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Division of Cardiovascular Medicine, Departments of Internal Medicine and Human Physiology, University of California, Davis, California 95616
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
ACKNOWLEDGEMENTS
FOOTNOTES
REFERENCES
ABSTRACT 
Adreani, Christine M., Janeen M. Hill, and Marc P. Kaufman.
Responses of group III and IV muscle afferents to dynamic exercise. J. Appl. Physiol. 82(6):
1811-1817, 1997.
Tetanic contraction of hindlimb skeletal muscle,
induced by electrical stimulation of either ventral roots or peripheral
nerves, is well known to activate group III and IV afferents.
Nevertheless, the effect of dynamic exercise on the discharge of these
thin fiber afferents is unknown. To shed some light on this question,
we recorded in decerebrate cats the discharge of 24 group III and 10 group IV afferents while the mesencephalic locomotor region (MLR) was
stimulated electrically. Each of the 34 afferents had their receptive
fields in the triceps surae muscles. Stimulation of the MLR for 1 min caused the triceps surae muscles to contract rhythmically, an effect
induced by an 
-motoneuron discharge pattern and recruitment order
almost identical to that occurring during dynamic exercise. Eighteen of
the 24 group III and 8 of the 10 group IV muscle afferents were
stimulated by MLR stimulation. The oxygen consumption of the
dynamically exercising triceps surae muscles was increased by 2.5-fold
over their resting levels. We conclude that low levels of dynamic
exercise stimulate group III and IV muscle afferents.
mesencephalic locomotor region; reflex control of the circulation; C fibers; A INTRODUCTION DYNAMIC EXERCISE INCREASES sympathetic nerve discharge,
cardiac rate, cardiac contractility, and ventilation. If severe enough, it also increases mean arterial pressure (13, 29). Two neural mechanisms have been postulated to cause these effects, namely central
command and the muscle reflex. The first mechanism, central command, is
believed to consist of the parallel activation of brain stem locomotor,
autonomic, and ventilatory circuits at the onset of exercise (5, 6,
16). The second mechanism, the reflex, is believed to consist of the
activation of these brain stem autonomic and ventilatory circuits by
the exercise-induced stimulation of group III and IV muscle afferents
(1, 4, 17).
Substantial evidence exists demonstrating that both neural mechanisms
are likely to play important roles in causing the cardiovascular and
respiratory responses to dynamic exercise (13, 29). Nevertheless, the
effect of dynamic exercise on the impulse activity of group III and IV
muscle afferents has received little attention. Previously, these thin
fiber afferents have been shown to be stimulated by both maintained
(14, 15) and intermittent (19) tetanic contraction, which, in turn, was
evoked by electrical stimulation of either the ventral roots or the
peripheral nerves.
This method of electrical stimulation has provided important
information about the discharge properties of group III and IV muscle
afferents. However, electrical stimulation of peripheral nerves or
ventral roots recruits This possibility prompted us to determine the effect of dynamic
exercise on the impulse activity of group III and IV afferents with
endings in the triceps surae muscles of decerebrate cats. Dynamic
exercise was evoked by electrical stimulation of the mesencephalic locomotor region, which is located in the cuneiform nucleus of the
midbrain (27). The impulse activity of these thin fiber muscle
afferents was recorded from the dorsal roots while the triceps surae
muscles were contracting rhythmically, an effect induced by an
METHODS 
fibers; autonomic nervous system
-motoneurons with the fastest conduction
velocities first, whereas dynamic exercise recruits these
-motoneurons last (9). In addition, electrical stimulation causes
motoneurons to discharge synchronously, whereas exercise causes them to
discharge asynchronously (12). The mechanical forces distorting
receptive fields of group III and IV afferents during tetanic
contraction and those distorting receptive fields during dynamic
exercise might be different. Similarly, the metabolites produced during
tetanic contraction and those produced during dynamic exercise might be
different. Consequently, the responses of group III and IV afferents to
tetanic contraction, which have been previously documented (14, 15,
19), might be different from the responses of these afferents to
dynamic exercise.
-motoneuron recruitment order and discharge pattern almost identical
to that observed during dynamic exercise.
Table 1.
Effect of dynamic exercise, induced by stimulation of mesencephalic
locomotor region, on blood flow, oxygen consumption, and metabolism of left triceps surae muscles
n
Rest
Exercise
Popliteal arterial blood
flow, ml/min
12
3.5 ± 0.3
6.5 ± 0.7*
Arterial lactate concentration,
mmol/l
9
3.7 ± 0.8
4.3 ± 0.9
Venous lactate concentration, mmol/l
9
3.9 ± 0.7
4.6 ± 0.9
Lactate production,
mmol/min
9
0.7 ± 0.5
0.9 ± 0.7
Arterial pH
9
7.41 ± 0.03
7.37 ± 0.03
Venous pH
9
7.34 ± 0.04
7.31 ± 0.04
Arterial PCO2,
Torr
9
35.0 ± 3.0
37.2 ± 2.4
Venous
PCO2, Torr
9
44.7 ± 2.9
46.4 ± 2.8
Arterial PO2, Torr
9
168.7 ± 7.1
163.5 ± 10.1
Venous
PO2, Torr
9
44.3 ± 5.7
37.6 ± 4.2
Arterial oxygen content, ml
O2/100 ml blood
9
12.7 ± 0.9
12.9 ± 1.1
Venous oxygen content, ml
O2/100 ml blood
9
9.2 ± 0.9
7.1 ± 1.1
Arteriovenous oxygen difference, ml
O2/100 ml blood
9
3.5 ± 1.6
5.8 ± 2.7*
Triceps surae oxygen consumption, ml
O2/min
9
0.13 ± 0.03
0.32 ± 0.04*
Triceps surae developed tension, g/step
12
0
365 ± 30*
Values are means ± SE; n, no. of observations.
*
Values that are significantly higher during exercise than during
rest, P < 0.05.
Dynamic exercise. Dynamic exercise (i.e., locomotion) was evoked by electrical stimulation (20 Hz, 0.7 ms, 80-100 µA) of the mesencephalic locomotor region (MLR). A monopolar stainless steel electrode (model SNEX-300, Rhodes) was positioned stereotaxically 4 mm lateral to the midline of the brain, 1 mm caudal to the sulcus between the superior and inferior colliculi, and 2 mm below the surface of the midbrain. The treadmill was turned on at a speed of 0.45 m/s, and then the midbrain was stimulated electrically. The electrode was lowered in 0.5-mm increments until locomotion was evoked. The criteria for locomotion included rhythmic alternating movement of the three limbs, which were placed on the treadmill, and rhythmic contractions of the left triceps surae muscles, which were fixed in place. Locomotion was evidenced both by recording the isometric tension developed by the contracting left triceps surae muscles and by recording the EMG activity of the right gastrocnemius muscle. The duration of the step cycle, although largely determined by the speed of the treadmill, varied among the cats depending on their size. Step cycle duration was calculated by measuring the time from the start of the contraction phase of one step to the start of the contraction phase of the subsequent step. The average step cycle duration, when the treadmill was hand driven, was 0.60 ± 0.02 s per step (n = 19). Recording of impulse activity from group III and IV afferents. Single-unit activity of group III and IV afferents with receptive fields in the left triceps surae muscles was recorded from fine filaments split from the left L7 or S1 dorsal roots. These filaments were dissected from the roots and placed on one foot of a bipolar hook electrode. The other foot was grounded to the cat with a thin string soaked in saline. The neural signals were passed through a high-impedance probe (model HIP511, Grass Instruments), amplified, and filtered (100-3,000 Hz). Action potentials were displayed on a monitor (model V1000, Gould) and a storage oscilloscope (model HP 54603B, Hewlett-Packard). Conduction velocity of an afferent was calculated by dividing the conduction distance between the recording electrode on the dorsal root and the stimulating electrode on the tibial nerve by the conduction time, which was measured on the storage oscilloscope. Afferents conducting impulses between 2.5 and 30 m/s were classified as group III fibers. Afferents conducting impulses at <2.5 m/s were classified as group IV fibers (21). The receptive fields of the afferents were located by applying pressure to the triceps surae muscles. Pressure was applied by squeezing the muscles between the experimenter's thumb and index finger in both a nonnoxious and noxious manner. The pressure was graded according to the subjective sensation reported by a fellow experimenter when similar pressure was applied to the forearm. The responses of the afferents to "tendon stretch" was assessed by turning the rack and pinion, which in turn lengthened the triceps surae muscles and the calcaneal tendon. Group I and II afferents were easily identified by their conduction velocities and their responses to stretch and twitch contraction; these thick fiber afferents were discarded. Once a group III or IV afferent with its receptive field in the triceps surae muscles was identified and a resting level of discharge was established, the response of this afferent to 60 s of dynamic exercise (i.e., locomotion) was recorded. Moreover, the afferent's activity during the 30 s after the exercise period was recorded. Blood flow, oxygen consumption, and lactate production measurements. Blood flow was measured by placing a 1.0-mm ultrasonic flow probe (model 1RS, Transonic Systems) around the popliteal artery. The space between the vessel and the probe was filled with acoustic couplant (Aquasonic ultrasound transmission gel), and the probe was fixed to the surrounding tissue with suture. The probe was connected to a flowmeter (model T206, Transonic Systems). In nine cats, oxygen consumption of the triceps surae muscles at rest and during locomotion was calculated to quantify the intensity of exercise performed. Oxygen consumption (
O2) was calculated by
using the Fick equation: 
× (CaO2 
CvO2) = O2, where
is popliteal blood flow,
CaO2 is arterial oxygen content, and
CvO2 is venous oxygen
content. Arterial oxygen content was calculated after
blood was obtained from the carotid artery (model ABL-3, Radiometer). A
side branch of the popliteal vein (i.e., the caudal genicular vein) was
cannulated such that the tip of the cannula was in the popliteal vein
just after its exit from the triceps surae muscles. Venous oxygen
content was calculated by obtaining and analyzing samples from the
popliteal vein (model ABL-3, Radiometer). Blood flow measurements and
arterial as well as venous blood samples were taken at rest and just
before the conclusion (i.e., the last 5 s) of dynamic exercise.
Arterial and venous blood samples were also analyzed for lactate
concentrations (model 2300, Yellow Springs Instruments). In addition,
the tension developed by the contracting triceps surae muscles during
each step of dynamic exercise was calculated.
Data analysis.
The discharge rate of each afferent was counted and placed in 2-s bins
for the 1-min period immediately preceeding dynamic exercise, for the 1 min of dynamic exercise, and for the first 30 s of recovery. The phase
of the step cycle (i.e., contraction or relaxation) during which the
afferent fired was recorded. The contraction phase of the step cycle
was defined as the period of time during the generation of developed
tension, and the relaxation phase was defined as the period of time
before the generation of developed tension by the left triceps surae
muscles. Comparisons of discharge rates during rest with those during
exercise were done with paired
t-tests. Similarly, comparisons of
oxygen consumption and lactate production during rest with those during
exercise were done with paired
t-tests. The criterion for statistical
significance was P < 0.05. All
values are expressed as means ± SE.
RESULTS
Responses of group IV afferents to dynamic exercise. We recorded the impulse activity of 10 group IV afferents with receptive fields in the left triceps surae muscles (conduction velocity: 1.3 ± 0.2 m/s; range: 0.7-2.4 m/s). Each of the 10 group IV afferents responded to noxious probing of the muscles; they did not, however, respond to nonnoxious probing. Similarly, none of the 10 responded to mild tendon stretch, which was induced by turning the rack and pinion. Eight of the 10 afferents displayed some spontaneous activity during rest, their discharge frequency averaging 0.5 ± 0.2 impulses/s. Eight of the 10 group IV afferents were stimulated by dynamic exercise (Figs. 5 and 6). Of the eight group IV afferents stimulated by exercise, only two discharged synchronously with the contraction phase of the step cycle (Fig. 5). Like the group III afferents that responded to exercise, the group IV afferents responded to exercise within the first 2 s of its onset. Morever, this increase in activity was maintained throughout the entire bout of exercise. When averaged over the 60-s exercise period, the mean discharge rate of the 10 group IV afferents was 1.0 ± 0.3 impulses/s, a significant (P < 0.05) increase over the resting discharge rate. After the exercise period ended, the afferents' discharge rates rapidly returned to their resting levels (i.e., 0.5 ± 0.2 impulses/s; Figs. 3 and 4). During exercise, 44 ± 4% of the action potentials discharged by the group IV afferents occurred during the contraction phase of the step cycle.
Intensity of dynamic exercise. Blood flow to the triceps surae muscles during exercise was almost twice that during rest (n = 12; P < 0.05; Table 1). Similarly, oxygen consumption by this muscle group during exercise was almost 2.5 times that during rest (n = 9; P < 0.05; Table 1). Furthermore, the arteriovenous oxygen difference during exercise was significantly greater than that during rest (n = 9; P < 0.05; Table 1). Other metabolic variables did not change significantly from rest to exercise (Table 1). The triceps surae muscles developed, on average, 365 ± 30 g of tension per step.
DISCUSSION
We have shown that group III and IV muscle afferents were stimulated by
rhythmic contractions, which, in turn, were induced by stimulation of
the MLR. The recruitment order and discharge pattern of the
-motoneurons activated by stimulation of the MLR are almost
identical to the recruitment order and discharge pattern of these
motoneurons during dynamic exercise (10-12, 28, 31). Moreover, the
level of dynamic exercise used in our experiments to stimulate these
thin fiber muscle afferents was low. This was evidenced by the fact
that the oyxgen consumption of the dynamically exercising triceps surae
muscles increased over resting levels by only 2.5-fold. In contrast,
oxygen consumption of cat hindlimb muscles during forceful intermittent
contractions can increase over resting levels by 10-fold (2, 3).
A substantial number of group IV afferents are thought to be nociceptors (18). Others are thought to be metaboreceptors, signaling that the oxygen and/or blood supply in the exercising muscles is not satisfying demand. In our experiments, the group IV afferents stimulated by dynamic exercise did not appear to signal either nociceptive or metaboreceptive events, the latter being caused by a lack of blood and/or oxygen supply. Specifically, the amount of dynamic exercise performed by the cats was low and, therefore, probably not noxious; moreover, it probably did not create a mismatch between oxygen supply and demand in the working muscles. These facts make our finding that group IV afferents were responsive to a low level of exercise surprising. Because most of the group IV afferents did not discharge in synchrony with the rhythmic contractions, their sensitivity to mechanical stimuli did not appear to be high. These findings lead to the speculation that these unmyelinated afferents responded to metabolic stimuli that were unrelated to a mismatch between blood supply and demand in the exercising muscle.
Group III muscle afferents, in contrast to group IV afferents, are sensitive to mechanical distortion of their receptive fields. For example, group III afferents respond vigorously to maneuvers such as tendon stretch and nonnoxious probing of their receptive fields (14, 19). Moreover, group III afferents often respond briskly at the onset of tetanic contraction (14, 25). The sensitivity to mechanical distortion possessed by group III afferents probably explains our finding that during dynamic exercise these thinly myelinated afferents frequently discharged in synchrony with the contraction phase of the step cycle.
We do not know whether the discharge rates of the group III and IV afferents stimulated by the low level of dynamic exercise used in our experiments were sufficient to evoke reflex autonomic and ventilatory effects. Nevertheless, some previous studies performed in anesthetized animals lead us to speculate that this might be the case. Sato et al. (26), for example, measured cardioaccelerator responses to different frequencies of electrical stimulation applied to hindlimb muscle nerves of chloralose-anesthetized, vagotomized cats. When the currents were sufficient to recruit group IV afferents, Sato et al. found that the minimum effective frequency needed to increase heart rate was only 0.25 Hz. In addition, Mizumura and Kumazawa (22) found that 2-Hz electrical stimulation of hindlimb muscle nerves with current intensities that recruited group IV afferents increased ventilation in barbiturate-anesthetized dogs. These investigators did not report the ventilatory effects of stimulation frequencies lower than 2 Hz.
In our preparation, the triceps surae muscles from which afferent activity was recorded were fixed in place and, consequently, did not participate in the locomotion evoked by stimulation of the MLR. The peak tensions developed by the restrained triceps surae muscles in our experiments were similar but lower than those measured during walking in unrestrained intact cats (30). This lower developed tension can be attributed to two causes. First, the triceps surae muscles were partially denervated in our preparation and as a result received less than normal spindle support. Second, in unrestrained cats, peak muscle tension occurs when the contracting triceps surae muscles are lengthening [i.e., contracting eccentrically (7, 30)]. Muscle tension developed during eccentric contraction has been shown to exceed that developed during isometric contraction (8, 23), the latter of which was measured in our preparation. Based on these facts, we think it is reasonable to speculate that the mechanical stimulus (i.e., developed tension) to the group III and IV afferents having activity that was recorded in our experiments would have been greater if the triceps surae muscles had been allowed to move freely . Despite this restraint, 75% of the group III afferents and 80% of the group IV afferents tested in our experiments were stimulated by a low level of dynamic exercise.
In a previous study from this laboratory, Pickar et al. (24) found that group III afferents with endings in the triceps surae muscles of decerebrate cats were stimulated by a brief period (i.e., 20 s) of dynamic exercise. In the present study we confirmed and extended this finding by showing that these thinly myelinated afferents were stimulated by a longer period (i.e., 60 s) of exercise. Moreover, we quantified the amount of oxygen consumed by the exercising triceps surae muscles and found that it was low. Perhaps our most important finding was that group III afferents displayed a maintained discharge during the entire exercise period (i.e., 60 s); adaptation was not observed. These results are consistent with the notion that group III afferents are capable of initiating and maintaining reflex autonomic and ventilatory responses to mild exercise.
In our experiments, the dynamically exercising triceps surae muscles
developed only a small amount of tension (i.e., 365 g); nevertheless, a
large percentage (i.e., 75%) of group III afferents were stimulated.
This finding contrasts with that reported previously by our laboratory
(14) in which a similar percentage of group III afferents appeared to
require at least 2 kg of developed tension to stimulate them during
tetanic (static) contractions. One explanation for this discrepancy
might be that during dynamic exercise, such as that induced by
stimulation of the mesencephalic locomotor center, muscle contraction
is caused by an -motoneuron recruitment order and discharge pattern
that are physiological, whereas during tetany, such as that induced by
electrical stimulation of the ventral roots, muscle contraction is
caused by an -motoneuron recruitment order and discharge pattern
that are not physiological. This difference in -motoneuron discharge
might result in greater mechanical stimulation of the receptive fields
of group III afferents during dynamic exercise than during tetany.
In conclusion, we have shown for the first time that muscle afferents are stimulated by low levels of dynamic exercise. This stimulation did not appear to depend on the production of a metabolite signaling that blood supply did not satisfy demand in the exercising muscles. Our present and past findings (24) are consistent with the hypothesis that the exercise pressor reflex (20), the afferent arm of which is composed of group III and IV muscle afferents (17), plays a role in the cardiovascular and respiratory adjustments to low levels of muscular activity.
ACKNOWLEDGEMENTS
This work was supported by National Heart, Lung, and Blood Institute (NHLBI) Grant R01 HL-30710. C. M. Adreani was supported, in part, by NHLBI Grant T32 HL-07682.
FOOTNOTES
Address for reprint requests: M. P. Kaufman, Div. of Cardiovascular Medicine, TB 172, Bioletti Way, Univ. of California, Davis, CA 95616.
Received 11 November 1996; accepted in final form 3 February 1997.
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 A. R. Light, R. W. Hughen, J. Zhang, J. Rainier, Z. Liu, and J. Lee Dorsal Root Ganglion Neurons Innervating Skeletal Muscle Respond to Physiological Combinations of Protons, ATP, and Lactate Mediated by ASIC, P2X, and TRPV1 J Neurophysiol, September 1, 2008; 100(3): 1184 - 1201. [Abstract] [Full Text] [PDF]
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 J. Cui, R. Moradkhan, V. Mascarenhas, A. Momen, and L. I. Sinoway Cyclooxygenase inhibition attenuates sympathetic responses to muscle stretch in humans Am J Physiol Heart Circ Physiol, June 1, 2008; 294(6): H2693 - H2700. [Abstract] [Full Text] [PDF]
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 A. Crisafulli, R. Milia, A. Lobina, M. Caddeo, F. Tocco, A. Concu, and F. Melis Haemodynamic effect of metaboreflex activation in men after running above and below the velocity of the anaerobic threshold Exp Physiol, April 1, 2008; 93(4): 447 - 457. [Abstract] [Full Text] [PDF]
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R. C. Drew, M. P. D. Bell, and M. J. White Modulation of spontaneous baroreflex control of heart rate and indexes of vagal tone by passive calf muscle stretch during graded metaboreflex activation in humans J Appl Physiol, March 1, 2008; 104(3): 716 - 723. [Abstract] [Full Text] [PDF]
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J. Cui, V. Mascarenhas, R. Moradkhan, C. Blaha, and L. I. Sinoway Effects of muscle metabolites on responses of muscle sympathetic nerve activity to mechanoreceptor(s) stimulation in healthy humans Am J Physiol Regulatory Integrative Comp Physiol, February 1, 2008; 294(2): R458 - R466. [Abstract] [Full Text] [PDF]
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J.-W. Yang, H.-C. Shih, and B.-C. Shyu Intracortical Circuits in Rat Anterior Cingulate Cortex Are Activated by Nociceptive Inputs Mediated by Medial Thalamus J Neurophysiol, December 1, 2006; 96(6): 3409 - 3422. [Abstract] [Full Text] [PDF]
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S. G. Hayes, A. E. Kindig, and M. P. Kaufman Cyclooxygenase blockade attenuates responses of group III and IV muscle afferents to dynamic exercise in cats Am J Physiol Heart Circ Physiol, June 1, 2006; 290(6): H2239 - H2246. [Abstract] [Full Text] [PDF]
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T. Nishiyasu, T. Maekawa, R. Sone, N. Tan, and N. Kondo Effects of rhythmic muscle compression on cardiovascular responses and muscle oxygenation at rest and during dynamic exercise Exp Physiol, January 1, 2006; 91(1): 103 - 109. [Abstract] [Full Text] [PDF]
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P. Haouzi and B. Chenuel Control of arterial PCO2 by somatic afferents in sheep J. Physiol., December 15, 2005; 569(3): 975 - 987. [Abstract] [Full Text] [PDF]
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J. P Fisher, M. P. D Bell, and M. J White Cardiovascular responses to human calf muscle stretch during varying levels of muscle metaboreflex activation Exp Physiol, September 1, 2005; 90(5): 773 - 781. [Abstract] [Full Text] [PDF]
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L. I. Sinoway and J. Li A perspective on the muscle reflex: implications for congestive heart failure J Appl Physiol, July 1, 2005; 99(1): 5 - 22. [Abstract] [Full Text] [PDF]
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H. R. Middlekauff, J. Chiu, M. A. Hamilton, G. C. Fonarow, W. R. MacLellan, A. Hage, J. Moriguchi, and J. Patel Muscle mechanoreceptor sensitivity in heart failure Am J Physiol Heart Circ Physiol, November 1, 2004; 287(5): H1937 - H1943. [Abstract] [Full Text] [PDF]
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R. L. Hanna and M. P. Kaufman Activation of thin-fiber muscle afferents by a P2X agonist in cats J Appl Physiol, March 1, 2004; 96(3): 1166 - 1169. [Abstract] [Full Text] [PDF]
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P. Haouzi, B. Chenuel, and A. Huszczuk Sensing vascular distension in skeletal muscle by slow conducting afferent fibers: neurophysiological basis and implication for respiratory control J Appl Physiol, February 1, 2004; 96(2): 407 - 418. [Abstract] [Full Text] [PDF]
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Y. M. Kang, M. J. Kenney, K. F. Spratt, and J. G. Pickar Somatosympathetic Reflexes From the Low Back in the Anesthetized Cat J Neurophysiol, October 1, 2003; 90(4): 2548 - 2559. [Abstract] [Full Text] [PDF]
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 L. Spicuzza, L. Bernardi, A. Calciati, and G. U. Di Maria Autonomic Modulation of Heart Rate during Obstructive versus Central Apneas in Patients with Sleep-disordered Breathing Am. J. Respir. Crit. Care Med., March 15, 2003; 167(6): 902 - 910. [Abstract] [Full Text] [PDF]
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 T. A. Markel, J. C. Daley III, C. S. Hogeman, M. D. Herr, M. H. Khan, K. S. Gray, A. R. Kunselman, and L. I. Sinoway Aging and the Exercise Pressor Reflex in Humans Circulation, February 11, 2003; 107(5): 675 - 678. [Abstract] [Full Text] [PDF]
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J. Li and L. I. Sinoway ATP stimulates chemically sensitive and sensitizes mechanically sensitive afferents Am J Physiol Heart Circ Physiol, December 1, 2002; 283(6): H2636 - H2643. [Abstract] [Full Text] [PDF]
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T Graven-Nielsen, L Arendt-Nielsen, and S Mense Thermosensitivity of muscle: high-intensity thermal stimulation of muscle tissue induces muscle pain in humans J. Physiol., April 15, 2002; 540(2): 647 - 656. [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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L. B. Wilson, D. Andrew, and A. D. Craig Activation of Spinobulbar Lamina I Neurons by Static Muscle Contraction J Neurophysiol, March 1, 2002; 87(3): 1641 - 1645. [Abstract] [Full Text] [PDF]
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 S. C. Gandevia Spinal and Supraspinal Factors in Human Muscle Fatigue Physiol Rev, October 1, 2001; 81(4): 1725 - 1789. [Abstract] [Full Text] [PDF]
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J. M. Kramer, A. Aragones, and T. G. Waldrop Reflex cardiovascular responses originating in exercising muscles of mice J Appl Physiol, February 1, 2001; 90(2): 579 - 585. [Abstract] [Full Text] [PDF]
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K. J. Doerzbacher and C. A. Ray Muscle sympathetic nerve responses to physiological changes in prostaglandin production in humans J Appl Physiol, February 1, 2001; 90(2): 624 - 629. [Abstract] [Full Text] [PDF]
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A. C Scott, D. P Francis, L C. Davies, P. Ponikowski, A. J S Coats, and M. F Piepoli Contribution of skeletal muscle 'ergoreceptors' in the human leg to respiratory control in chronic heart failure J. Physiol., December 15, 2000; 529(3): 863 - 870. [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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S. Mostoufi-Moab, M. D. Herr, D. H. Silber, K. S. Gray, U. A. Leuenberger, and L. I. Sinoway Limb congestion enhances the synchronization of sympathetic outflow with muscle contraction Am J Physiol Regulatory Integrative Comp Physiol, August 1, 2000; 279(2): R478 - R483. [Abstract] [Full Text] [PDF]
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J. M. Legramante, G. Raimondi, C. M. Adreani, S. Sacco, F. Iellamo, G. Peruzzi, and M. P. Kaufman Group III muscle afferents evoke reflex depressor responses to repetitive muscle contractions in rabbits Am J Physiol Heart Circ Physiol, March 1, 2000; 278(3): H871 - H877. [Abstract] [Full Text] [PDF]
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P. Haouzi, J. M. Hill, B. K. Lewis, and M. P. Kaufman Responses of group III and IV muscle afferents to distension of the peripheral vascular bed J Appl Physiol, August 1, 1999; 87(2): 545 - 553. [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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J. T Potts, I. E Fuchs, J. Li, B. Leshnower, and J. H Mitchell Skeletal muscle afferent fibres release substance P in the nucleus tractus solitarii of anaesthetized cats J. Physiol., February 1, 1999; 514(3): 829 - 841. [Abstract] [Full Text] [PDF]
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T Graven-Nielsen, L Arendt-Nielsen, and S Mense Thermosensitivity of muscle: high-intensity thermal stimulation of muscle tissue induces muscle pain in humans J. Physiol., April 15, 2002; 540(2): 647 - 656. [Abstract] [Full Text] [PDF]
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