 20 (P < 0.01) and 22% (P < 0.01) of the control values, respectively, during the 2nd min of exercise and returned to the precontraction level after the contraction ceased, For 2 min during handgrip
I
J
control
1
4
I
I
1
.O
1
2
3
4
J 5 mln
FIG. 3. Changes in SSA and MSA, heart rate, and mean blood pressure before, during, and after static handgrip, Values are means & SE of 8 subjects. * Different from control value (paired t test).
=u
control
1
I
I
I
I
0
1
2
3
4
I
5 min
FIG. 4. Changes in sweat rate, skin blood flow, and skin vascular resistance before, during, and after handgrip. Values are means k SE of 6 subjects. * Different from control value (paired t test).
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2088
SKIN SYMPATHETIC handgrip
ACTIVITY
AND STATIC
EXERCISE occlusion
handOr@
1 occlusion
l
i
-+
l
tit t+t+
+ -m
l
-
i
.a -w---m
iiiiiiif
-,
t
+ T-+
-w
s-m
t+++t,it
40
r
b -+=F -t 1OL
I control
th
I 1 0
t t ----a-t\ttti
--%
t
--t-M
t
t
I I
1
I
I
1
I
J
1
2
3
4
5
6
7,1,
FIG. 6. Changes in sweat rate, skin blood flow, and skin vascular resistance during handgrip and during consecutive arterial occlusion after handgrip. Values are means & SE of 5 subjects. * Different from control value (paired t test).
-4, t t +-+
110~
+
*
l
/
-
I control
i
,+3\
y-+-
I
1
I
I
I
I
1
L
0
1
2
3
4
5
6
7,,,
FIG. 5. Responses in SSA and MSA, heart rate, and mean blood pressure during static handgrip and during consecutive arterial occlusion after handgrip. Values are means t SE of 8 subjects. * Different from control value (paired t test).
the arterial occlusion, the average value of heart rate decreased to and maintained the preexercise level. However, the average value of mean blood pressure remained as high as 113% of the control value. Involuntary muscle contraction. During involuntary muscle contraction, MSA and SSA increased significantly, by 11 and 18% of the control values, respectively (Fig. 7). The average increase in sweat rate for 2 min of stimulated contraction was 16% of the control value, but there was no statistical significance because of the large interindividual variation in the sweating response. SBF and skin vascular resistance showed no significant response. DISCUSSION
We have demonstrated that SSA supplying the foot sole as well as the sweat rate in the sole increased during static handgrip and decayed to the preexercise level during occlusion after exercise and that skin blood flow in the sole did not decrease during static handgrip. MSA rose during handgrip exercise and remained higher dur-
10 0 -10
L MSA
SSA
Sweat Rate
SBF
Resistance
7. Percent changes in MSA, SSA, sweat rate, skin blood flow and skin vascular resistance during involuntary muscle contraction produced by electrical stimulation for 2 min. MSA was represented as changes in MSA burst rate. Values are means & SE of 6 subjects. * Different from control value for 2 min before electrical stimulation (analysis of variance). FIG.
(SBF),
ing the occlusion than before handgrip. These results indicate that the increase in SSA during static contraction is composed mainly of sudomotor nerves, which seemed to respond to input from peripheral mechanoreceptors and central command, but is influenced little by the afferent input from the muscle chemoreceptors. This finding is in contrast with the response of MSA, where the contribution from muscle chemoreceptors is great. The apparent increase in MSA during volitional (14, 21, 23) and involitional static contraction (14) as well as the high level of MSA maintained during arterial occlusion (14) after the handgrip agree with previous studies.
Furthermore our results showing the increase of SSA supplying the foot volar skin during voluntary muscle
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SKIN SYMPATHETIC
ACTIVITY
contraction coincide with previous results demonstrated on the radial nerve by Bini et al. (2) and on the hairy
skin of the leg (peroneal nerve) by Vissing and Victor (27) As reported by Wallin et al. (29), MSA and SSA may be altered before exercise by anticipation and attention to exercise. In our study, the subject was made to hold the grip very lightly and to be completely alert 4-5 min before commencement of the muscle contraction. The average values in SSA and MSA for 1 min immediately before handgrip did not differ from the control values, which indicates that the experimental condition before exercise was satisfactorily controlled. Although the verbal instruction of the exercise and inflation of the cuff for arterial occlusion evoked SSA for a brief period, it seems that the significant increase in SSA during the contraction was induced by the voluntary muscle contraction. SSA supplying hairless skin is elicited reflexly by
AND STATIC
2089
EXERCISE
Bini et al. (2) did not observed any changes in SSA leading to the volar aspect of the hand by muscle work at normal room temperature, which differs from our results. One reason for the differences may be the difference between the responses in SSA innervating the volar surface of the hands (median nerve) and the foot (tibia1 nerve) or the different kind of sympathetic nerve traffic that was recorded in the studies. Based on the simultaneous observation of sweat rate and skin blood flow, we conclude that the sudomotor activity was the dominant SSA in our study, but Bini et al. (2) have stated that the vasomotor activity was dominant. The second reason may lie in the different method of muscle contraction used (Jendrassik-like maneuver vs. static handgrip). We are grateful to Drs. Satoshi Iwase and Kiyohito Yamamoto for experimental support. Address for reprint requests: M. Saito, Toyota Technological Institute, 2-12, Hisakata, Tempaku-ku, Nagoya 468, Japan.
stimulating mechanoreceptors in the skin in the anesthetized cat (11) as well as by stimulating mechanorecep-
Received 5 September 1989; accepted in final form 24 July ‘1990.
tors in the contralateral
REFERENCES
hand by vibration
in awake
humans (15). Not only afferent impulses from mechan-
oreceptors in muscle, tendon, and skin conveyed by thick myelinated fibers but also afferent volleys via thin group III fibers from chemo- and mechanoreceptors in the working muscle are increased by static handgrip (13). In addition, involuntary biceps contraction produced by electrical stimulation evoked SSA in this study. Thus we could not exclude the possibility that the increase in SSA during voluntary contraction may be evoked by a reflex at the spinal level (10). However, SSA is strongly related to the arousal level in the human subject (28), and impulses through the afferent nerves evoked by stimulation of the cutaneous, muscle, and tendon receptors in awake humans activate the higher central nervous system. It might be argued that the cortical motor command and the activity of the reticular formation have greater roles in activating SSA during voluntary isometric contraction than during occlusion. Additional studies in awake humans for detailed reflex mechanisms are
needed. According to Janig et al. (X2-), SSA supplying hairless skin consists of sudo- and vasomotor nerves. As judged from simultaneous determination of sweat rate and skin blood flow, the activity of skin sympathetic nerves recorded in this study was composed of both sudo- and vasomotor fibers. At the initial phase of handgrip, there was a concomitant and abrupt increase in SSA and sweat rate, with no significant change in skin blood flow and skin vascular resistance. With the lack of vasodilator fibers in the sole of the foot taken into consideration (20), the reason for skin blood flow and vascular resistance showing no significant response to handgrip may
be a lack of response in vasomotor nerves and/or humoral factors, i.e., acetylcholine released at the sweat glands (6). It is likely that the influence of sweating on skin vessels may be small, because the blood flow did not increase at the initial phase of contraction despite strong sweat responses at the initial phase. Thus it seems that the SSA activated during contraction was composed pre-
dominantly
of the sudomotor
nerve.
G., K.-E. HAGBARTH, P. HYNNINEN, AND B. G. WALLIN. Thermoregulatory and rhythm-generating mechanisms governing the sudomotor and vasomotor outflow in human cutaneous nerves.
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K.-E. HAGBARTH, P. HYNNINEN, AND B. G. WALLIN. Regional similarities and differences in thermoregulatory vasoand sudomotor tone. J. Physiol. Lond. 306: 553-565,198O. BLAIR, D. A., W. E. GLOVER, AND I. C. RODDIE. Vasomotor fibers to skin in the upper arm, calf and thigh. J. Physiol. Lond. 153: 232-238,196O. DELIUS, W., K.-E. HAGBARTH, A. HONGELL, AND B. G. WALLIN. General characteristics of sympathetic activity in human muscle nerves. Acta Physiol. Stand. 84: 65-81, 1972. DELIUS, W., K.-E. HAGBARTH, A. HONGELL, AND B. G. WALLIN. Manoeuvres affecting sympathetic outflow in human skin nerves. Acta Physiol. &and. 84: 177-186, 1972. DUFF, F., A. D. M. GREENFIELD, J. T. SHEPHERD, AND J. D, THOMPSON. A quantitative study of the response to acetylcholine and histamine of the blood vessels of human hand and forearm. J. Physiol.
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7. HAGBARTH, K.-E., R. G. HALLIN, A. HONGELL, H. E. TOREBJ~RK, AND B. G. WALLIN. General characteristics of sympathetic activity in human skin nerves. Acta Physiol. Stand. 84; 164-176, 1972. a. HALLIN, R. G., AND H. E. TOREBJ~RK. Single unit sympathetic activity in human skin nerves during rest and various manoeuveres. Acta Physiol.
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9. IWASE, S., T. MANO, J. SUGENOYA, M. SAITO, AND S. HAKUSUI. Relationship among skin sympathetic nerve activity, sweating and skin blood flow. Environ. Med. 32: 55-67, 1988. 10. JANIG, W., AND I-I. K~MMEL. Organization of the sympathetic innervation supplying the hairless skin of the cat’s paw. J. Auton. Nerv. Syst. 3: 215-230, 1981, 11. JANIG, W., AND B. RATH. Effects
of anaesthetics on reflexes elicited in the sudomotor system by stimulation of patinian corpuscles and of cutaneous nociceptors. J. Auton. New. Syst. 2: 1-14, 1980. 12. JANIG, W., G. SUNDL~F, AND B. G. WALLIN. Discharge patterns of sympathetic neurons supplying skeletal muscle and skin in man and cat. J. A&on. Nerv. Syst. 7: 239-256, 1983. 13. KAUFMAN, M. D., J. C. LONGHURST, K. J. RYBICKI, J. H. WALLACH, AND J. H. MITCHELL. Effects of static muscular contraction on impulse activity of groups III and IV afferents in cat. J. Appl. Physiol. 55: 105-112, 1983. 14. MARK, A. L., R. G. VICTOR, C. NERHED, AND B. G. WALLIN. Microneurographic studies of the mechanisms of sympathetic nerve responses to static exercise in humans. Circ. Res. 57: 461469,1985. 15, NAITO, M. Experimental Noise on Skin Swmathetic
Studies on the Effect of Vibration and Activitv (PhD thesis in Jananese).
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ACTIVITY
Kanazawa, Japan: Kanazawa Univ., 1989. T. Thermal influence on palmar sweating and mental influence on generalized sweating in man. Jpn. J. Physiul. 25: 525
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T., M. ASAYAMA, AND M. ITO. Comparison of sudomotor neural activities between palmar and non-palmar sweating. Proc. ht. Gong. Neuroveg. Res. 18th Tokyo 1977, p. 236-238. RICHARDSON, D., M. SCHMITZ, AND N. BORCHERS. Relative effects of static muscle contraction on digital artery and nailfold capillary blood flow velocities. Microuasc. Res. 31: 157-169, 1986. RODDIE, I. C. Circulation to skin and adipose tissue, In: Hun&o& of Physiology. The Curdimzsculur System. Peripheral Circulatim and Organ Blood Flow. Bethesda, MD: Am. Physiol. Sot., 1983, sect. 2, vol. III, pt. 1, chap& 10, p. 285-317. RODDIE, I. C., J. T. SHEPHERD, AND R. F. WHELAN. The contribution of constrictor and dilator nerves to the skin vasodilation during body heating. J. Physiol. L.md. 136: 489-497, 1957. SAITO, M., T. MANO, AND S. IWASE. Sympathetic nerve activity related to local fatigue sensation during static contraction. J. Appl. Physiol. 67: 980-984, 1989. SAIT~, M., T, MANO, AND S. SATOSHI. Different responsiveness in muscle and skin sympathetic nerve activity during muscle contraction (Abstract). Jpn. J. Physiol. 39, Suppl.: s224, 1989.
AND STATIC
EXERCISE
D. R., P. B. CHASE, AND J. A. TAYLOR. Autonomic mediathe pressure response to static exercise in humans. J. Appl. Physiol. 64: 2190-2196,19&3. TAYLOR, W, F., J. M. JOHNSON, W. A. KOSIBA, AND C. M. KWAN. Cutaneous vascular responses to isometric handgrip exercise. J. Appl. Physiol. 66: 1586-1592, 1989. VALLBO, A. B., K.-E. HAGBARTH, H. E. TOREWORK, AND EL G. WALLIN. Somatosensory proprioceptive, and sympathetic activity in human peripheral nerves. Physiol. Reu. 59: 919-957, 1979. VKTOR, R. G., L. A. BERTOCCI, S. L. PRYOR, AND R. L. NUNNALLY. Sympathetic nerve discharge is coupled to muscle cell pH during exercise in humans. J. CEin. Inuest. 82: 1301-1305,1988. VISSING, S. F., AND R. G. VICTOR. Central motor command activates sympathetic outflow to skin during static exercise (Abstract). Acta Physiol. Stand. 136, Suppl. 584: 44, 1989. WALLIN, B. G., AND U. KONIG. Changes of skin nerve sympathetic activity during induction of general anaesthesia with thiopentone in man. Bruin Res. 103: 157-160, 1976. WALLIN, B. G., C. MORIN, AND P. HJEMDAHL. Muscle sympathetic activity and venous plasma noradrenaline concentrations during static exercise in normotensive and hypertensive subjects. Actu Physiol. Scwtd. 129: 489-497,1987.
23. SEALS, tion of 24.
25.
26.
27.
28.
29.
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MITSURU,
MARI
NAITO,
AND TADAAKI
MANO.
oiffer-
ent responses in skin and musclesympathetic nerve activity to static musclecontraction. J. Appl. Physiol. 69(6): 2085-2090, 1990.-We microneurographically recorded the traffic of sympathetic nerves leading to foot volar skin activity (SSA) and leg skeletal muscleactivity (MSA) during isometric handgrip and simultaneously determined sweat rate by the ventilated capsulemethod and skin blood flow by laser-Dopplerflowmetry in the innervating area of SSA. SSA increasedabruptly and was almost constant during handgrip, accompaniedby an increasein sweatrate, whereasskin blood flow showedno significant changeduring the handgrip. MSA showeda time-dependent increase during the course of handgrip. During arterial occlusionof the working forearm after handgrip, SSA decayed to the precontraction control level, whereasMSA remained at a higher level than during control. During involuntary biceps musclecontraction inducedby electrical stimulation, both SSA and MSA increased.The resultssuggestthat the SSA response during voluntary handgrip, which was demonstratedto contain mainly sudomotor activity, might be influenced by central commandand input from peripheral mechanoreceptorsbut be influenced little by input from musclechemoreceptors.
predominantly vasoconstrictor nerves, were shown to have arteriovenous anastomoses. Thermal sweating, which is seen in the forearm skin, is absent in the palm of the hand and the sole of the foot. In addition, stronger responses to muscle work as well as to mental and emotional stress are seen on the volar aspect of the hand (hairless region) compared with the forearm (hairy region) (16, 17). Such results suggest that the sympathetic nerves innervating nonhairy skin may be activated during voluntary static contraction. This study aimed to examine whether SSA led to nonhairy skin increases during static voluntary muscle contraction and to compare the response patterns of SSA and MSA to muscle contraction. A preliminary report of the experiments has been presented (22). METHODS
Subjects. Eight healthy males, aged 21-27 yr, were engaged as subjects. They were informed of the purpose and procedures of this study and gave their consent to central command; reflex control; sudomotor and vasomotor participate in the experiment. All subjects previously nerves; hairlessskin and hairy skin sympathetic nerves; non- participated in studies using microneurography and were thermoregulatory sweating very familiar with this kind of protocol. The approval of this study was given by the Ethical Committee of the Research Institute of Environmental Medicine, Nagoya ALTHOUGH muscle sympathetic nerve activity (MSA) is University. known to increase during muscle work (14, 21, 23,26), it Recordings of sympathetic nerve activity. The subject is unclear whether skin sympathetic nerve activity (SSA) lay on a special bed with an opening that allowed access increases during muscle work. Delius et al. (5) demonof the recording electrode. Sympathetic nerve discharges strated that, during static muscle contraction, one-half were recorded by the microneurographic technique. A of the subjects showed an increase in SSA but the other tungsten microelectrode with a shaft diameter of 0.1 mm and an impedance of l-5 MQ was inserted manually by half did not show any apparent alteration in SSA. Bini et al. (2) reported that, during muscle contraction, the an experimenter into the tibia1 nerve at the popliteal activity of sympathetic nerves innervating the forearm fossa through the opening from under the bed (21). At skin increased but that there was no change in the first, traffic of sympathetic nerves leading to triceps activity of nerves innervating the palm of the hand. surae in the right leg was recorded; the second electrode Recently, Richardson et al. (18) observed finger vasoconwas then impaled into the skin fasicular nerve, of which striction during static muscle contraction, but no de- the innervating area was on the volar aspect of the left crease in forearm skin blood flow has been demonstrated foot. The sympathetic nerve activity supplying skeletal by Taylor et al. (24). Such inconsistency in response to muscle and nonhairy skin of the foot was judged as muscle work in SSA in the different regions may be follows: MSA showed 1) an appearance of afferent disattributed to the functional difference in the skin vessels charges with tapping or stretching of calf muscle but not between hairy and nonhairy regions. Forearm skin is with light touch on the calf skin, 2) spontaneously supplied by both vasoconstrictor and vasodilator nerves grouped burst discharges in synchrony with heartbeat, (3,20), but arteriovenous anastomoses have not yet been and 3) rhythmic discharges not altered by applying arousal or weak electrical stimulation (4, 25); the volar found (19), although the hand vessels, which contain 0161-7567/90 $1.50 Copyright
0 1990 the American
Physiological
Society
2085
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2086
SKIN
SYMPATHETIC
ACTIVITY
SSA, after the fascicular receptive field was confirmed from the appearance of mechanoreceptive afferent discharges arising in response to touch stimuli on the volar aspect of the foot, showed spontaneous and/or evoked sympathetic activity induced by emotional or electrical stimuli, with discharges independent of the heartbeat (1, 7, 8). MSA was represented quantitatively as total sympathetic nerve activity expressed as burst number multiplied by the peak of the mean voltage neurogram (Fig.
1A ). It is easy to distinguish
MSA burst
discharges
and
to determine
the number of bursts and amplitude, but it is slightly difficult to determine SSA burst number and amplitude (Fig. lA). Therefore the total SSA was represented as total voltage, which was calculated from the tracing of the full-wave rectified and integrated (bin width 1 s) neurogram (Fig. 1B). Total MSA and total SSA were calculated every 30 s and represented as percentages of the control value. Determination of sweat rate and skin blood flow. Sweat rate and skin blood flow were monitored along with the recording of SSA in six of eight subjects who took part in the experiment
under the same protocol
with the same
physiological measurements as on the previous day. The ventilation capsule method (Hidrograph AMU 3, Fourtion) was employed for the determination of sweat rate (9). A plastic capsule possessing an open surface area of 1 cm2 was fixed on the receptive field of the foot volar skin. Dry nitrogen gas was allowed to flow into this capsule at a rate of 0.2 l/min and drained. This humidified gas was then led to a highly sensitive capacitance hydrometer. The skin blood flow was determined by a laser-Doppler flow device (wavelength 780 nm; AFL210, Advance), and the probe was tightly fixed to the volar surface of the foot 0.5 cm from the capsule. Every 15 s, the sweat rate was represented by a relative change in
A
a.u.
Mean Voltage Neurogram
5s
B
AND
STATIC
EXERCISE
humidity calculated from the tracing of the hydrometer, and skin blood flow was determined from the flowmeter. Heart rate and blood pressure. Heart rate was determined from the electrocardiogram recorded from the chest. Systolic and diastolic blood pressures were recorded from the resting upper arm by a semiautomatic sphygmomanometer (Nippon Colin BP-203Y). Mean blood pressure was calculated as one-third of pulse pressure plus diastolic pressure. Skin vascular resistance was calculated as mean blood pressure divided by laser-Doppler flow. Static muscle contraction. The static handgrip was performed in the supine position for 2 min in each subject using an electrodynamometer. The subject was asked to exert constant force corresponding to the trace on the oscilloscope set before the test at a tension of 30% of maximal voluntary contraction, determined before the experiment. Observation of the subject was made throughout the investigation to ensure that he did not contract any muscle other than those of his exercising forearm and that he did not hold his breath. In the second handgrip trial, arterial occlusion of the exercising arm was performed starting 5 s before the handgrip
ceased at a cuff pressure of 260 mmHg and maintained for 2 min. The handgrip exercise was performed once on each side. The first exercise was on the left hand, and
after a 15min rest period the second handgrip exercise was exerted on the right hand. Arterial occlusion was applied arbitrarily on either side. The subject was made to hold the grip very lightly and to be completely alert 4-5 min before commencement of the muscle contraction, For the third experiment, involuntary biceps muscle contraction for 2 min was performed after a 2-min control period. The muscle contraction was induced by electrical stimulation to stimulate the peripheral receptors in the arm without the effect of central motor command. Two surface electrodes (5 mm diam) were set on the musculocutaneous nerve at the proximal site of the medial upper arm, and square pulses of 1-ps duration with 70- to 80-V intensity at a 20-Hz frequency were delivered. This stimulus strength did not produce any discomfort or pain. The contraction force induced by this electrical stimulation was on average 11% of the tension needed for maximum voluntary elbow flexion. Throughout the experiment, uncontrolled external in1 mln
a.u. 20
2oy*
Yean
Yottrga MSA a 1. 2ctl;y’
Mean Voltage Neurogram
Man Voltrgo SSA
I
0 x
0t
10 Swart
Rata
01 IV lkln Blood
integrated Neurogram
Twwton
Ffow
0 CL*
of
r
HmdQrip I
5s
FIG. 1. Mean voltage neurograms (time constant 0.1 s) of MSA (A) and SSA (B) and integrated neurogram of SSA (bin width 1 s). au, arbitrary unit.
salore
FIG. 2. neurograms),
Simultaneous
maximum
voluntary
’
.
Handwip
[SO% MVCI
’
Racovwy
recordings of MSA and SSA (mean voltage and skin blood flow in the foot volar aspect and of tension of handgrip before, during, and after handgrip. MVC, sweat
rate,
contraction.
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1
SKIN SYMPATHETIC
ACTIVITY
fluences, such as sudden loud noise, as well as visual and tactile stimuli were avoided as carefully as possible. The ambient temperature was maintained at 23 t l*C, and the basal noise level in the room was ~20 dB. S&&&s. The control value of each variable was shown as the average during the time between 3 and 1 min before commencement of handgrip. The significance of change among tested periods was checked with repeated measurements by a one-way multivariable analysis of variance. Only results with P 5 0.05 were considered significant. After this, the possibility of a difference between the variables and the control values was investigated by a paired Student’s t test. Values were represented as means t SE. RESULTS
Voluntary muscle ccmtruction. For 1 min just before static muscle contraction, there was no significant difference from the control value in SSA and MSA, whereas both SSA and MSA increased during muscle contraction (Figs. 2 and 3). However, the response patterns in SSA ---
AND STATIC
2087
EXERCISE
and MSA were apparently different. SSA showed an abrupt increase with commencement of the contraction and thereafter was constant at ~35% higher than the control value during the contraction. MSA increased gradually in a time-dependent pattern until the end of the handgrip. During the last 30 s of the contraction, the magnitude of MSA was -2OO-300% of the control value. A marked increase in sweat rate was seen immediately after commencement of muscle contraction, and the high rate remained during handgrip, which corresponded with the change in SSA (Figs. 2 and 4). Blood flow in the foot volar skin and skin vascular resistance showed no significant change during handgrip compared with the control value. During the recovery period after the handgrip, SSA, sweat rate, and skin blood flow returned quickly to control levels. Posthandgrip arterial occlusion of the exercising arm did not produce high SSA, whereas MSA remained as high as during muscle contraction. SSA and sweat rate decayed gradually during the ischemia and during the recovery, resulting in no significant difference from the control value during and after the occlusion (Figs. 5 and 6) ‘Heart rate and MBP increased by 20 (P < 0.01) and 22% (P < 0.01) of the control values, respectively, during the 2nd min of exercise and returned to the precontraction level after the contraction ceased, For 2 min during handgrip
I
J
control
1
4
I
I
1
.O
1
2
3
4
J 5 mln
FIG. 3. Changes in SSA and MSA, heart rate, and mean blood pressure before, during, and after static handgrip, Values are means & SE of 8 subjects. * Different from control value (paired t test).
=u
control
1
I
I
I
I
0
1
2
3
4
I
5 min
FIG. 4. Changes in sweat rate, skin blood flow, and skin vascular resistance before, during, and after handgrip. Values are means k SE of 6 subjects. * Different from control value (paired t test).
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2088
SKIN SYMPATHETIC handgrip
ACTIVITY
AND STATIC
EXERCISE occlusion
handOr@
1 occlusion
l
i
-+
l
tit t+t+
+ -m
l
-
i
.a -w---m
iiiiiiif
-,
t
+ T-+
-w
s-m
t+++t,it
40
r
b -+=F -t 1OL
I control
th
I 1 0
t t ----a-t\ttti
--%
t
--t-M
t
t
I I
1
I
I
1
I
J
1
2
3
4
5
6
7,1,
FIG. 6. Changes in sweat rate, skin blood flow, and skin vascular resistance during handgrip and during consecutive arterial occlusion after handgrip. Values are means & SE of 5 subjects. * Different from control value (paired t test).
-4, t t +-+
110~
+
*
l
/
-
I control
i
,+3\
y-+-
I
1
I
I
I
I
1
L
0
1
2
3
4
5
6
7,,,
FIG. 5. Responses in SSA and MSA, heart rate, and mean blood pressure during static handgrip and during consecutive arterial occlusion after handgrip. Values are means t SE of 8 subjects. * Different from control value (paired t test).
the arterial occlusion, the average value of heart rate decreased to and maintained the preexercise level. However, the average value of mean blood pressure remained as high as 113% of the control value. Involuntary muscle contraction. During involuntary muscle contraction, MSA and SSA increased significantly, by 11 and 18% of the control values, respectively (Fig. 7). The average increase in sweat rate for 2 min of stimulated contraction was 16% of the control value, but there was no statistical significance because of the large interindividual variation in the sweating response. SBF and skin vascular resistance showed no significant response. DISCUSSION
We have demonstrated that SSA supplying the foot sole as well as the sweat rate in the sole increased during static handgrip and decayed to the preexercise level during occlusion after exercise and that skin blood flow in the sole did not decrease during static handgrip. MSA rose during handgrip exercise and remained higher dur-
10 0 -10
L MSA
SSA
Sweat Rate
SBF
Resistance
7. Percent changes in MSA, SSA, sweat rate, skin blood flow and skin vascular resistance during involuntary muscle contraction produced by electrical stimulation for 2 min. MSA was represented as changes in MSA burst rate. Values are means & SE of 6 subjects. * Different from control value for 2 min before electrical stimulation (analysis of variance). FIG.
(SBF),
ing the occlusion than before handgrip. These results indicate that the increase in SSA during static contraction is composed mainly of sudomotor nerves, which seemed to respond to input from peripheral mechanoreceptors and central command, but is influenced little by the afferent input from the muscle chemoreceptors. This finding is in contrast with the response of MSA, where the contribution from muscle chemoreceptors is great. The apparent increase in MSA during volitional (14, 21, 23) and involitional static contraction (14) as well as the high level of MSA maintained during arterial occlusion (14) after the handgrip agree with previous studies.
Furthermore our results showing the increase of SSA supplying the foot volar skin during voluntary muscle
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SKIN SYMPATHETIC
ACTIVITY
contraction coincide with previous results demonstrated on the radial nerve by Bini et al. (2) and on the hairy
skin of the leg (peroneal nerve) by Vissing and Victor (27) As reported by Wallin et al. (29), MSA and SSA may be altered before exercise by anticipation and attention to exercise. In our study, the subject was made to hold the grip very lightly and to be completely alert 4-5 min before commencement of the muscle contraction. The average values in SSA and MSA for 1 min immediately before handgrip did not differ from the control values, which indicates that the experimental condition before exercise was satisfactorily controlled. Although the verbal instruction of the exercise and inflation of the cuff for arterial occlusion evoked SSA for a brief period, it seems that the significant increase in SSA during the contraction was induced by the voluntary muscle contraction. SSA supplying hairless skin is elicited reflexly by
AND STATIC
2089
EXERCISE
Bini et al. (2) did not observed any changes in SSA leading to the volar aspect of the hand by muscle work at normal room temperature, which differs from our results. One reason for the differences may be the difference between the responses in SSA innervating the volar surface of the hands (median nerve) and the foot (tibia1 nerve) or the different kind of sympathetic nerve traffic that was recorded in the studies. Based on the simultaneous observation of sweat rate and skin blood flow, we conclude that the sudomotor activity was the dominant SSA in our study, but Bini et al. (2) have stated that the vasomotor activity was dominant. The second reason may lie in the different method of muscle contraction used (Jendrassik-like maneuver vs. static handgrip). We are grateful to Drs. Satoshi Iwase and Kiyohito Yamamoto for experimental support. Address for reprint requests: M. Saito, Toyota Technological Institute, 2-12, Hisakata, Tempaku-ku, Nagoya 468, Japan.
stimulating mechanoreceptors in the skin in the anesthetized cat (11) as well as by stimulating mechanorecep-
Received 5 September 1989; accepted in final form 24 July ‘1990.
tors in the contralateral
REFERENCES
hand by vibration
in awake
humans (15). Not only afferent impulses from mechan-
oreceptors in muscle, tendon, and skin conveyed by thick myelinated fibers but also afferent volleys via thin group III fibers from chemo- and mechanoreceptors in the working muscle are increased by static handgrip (13). In addition, involuntary biceps contraction produced by electrical stimulation evoked SSA in this study. Thus we could not exclude the possibility that the increase in SSA during voluntary contraction may be evoked by a reflex at the spinal level (10). However, SSA is strongly related to the arousal level in the human subject (28), and impulses through the afferent nerves evoked by stimulation of the cutaneous, muscle, and tendon receptors in awake humans activate the higher central nervous system. It might be argued that the cortical motor command and the activity of the reticular formation have greater roles in activating SSA during voluntary isometric contraction than during occlusion. Additional studies in awake humans for detailed reflex mechanisms are
needed. According to Janig et al. (X2-), SSA supplying hairless skin consists of sudo- and vasomotor nerves. As judged from simultaneous determination of sweat rate and skin blood flow, the activity of skin sympathetic nerves recorded in this study was composed of both sudo- and vasomotor fibers. At the initial phase of handgrip, there was a concomitant and abrupt increase in SSA and sweat rate, with no significant change in skin blood flow and skin vascular resistance. With the lack of vasodilator fibers in the sole of the foot taken into consideration (20), the reason for skin blood flow and vascular resistance showing no significant response to handgrip may
be a lack of response in vasomotor nerves and/or humoral factors, i.e., acetylcholine released at the sweat glands (6). It is likely that the influence of sweating on skin vessels may be small, because the blood flow did not increase at the initial phase of contraction despite strong sweat responses at the initial phase. Thus it seems that the SSA activated during contraction was composed pre-
dominantly
of the sudomotor
nerve.
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ACTIVITY
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AND STATIC
EXERCISE
D. R., P. B. CHASE, AND J. A. TAYLOR. Autonomic mediathe pressure response to static exercise in humans. J. Appl. Physiol. 64: 2190-2196,19&3. TAYLOR, W, F., J. M. JOHNSON, W. A. KOSIBA, AND C. M. KWAN. Cutaneous vascular responses to isometric handgrip exercise. J. Appl. Physiol. 66: 1586-1592, 1989. VALLBO, A. B., K.-E. HAGBARTH, H. E. TOREWORK, AND EL G. WALLIN. Somatosensory proprioceptive, and sympathetic activity in human peripheral nerves. Physiol. Reu. 59: 919-957, 1979. VKTOR, R. G., L. A. BERTOCCI, S. L. PRYOR, AND R. L. NUNNALLY. Sympathetic nerve discharge is coupled to muscle cell pH during exercise in humans. J. CEin. Inuest. 82: 1301-1305,1988. VISSING, S. F., AND R. G. VICTOR. Central motor command activates sympathetic outflow to skin during static exercise (Abstract). Acta Physiol. Stand. 136, Suppl. 584: 44, 1989. WALLIN, B. G., AND U. KONIG. Changes of skin nerve sympathetic activity during induction of general anaesthesia with thiopentone in man. Bruin Res. 103: 157-160, 1976. WALLIN, B. G., C. MORIN, AND P. HJEMDAHL. Muscle sympathetic activity and venous plasma noradrenaline concentrations during static exercise in normotensive and hypertensive subjects. Actu Physiol. Scwtd. 129: 489-497,1987.
23. SEALS, tion of 24.
25.
26.
27.
28.
29.
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