Responses of group III and IV muscle afferents to distension of the peripheral vascular bed

1999 ◽  
Vol 87 (2) ◽  
pp. 545-553 ◽  
Author(s):  
Philippe Haouzi ◽  
Janeen M. Hill ◽  
Brock K. Lewis ◽  
Marc P. Kaufman
Keyword(s):  
Receptive Fields ◽  
Venous Drainage ◽  
Muscle Afferents ◽  
Group Iv ◽  
Triceps Surae ◽  
Peripheral Vascular ◽  
Group Iii ◽  
Triceps Surae Muscles ◽  
Muscular Pump ◽  
Pressure Changes

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.

scholarly journals Responses of group III and IV muscle afferents to dynamic exercise

1997 ◽  
Vol 82 (6) ◽  
pp. 1811-1817 ◽  
Author(s):  
Christine M. Adreani ◽  
Janeen M. Hill ◽  
Marc P. Kaufman
Keyword(s):  
Receptive Fields ◽  
Muscle Afferents ◽  
Group Iv ◽  
Dynamic Exercise ◽  
Triceps Surae ◽  
Group Iii ◽  
Low Levels ◽  
Triceps Surae Muscles ◽  
Decerebrate Cats ◽  
Stimulation Of

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.

scholarly journals Cyclooxygenase blockade attenuates responses of group III and IV muscle afferents to dynamic exercise in cats

2006 ◽  
Vol 290 (6) ◽  
pp. H2239-H2246 ◽  
Author(s):  
Shawn G. Hayes ◽  
Angela E. Kindig ◽  
Marc P. Kaufman
Keyword(s):  
Muscle Afferents ◽  
Group Iv ◽  
Dynamic Exercise ◽  
Triceps Surae ◽  
Afferent Activity ◽  
Mesencephalic Locomotor Region ◽  
Thin Fiber ◽  
Group Iii ◽  
Triceps Surae Muscles ◽  
Stimulation Of

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.

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
Keyword(s):  
Receptive Field ◽  
Receptive Fields ◽  
Muscle Afferents ◽  
Dynamic Exercise ◽  
Triceps Surae ◽  
Step Cycle ◽  
Group Iii ◽  
Afferent Fibers ◽  
Triceps Surae Muscles ◽  
Flexor Digitorum

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)

Effects of contraction and lactic acid on the discharge of group III muscle afferents in cats

1993 ◽  
Vol 69 (4) ◽  
pp. 1053-1059 ◽  
Author(s):  
L. I. Sinoway ◽  
J. M. Hill ◽  
J. G. Pickar ◽  
M. P. Kaufman
Keyword(s):  
Lactic Acid ◽  
Mechanical Stimulation ◽  
Pyruvate Dehydrogenase ◽  
Active Form ◽  
Receptive Fields ◽  
Muscle Afferents ◽  
Triceps Surae ◽  
Group Iii ◽  
Static Contraction ◽  
Triceps Surae Muscles

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)

Gadolinium attenuates exercise pressor reflex in cats

2001 ◽  
Vol 280 (5) ◽  
pp. H2153-H2161 ◽  
Author(s):  
Shawn G. Hayes ◽  
Marc P. Kaufman
Keyword(s):  
Pressor Response ◽  
Oxygen Demand ◽  
Muscle Afferents ◽  
Triceps Surae ◽  
Mechanical Stimuli ◽  
Group Iii ◽  
Exercise Pressor Reflex ◽  
Static Contraction ◽  
Pressor Reflex ◽  
Triceps Surae Muscles

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.

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
Keyword(s):  
Pyridoxal Phosphate ◽  
Muscle Afferents ◽  
Group Iv ◽  
Triceps Surae ◽  
Disulfonic Acid ◽  
P2 Receptor ◽  
Thin Fiber ◽  
Group Iii ◽  
Decerebrate Cats ◽  
Stimulation Of

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.

Effects of hypoxia on the discharge of group III and IV muscle afferents in cats

1992 ◽  
Vol 73 (6) ◽  
pp. 2524-2529 ◽  
Author(s):  
J. M. Hill ◽  
J. G. Pickar ◽  
M. D. Parrish ◽  
M. P. Kaufman
Keyword(s):  
Blood Supply ◽  
Discharge Rate ◽  
Pressor Response ◽  
Supply And Demand ◽  
Venous Blood ◽  
Group Iv ◽  
Triceps Surae ◽  
Group Iii ◽  
Triceps Surae Muscles ◽  
Sensitive Group

The reflex pressor response evoked by static muscular contraction is widely believed to be caused by the stimulation of group III and IV afferents. Although the specific nature of the contraction-induced stimulus to these thin-fiber afferents is unknown, they are thought to be stimulated in part by a condition arising from a mismatch between blood supply and demand in the exercising muscle. Hypoxia, a condition found in skeletal muscle during such a mismatch, may stimulate these afferents. We have therefore tested the hypothesis that perfusion of the triceps surae muscles with hypoxic blood stimulates group III and IV afferents in barbiturate-anesthetized cats. We found that 3–3.5 min of hypoxia with the triceps surae muscles at rest significantly (P < 0.05) increased the average discharge rate of contraction-sensitive group IV afferents but had no effect on the average discharge rate of contraction-sensitive group III afferents. Hypoxia had only trivial effects on the discharge of contraction-insensitive group III and IV afferents. Hypoxia stimulated 4 of 11 contraction-sensitive group IV afferents and 2 of 13 contraction-sensitive group III afferents. The responses of the afferents stimulated by hypoxia were small in magnitude. Hypoxia with the muscles at rest appeared to have no effect on either hydrogen or lactate ion concentrations in the femoral venous blood. In addition, hypoxia increased the responses to contraction in only 3 of 22 group III and 4 of 21 group IV afferents tested. We conclude that muscle tissue hypoxia is a minor stimulus to afferents that sense a mismatch between blood supply and demand during static contraction.

Identification of muscle afferents subserving sensation of deep pain in humans

1994 ◽  
Vol 72 (2) ◽  
pp. 883-889 ◽  
Author(s):  
D. A. Simone ◽  
P. Marchettini ◽  
G. Caputi ◽  
J. L. Ochoa
Keyword(s):  
Conduction Velocity ◽  
Receptive Fields ◽  
Extensor Tendon ◽  
Common Peroneal Nerve ◽  
Muscle Afferents ◽  
Group Iv ◽  
High Threshold ◽  
Group Iii ◽  
Muscle Afferent ◽  
Afferent Unit

1. Intraneural microstimulation (INMS) and microneurography were used in combination to stimulate and record from muscle nociceptor primary afferent fibers of the common peroneal nerve of healthy volunteers. When pain evoked by INMS was projected to muscle, afferent activity could be evoked by innocuous and noxious pressure applied within the projected painful area. Conduction velocity of single fibers was determined by stimulating the receptive fields (RFs) electrically via needle electrodes inserted into the RF and measuring conduction latency and distance between the RF and recording electrode. 2. Pain projected to muscle during INMS trains 5–10 s in duration at threshold intensity for pain sensation was typically described as cramping and was well localized. Subjects mapped the area of the painful projected field (PF) over the skin using a pointer. 3. Fourteen slowly adaping mechanoreceptors with RF in muscle and with moderate to high receptor threshold were identified within or near the painful PF. Conduction velocities were in the range of Group III (n = 8) and Group IV (n = 6) fibers. Mean RF areas of Group III and Group IV afferents, determined by applying pressure percutaneously, were 2.71 +/- 1.14 (SE) cm2 and 3.40 +/- 1.08 (SE) cm2, respectively. Only one Group III afferent unit exhibited spontaneous activity (< 1 Hz). 4. One additional high-threshold mechanoreceptor was identified, with its RF located in the extensor tendon at the base of the big toe. This fiber had a conduction velocity of 32 m/s. During INMS, a well-localized sharp pain was projected to the tendon.(ABSTRACT TRUNCATED AT 250 WORDS)

Comparison between the effect of static contraction and tendon stretch on the discharge of group III and IV muscle afferents

2005 ◽  
Vol 99 (5) ◽  
pp. 1891-1896 ◽  
Author(s):  
Shawn G. Hayes ◽  
Angela E. Kindig ◽  
Marc P. Kaufman
Keyword(s):  
Muscle Metabolism ◽  
Muscle Afferents ◽  
Group Iv ◽  
Triceps Surae ◽  
Tension Development ◽  
Group Iii ◽  
Exercise Pressor Reflex ◽  
Mechanical Component ◽  
Static Contraction ◽  
Pressor Reflex

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.

Mechanical sensitivity of group III and IV afferents from posterior articular nerve in normal and inflamed cat knee

1986 ◽  
Vol 55 (4) ◽  
pp. 635-643 ◽  
Author(s):  
P. Grigg ◽  
H. G. Schaible ◽  
R. F. Schmidt
Keyword(s):  
Sciatic Nerve ◽  
Knee Joint ◽  
Conduction Velocity ◽  
Mechanical Stimulation ◽  
Dorsal Root ◽  
Receptive Fields ◽  
Group Iv ◽  
Mechanical Sensitivity ◽  
Group Iii ◽  
Stimulation Of

Recordings were performed from sciatic nerve or dorsal root filaments in 28 cats to study single group III (conduction velocity 2.5-20 m/s) and group IV (conduction velocity less than 2.5 m/s) units supplying the knee joint via the posterior articular nerve (PAN). In seven of these cats the knee joint had been inflamed artificially. Recordings from sciatic nerve filaments revealed responses to local mechanical stimulation of the joint in only 3 of 41 group IV units and in 12 of 18 group III units from the normal joint. In the inflamed joint 14 of 36 group IV units and 24 of 36 group III units were excited with local mechanical stimulation. In recordings from dorsal root filaments (normal joint) 4 of 11 group IV units and 7 of 13 group III units were activated by stimulating the joint locally. In the normal joint four group IV units (recorded from dorsal root filaments) responded only to rotations against the resistance of the tissue, whereas the majority of the fibers did not respond even to forceful movements. Group III units with local mechanosensitivity in the normal joint reacted strongly or weakly to movements in the working range of the joint or only to movements against resistance of the tissue. In the inflamed joint, group IV fibers (recorded in sciatic nerve filaments) with detectable receptive fields responded strongly to gentle movements or only to movements against resistance of tissue. Some did not react to movements. Group III units reacted strongly or weakly to gentle movements or only to movements against resistance of the tissue.(ABSTRACT TRUNCATED AT 250 WORDS)

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