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Am J Physiol Heart Circ Physiol 278: H871-H877, 2000;
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Vol. 278, Issue 3, H871-H877, March 2000

Group III muscle afferents evoke reflex depressor responses to repetitive muscle contractions in rabbits

J. M. Legramante1, G. Raimondi1, C. M. Adreani2, S. Sacco1, F. Iellamo1, G. Peruzzi1, and M. P. Kaufman2

1 Dipartimento di Medicina Interna, Cattedra di Fisiopatologia Medica, Universita' di Roma "Tor Vergata," 00173 Rome, Italy; and 2 Division of Cardiovascular Medicine, Departments of Internal Medicine and Human Physiology, University of California, Davis, California 95616


    ABSTRACT
TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES

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.

dynamic exercise; autonomic nervous system; arterial blood pressure; sensory nerves; somatic afferents; breathing


    INTRODUCTION
TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES

TWO NEURAL MECHANISMS are thought to evoke the cardiovascular and respiratory adjustments to muscular activity. The first is central command, a feedforward mechanism characterized by the parallel activation of central neural circuits controlling locomotion and autonomic discharge (9, 16). The second mechanism is a reflex arising from the exercising muscles (2, 7). The afferent arm of the reflex is composed of thinly myelinated group III and unmyelinated group IV fibers (19, 27, 28). Static (i.e., tetanic) contraction of skeletal muscle is well known to increase reflexively arterial pressure, heart rate, and ventilation, i.e., exercise pressor reflex (20, 21), in anesthetized animals (5, 6, 12, 25, 26).

Nevertheless, the pattern of reflex cardiovascular and respiratory responses to dynamic muscular contraction is less clear. In anesthetized cats, repetitive-twitch contraction of hindlimb muscles decreased arterial pressure in about one-half of the preparations tested; the section of the dorsal roots innervating the contracting muscles had no effect on this depressor response (12, 15). This effect, therefore, was attributed to metabolic vasodilation and not to a neural mechanism (15). On the other hand, in anesthetized rabbits (25) and dogs (4, 26), the depressor responses and the hyperventilation evoked by repetitive-twitch contractions of hindlimb muscles were reflex in origin because they were abolished by cutting either the dorsal roots (4) or the peripheral nerves (25, 26).

This reflex depressor response appears to be particularly strong in anesthetized rabbits. The discharge properties of the sensory nerves responsible for evoking these contraction-induced depressor reflexes have not been identified unequivocally. However, electrical stimulation of rapidly conducting group III muscle afferents (i.e., low-threshold group III afferents) decreased arterial pressure (13, 17), whereas electrical stimulation of slowly conducting group III (i.e., high-threshold group III afferents) and group IV muscle afferents consistently increased arterial pressure (10, 13). Direct electrical stimulation of the gastrocnemius nerves at low frequency and at low intensity produced a "depressor" and a hyperventilatory response pattern in anesthetized rabbits (23), which was similar to that induced by repetitive-twitch contractions of the triceps surae muscles (25, 26).

Therefore, the main goal of our study was to test the hypothesis that rapidly conducting group III muscle afferents were stimulated by repetitive-twitch contraction of the triceps surae muscles in anesthetized rabbits. Moreover, because preliminary data from our laboratory suggested that the reflex drive arising from repetitive-twitch contractions is operative not only at the onset but also during the steady state (3), a second aim of our study was to evaluate both the impulse activity of group III and IV muscle afferents as well as the cardiorespiratory responses to prolonged (steady-state phase) repetitive-twitch contraction of the triceps surae muscles.


    METHODS
TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES

General. Thirty-three adult rabbits of both sexes, weighing between 2.5 and 3.5 kg, were initially anesthetized by pentobarbital sodium (35 mg/kg iv) via a cannula placed in the marginal vein of the ear. A stable level of anesthesia was maintained by supplemental doses (10-20 mg/kg) every 60 min. The trachea, a common carotid artery, and an external jugular vein were cannulated. The left hindlimb was fixed in place by clamps, and the triceps surae muscles, calcaneal tendon, tibial nerve, and sciatic nerve were exposed. The tendon was severed from the calcaneal bone. The left triceps surae muscles were isolated from surrounding tissue so that the receptive fields of group III and IV afferents could be accurately located. The left femoral, peroneal, sural, and gluteal nerves as well the muscular branch of the sciatic nerve were cut.

In 13 rabbits, a lumbosacral laminectomy was performed to expose the dorsal roots from L5 to the cauda equina, whereas in 8 rabbits the sciatic nerve was isolated up to its entrance into the ischiopubic region. The skin overlying the exposed spinal roots, the sciatic, and the tibial nerves was tied to curved stainless steel bars to form a pool, which was filled with warm (37°C) mineral oil. The temperature in the pool was controlled and maintained in the range of 37-38°C by means of a heat lamp.

Measurements. Arterial blood pressure was measured by connecting the carotid arterial cannula to a pressure transducer (Gould P23 XL). Heart rate (HR) was calculated beat-to-beat on-line by a tachograph (Gould), which was triggered by the pressure pulse or by the electrocardiogram. Respiratory airflow was recorded by a pneumotachograph (Gould Fleisch n° 000) connected to the tracheal cannula and to a differential pressure transducer (Valydine DP45). The airflow signal was integrated (Gould) to give tidal volume and minute volume of ventilation. Breathing frequency was calculated from the interbreath period.

Arterial blood O2 and CO2 partial pressure (PaO2 and PaCO2) and arterial pH (pHa) concentrations were determined at 37°C using a blood gas analyzer (Radiometer ABL 3); the results were corrected for temperature. PaCO2, PaO2, and pHa were measured at the beginning of each experiment and maintained within the following ranges: PaCO2 28-36 Torr; PaO2 >90 Torr; pHa 7.35-7.40. When necessary, PaO2 was increased by enriching the inhaled air with O2, and pHa was corrected by infusing a 10 meq/ml solution of sodium bicarbonate.

The tension (in g) developed by the contracting triceps surae muscles was measured from the severed calcaneal tendon, which was attached to a force transducer (model FT-10, Grass Instruments).

Repetitive-twitch contractions. Repetitive contractions of the triceps surae muscles were induced by stimulating (1 Hz, 0.025 ms) the tibial nerve for 5 min with a hook electrode connected via a Grass Stimulus Isolation Unit (PSIU-6) to a Grass Stimulator (model S-88). The intensity of stimulation was expressed in multiples of the threshold (×T) for the first signs of twitch contraction (activation of the alpha -motoneurons). Stimulus strengths of 2.0-2.5 times threshold were used. To assure that the cardiorespiratory responses to prolonged (i.e., 5 min) repetitive-twitch muscular contractions were reflex in origin and caused by stimulation of receptors located in the triceps surae muscles, the central and the peripheral ends of the cut tibial nerve were also stimulated (5-min duration), and the possible cardiorespiratory changes were evaluated.

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 severed left L7 or S1 dorsal roots or from the cut peripheral sciatic nerve. The neural signals were passed through a high-impedence 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 distance between the recording electrode on the dorsal root or on the sciatic nerve 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 (20, 21). Even though the definition of rapidly and slowly conducting group III afferents is not precise, Coote and Perez-Gonzalez (7) considered as "rapid" the group III afferents conducting impulses between 17 and 30 m/s and as "slow" those conducting impulses >= 2.5 and <= 17 m/s. The receptive fields of 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 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 velocity and their response to stretch and twitch contraction and were discarded because their stimulation does not evoke reflex cardiovascular and respiratory effects (18, 28).

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 the afferent to 5 min of repetitive-twitch contractions of the triceps surae muscles was recorded (Fig. 1). Although the parameters used to stimulate the tibial nerve in our study (1 Hz, 0.025 ms, 2.0-2.5 times threshold for motor fibers) are not enough to electrically activate group III and IV afferents in cats (8, 11) and dogs (22, 24), there is no electrophysiological study that directly addresses the threshold for the electrical activation of afferents during tibial nerve stimulation in rabbits. We, therefore, recorded the responses of five group III afferents to the stimulation of the tibial nerve with the same intensities used during the twitch-contraction protocol described above while the rabbits were paralyzed (triethiodide gallamine, 3-5 mg/kg iv) and artificially ventilated (Harvard).


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  		Fig. 1.   Stimulation of a group III muscle afferent (conduction velocity = 10 m/s) by prolonged repetitive-twitch contractions of triceps surae muscles at a frequency of 1 Hz. Note that firing of fiber, when it occurred, is generally synchronized to muscle twitch. ABP, arterial blood pressure.

Data analysis. The discharge of each afferent was counted and placed in 1-min bins for the 1-min period immediately preceeding the muscular contractions, for the 5-min period of repetitive-twitch contractions, and for the first 1-min of recovery. A previously silent afferent was considered to be contraction sensitive if it discharged at least 10 impulses during the first 120 s of the repetitive-twitch contraction period. In units having a background discharge, an increase by at least 100% in the first 120 s of rhythmic contractions was accepted as a response.

All circulatory and respiratory measurements were recorded on a Hewlett-Packard eight-channel magnetic tape recorder (3968A) and on a Gould eight-channel polygraph (TA4000). The values of the investigated parameters were calculated by means of a computerized on-line system for biological data acquisition. All values reported represent means ± SE.

An ANOVA followed by Newman-Keuls post hoc analysis was used to determine the statistical significance of differences between the impulse activity of the muscle afferents during control and during each minute of the repetitive-twitch contraction periods. The statistical significance of differences between the impulse activity of rapidly conducting and slowly conducting group III muscle afferents in response to repetitive-twitch contractions was assessed by a t-test. The statistical significance of the cardiovascular and respiratory responses to each minute of repetitive-twitch contractions of the triceps surae muscles was evaluated by ANOVA or by a Friedman repeated-measures ANOVA on ranks when the data were or were not, respectively, normally distributed. Pairwise multiple-comparison procedures were performed by Student-Newman-Keuls methods. P values <0.05 were considered statistically significant.


    RESULTS
TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES

Effects of repetitive-twitch contractions on impulse activity of group III and IV muscle afferents. We examined in 21 rabbits the effect of prolonged (5-min duration) repetitive-twitch contractions of the triceps surae muscles on the impulse activity of 20 group III afferents (conduction velocity 13.3 ± 1.8 m/s; range 2.7-29.1 m/s) and 10 group IV afferents (conduction velocity 1.18 ± 0.1 m/s; range 0.7-2.2 m/s). The endings of each of the 30 group III and IV afferents were located in the triceps surae muscles. Eighteen of twenty (90%) group III muscle afferents responded to nonnoxious probing of the triceps surae muscles. Fourteen of twenty (70%) group III muscle afferents responded to stretching of the calcaneal tendon. Eight of ten (80%) group IV muscle afferents responded to noxious, but not to nonnoxious, probing of the muscle. None of the 10 group IV muscle afferents responded to tendon stretch. Repetitive-twitch contractions of these muscles stimulated 13 (65%) of 20 group III afferents and none of the 10 group IV afferents. Peak tension, generated by the contracting triceps surae muscles, averaged 442 ± 34.7 g in the first minute and 318 ± 13.4 g in the last minute of contraction for the 30 afferents tested.

In control experiments, we examined the responses of five group III afferents to tibial-nerve stimulation both before and while the rabbits were paralyzed with gallamine. Before paralysis, tibial nerve stimulation (1 Hz), which caused the triceps surae muscles to twitch repetitively, activated each of the five group III afferents. In contrast, during paralysis tibial nerve stimulation (1 Hz) at the same current intensities and pulse durations as those used before paralysis did not affect the discharge of the five group III afferents.

The impulse activity of the group III afferents considered as a whole (i.e., n = 20) significantly increased in the first minute of repetitive-twitch contraction and was significantly higher, compared with the control condition, during each minute of the 5-min period of repetitive-twitch contractions (Fig. 2). Once firing started, 10 (6 rapidly and 4 slowly conducting) of the 13 group III afferents stimulated by twitch contractions maintained their increased discharge throughout the duration (5 min) of the contraction period. The remaining three group III afferents (2 slowly and 1 rapidly conducting) fired during the first 2 min of contraction and then stopped firing in the third minute of this maneuver. A most impressive feature of the discharge pattern of the group III afferents stimulated by repetitive contractions (11 of 13 afferents) was that their firing, when it occurred, was synchronized to the muscle twitch (Fig. 1).


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  		Fig. 2.   Summary data (means ± SE) for time course of effects of prolonged repetitive-twitch contractions of triceps surae muscle on activity of group III (n = 20) and group IV (n = 10) muscle afferents. *P < 0.05 vs. rest.

As suggested previously by Coote and Perez-Gonzalez (7), we divided the group III afferents into two subgroups: rapidly (conduction velocity: 17-30 m/s) and slowly (conduction velocity: 2.5 to <17 m/s) conducting. Six of twelve slowly conducting (50%) and seven of eight rapidly conducting (87%) group III afferents were stimulated by repetitive-twitch contraction of triceps surae muscles. When averaged over the 5-min period of twitch contraction, the responses of the rapidly conducting afferents were significantly greater (P < 0.05) than those of the slowly conducting group III afferents (Fig. 3). Furthermore, the rapidly conducting afferents showed a significant increase in impulse activity along the whole period of twitch contractions, whereas the slowly conducting afferents increased significantly their impulse activity only during the first minute of repetitive-twitch contractions of the triceps surae muscles.


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  		Fig. 3.   Histograms showing averaged responses of rapidly (n = 8) and slowly (n = 12) conducting group III muscle afferents to prolonged (5 min) repetitive-twitch contractions of triceps surae muscle. Note that the increase in firing activity of rapidly conducting is significantly (P < 0.05) greater compared with the increase in firing activity of slowly conducting muscle afferents. Values are means ± SE. *P < 0.05 vs. rest.

Cardiovascular and respiratory responses to repetitive-twitch contractions of gastrocnemius muscles. Repetitive-twitch contractions of the triceps surae muscles of 12 anesthetized rabbits significantly decreased arterial pressure and significantly increased both pulmonary ventilation and breathing frequency. Contraction had no effect on either heart rate or tidal volume. Tension, generated by the contracting muscles, averaged 420 ± 33.1 g in the first minute and decreased in the following minutes, averaging 316 ± 13.3 g in the last minute of contraction. The cardiorespiratory responses started immediately (~1-5 s) after the stimulation of the tibial nerve (Fig. 4). The mean arterial pressure changes from control values were consistent in the first minute but tended to be smaller in the other minutes of twitch contraction. Nevertheless, they were significant. On the other hand, the ventilatory responses were similar during each minute of repetitive-twitch contractions (Fig. 4).


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  		Fig. 4.   Time course of cardiovascular and respiratory responses to prolonged repetitive-twitch contractions of intact (IN) (n = 12) and of neurally isolated (NI) (n = 9) triceps surae muscles. Values are means ± SE. MAP, mean arterial pressure; HR, heart rate; BF, breathing frequency; VT, tidal volume; VE, pulmonary ventilation. *P < 0.05 vs. rest.

To confirm the reflex nature of these cardiovascular and respiratory responses to repetitive-twitch contractions, we stimulated the peripheral cut end of the tibial nerve with the same stimulation parameters as those used when the nerve was intact. This was done in 9 of the 12 rabbits studied above. The averaged tension generated was similar to that evoked in the intact protocol, decreasing from 425 ± 35.2 g in the first minute to 310 ± 11.5 g in the last minute of contraction. The prolonged (5-min duration) rhythmic twitch contraction of the neurally isolated triceps surae muscle did not evoke any significant cardiovascular and ventilatory effects (Fig. 4). Likewise, stimulation of the central cut end of the tibial nerve (n = 12) did not evoke any circulatory and ventilatory effects when the stimulus strength remained at 2.0-2.5 ×T.


    DISCUSSION
TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES

The new finding of our study is that 1-Hz repetitive-twitch contraction of the triceps surae muscles in anesthetized rabbits stimulated group III muscle afferents but did not stimulate group IV afferents. This finding is consistent with the hypothesis that in anesthetized rabbits the afferent arm of the reflex arc arising from hindlimb muscles during repetitive-twitch contractions is comprised of group III afferents. The cardiovascular reflex response to repetitive-twitch contractions in rabbits, in contrast with that in cats, is characterized by a decrease in arterial pressure and includes a decrease in vascular resistance in nonactive limbs (25).

Previous studies suggested that group III afferents mediate the depressor response. In these studies (13, 17), the direct electrical stimulation of muscular nerves, likely activating group III afferents, evoked a decrease in arterial pressure.

Our study extends these previous results by directly linking the afferent fiber recording to the cardiovascular responses to muscular contraction, and our data represent the first electrophysiological evidence strongly suggesting that the depressor reflex response to twitch contraction is evoked by the activation of group III afferents.

Even though we cannot completely exclude the possibility that anesthetics could interfere with autonomic nervous system thus possibly altering the reflex cardiovascular responses, two considerations lead us to suggest that anesthesia is not the main determinant for the reflex depressor response to repetitive-twitch contractions observed in our rabbits. First, we (25) have previously reported that the cardiovascular and respiratory responses to muscular contraction in anesthetized rabbits are independent from the anesthetic agents used. Second, Wilson et al. (29) clearly showed that experimentally induced muscular contractions evoked in decerebrated rabbits the same pattern of cardiorespiratory responses previously reported in anesthetized rabbits (25).

Previous studies in anesthetized cats (13, 17) showed that the direct electrical stimulation of rapidly conducting group III fibers reflexly decreased arterial pressure. Recently, in anesthetized rabbits low-frequency electrical stimulation of gastrocnemius nerves with current intensities that only activated rapidly conducting group III muscle afferents evoked a "depressor" and a hyperventilatory response pattern (23) that was similar to that induced by repetitive-twitch contractions of the triceps surae muscles (25, 26). In this study (23), high-frequency electrical stimulation with current intensities that activated slowly conducting group III and group IV muscle afferents evoked a pressor response pattern similar to that previously described in cats (6, 12, 18, 19), in dogs (5, 26), and in rabbits (25, 26).

Group III and IV afferents are believed to display polymodal discharge properties, responding to both chemical and mechanical stimuli (14). Nevertheless, in response to muscular contraction, rapidly conducting group III afferents appear to be stimulated mainly by mechanical stimuli, whereas slowly conducting group III and group IV afferents appear to be stimulated mainly by chemical stimuli (14). The sensitivity to mechanical distortion of receptive fields possessed by group III afferents has been confirmed in our study because they discharged in synchrony with the muscle twitch (Fig. 1). This observation is in line with previous studies in which the activity of group III muscle afferents was evaluated during both repetitive-twitch contractions (15) and dynamic exercise (1).

In an attempt to disentangle the roles played by rapidly conducting and slowly conducting group III muscle afferents in evoking the reflex depressor response to twitch contractions, we evaluated separately their responses to this stimulus. As expected, the responses of the rapidly conducting group III afferents were greater than the responses of the slowly conducting group III afferents. Furthermore, rapidly conducting group III afferents, on average, maintained their response for the duration of the contraction period, whereas slowly conducting group III afferents did not, discharging only during the first two min of the contraction period. These findings raise the possibility that rapidly conducting group III afferents are mainly responsible for evoking the reflex depressor response to repetitive-twitch contractions.

We also evaluated the role played by the muscle reflex in evoking the cardiovascular and respiratory responses to prolonged (i.e., 5 min) repetitive-twitch contractions in anesthetized rabbits. Although the reflex origin of the cardiorespiratory responses to repetitive-twitch contraction of the triceps surae muscles has been established at the onset of muscle activity (15, 25, 26), it is not clear whether this reflex arising from contracting muscle is operative during the steady-state phase of the prolonged (i.e., 5 min) twitch contraction period. Preliminary results from our laboratory (3) seemed to suggest that the cardiovascular and respiratory responses observed during 120 s of repetitive-twitch contraction were reflex in origin. However, the time course of this reflex was not clearly addressed. The present study showed that the reflex arising from muscles is operative not only at the onset but also during the whole duration of prolonged repetitive-twitch contractions in anesthetized rabbits.

Repetitive-twitch contraction had no effect on heart rate in our study, whereas this stimulus decreased heart rate in the studies of Tallarida et al. (25, 26). Although at first glance our findings appear to contrast with those reported by Tallarida et al. (25, 26), two important differences may explain this apparent conflict. First, we twitch contracted the triceps surae muscles only once per second, whereas Tallarida et al. (25, 26) twitch contracted this muscle group three times per second. Thus the stimulus to decrease heart rate may have been less in our study than it was in the studies by Tallarida et al. (25, 26). Second, the vagus, aortic and carotid sinus nerves were intact in our study, whereas these nerves were cut bilaterally in the studies by Tallarida et al. (25). Thus the baroreflex could have countered the bradycardic response to twitch contraction in our study, but it could not have in the studies of Tallarida et al. (25).

In conclusion, our study shows for the first time that repetitive-twitch contractions are characterized by the activation of group III afferents in anesthetized rabbits. Within this population of thinly myelinated fibers, rapidly conducting group III afferents, which display mechanical sensitivity, appeared to be mainly responsible for evoking this reflex effect. This represents, to our knowledge, the first experimental evidence that mechanically sensitive muscle afferents play a major role in the afferent arm of the reflex arc arising from contracting muscles during repetitive-twitch contractions. Finally, our data show that the cardiovascular and respiratory reflex responses to repetitive-twitch contractions were operative not only at the onset but also during the steady-state phase of muscle activity.


    ACKNOWLEDGEMENTS

We thank Marco Pallante and Alessandro Massimi for technical assistance, Nicholas Moya Del Pino for surgical assistance, and Penny Jones for typing the manuscript.


    FOOTNOTES

This study was supported by Consiglio Nazionale delle Ricerche Grants AI95.00266.04, AI96.00222.04, and AI97.00175.04 (to J. M. Legramante) and by National Heart, Lung, and Blood Institute Grant HL-30710 (to M. P. Kaufman).

Preliminary data were submitted to Experimental Biology '99.

The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. §1734 solely to indicate this fact.

Address for reprint requests and other correspondence: J. M. Legramante, Dipartimento Medicina Interna, Universita' di Roma "Tor Vergata", Via O. Raimondo, snc 00173, Rome, Italy (E-mail: Legramante{at}med.uniroma2.it).

Received 19 January 1999; accepted in final form 7 October 1999.


    REFERENCES
TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES

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Am J Physiol Heart Circ Physiol 278(3):H871-H877
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