© 1995 American Heart Association, Inc.
Articles |
Central Command Increases Muscle Sympathetic Nerve Activity During Intense Intermittent Isometric Exercise in Humans
From the Copenhagen Muscle Research Center, Department of Anaesthesia, Rigshospitalet, University of Copenhagen (Denmark).
Correspondence to Ronald G. Victor, MD, UT Southwestern Medical Center, 5323 Harry Hines Blvd, Dallas, TX 75235-8573.
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Abstract |
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Abstract During sustained isometric exercise, central command has very little effect on muscle sympathetic nerve activity (MSNA). To determine if central command has a greater effect on MSNA during intermittent than during sustained contractions, MSNA was recorded with microelectrodes (peroneal nerve) during intermittent isometric handgrip at 25%, 50%, and 75% maximum voluntary contraction (MVC) in 9 human subjects with paced breathing. Similar experiments were performed in 11 additional subjects before and after partial neuromuscular blockade (intravenous curare) to isolate the influence of central command while minimizing force output and thus muscle afferent feedback. Before curare, handgrip at 25% and 50% MVC had no effect on MSNA, whereas handgrip at 75% MVC synchronized the MSNA to the handgrip such that MSNA was 5.7±1.3 times higher (mean±SEM, P<.001) during the contraction periods than during the relaxation periods. After curare, this synchronization of MSNA persisted without attenuation, even though force output fell to <25% of the initial MVC. From these observations, we conclude that central command causes synchronization of motor activity and muscle sympathetic activity during intense intermittent isometric exercise.
Key Words: central command • muscle sympathetic nerve activity • isometric exercise
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Introduction |
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Classically, the mammalian nervous system has been separated into the somatic part, which is under volitional control, and the autonomic part, which is under reflex control. However, under certain conditions, such as the fundamental behavior of exercise, common central neural mechanisms appear to integrate and coordinate the efferent activities of both the somatic and the autonomic nervous systems.1 2 3 4 Thus, in 1913 Krogh and Lindhard5 proposed that "the increase in heart rate [during voluntary exercise] is not produced reflexly but by irradiation of impulses from the motor cortex."
In humans, many subsequent studies have provided additional evidence that a central neural mechanism, "central command," is important in determining the cardiovascular responses to exercise.6 7 8 9 10 11 12 13 14 In decerebrate cats, electrical or chemical stimulation of the subthalamic locomotor region in the rostral brain causes parallel activation of motor neurons and of neuronal pools regulating respiration and cardiovascular function.15 16 17 In conscious cats, the rapid increase in sympathetic outflow to the kidney and, in conscious humans, the rapid increase in sympathetic outflow to the skin during voluntary static exercise are also consistent with this hypothesis.18 19 However, the latter increase in skin sympathetic activity mainly affected sudomotor rather than vasomotor function,19 and the importance of central command in the neural regulation of the human circulatory system still remains poorly understood.
Indeed, previous studies have suggested that during static exercise central command plays only a very small role in producing the large increase in sympathetic outflow to the human skeletal muscle circulation, the latter being regulated reflexly by excitatory afferents arising in the exercising skeletal muscles.20 21 22 23 24 25 However, those previous studies in humans examined responses only to sustained isometric exercise, whereas stimulation of the subthalamic locomotor region in cats, the animal model of central command, typically produces intermittent rather than sustained isometric contractions.15 16 17 Accordingly, we recorded muscle sympathetic nerve activity (MSNA) during intermittent isometric handgrip to reexamine the importance of central command in the regulation of MSNA. To isolate the autonomic effects of central command from those of skeletal muscle afferents, the exercise was performed alone and in combination with partial neuromuscular blockade, which exaggerates the degree of motor effort (ie, central command) required to generate tension in the weakened muscles.6 8 10 11 25
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Materials and Methods |
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Experiments were performed on healthy human subjects in the Anesthesiology Department of Rigshospitalet of the University of Copenhagen. The experimental protocol was approved by the Municipal Ethical Committee of Copenhagen, and each subject gave informed consent to participate. Multiunit recordings of postganglionic sympathetic action potentials were obtained from muscle nerve fascicles of the right peroneal nerve posterior to the fibular head by using unipolar tungsten microelectrodes.26 Nerve action potentials were amplified 50 000- to 100 000-fold, filtered (bandwidth, 700 to 2000 Hz), rectified, and integrated (time constant, 0.1 second [s]) to obtain a mean voltage neurogram. Inadvertent contraction of the leg muscle adjacent to the recording electrode produces electromyographic artifacts that are easily distinguished from sympathetic action potentials, which have a cardiac rhythmicity and display a characteristic biphasic response to the Valsalva maneuver (increased activity during phases II and III and decreased activity during phase IV).27 After analog-to-digital conversion, the mean voltage signal was routed to a software routine for signal-average analysis; the area under the curve was integrated to obtain a relative measure of sympathetic nerve activity. On the mean voltage neurograms, the sympathetic activity is proportional to the frequency and amplitude of the narrow-based peaks, or "bursts." The signal-averaged neurogram is a time activity curve of MSNA averaged over 15 consecutive contraction-relaxation periods, the averaging being triggered by the onset of force.
Arterial pressure was measured via a catheter inserted into the left brachial artery and connected to a pressure transducer, heart rate was measured from the electrocardiogram, the force of handgrip muscle contraction was measured with a force transducer, and breathing movements were measured with a pneumobelt. All data were recorded on FM tape for subsequent computer analysis.
Experimental Protocols
Protocol 1: Responses to Intermittent Handgrip
The aim of this protocol was to characterize the MSNA response
to graded intermittent handgrip. The maximal voluntary contraction
(MVC) of the subjects (n=9) was determined at the beginning of each
experiment. Subjects were instructed to pace their breathing to a
metronome (12 breaths per minute) and not to alter their breathing
during the handgrip. MSNA, blood pressure, heart rate, breathing
movements, and force were recorded during 3-minute bouts of
intermittent isometric handgrip (contract for 3 s, relax for 6 s) at
25%, 50%, and 75% MVC. Subjects performed exercise with the right
forearm while MSNA was recorded from the right peroneal nerve. Each
level of handgrip was repeated twice, with the order being random and
with 10-minute rest periods between bouts.
Protocol 2: Effects of Curare on Responses to Intermittent Handgrip
The aim of this protocol was to test effects of partial
neuromuscular blockade with intravenous curare on the relation between
force and MSNA. During the curare protocol, subjects (n=11) began to
perform intermittent handgrip at 75% MVC for 1 minute and then
attempted to continue to perform this exercise while tubocurarine
chloride (curare; Nordisk Droge) was infused intravenously (initial
dose, 0.075 mg/kg) and titrated to decrease maximal handgrip force to a
value that was <25% of the initial maximum.
Protocol 2a: Effects of Curare Plus Local Anesthetic Blockade of
the Axillary Nerve on Responses to Intermittent Handgrip
The aim of this subprotocol was to eliminate muscle afferent
activation in the exercising muscles. In a subset of subjects (n=3)
studied in protocol 2, the attempted handgrip during curare was
repeated after local anesthetic blockade of the axillary nerve was
performed by use of 2% lidocaine.
In all, we studied 20 healthy male subjects (9 subjects in protocol 1 and 11 in protocol 2) from 19 to 42 years of age (mean±SEM, 29±3 years). The average weight of the subjects was 79±3 kg. The baseline heart rate was 69±3 beats per minute. The average baseline mean arterial pressure was 102±2 mm Hg.
Data Analysis
Statistical analysis was performed by using Student's
paired t test. Values of P<.05 were considered
statistically significant. Values in the text are represented as
mean±SEM.
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Results |
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Protocol 1: Responses to Intermittent Handgrip
Handgrip at 25% and 50% MVC had no detectable effect on MSNA, whereas handgrip at 75% MVC synchronized the sympathetic activity to the pattern of voluntary motor activity (Figs 1
and 2). Each 3-s handgrip contraction was
accompanied by one or more large bursts of sympathetic activity,
followed by a reduction in sympathetic activity in the 6-s relaxation
periods between successive contractions. During intermittent handgrip
at 25% and 50% MVC, the ratio of the MSNA during the contraction
periods to that during the relaxation periods was 1.1:1 and 1.3:1,
respectively. These values are not statistically different from a ratio
of 1:1. During intermittent handgrip at 75% MVC, this ratio increased
to 7.8:1 (P<.05), indicating that 88% of the total neural
discharge became aligned with the periods of muscle contraction. Thus,
the precise threshold for detection of exercise-induced synchronization
of MSNA was between 50% and 75% MVC.
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With the handgrip-related bursts of sympathetic activity, blood
pressure increased briskly and then returned to baseline before the
next contraction (Fig 1
).
Protocol 2: Effects of Curare on Responses to Intermittent
Handgrip
As in the first series of experiments, handgrip at 25% MVC had no
effect on MSNA in the second series of experiments before the
administration of curare: the ratio of sympathetic activity during the
contraction to the relaxation periods was 1.4:1. In contrast, handgrip
at 75% MVC increased this ratio to 5.7:1, indicating significant
synchronization (Fig 3). Curare reduced force output to
10% of the initial maximum, but the exercise-induced synchronization
of sympathetic discharge persisted, with the ratio of sympathetic
activity during the attempted contraction to relaxation periods being
3.7:1, which is not statistically different from the value during
handgrip at 75% MVC before curare.
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Mean arterial pressure did not increase significantly between
handgrip contractions at 25% or 50% MVC but increased comparably
during handgrip contractions at 75% MVC before curare and during
attempted maximal contractions during curare (101±2 to 112±3 versus
104±2 to 116±3 mm Hg [P>.1 for 75% MVC versus
curare]). The latency from the onset of contraction to the onset of
the peak increase in blood pressure was 3 s for both conditions (75%
MVC, 3.1±0.1 s; curare, 2.9±0.4 s). Under both conditions, the
increased blood pressure returned to baseline 4 to 5 s before the onset
of the next contraction (75% MVC, 3.8±0.5 s; curare, 4.7±0.5 s) (Fig 3B).
Protocol 2a: Effects of Curare Plus Local Anesthetic Axillary
Block on Responses to Intermittent Handgrip
In the three subjects in this subset of protocol 2, the MSNA
ratios (contraction to relaxation) during handgrip at 75% MVC alone
and during intended maximal handgrip after the combination of axillary
block plus curare were as follows: 2.1 versus 2.3 (subject 1), 4.3
versus 3.3 (subject 2), and 13.3 versus 8.1 (subject 3).
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Discussion |
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TopAbstractIntroductionMaterials and MethodsResultsDiscussionReferences |
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The principal conclusions from the present study are twofold. First, in conscious humans intense intermittent isometric exercise produces a one-to-one synchronization of motor activity and MSNA in such a way that each burst of voluntary motor activity is accompanied by one or more large bursts of sympathetic nerve activity. Second, such synchronization is caused mainly by central command. During partial neuromuscular blockade with curare, the intent to exercise alone (ie, central command) was sufficient to produce the repetitive bursts of MSNA despite a substantial reduction in handgrip force and thus in muscle afferent activation. This effect of central command was evident even after local anesthetic block of the arm nerves to eliminate skeletal muscle afferent activation during handgrip. However, it should be emphasized that this effect was evident only during intense motor effort and not during mild or moderate exercise.
Analysis of the signal-averaged neurograms indicated that within each period of repetitive static muscle contraction, the sympathetic activity increased with a latency of 1.0 to 1.5 s after the onset of tension development and then returned to baseline just before the end of the 3-s contraction. To explain this repetitive pattern of sympathetic activation, several possible mechanisms were explored.
First, the synchronization of sympathetic activity during intermittent
handgrip was a primary effect of the exercise rather than a secondary
consequence of concomitant alterations in the activity of
cardiopulmonary and/or arterial baroreceptor reflexes. Because
alterations in breathing pattern can alter MSNA,26 27 28
subjects were instructed to pace their breathing with a metronome. The
absence of any detectable effect of intermittent handgrip on
signal-average analysis of breathing movements demonstrates the
efficacy of this pacing procedure. In particular, the repetitive bursts
of MSNA were not preceded by alterations in respiratory movements or in
blood pressure, indicative of inadvertent Valsalva maneuvers. Two
observations argue against a primary role for the arterial baroreflex
in mediating this sympathetic response: (1) During bouts of handgrip at
75% MVC alone, MSNA increased with the very first contraction, which
was preceded by a stable baseline level of blood pressure. (2) During
repeated handgrip contractions at 75% MVC alone and with repeated
attempted maximal contractions during the administration of curare, the
elevated blood pressure from each previous contraction period returned
to baseline >4 s before the next contraction. Because 
1.5 s is the
expected latency between a decrease in blood pressure and a subsequent
baroreflex-mediated burst of MSNA,26 the recovery in the
exercise-induced increase in blood pressure from a preceding
contraction cannot explain the bursts of MSNA occurring 1.5 s after the
onset of a subsequent contraction.
Second, it would be difficult to explain increases in MSNA during intermittent handgrip on the basis of metaboreceptor muscle afferent activation. During sustained isometric muscle contraction, the local accumulation in the muscle interstitium of chemical products of muscle metabolism (possibly such as H+ and K+) activates sensory nerve endings (metaboreceptors), which send afferent signals to the ventrolateral medulla and reflexly increase efferent sympathetic nerve activ- ity.21 22 23 24 29 30 31 32 33 34 This mechanism, however, cannot explain the rapidity of this muscle sympathetic nerve response. In animals, metaboreceptor afferents show a much slower and more progressive pattern of activation with a minimal latency of 6 to 9 s from the onset of contraction to the onset of afferent neural activation.30 31 In humans, a similar or even longer latency (up to 30 to 60 s) is seen in the onset of the increase in efferent MSNA during sustained isometric handgrip.20 21 22 24 25 Furthermore, muscle ischemia, which greatly augments the response of metaboreceptor muscle afferents to electrically induced muscle contraction in cats,35 had no effect on the increases in MSNA during intermittent handgrip contractions (data not shown).
Third, the possibility was considered that the rapid onset and offset of the muscle sympathetic nerve response might be a reflex caused by repetitive activation and deactivation of mechanoreceptor,30 not metaboreceptor, skeletal muscle afferents. During repetitive electrical stimulation of ventral spinal roots in anesthetized cats, intermittent tetanic hind-limb muscle contractions cause a one-to-one synchronization of efferent renal sympathetic nerve activity,36 resembling the synchronization of MSNA in the present human experiments. The response in the anesthetized cat is caused by a reflex mechanism mediated by skeletal muscle mechanoreceptor afferents, because it is abolished by either sectioning the dorsal spinal roots that contain these afferents or by neuromuscular blockade.36 In contrast, the synchronization of motor and sympathetic activity in conscious humans was not abolished, or even attenuated, by neuromuscular blockade alone or in combination with local anesthetic blockade of the axillary nerve containing the muscle afferents from the exercising arm. Because an exaggerated degree of voluntary motor effort was required to generate even a small amount of tension in the weakened muscles, these observations clearly indicate that central command can increase MSNA in the absence of muscle afferent input. These observations, however, by no means exclude the possibility that there may normally be some redundancy in the regulation of MSNA during intense intermittent isometric exercise by central command and mechanoreceptor muscle afferents.
The present study differs markedly from previous studies, which have indicated that central command plays only a minor role in the activation of sympathetic outflow to skeletal muscle during static exercise in humans.20 21 22 23 24 25 However, those studies investigated sustained isometric exercise at 30% MVC, whereas the present study revealed an important role for central command during intermittent isometric exercise with intensities >50% MVC. Thus, the present data indicate that in humans central command plays a greater role in the regulation of sympathetic nerve discharge to the skeletal muscle vasculature during intense rather than moderate and during repetitive rather than sustained isometric muscle contraction. The underlying mechanisms causing these nonlinearities remain to be determined. Nevertheless, explosive bursts of sympathetic discharge to the vasculature of nonexercising skeletal muscle are likely to be an important mechanism by which cardiac output is redistributed to the working muscle during intense bursts of isometric exercise.
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Acknowledgments |
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This study was supported by the Frank M. Ryburn Jr Chair in Heart Research and the Lawson and Rogers Lacy Research Fund in Cardiovascular Disease. We thank Richard Cooley for research assistance and Pam Maass for secretarial assistance. Also, we would like to thank Dr Gary Iwamoto for his assistance with the signal-averaging analysis. Dr Victor is an Established Investigator of the American Heart Association.
Received July 22, 1994; accepted September 12, 1994.
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P. J Fadel, Z. Wang, M. Tuncel, H. Watanabe, A. Abbas, D. Arbique, W. Vongpatanasin, R. W Haley, R. G Victor, and G. D Thomas Reflex sympathetic activation during static exercise is severely impaired in patients with myophosphorylase deficiency J. Physiol., May 1, 2003; 548(3): 983 - 993. [Abstract] [Full Text] [PDF]
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V. Donadio, M. Kallio, T. Karlsson, M. Nordin, and B G. Wallin Inhibition of human muscle sympathetic activity by sensory stimulation J. Physiol., October 1, 2002; 544(1): 285 - 292. [Abstract] [Full Text] [PDF]
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A. W. Sheel, P. A. Derchak, D. F. Pegelow, and J. A. Dempsey Threshold effects of respiratory muscle work on limb vascular resistance Am J Physiol Heart Circ Physiol, May 1, 2002; 282(5): H1732 - H1738. [Abstract] [Full Text] [PDF]
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P. A. Derchak, A. W. Sheel, B. J. Morgan, and J. A. Dempsey Effects of expiratory muscle work on muscle sympathetic nerve activity J Appl Physiol, April 1, 2002; 92(4): 1539 - 1552. [Abstract] [Full Text] [PDF]
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S. G. Hayes and M. P. Kaufman MLR stimulation and exercise pressor reflex activate different renal sympathetic fibers in decerebrate cats J Appl Physiol, April 1, 2002; 92(4): 1628 - 1634. [Abstract] [Full Text] [PDF]
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Y. Nishida, Q. H. Chen, M.-S. Zhou, and J. Horiuchi Sinoaortic denervation abolishes pressure resetting for daily physical activity in rabbits Am J Physiol Regulatory Integrative Comp Physiol, March 1, 2002; 282(3): R649 - R657. [Abstract] [Full Text] [PDF]
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A. R. Saad, D. P. Stephens, L. A. T. Bennett, N. Charkoudian, W. A. Kosiba, and J. M. Johnson Influence of isometric exercise on blood flow and sweating in glabrous and nonglabrous human skin J Appl Physiol, December 1, 2001; 91(6): 2487 - 2492. [Abstract] [Full Text] [PDF]
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K M Gallagher, P J Fadel, M Stromstad, K Ide, S A Smith, R G Querry, P B Raven, and N H Secher Effects of partial neuromuscular blockade on carotid baroreflex function during exercise in humans J. Physiol., June 15, 2001; 533(3): 861 - 870. [Abstract] [Full Text] [PDF]
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R. G. Querry, S. A. Smith, M. Stromstad, K. Ide, P. B. Raven, and N. H. Secher Neural blockade during exercise augments central command's contribution to carotid baroreflex resetting Am J Physiol Heart Circ Physiol, April 1, 2001; 280(4): H1635 - H1644. [Abstract] [Full Text] [PDF]
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C. M St Croix, B. J Morgan, T. J Wetter, and J. A Dempsey Fatiguing inspiratory muscle work causes reflex sympathetic activation in humans J. Physiol., December 1, 2000; 529(2): 493 - 504. [Abstract] [Full Text] [PDF]
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P. K Winchester, J. W Williamson, and J. H Mitchell Cardiovascular responses to static exercise in patients with Brown-Sequard syndrome J. Physiol., August 15, 2000; 527(1): 193 - 202. [Abstract] [Full Text] [PDF]
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R. A. Augustyniak, E. J. Ansorge, and D. S. O'Leary Muscle metaboreflex control of cardiac output and peripheral vasoconstriction exhibit different latencies Am J Physiol Heart Circ Physiol, February 1, 2000; 278(2): H530 - H537. [Abstract] [Full Text] [PDF]
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D. H. Silber, L. I. Sinoway, U. A. Leuenberger, and V. E. Amassian Magnetic stimulation of the human motor cortex evokes skin sympathetic nerve activity J Appl Physiol, January 1, 2000; 88(1): 126 - 134. [Abstract] [Full Text] [PDF]
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C. A. Ray Sympathetic adaptations to one-legged training J Appl Physiol, May 1, 1999; 86(5): 1583 - 1587. [Abstract] [Full Text] [PDF]
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H.-S. Chang, K. Staras, J. E. Smith, and M. P. Gilbey Sympathetic Neuronal Oscillators are Capable of Dynamic Synchronization J. Neurosci., April 15, 1999; 19(8): 3183 - 3197. [Abstract] [Full Text] [PDF]
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D. I. Carrasco, M. D. Delp, and C. A. Ray Effect of concentric and eccentric muscle actions on muscle sympathetic nerve activity J Appl Physiol, February 1, 1999; 86(2): 558 - 563. [Abstract] [Full Text] [PDF]
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M. D. Herr, V. Imadojemu, A. R. Kunselman, and L. I. Sinoway Characteristics of the muscle mechanoreflex during quadriceps contractions in humans J Appl Physiol, February 1, 1999; 86(2): 767 - 772. [Abstract] [Full Text] [PDF]
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C. A. Ray, E. T. Mahoney, and K. M. Hume Exercise-induced muscle injury augments forearm vascular resistance during leg exercise Am J Physiol Heart Circ Physiol, August 1, 1998; 275(2): H443 - H447. [Abstract] [Full Text] [PDF]
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J T Potts and J H Mitchell Synchronization of somato-sympathetic outflows during exercise: role for a spinal rhythm generator J. Physiol., May 1, 1998; 508(3): 646 - 646. [Full Text] [PDF]
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B. A Chizh, P M. Headley, and J. F R Paton Coupling of sympathetic and somatic motor outflows from the spinal cord in a perfused preparation of adult mouse in vitro J. Physiol., May 1, 1998; 508(3): 907 - 918. [Abstract] [Full Text] [PDF]
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C. A. Ray, K. M. Hume, K. H. Gracey, and E. T. Mahoney Muscle cooling delays activation of the muscle metaboreflex in humans Am J Physiol Heart Circ Physiol, November 1, 1997; 273(5): H2436 - H2441. [Abstract] [Full Text] [PDF]
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C. A. Ray and K. H. Gracey Augmentation of exercise-induced muscle sympathetic nerve activity during muscle heating J Appl Physiol, June 1, 1997; 82(6): 1719 - 1733. [Abstract] [Full Text] [PDF]
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