| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
|
|
|
|||||||
|
|||||||||
Dipartimento di Medicina Interna, Cattedra di Fisiopatologia Medica, Università di Roma "Tor Vergata," Rome 00173, Italy
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
ACKNOWLEDGEMENTS
FOOTNOTES
REFERENCES
ABSTRACT 
Raimondi, G., J. M. Legramante, F. Iellamo, G. Frisardi, S. Cassarino, and G. Peruzzi. Noxious stimuli do not determine reflex
cardiorespiratory effects in anesthetized rabbits. J. Appl. Physiol. 81(6): 2421-2427, 1996.
The
main purpose of this study is to examine whether the stimulation of an
exclusively pain-sensing receptive field (dental pulp) could determine
cardiorespiratory effects in animals in which the cortical integration
of the peripheral information is abolished by deep anesthesia. In 15 anesthetized (
-chloralose and urethan) rabbits, low (3-Hz)- and
high-frequency (100-Hz) electrical dental pulp stimulation was
performed. Because this stimulation caused dynamic and static reflex
contractions of the digastric muscles leading to jaw opening
[jaw-opening reflex (JOR); an indirect sign of algoceptive fiber
activation], experimentally induced direct dynamic and static
contractions of the digastric muscle were also performed. The low- and
high-frequency stimulation of the dental pulp determined cardiovascular
[systolic arterial pressure (SAP): 
21.7 ± 4.6 and 10.8 ± 4.7 mmHg, respectively] and
respiratory [pulmonary ventilation
(
E): 145.1 ± 44.9 and 109.3 ± 28.4 ml /min, respectively] reflex
responses similar to those observed during experimentally induced
dynamic (SAP: 17.5 ± 4.2 mmHg;
E: 228.0 ± 58.5 ml /min) and static (SAP: 5.8 ± 1.5 mmHg;
E: 148.0 ± 75.3 ml /min) muscular contractions. The elimination of
digastric muscular contraction (JOR) obtained by muscular paralysis did
away with the cardiovascular changes induced by dental pulp
stimulation, the effectiveness of which in stimulating dental pulp
receptors has been shown by recording trigeminal-evoked potentials in
six additional rabbits. The main conclusion was that, in
deeply anesthetized animals, an algesic stimulus is unable to determine
cardiorespiratory effects, which appear to be exclusively linked to the
stimulation of ergoreceptors induced by muscular contraction.
pseudoaffective reflexes; cardiorespiratory reflexes; nociception; muscular reflex drive
INTRODUCTION GROUP III AND IV somatic afferent fibers can be excited
in muscle tissue by both nonnoxious and noxious stimuli (10). The distinction between sensory modalities transduced by these group III
and IV afferents is arbitrary because both groups respond to a variety
of chemical and mechanical stimuli. In fact, activation of group III
and IV somatic afferent fibers produces cardiovascular and respiratory
reflex responses that have been ascribed to
1) a receptive function of
mechanochemical modifications taking place in the tissue during
muscular work (ergoceptive function) (5, 7, 18, 26) and /or
2) a nociceptive function signaling noxious events (15, 16, 19).
Our previous studies in anesthetized animals have suggested the
presence of two different types of muscular chemoreceptors (probably
free endings of contraction-responding afferent fibers of group III and
IV) sensitive to various chemical substances (products of muscular
contraction such as kinins, weak acids, and so on) and to
hyperosmolarity (21, 23). Furthermore, we have shown that these
chemically sensitive receptors contribute, together with mechanically
sensitive receptors, to reflexly modulate the cardiocirculatory and
respiratory centers, thereby activating circulatory and respiratory
functions in response to muscular contraction (22, 24, 25).
However, the role played by high-threshold muscular units, which
respond to noxious stimuli, during muscular contraction has not been
yet defined. In fact, the physiological meaning of the cardiovascular
responses mediated by the "muscular reflex drive" reported by
Kaufman et al. (5) has been questioned by Weissman et al. (28),
suggesting that these responses could have resulted from stimulation of
pain afferents normally not activated during muscular exercise.
The purpose of the present study was to verify our hypothesis that the
stimulation of nociceptive afferents could determine cardiorespiratory
reflex responses in animals in which any cortical integration of the
peripheral information and thus the conscious perception of pain are
avoided by deep anesthesia.
Accordingly, we have evaluated in anesthetized rabbits the
cardiorespiratory responses to electrical stimulation of a
pain-sensitive field, the dental pulp, which is mainly served by
sensitive fibers having almost exclusively a nocialgoceptive function
(1, 6, 9, 14).
MATERIALS AND METHODS Experiments were carried out on 21 rabbits of both sexes (2.5-3.5
kg). Animals were anesthetized initially with intravenous The trachea was intubated with a polyethylene cannula. Rectal
temperature was continuously monitored by a thermocouple
(Hewlett-Packard 210558A, Palo Alto, CA) and maintained at 38 ± 0.5°C by means of a steel hot plate on the operating table and by
use of infrared lamps.
To obtain anaerobic arterial blood samples (0.25 ml), a perforable
bypass consisting of two polyethylene cannulas connected by a silicone
rubber tube was inserted into the femoral artery. Heparin was given
intravenously (10 mg/ kg, with supplementary hourly doses of 2 mg/ kg) to prevent blood clotting.
Measurements
-chloralose (50 mg/ kg) and urethan (500 mg/ kg) and
maintained with supplementary doses of -chloralose (10 mg/ kg)
and urethan (100 mg/ kg) every 50-60 min.
The respiratory airflow was recorded by a pneumotachograph
(Gould-Fleisch 000) connected to the tracheal cannula and to a differential gas pressure transducer (Validyne DP45). The airflow signal was integrated with a Gould integrator amplifer to give tidal
volume (VT) and pulmonary
ventilation
(E).
Breathing frequency was calculated from the interbreath periods.
CO2 in expired air was monitored
with a rapid CO2 analyzer
(Gould-Godart Capnograph Mark III) by continuous sampling from the
tracheal tube. End-tidal PCO2
(PETCO2) was
determined from the CO2
concentration tracing corrected for water vapor and barometric
pressure.
Arterial blood PO2 and PCO2 (PaO2 and PaCO2, respectively) and arterial pH (pHa) concentrations were determined at 37°C by using a blood-gas analyzer (Radiometer ABL 330); 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; and pHa, 7.35-7.40. When necessary, PaO2 was increased by enriching the inhaled air with O2 supply, and pHa was corrected by infusing a 10 meq/ml solution of sodium bicarbonate.
Trigeminal-evoked potentials due to the electrical stimulation of the dental pulp were also recorded. The electrical pulse used was a square wave with a duration of 0.5 ms, a frequency of 1 Hz, and intensities ranging from 4.0 to 20 mA (mean 11.7 ± 3.1 mA). The recording electrodes were placed on the skull both in cephalic (Cz-Fz) and extracephalic (Cz-C7) manner according to the type of recorded wave and to reduce the artifact amplitude, thus optimizing the recording. In fact, our purpose was to record waves characterized by short latencies, which are considered to be markers of activation of both mono- and disynaptic-sensitive trigeminal nuclei. For this reason, the extracephalic recording reducing the artifact amplitude sometimes allowed us a better recording.
The recording device (Phasis, Ote-Biomedica, Firenze, Italy) was set to an amplitude sensitivity of 10-50 µV, and a filter bandwidth of 200-1 kHz was used.
Electrical stimulation of tooth pulp. A section at full thickness to the alveolar growth was made in the inferior incisors. Two metal pivots (parapost studs, Wholedent) were inserted into the dental pulp, isolated with suitable cement (Ketacement, ESPE, Germany), and connected to the electrostimulating unit with automatic control of the resistance and regulation of outgoing current (Phasis, Ote-Biomedica). The stimulation of dental pulp caused a delayed (6- to 12-ms) reflex contraction of the digastric muscle (6), i.e., the jaw-opening reflex (JOR), widely considered as a marker of nociceptive stimulation in experimental animal models (3, 4, 6, 11, 12). The JOR has been demonstrated by electromyographic (Phasis, Ote-Biomedica) responses recorded from the anterior belly of the digastric muscle by means of two unipolar electrodes inserted in that muscle. The electrical pulse used was a square wave with a duration of 0.5 ms and frequencies of 3 and 100 Hz. The dental pulp was stimulated with intensities ranging from 3.6 to 24 mA (mean 12.1 ± 2.9 mA) and from 3.6 to 21 mA (mean 11.3 ± 2.6 mA) for 3 and 100 Hz, respectively. These intensities represented twofold the threshold for the JOR, and the stimulations lasted 30 s. Simulated muscular contractions. Dynamic and static contractions of the digastric muscle were obtained by means of direct electrical stimulation. Digastric muscle was carefully isolated and, by means of unipolar electrodes inserted in its anterior belly, was electrically stimulated by using an isolated stimulator (Grass 88-S) with square-wave pulses of 0.5-ms duration and at a stimulation frequency of 3 Hz (dynamic contractions) and of 100 Hz (static contractions) for periods of 30 s. The anterior belly of the digastric muscle was cut, and the tendon was connected to a force transducer (Grass F10). The intensity of stimulation was such that it matched the tension measured during the JOR after the dental pulp stimulation.Experimental Protocol
After the surgical procedures, the anesthetized rabbits were allowed to stabilize for 20-30 min before the experiments began. Then we evaluated, in 15 rabbits, the cardiorespiratory responses to 1) electrical stimulation of the tooth pulp and 2) muscular contractions of digastric muscle.After these stimulations, the animals were paralyzed (triethiodide gallamine, 3-5 mg/ kg iv) and artificially ventilated with an automatic, electronically controlled ventilator (Palmer model 5255) set to maintain PETCO2 baseline values in the range 35-40 Torr. After muscular paralysis, the tooth pulp was stimulated and cardiovascular parameters were recorded with the same protocol as for the preparalysis. Finally, we again evaluated the cardiovascular responses to the direct electrical stimulation of digastric muscle with intensities able to induce comparable contractions as those induced in the preparalysis state.
In a separate series of experiments (n = 6 rabbits), we have recorded the trigeminal-evoked potentials due to the electrical stimulation of the dental pulp before and after the muscular paralysis to demonstrate that the dental pulp receptors were also effectively stimulated in the paralyzed preparation.
Analysis of Data
The evoked potentials were stored and analyzed by means of dedicated software (Phasis, Ote-Biomedica). The waves detected during the recording of the trigeminal potentials evoked by the dental pulp stimulation were evaluated both in quality (shape) and in a quantity (latency). Each evoked potential was obtained by recording and averaging the waves induced by 2 series of 200 repetitive dental pulp stimulations.All circulatory and respiratory measurements were recorded on a Hewlett-Packard eight-channel magnetic tape recorder (3968A) and on a Gould eight-channel polygraph (TA 4000); the values of the investigated parameters were calculated by means of a computerized on-line system for biological data acquisition set up in our laboratory.
All values measured during the control period (1 min) were averaged to give the mean control value. Data reported from stimulation periods represent the average of all values recorded during 5 s of stimulation beginning ~10 s after the onset of stimulation (maximum changes in cardiovascular and ventilatory parameters). Data are presented as means ± SE both in absolute units and as changes and percent changes from control. The statistical significance of differences between the control and experimental measurements was determined by using a paired t-test. A P value < 0.05 was considered statistically significant.
RESULTS
The cardiorespiratory responses to the electrical stimulation of the
tooth pulp at 3 Hz were characterized by a significant decrease in AP,
both systolic and diastolic, a small decrease in HR, and a marked
increase in E
and in breathing frequency, with no significant changes in
VT.
PETCO2 levels did not change
significantly (Table 1, Fig.
1A).
|
||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
Electrical stimulation of the dental pulp at 100 Hz evoked a cardiorespiratory response pattern characterized by an increase in AP, both systolic and diastolic, in HR, and by hyperpnea mainly due to an increase in VT. PETCO2 did not show significant changes from the resting values (Table 1, Fig. 1B).
Because the stimulation of tooth pulp at 3 and 100 Hz caused, respectively, dynamic and static contractions of the digastric muscle (JOR), we induced in the same animals direct dynamic (3-Hz) and static (100-Hz) contractions of the digastric muscle. These direct muscle contractions, which induced muscular tensions similar to those evoked by tooth pulp stimulations, provoked cardiorespiratory responses similar to those obtained during 3- and 100-Hz dental pulp electrical stimulation, respectively (Table 2, Fig. 2).
|
||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
E, pulmonary
ventilation. Significantly different from control value:
* P < 0.05;
** P <0.01.
In paralyzed and artificially ventilated animals, the cardiocirculatory
responses to both 3- and 100-Hz stimulation of the tooth pulp were
completely prevented. However, dynamic or static contractions of the
digastric muscle directly induced by stimulation of the muscular masses
evoked cardiocirculatory responses similar to those obtained in the
nonparalyzed state (Fig. 3).
The trigeminal potentials evoked by the dental pulp stimulation
produced three different waves that were the more repetitive both in
the same and among the different animals. They have been identified,
according to the time latency, as 1)
W4 (3-5 ms), 2) W6 (6-8
ms), and 3) UW10 (10 ms). These
trigeminal-evoked potentials did not show significant differences, both
in terms of shape (Fig. 4) and in terms of
latencies (Table 3), when recorded before and after the muscular paralysis.
|
||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
DISCUSSION
In deeply anesthetized rabbits, we have investigated whether the stimulation of specific nociceptive afferents could determine reflex cardiocirculatory and respiratory responses. For this purpose, we evaluated the cardiorespiratory responses to the electrical stimulation of an exclusively nociceptive receptive field, namely, the dental pulp. This area has been generally regarded as a trigeminal sensor with pain-related functions (14), and tooth afferent fibers are considered to provide almost exclusively nociceptive information (1). Although we did not record the activity of afferent nociceptive fibers, the experimental evidence of the start of noxious impulses from the dental pulp has been provided by the JOR, i.e., a digastric muscle reflex contraction, which is widely considered as a marker for nociceptive trigeminal stimulation in animal models (3, 4, 6, 11, 12).
Our results suggest that the stimulation of afferent fibers promoting mainly a nociceptive function (tooth pulp fibers) is not able to cause cardiorespiratory responses in deeply anesthetized animals. In fact, low- and high-frequency tooth pulp stimulation evoked cardiorespiratory responses only when it was associated with muscular contractions of the digastric muscle (JOR). In contrast, when the animals were paralyzed and artificially ventilated to avoid the reflex muscular contractions, dental pulp stimulations were no longer able to induce cardiovascular changes. On the contrary, direct stimulation of the digastric muscle in these paralyzed animals led to cardiovascular effects similar to those observed during both the electrical stimulation of the dental pulp and the experimentally induced dynamic and static muscular exercise of the digastric muscle (Fig. 2) in the preparalysis state.
The effectiveness of the stimulation in activating the dental pulp receptors has been demonstrated by recording the trigeminal-evoked potentials when the JOR had been avoided by the muscular paralysis. The latencies of the more repetitive waves were 3-5 ms for W4 waves and 6-8 ms for W6 waves. Probably, W4 waves were the expression of the activation of the first relays in the caudatus or oralis nuclei, whereas W6 waves represented the activation of the main trigeminal nucleus in response to the dental pulp stimulation. Moreover, in some experiments, we also recorded a wave characterized by a longer latency (~10 ms) that we named "unknown wave" (UW10). Both the UW10 onset latency and its presence also after muscular paralysis allow us to hypothesize that it represents the activation of the digastric motor nuclei due to the JOR.
The similarity of the patterns of the trigeminal-evoked potentials recorded in the preparalysis state and after the muscular paralysis, both in terms of shape (Fig. 4) and in terms of time latency (Table 3), allows us to consider that the dental pulp receptors were also effectively stimulated in the paralyzed preparation.
In addition, the analysis of ventilatory responses to our stimulations
offers some further insights for substantiating our conclusions. In
fact, in our rabbits, in which the conscious perception of pain was
prevented by anesthesia, the ventilatory response patterns during the
electrical stimulation of the dental pulp and of the digastric muscle
were always characterized by an isocapnic hyperpnea, i.e., by the
constancy of the PETCO2
values in spite of the increase in
E (Fig. 2),
which is a peculiar feature of the cardiorespiratory adjustments to
mild-intensity muscular activity (17, 27). On the other hand, the
findings of Duranti et al. (2) clearly show that increases in
E
associated with pain sensation are always characterized by a
significant decrease in
PETCO2.
Our data would appear to be in contrast to the classic study of Woodworth and Sherrington (30), which showed that the electrical stimulation of somatic nerves evoked in awake animals systemic hypertension, peripheral vasoconstriction, tachycardia, and hyperventilation, which persisted when the perception of pain was abolished by the decerebration. These authors called these reactions "pseudoaffective reflexes" and suggested that a reflex arc between the somatic afferents and the central nuclei related to circulatory and respiratory control was the neurophysiological pathway of these reactions.
These contrasting findings might be related to the different experimental approach and animal species (cats) used by these investigators. In fact, the decerebration could have modified the autonomic and respiratory reactivities as a consequence of the complete ablation of the upper inhibitory controls. This lack of inhibition might have resulted in an altered balance of the autonomic nervous system in such a way as to increase the excitatory effects. Indirect evidence of this could be drawn by the observation that the decerebrated animals usually respond to stimuli of different types, always with excitatory cardiovascular effects (13, 30).
On the other hand, the anesthesia used in our experiments could have somehow "distorted" the patterns of cardiorespiratory responses to the stimulation of somatic afferents. However, recently Wilson et al. (29) clearly showed that experimentally induced isometric muscular contractions performed in decerebrated rabbits evoke the same pattern of cardiovascular responses (hypertension, tachycardia) observed in previous studies in anesthetized rabbits (22, 24, 25). This weighs against an effect of anesthesia in altering the cardiorespiratory responses to muscular contractions in our study.
The present findings are contingent on the ability of the experimental strategy used in our study to have really activated nociceptor afferents. An amount of evidence clearly shows that tooth pulp is mainly served by sensitive fibers having almost exclusively a nocialgoceptive function (1, 6, 9, 14). Although Sessle (20) raised some doubts on this issue, he clearly stated that "the predominant effects of stimulation confined to the dental pulp are related to dental pain and suprathreshold stimuli evoke responses that are almost exclusively related to nociception" (20). Also, if we cannot completely exclude having activated some afferents belonging to fiber classes generally associated with functions other than pain, such as touch, we do believe that this should have not biased our results.
Also, the reliability of JOR induced by the tooth pulp stimulation as a marker of nociceptive stimulation has been questioned. In fact, it has been reported that this reflex contraction can be elicited by pulpal stimuli at intensities that evoke no overt aversive behavior in anesthetized animals and only the "prepain" sensory experience in humans. The latter is described as a sensation that is variably experienced as "tingling," "cold," and "warm" induced by threshold stimulation of tooth pulp and is probably related to neural mechanisms somewhat involved in nociception (20). Two reasons allow us to really consider the JOR as a marker of nociceptive stimulation in our experiment. First, we used suprathreshold stimulations of the dental pulp. Second, we experienced that when occasionally the anesthesia level decreased, rabbits showed overt aversive behavior in response to dental pulp stimulation, cleary indicating a sensation of pain (data not used).
In conclusion, our findings do not support our initial hypothesis that stimulation of nociceptive afferents could determine cardiorespiratory reflex responses in deeply anesthetized animals in which any cortical integration of the peripheral information and thus the conscious perception of pain are avoided by deep anesthesia and suggest that, in these experimental conditions, the cardiorespiratory reflex responses to muscular exercise are exclusively linked to the activation of chemically and mechanically sensitive muscular afferent fibers ("reflex drive from muscles").
ACKNOWLEDGEMENTS
The authors acknowledge the invaluable advice and encouragement of Dr. G. Tallarida, who died in November 1993. The authors gratefully acknowledge Marco Pallante and Alberto Vespa for technical assistance.
FOOTNOTES
Address for reprint requests: G. Raimondi, Dip. Medicina Interna, Universita' di Roma "Tor Vergata" Via O. Raimondo, snc, 00173 Rome, Italy.
Received 28 December 1995; accepted in final form 19 July 1996.
REFERENCES
| 1. | Anderson, D. J., A. G. Hannam, and B. Matthews. Sensory mechanism in mammalian teeth and their supporting structures. Physiol. Rev. 50: 171-195, 1970. |
| 2. | Duranti, R., T. Pantaleo, F. Bellini, F. Bongianni, and G. Scano. Respiratory responses induced by the activation of somatic nociceptive afferents in humans. J. Appl. Physiol. 71: 2440-2446, 1991. |
| 3. | Fung, D. T., J. C. Hwang, S. H. H. Chan, and Y. S. Chan. Jaw-opening reflex as pain response in rabbit: preliminary report. J. Dent. Res. 55: 917, 1976. |
| 4. | Fung, D. T., J. C. Hwang, S. H. H. Chan, and Y. S. Chan. Further evidence for jaw opening reflex as pain response in rabbit. J. Dent. Res. 56: 441, 1977. |
| 5. | Kaufman, M. P., J. C. Longhurst, K. J. Rybicki, J. H. Wallach, and J. H. Mitchell. Effects of static muscular contraction on impulse activity of groups III and IV afferents in cats. J. Appl. Physiol. 55: 105-112, 1983. |
| 6. |
Keller, O.,
L. Vyklicky,
and
E. Sykova.
Reflexes from A and A trigeminal afferents.
Brain Res.
37:
330-332,
1972.
|
| 7. | Kniffki, K. D., S. Mense, and R. F. Schimdt. Muscle receptors with fine afferent fibers which may evoke circulatory reflexes. Circ. Res. 48, Suppl. 1: S1-S25, 1981. |
| 8. | Matthews, B. Mastication. In: Applied Physiology of the Mouth, edited by C. L. B. Lavelle. Bristol, UK: Wright, 1975, p. 109-242. |
| 9. | Matthews, B., and B. N. Searle. Electrical stimulation of teeth. Pain 2: 245-251, 1976. |
| 10. | Mitchell, J. H., and R. F. Schmidt. Cardiovascular reflex control by afferent fibers from skeletal muscle receptors. In: Handbook of Physiology. The Cardiovascular System. Peripheral Circulation and Organ Blood Flow. Bethesda, MD: Am. Physiol. Soc., 1983. sect. 2, vol. III, pt. 2, chapt. 17, p. 623-658. |
| 11. | Mumford, J. M., and D. Bowsher. Pain and protopathic sensibility. A review with particular references to the teeth. Pain 2: 223-243, 1976. |
| 12. | Narhi, M., A. Virtanen, T. Hirvonen, and T. Huopaniemi. Comparison of electrical thresholds of intradental nerves and jaw-opening reflex in the cat. Acta Physiol. Scand. 119: 399-403, 1983. |
| 13. | Ness, T. J., and G. F. Gebhart. Visceral pain: a review of experimental studies. Pain 41: 167-234, 1990. |
| 14. | Nord, S. G. Electrical stimulation of the tooth pulp in the study of pain. Brain Res. Bull. 1: 251-254, 1976. |
| 15. | Paintal, A. S. Functional analysis of group III afferent fibres of mammalian muscle. J. Physiol. Lond. 152: 250-270, 1960. |
| 16. | Perryman, J. H., S. Katz, and L. J. Goldberger. Effects of peripheral nerve stimulation and muscle activation on respiration and blood pressure nociceptive reflex pattern (Abstract). Federation Proc. 19: 301, 1960. |
| 17. | Raimondi, G., J. M. Legramante, F. Iellamo, S. Cassarino, and G. Peruzzi. Cardiorespiratory response patterns to afferent stimulation of muscle nerves in the rabbit. J. Appl. Physiol. 81: 266-273, 1996. |
| 18. | Rotto, D. M., and M. P. Kaufman. Effect of metabolic products of muscular contraction on discharge of group III and IV afferents. J. Appl. Physiol. 64: 2306-2313, 1988. |
| 19. | Sato, A., Y. Sato, and R. F. Schmidt. Changes in heart rate and blood pressure upon injection of algesic agents into skeletal muscle. Pfluegers Arch. 393: 31-36, 1982. |
| 20. | Sessle, B. J. Is the tooth pulp a "pure" source of noxious input? Adv. Pain Res. Ther. 3: 245-259, 1975. |
| 21. | Tallarida, G., F. Baldoni, G. Peruzzi, F. Brindisi, G. Raimondi, and M. Sangiorgi. Cardiovascular and respiratory chemoreflexes from the hindlimb sensory receptors evoked by intraarterial injection of bradykinin and other chemical agents in the rabbit. J. Pharmacol. Exp. Ther. 208: 319-329, 1979. |
| 22. | Tallarida, G., F. Baldoni, G. Peruzzi, G. Raimondi, P. Di Nardo, M. Massaro, G. Visigalli, G. Franconi, and M. Sangiorgi. Cardiorespiratory reflexes from muscles during dynamic and static exercise in the dog. J. Appl. Physiol. 58: 844-852, 1985. |
| 23. | Tallarida, G., F. Baldoni, G. Peruzzi, G. Raimondi, M. Massaro, A. Abate, and M. Sangiorgi. Different patterns of respiratory responses to chemical stimulation of muscle receptors in the rabbit. J. Pharmacol. Exp. Ther. 223: 552-559, 1982. |
| 24. | Tallarida, G., F. Baldoni, G. Peruzzi, G. Raimondi, M. Massaro, and M. Sangiorgi. Cardiovascular and respiratory reflexes from muscles during dynamic and static exercise. J. Appl. Physiol. 50: 784-791, 1981. |
| 25. | Tallarida, G., F. Baldoni, G. Peruzzi, G. Raimondi, P. Di Nardo, M. Massaro, A. Abate, and M. Sangiorgi. Different patterns of respiratory reflexes originating in the exercising muscle. J. Appl. Physiol. 55: 84-91, 1983. |
| 26. | Tibes, U. Reflex inputs to the cardiovascular and respiratory centers from dynamically working canine muscles. Some evidence for involvement of group III or IV nerve fibers. Circ. Res. 41: 332-341, 1977. |
| 27. | Weissman, M. L., P. W. Jones, A. Oren, N. Lamarra, B. J. Whipp, and K. Wasserman. Cardiac output increase and gas exchange at start of exercise. J. Appl. Physiol. 52: 236-244, 1982. |
| 28. | Weissman, M. L., B. J. Whipp, D. J. Huntsman, and K. Wasserman. Role of neural afferents from working limbs in exercise hyperpnea. J. Appl. Physiol. 49: 239-248, 1980. |
| 29. | Wilson, L. B., C. K. Dyke, J. A. Pawelczyk, P. T. Wall, and J. H. Mitchell. Cardiovascular and renal nerve responses to static muscle contraction of decerebrate rabbits. J. Appl. Physiol. 77: 2449-2455, 1994. |
| 30. | Woodworth, R. S., and C. S. Sherrington. A pseudoaffective reflex and its spinal path. J. Physiol. Lond. 31: 234-243, 1904. |
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
| Visit Other APS Journals Online |
