Activation of thin-fiber muscle afferents by a P2X agonist in cats

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.

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.


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.


2006 ◽  
Vol 290 (3) ◽  
pp. H1214-H1219 ◽  
Author(s):  
Angela E. Kindig ◽  
Shawn G. Hayes ◽  
Ramy L. Hanna ◽  
Marc P. Kaufman

Injection into the arterial supply of skeletal muscle of pyridoxal phosphate-6-azophenyl-2′,4′-disulfonic acid (PPADS), a P2 receptor antagonist, has been shown previously to attenuate the reflex pressor responses to both static contraction and to tendon stretch. In decerebrated cats, we tested the hypothesis that PPADS attenuated the responses of groups III and IV muscle afferents to static contraction as well as to tendon stretch. We found that injection of PPADS (10 mg/kg) into the popliteal artery attenuated the responses of both group III ( n = 16 cats) and group IV afferents ( n = 14 cats) to static contraction. Specifically, static contraction before PPADS injection increased the discharge rate of the group III afferents from 0.1 ± 0.05 to 1.6 ± 0.5 impulses/s, whereas contraction after PPADS injection increased the discharge of the group III afferents from 0.2 ± 0.1 to only 1.0 ± 0.5 impulses/s ( P < 0.05). Likewise, static contraction before PPADS injection increased the discharge rate of the group IV afferents from 0.3 ± 0.1 to 1.0 ± 0.3 impulses/s, whereas contraction after PPADS injection increased the discharge of the group IV afferents from 0.2 ± 0.1 to only 0.3 ± 0.1 impulses/s ( P < 0.05). In addition, PPADS significantly attenuated the responses of group III afferents to tendon stretch but had no effect on the responses of group IV afferents. Our findings suggest that both groups III and IV afferents are responsible for evoking the purinergic component of the exercise pressor reflex, whereas only group III afferents are responsible for evoking the purinergic component of the muscle mechanoreflex that is evoked by tendon stretch.


1998 ◽  
Vol 84 (6) ◽  
pp. 1827-1833 ◽  
Author(s):  
Christine M. Adreani ◽  
Marc P. Kaufman

Our laboratory has shown previously that a low level of dynamic exercise induced by electrical stimulation of the mesencephalic locomotor region (MLR) stimulated group III and IV muscle afferents in decerebrate unanesthetized cats (C. M. Adreani, J. M. Hill, and M. P. Kaufman. J. Appl. Physiol. 83: 1811–1817, 1997). In the present study, we have extended these findings by examining the effect of occluding the arterial supply to the dynamically exercising muscles on the afferents’ responses to MLR stimulation. In decerebrate cats, we found that arterial occlusion increased the responsiveness to a low level of dynamic exercise in 44% of the group III and 47% of the group IV afferents tested. Occlusion, compared with the freely perfused state, did not increase the concentrations of either hydrogen ion or lactate ion in the venous effluent from the exercising muscles. We conclude that arterial occlusion caused some unspecified substance to accumulate in the working muscles to increase the sensitivity of equal percentages of group III and IV afferents to dynamic exercise.


1998 ◽  
Vol 274 (5) ◽  
pp. H1552-H1559 ◽  
Author(s):  
Janeen M. Hill ◽  
Marc P. Kaufman

We determined the effects of stimulation of the mesencephalic locomotor region (MLR) and the muscle reflex, each evoked separately, on the discharge of cutaneous sympathetic fibers innervating the hairy skin of decerebrate cats. Electrical stimulation of the MLR was performed while the cats were paralyzed with vecuronium bromide. The muscle reflex was evoked while the cats were not paralyzed by electrical stimulation of the tibial nerve at current intensities that did not activate directly group III and IV muscle afferents. MLR stimulation increased, on average, the discharge of the 23 cutaneous sympathetic fibers tested ( P < 0.05). The muscle reflex, in contrast, had no overall effect on the discharge of 21 sympathetic fibers tested ( P > 0.05). Both maneuvers markedly increased mean arterial pressure and heart rate ( P < 0.05). Prevention of the baroreceptor reflex with the α-adrenergic blocking agent phentolamine did not reveal a stimulatory effect of the muscle reflex on cutaneous sympathetic discharge. We conclude that the MLR is a more important mechanism than is the muscle reflex in controlling sympathetic discharge to hairy skin during dynamic exercise.


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.


2000 ◽  
Vol 278 (3) ◽  
pp. H871-H877 ◽  
Author(s):  
J. M. Legramante ◽  
G. Raimondi ◽  
C. M. Adreani ◽  
S. Sacco ◽  
F. Iellamo ◽  
...  

Repetitive-twitch contraction of the hindlimb muscles in anesthetized rabbits consistently evokes a reflex depressor response, whereas this type of contraction in anesthetized cats evokes a reflex pressor response in about one-half of the preparations tested. Rapidly conducting group III fibers appear to comprise the afferent arm of the reflex arc, evoking the depressor response to twitch contraction in rabbits because electrical stimulation of their axons reflexly decreases arterial pressure. In contrast, electrical stimulation of the axons of slowly conducting group III and group IV afferents reflexly increases arterial pressure in rabbits. In the present study, we examined the discharge properties of group III and IV muscle afferents and found that the former (i.e., 13 of 20), but not the latter (i.e., 0 of 10), were stimulated by 5 min of repetitive-twitch contraction (1 Hz) of the rabbit triceps surae muscles. Moreover, most of the group III afferents responding to contraction appeared to be mechanically sensitive, discharging in synchrony with the muscle twitch. On average, rapidly conducting group III afferents responded for the 5-min duration of 1-Hz repetitive-twitch contraction, whereas slowly conducting group III afferents responded only for the first 2 min of contraction. We conclude that rapidly conducting group III afferents, which are mechanically sensitive, are primarily responsible for evoking the reflex depressor response to repetitive-twitch contractions in anesthetized rabbits.


2015 ◽  
Vol 113 (10) ◽  
pp. 3961-3966 ◽  
Author(s):  
Audrey J. Stone ◽  
Steven W. Copp ◽  
Jennifer L. McCord ◽  
Marc P. Kaufman

Previous evidence has shown that ligating the femoral artery for 72 h resulted in an exaggerated exercise pressor reflex. To provide electrophysiological evidence for this finding, we examined in decerebrated rats whose femoral arteries were either freely perfused or ligated for 72 h the responses of thin-fiber (i.e., groups III and IV) afferents to static contraction of the hindlimb muscles. We found that contraction increased the combined activity of group III and IV afferents in both freely perfused ( n = 29; baseline: 0.3 ± 0.1 imp/s, contraction: 0.8 ± 0.2 imp/s; P < 0.05) and ligated rats ( n = 28; baseline: 0.4 ± 0.1 imp/s, contraction: 1.4 ± 0.1 imp/s; P < 0.05). Most importantly, the contraction-induced increase in afferent activity was greater in ligated rats than it was in freely perfused rats ( P = 0.005). In addition, the responses of group III afferents to contraction in ligated rats ( n = 15; baseline 0.3 ± 0.1 imp/s, contraction 1.5 ± 0.2 imp/s) were greater ( P = 0.024) than the responses to contraction in freely perfused rats ( n = 18; baseline 0.3 ± 0.1 imp/s, contraction 0.9 ± 0.2 imp/s). Likewise, the responses of group IV afferents to contraction in ligated rats ( n = 13; baseline 0.5 ± 0.1 imp/s, contraction 1.3 ± 0.2 imp/s) were greater ( P = 0.048) than the responses of group IV afferents in freely perfused rats ( n = 11; baseline 0.3 ± 0.1 imp/s, contraction 0.6 ± 0.2 imp/s). We conclude that both group III and IV afferents contribute to the exaggeration of the exercise pressor reflex induced by femoral artery ligation.


1983 ◽  
Vol 55 (1) ◽  
pp. 105-112 ◽  
Author(s):  
M. P. Kaufman ◽  
J. C. Longhurst ◽  
K. J. Rybicki ◽  
J. H. Wallach ◽  
J. H. Mitchell

Static contraction of the hindlimb muscles, induced by electrical stimulation of the ventral roots, reflexly increases arterial blood pressure and heart rate. Although stimulation of groups III and IV muscle afferents is believed to cause these reflex increases, the responses of these afferents to a level of static contraction that increases arterial pressure have not yet been determined. Therefore, in barbiturate-anesthetized cats, afferent impulses arising from endings in the gastrocnemius muscle were recorded from the L7 or S1 dorsal roots, while the cut peripheral end of the L7 ventral root was stimulated. In addition, the effects of capsaicin (100-200 micrograms) and bradykinin (25 micrograms) on the activity of the groups III and IV afferents stimulated by contraction were examined. Contraction of the gastrocnemius muscle to a level equal to or greater than that needed to cause a pressor response stimulated 12 of 19 (63%) group III afferents and 13 of 19 (68%) group IV afferents. However, the discharge patterns of the group III afferents stimulated by contraction were very different from those of the group IV fibers. No relationship was found between those fibers stimulated by contraction and those stimulated by chemicals. Our results suggest that although both groups III and IV muscle afferents contribute to the reflex cardiovascular increases evoked by static exercise, group III fibers were likely to be stimulated by the mechanical effects of muscular contraction, whereas at least some group IV fibers were likely to be stimulated by the metabolic products of muscular contraction.


2005 ◽  
Vol 99 (5) ◽  
pp. 1891-1896 ◽  
Author(s):  
Shawn G. Hayes ◽  
Angela E. Kindig ◽  
Marc P. Kaufman

The exercise pressor reflex is evoked by both mechanical and metabolic stimuli. Tendon stretch does not increase muscle metabolism and therefore is used to investigate the mechanical component of the exercise pressor reflex. An important assumption underlying the use of tendon stretch to study the mechanical component of the exercise pressor reflex is that stretch stimulates the same group III mechanosensitive muscle afferents as does static contraction. We have tested the veracity of this assumption in decerebrated cats by comparing the responses of group III and IV muscle afferents to tendon stretch with those to static contraction. The tension-time indexes as well as the peak tension development for both maneuvers did not significantly differ. We found that static contraction of the triceps surae muscles stimulated 18 of 30 group III afferents and 8 of 11 group IV afferents. Similarly, tendon stretch stimulated 14 of 30 group III afferents and 3 of 11 group IV afferents. However, of the 18 group III afferents that responded to static contraction and the 14 group III afferents that responded to tendon stretch, only 7 responded to both stimuli. On average, the conduction velocities of the 18 group III afferents that responded to static contraction (11.6 ± 1.6 m/s) were significantly slower ( P = 0.03) than those of the 14 group III afferents that responded to tendon stretch (16.7 ± 1.5 m/s). We have concluded that tendon stretch stimulated a different population of group III mechanosensitive muscle afferents than did static contraction. Although there is some overlap between the two populations of group III mechanosensitive afferents, it is not large, comprising less than half of the group III afferents responding to static contraction.


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