Dynamic exercise stimulates group III muscle afferents

1994 ◽  
Vol 71 (2) ◽  
pp. 753-760 ◽  
Author(s):  
J. G. Pickar ◽  
J. M. Hill ◽  
M. P. Kaufman

1. In decerebrate cats, we investigated the responses of group III muscle afferents to dynamic exercise. The cats performed low intensity dynamic exercise on a treadmill. Group III afferent activity from the dynamically exercising triceps surae muscles was recorded from L7-S1 dorsal root filaments. 2. Single-unit recordings were obtained from 15 group III afferent fibers whose receptive fields were in the triceps surae muscles and from one group III afferent whose receptive field was in the flexor digitorum longus muscle. Conduction velocities for the 16 group III afferents ranged from 3.0 to 27.9 m/s (15.6 +/- 1.9 m/s, mean +/- SE). 3. Ten of 16 group III muscle afferents were stimulated by dynamic exercise. Of the 10, 7 were strongly responsive and 3 were mildly responsive to dynamic exercise. Each of the 10 afferents displayed at least some activity that was synchronized to the contraction phase of the step cycle. The mean developed tensions for strongly responsive afferents, mildly responsive afferents, and afferents that did not respond were 0.8 +/- 0.3, 1.3 +/- 0.5, and 0.7 +/- 0.3 Kg, respectively (P > 0.05). Thus differences in the responsiveness of the afferents to exercise were not attributable to differences in developed tensions. 4. The group III afferents that were strongly responsive to dynamic exercise were also mechanically sensitive. Each strongly responsive afferent (n = 7) was stimulated by nonnoxious pressure applied to its receptive field. Most strongly responsive afferents (n = 5) were stimulated by stretch of the triceps surae muscles.(ABSTRACT TRUNCATED AT 250 WORDS)

1997 ◽  
Vol 82 (6) ◽  
pp. 1811-1817 ◽  
Author(s):  
Christine M. Adreani ◽  
Janeen M. Hill ◽  
Marc P. Kaufman

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 α-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.


1999 ◽  
Vol 87 (2) ◽  
pp. 545-553 ◽  
Author(s):  
Philippe Haouzi ◽  
Janeen M. Hill ◽  
Brock K. Lewis ◽  
Marc P. Kaufman

This study was undertaken to test the hypothesis that group III and IV afferents with endings in skeletal muscle signal the distension of the peripheral vascular network. The responses of these slowly conducting afferents to pharmacologically induced vasodilation and to acute obstruction of the venous drainage of the hindlimbs were studied in barbiturate-anesthetized cats. Afferent impulses arising from endings in the triceps surae muscles were recorded from the L7 and S1 dorsal roots. Fifteen of the 48 group IV and 3 of the 19 group III afferents tested were stimulated by intra-aortic injections of papaverine (2–2.5 mg/kg). Sixty-two percent of the afferents that responded to papaverine also responded to isoproterenol (50 μg/kg). Seven of the 36 group IV and 2 of the 12 group III afferents tested were excited by acute distension of the hindlimb venous system. Four of the seven group IV afferents responding to venous distension also responded to papaverine (57 vs. 13% for the nonresponding). Finally, we observed that most of the group IV afferents that were excited by dynamic contractions of the triceps surae muscles also responded either to venous distension or to vasodilatory agents. These results are consistent with the histological findings that a large number of group IV endings have their receptive fields close to the venules and suggest that they can be stimulated by the deformation of these vascular structures when peripheral conductance increases. Moreover, such a mechanism offers the possibility of encoding both the effects of muscle contraction through intramuscular pressure changes and the distension of the venular system, thereby monitoring the activity of the veno-muscular pump.


2006 ◽  
Vol 290 (6) ◽  
pp. H2239-H2246 ◽  
Author(s):  
Shawn G. Hayes ◽  
Angela E. Kindig ◽  
Marc P. Kaufman

Cyclooxygenase products accumulate in statically contracting muscles to stimulate group III and IV afferents. The role played by these products in stimulating thin fiber muscle afferents during dynamic exercise is unknown. Therefore, in decerebrated cats, we recorded the responses of 17 group III and 12 group IV triceps surae muscle afferents to dynamic exercise, evoked by stimulation of the mesencephalic locomotor region. Each afferent was tested while the muscles were freely perfused and while the circulation to the muscles was occluded. The increases in group III and IV afferent activity during dynamic exercise while the circulation to the muscles was occluded were greater than those during exercise while the muscles were freely perfused ( P < 0.01). Indomethacin (5 mg/kg iv), a cyclooxygenase blocker, reduced the responses to dynamic exercise of the group III afferents by 42% when the circulation to the triceps surae muscles was occluded ( P < 0.001) and by 29% when the circulation was not occluded ( P = 0.004). Likewise, indomethacin reduced the responses to dynamic exercise of group IV afferents by 34% when the circulation was occluded ( P < 0.001) and by 18% when the circulation was not occluded ( P = 0.026). Before indomethacin, the activity of the group IV, but not group III, afferents was significantly higher during postexercise circulatory occlusion than during rest ( P < 0.05). After indomethacin, however, group IV activity during postexercise circulatory occlusion was not significantly different from group IV activity during rest. Our data suggest that cyclooxygenase products play a role both in sensitizing group III and IV afferents during exercise and in stimulating group IV afferents during postexercise circulatory occlusion.


1993 ◽  
Vol 69 (4) ◽  
pp. 1053-1059 ◽  
Author(s):  
L. I. Sinoway ◽  
J. M. Hill ◽  
J. G. Pickar ◽  
M. P. Kaufman

1. In barbiturate-anesthetized cats we examined the interaction of lactic acid and static contraction on the discharge of group III muscle afferents. Only afferents whose receptive fields were located in the triceps surae muscles were studied. 2. Twelve of 20 afferents were stimulated by a 60-s static contraction. The majority of firing occurred within the first few seconds of contraction. Thirteen of 20 afferents were stimulated by femoral arterial injections of 24 mM lactic acid (1-4 ml) with the muscle at rest. Repeated injections of lactic acid with the muscle at rest led to tachyphylaxis. Lactic acid was then injected (24 mM; 4 ml) during the last 15 s of static contraction. In eight of nine afferents that were tachyphylactic to lactic acid with the muscle at rest, we noted a restored sensitivity to lactic acid during contraction. 3. In separate experiments we examined the effects of dichloroacetate (DCA) on the responses of group III muscle afferents to static contraction. DCA reduces the production of lactic acid by increasing levels of the active form of the enzyme pyruvate dehydrogenase. 4. DCA lowered arterial and venous lactate concentrations at rest and during contraction. DCA significantly decreased (31%; P < 0.05) the responses of the afferents to contraction. This effect was most prominent within the first 10 s of contraction and was not due to a reduced level of mechanical stimulation after DCA, because peak tension levels were the same during the two bouts of contraction.(ABSTRACT TRUNCATED AT 250 WORDS)


2001 ◽  
Vol 280 (5) ◽  
pp. H2153-H2161 ◽  
Author(s):  
Shawn G. Hayes ◽  
Marc P. Kaufman

The exercise pressor reflex, which arises from the contraction-induced stimulation of group III and IV muscle afferents, is widely believed to be evoked by metabolic stimuli signaling a mismatch between blood/oxygen demand and supply in the working muscles. Nevertheless, mechanical stimuli may also play a role in evoking the exercise pressor reflex. To determine this role, we examined the effect of gadolinium, which blocks mechanosensitive channels, on the exercise pressor reflex in both decerebrate and α-chloralose-anesthetized cats. We found that gadolinium (10 mM; 1 ml) injected into the femoral artery significantly attenuated the reflex pressor responses to static contraction of the triceps surae muscles and to stretch of the calcaneal (Achilles) tendon. In contrast, gadolinium had no effect on the reflex pressor response to femoral arterial injection of capsaicin (5 μg). In addition, gadolinium significantly attenuated the responses of group III muscle afferents, many of which are mechanically sensitive, to both static contraction and to tendon stretch. Gadolinium, however, had no effect on the responses of group IV muscle afferents, many of which are metabolically sensitive, to either static contraction or to capsaicin injection. We conclude that mechanical stimuli arising in contracting skeletal muscles contribute to the elicitation of the exercise pressor reflex.


1995 ◽  
Vol 73 (2) ◽  
pp. 651-661 ◽  
Author(s):  
R. D. Johnson ◽  
J. S. Taylor ◽  
L. M. Mendell ◽  
J. B. Munson

1. In this study we investigate the peripheral receptive field properties and spinal cord connections of low-threshold muscle afferent fibers cross-regenerated into the skin to determine whether a cutaneous target can rescue physiological functions lost after chronic axotomy. 2. In adult cats the medial gastrocnemius (MG) muscle nerve was coated with the distal cut end of either the caudal or lateral cutaneous sural nerves and allowed to regenerate into the hairy skin (postoperative period 6-30 mo). During terminal acute experiments we made recordings of single MG afferent fibers in dorsal root filaments and peripheral nerve. Conduction velocity and receptive field characteristics were determined for each fiber. In addition, the MG nerve was stimulated to elicit cord dorsum potentials and monosynaptic excitatory postsynaptic potentials (EPSPs) in heteronymous motoneurons. As controls, studies were carried out after MG nerve axotomy (postoperative period 2.5-12 mo). 3. After innervation of the skin, MG muscle afferent fibers exhibited firing characteristics and proximal segment conduction velocities like those of normal MG afferents. Responses to skin and hair stimulation consisted primarily of slowly adapting, stretch-sensitive, and steady discharge patterns, all common in normal muscle afferents but not in cutaneous afferents. These properties were observed despite the innervation of touch domes and single hairs, suggesting that the peripheral physiology of muscle afferents is a function of the axonal membrane and is not respecified by a cutaneous target and/or receptors. 4. Cord dorsum potentials were characteristic of those elicited by intact muscle afferents rather than skin afferents and showed recovery of configurations lost after chronic axotomy. 5. The monosynaptic EPSPs elicited in lateral gastrocnemius-soleus motoneurons also recovered from the reduction in amplitude observed after chronic axotomy. The configurations of these EPSPs were characteristic of muscle afferents rather than skin afferents. 6. These experiments demonstrate that the peripheral and central physiological properties of muscle afferents are rescued from the axotomy state if the afferents are allowed to reinnervate skin. We found no evidence that respecification had occurred to bring the function of muscle afferents into accord with the new cutaneous target.


2001 ◽  
Vol 90 (1) ◽  
pp. 308-316 ◽  
Author(s):  
B. G. Leshnower ◽  
J. T. Potts ◽  
M. G. Garry ◽  
J. H. Mitchell

It is well known that the exercise pressor reflex (EPR) is mediated by group III and IV skeletal muscle afferent fibers, which exhibit unique discharge responses to mechanical and chemical stimuli. Based on the difference in discharge patterns of group III and IV muscle afferents, we hypothesized that activation of mechanically sensitive (MS) fibers would evoke a different pattern of cardiovascular responses compared with activation of both MS and chemosensitive (CS) fibers. Experiments were conducted in chloralose-urethane-anesthetized cats ( n = 10). Passive muscle stretch was used to activate MS afferents, and electrically evoked contraction of the triceps surae was used to activate both MS and CS muscle afferents. No significant differences were shown in reflex heart rate and mean arterial pressure (MAP) responses between passive muscle stretch and evoked muscle contraction. However, when the reflex responses were matched according to tension-time index (TTI), the peak MAP response (67 ± 4 vs. 56 ± 4 mmHg, P < 0.05) was significantly greater at higher TTI (427 ± 18 vs. 304 ± 13 kg · s, high vs. low TTI, P < 0.05), despite different modes of afferent fiber activation. When the same mode of afferent fiber activation was compared, the peak MAP response (65 ± 7 vs. 55 ± 5 mmHg, P < 0.05) was again predicted by the magnitude of TTI (422 ± 24 vs. 298 ± 19 kg · s, high vs. low TTI, P < 0.05). Total sensory input from skeletal muscle ergoreceptors, as predicted by TTI and not the modality of afferent fiber activation (muscle contraction vs. passive stretch), is suggested to be the primary determinant of the magnitude of the EPR-evoked cardiovascular response.


1986 ◽  
Vol 55 (1) ◽  
pp. 76-96 ◽  
Author(s):  
R. P. Yezierski ◽  
R. H. Schwartz

Recordings were made from 90 identified spinomesencephalic tract (SMT) cells in the lumbosacral spinal cord of cats anesthetized with alpha-chloralose and pentobarbital sodium. Recording sites were located in laminae I-VIII. Antidromic stimulation sites were located in different regions of the rostral and caudal midbrain including the periaqueductal gray, midbrain reticular formation, and the deep layers of the superior colliculus. Twelve SMT cells were antidromically activated from more than one midbrain level or from sites in the medial thalamus. The mean conduction velocity for the population of cells sampled was 45.2 +/- 21.4 m/s. Cells were categorized based on their responses to graded intensities of mechanical stimuli and the location of excitatory and/or inhibitory receptive fields. Four major categories of cells were encountered: wide dynamic range (WDR); high threshold (HT); deep/tap; and nonresponsive. WDR and HT cells had excitatory and/or inhibitory receptive fields restricted to the ipsilateral hindlimb or extending to other parts of the body including the tail, forelimbs, and face. Some cells had long afterdischarges following noxious stimulation, whereas others had high rates of background activity that was depressed by nonnoxious and noxious stimuli. Deep/tap cells received convergent input from muscle, joint, or visceral primary afferent fibers. The placement of mechanical lesions at different rostrocaudal levels of the cervical spinal cord provided information related to the spinal trajectory of SMT axons. Six axons were located contralateral to the recording electrode in the ventrolateral/medial or lateral funiculi while two were located in the ventrolateral funiculus of the ipsilateral spinal cord. Stimulation at sites used to antidromically activate SMT cells resulted in the inhibition of background and evoked responses for 22 of 25 cells tested. Inhibitory effects were observed on responses evoked by low/high intensity cutaneous stimuli and by the activation of joint or muscle primary afferent fibers. Based on the response and receptive-field properties of SMT cells it is suggested that the SMT may have an important role in somatosensory mechanisms, particularly those related to nociception.


2004 ◽  
Vol 96 (3) ◽  
pp. 1166-1169 ◽  
Author(s):  
Ramy L. Hanna ◽  
Marc P. Kaufman

The responses of group III and IV triceps surae muscle afferents to intra-arterial injection of α,β-methylene ATP (50 μg/kg) was examined in decerebrate cats. We found that this P2X3 agonist stimulated only three of 18 group III afferents but 7 of 9 group IV afferents ( P < 0.004). The three group III afferents stimulated by α,β-methylene ATP conducted impulses below 4 m/s. Pyridoxal phosphate-6-azophenyl-2′,4′-disulfonic acid, a P2-receptor antagonist, prevented the stimulation of these afferents by α,β-methylene ATP. We conclude that P2X3 agonists stimulate only the slowest conducting group III muscle afferents as well as group IV afferents.


1991 ◽  
Vol 66 (6) ◽  
pp. 2155-2158 ◽  
Author(s):  
R. D. Johnson ◽  
J. B. Munson

1. In cats, we studied the physiological properties of regenerating sprouts of muscle afferent fibers and compared them with sprouts from cutaneous afferent fibers. 2. Muscle nerves to the triceps surae and cutaneous sural nerves were axotomized in the popliteal fossa, and the proximal ends were inserted into nerve cuffs. Six days later, we recorded action potentials from single Groups I and II muscle and mostly Group II cutaneous afferents driven by mechanostimulation of the cuff. 3. Most muscle afferent sprouts (91%) had a regular slowly adapting discharge in response to sustained mechanical displacement of the cuff, particularly to sustained stretch stimuli, whereas most cutaneous afferents (92%) did not. Muscle afferents were more likely to have a spontaneous discharge and afterdischarge. 4. Group II muscle afferent sprouts had lower stretch thresholds and a higher incidence of spontaneous discharge compared with Group I fiber sprouts, whereas Group I fibers had a higher incidence of high-frequency afterdischarge to mechanical stimuli. 5. We conclude that, 6 days after axotomy, regenerating sprouts of muscle afferents, particularly Group II afferents, have become mechanosensitive in the absence of a receptor target and exhibit physiological properties similar to those found when innervating their native muscle but significantly different from sprouts of cutaneous afferents. Expression of these native muscle afferent firing patterns after the inappropriate reinnervation of hairy skin may be due to inherent properties of the muscle afferent fiber.


Sign in / Sign up

Export Citation Format

Share Document