Comprehensive Physiology Wiley Online Library

Reflexes from Respiratory Muscles and Costovertebral Joints

Full Article on Wiley Online Library



Abstract

The sections in this article are:

1 Reflexes from Thoracic Wall
1.1 Spinal Segmental and Intersegmental Effects of Intercostal Muscle Proprioceptors
1.2 Supraspinal Effects of Intercostal Muscle Proprioceptors on Respiratory Control
1.3 Intercostal Muscle Mechanoreceptors Other Than Tendon Organs and Muscle Spindle Endings
1.4 Cutaneous Reflex Effects on Respiratory Activity
1.5 Supraspinal Effects of Costovertebral Joint Mechanoreceptors on Respiratory Control
2 Reflexes from Abdominal Respiratory Muscles
2.1 Spinal Segmental and Intersegmental Effects of Abdominal Respiratory Muscle Proprioceptors
2.2 Supraspinal Effects of Abdominal Muscle Proprioceptors on Respiratory Control
3 Reflexes from Diaphragm
3.1 Spinal Segmental and Intersegmental Effects of Diaphragm Proprioceptors
3.2 Supraspinal Effects of Diaphragm Proprioceptors on Respiratory Control
Figure 1. Figure 1.

Effects of intercostal and abdominal muscle proprioceptor afferents on medullary inspiratory and pneumotaxic center neurons. eE, early expiratory; EIN, external intercostal nerve; DRG, dorsal respiratory group; I, inspiratory; IE, inspiratory‐expiratory; IIN, internal intercostal nerve; LINcb, cutaneous branch of lateral intercostal nerve; LINmb, muscle branch of lateral intercostal nerve; NA, nucleus ambiguus; NRA, nucleus retroambigualis; NTS, nucleus of tractus solitarius; VRG, ventral respiratory group. Dotted line, possible pathway; + and −, change in neuron firing rate after nerve stimulation.

Figure 2. Figure 2.

Effects of intercostal and abdominal muscle proprioceptor afferents on ventral respiratory group E neurons. Abbreviations as in Fig. 1. Dotted line, possible connection between I and E neurons; + and −, change in firing rate after nerve stimulation.

Figure 3. Figure 3.

Phrenic motoneuron response to stimulation of external intercostal nerve afferents. Top: phrenic efferent activity (PA). Bottom: superimposed traces of compound action potentials (CAP) from T6 dorsal root fibers while stimulating (S) T6 external intercostal nerve; recruitment of group I and II afferent fibers is shown. Stimulation of only group I fibers produces inhibition of PA; additional recruitment of group II fibers causes more pronounced inhibition.

From Shannon 97
Figure 4. Figure 4.

Response of dorsal and ventral respiratory group inspiratory (I) neurons and phrenic efferent activity (PA) to stimulation (S) of intercostal and abdominal muscle afferents. NRA, nucleus retroambigualis.

From Shannon and Freeman 99
Figure 5. Figure 5.

Response of expiratory (E) neurons of nucleus retroambigualis (NRA) to stimulation (S) of intercostal and abdominal muscle afferents. A: complete inhibition of phasic E neuron. B: multiple superimposed traces of E neuron during active phase showing transient inhibition. PA, phrenic efferent activity.

From Shannon and Freeman 99
Figure 6. Figure 6.

Response of pneumotaxic center inspiratory (I) neurons to stimulation (S) of intercostal and abdominal muscle afferents. PHR, phrenic efferent activity. Activity of phasic I neurons can be completely terminated (A). Continuously firing I neurons show reduction of inspiratory‐modulated activity (B) without alteration in tonic firing rate of most neurons (C).

From Shannon and Lindsey 101
Figure 7. Figure 7.

Response of pneumotaxic center inspiratory‐expiratory (IE) neurons to stimulation (S) of intercostal and abdominal muscle afferents. PHR, phrenic efferent activity. Top: nerve stimulation during inspiration (left) and expiration (right). Bottom: left record is control cycle and right record is during intercostal nerve stimulation (INS).

From Shannon and Lindsey 101
Figure 8. Figure 8.

Response of pneumotaxic center expiratory (E) neurons to stimulation (S) of intercostal and abdominal muscle afferents. A: tonic firing E neuron relative to phrenic efferent activity (PHR). B and C: two different neurons, left record is control cycle and right record is during intercostal nerve stimulation (INS).

From Shannon and Lindsey 101
Figure 9. Figure 9.

Inhibitory effect of internal intercostal muscle contraction elicited by ventral root stimulation (VRS) on inspiratory (phrenic) activity. Stimulation occurred during ongoing phrenic activity. A: control. B: test (VRS) cycle. (D. C. Bolser, B. G. Lindsey, and R. Shannon, unpublished observations.)

Figure 10. Figure 10.

Reduction in dorsal respiratory group inspiratory (I) neuron and phrenic (PHR) motor activity with vibration of single intercostal space. Vibration applied to rib during ongoing inspiratory activity. (D. C. Bolser, B. G. Lindsey, and R. Shannon, unpublished observations.)

Figure 11. Figure 11.

Effects of rib vibration on respiratory pattern. Vibrator (300 Hz) applied to 7th rib between arrows. Intercostal electromyogram (EMG) was recorded from 6th interspace. BP, blood pressure.

From Remmers 80
Figure 12. Figure 12.

Sample polygraph tracings of 2 animals breathing room air, showing effects of thoracic dorsal rhizotomies on breathing pattern. dV/dt, airflow; Vt, spirogram; BP, arterial blood pressure. Top panel: intact (Int.) after thoracic dorsal roots section (DR) and after secondary vagotomy (DRX). Bottom panel: intact (Int.) after vagotomy (X) and after secondary dorsal root section (XDR). Bars, 1 s each.

From Gautier 54
Figure 13. Figure 13.

One type of response to chest compression in vagotomized dog. End‐tidal CO2 () above records represents average over a few breaths at points denoted. V, volume; V, airflow; BP, arterial blood pressure.

From Shannon 96
Figure 14. Figure 14.

Second type of response to chest compression in vagotomized dogs. A and B are records from 2 dogs. PHR, phrenic efferent activity; V, airflow; BP, blood pressure.

From Shannon 96
Figure 15. Figure 15.

Phrenic efferent activity changes during costovertebral joint movement, on, Joints moved; off, joints returned to resting position; INT PHR, integrated (moving average) phrenic activity; , end‐tidal CO2. A: manual manipulation of neurally isolated costovertebral joints had inhibitory effect on inspiratory activity (phrenic motor discharge) and prolonged expiratory time. B: respiratory rate could be paced by moving joints in synchrony with PHR.

From Shannon 98


Figure 1.

Effects of intercostal and abdominal muscle proprioceptor afferents on medullary inspiratory and pneumotaxic center neurons. eE, early expiratory; EIN, external intercostal nerve; DRG, dorsal respiratory group; I, inspiratory; IE, inspiratory‐expiratory; IIN, internal intercostal nerve; LINcb, cutaneous branch of lateral intercostal nerve; LINmb, muscle branch of lateral intercostal nerve; NA, nucleus ambiguus; NRA, nucleus retroambigualis; NTS, nucleus of tractus solitarius; VRG, ventral respiratory group. Dotted line, possible pathway; + and −, change in neuron firing rate after nerve stimulation.



Figure 2.

Effects of intercostal and abdominal muscle proprioceptor afferents on ventral respiratory group E neurons. Abbreviations as in Fig. 1. Dotted line, possible connection between I and E neurons; + and −, change in firing rate after nerve stimulation.



Figure 3.

Phrenic motoneuron response to stimulation of external intercostal nerve afferents. Top: phrenic efferent activity (PA). Bottom: superimposed traces of compound action potentials (CAP) from T6 dorsal root fibers while stimulating (S) T6 external intercostal nerve; recruitment of group I and II afferent fibers is shown. Stimulation of only group I fibers produces inhibition of PA; additional recruitment of group II fibers causes more pronounced inhibition.

From Shannon 97


Figure 4.

Response of dorsal and ventral respiratory group inspiratory (I) neurons and phrenic efferent activity (PA) to stimulation (S) of intercostal and abdominal muscle afferents. NRA, nucleus retroambigualis.

From Shannon and Freeman 99


Figure 5.

Response of expiratory (E) neurons of nucleus retroambigualis (NRA) to stimulation (S) of intercostal and abdominal muscle afferents. A: complete inhibition of phasic E neuron. B: multiple superimposed traces of E neuron during active phase showing transient inhibition. PA, phrenic efferent activity.

From Shannon and Freeman 99


Figure 6.

Response of pneumotaxic center inspiratory (I) neurons to stimulation (S) of intercostal and abdominal muscle afferents. PHR, phrenic efferent activity. Activity of phasic I neurons can be completely terminated (A). Continuously firing I neurons show reduction of inspiratory‐modulated activity (B) without alteration in tonic firing rate of most neurons (C).

From Shannon and Lindsey 101


Figure 7.

Response of pneumotaxic center inspiratory‐expiratory (IE) neurons to stimulation (S) of intercostal and abdominal muscle afferents. PHR, phrenic efferent activity. Top: nerve stimulation during inspiration (left) and expiration (right). Bottom: left record is control cycle and right record is during intercostal nerve stimulation (INS).

From Shannon and Lindsey 101


Figure 8.

Response of pneumotaxic center expiratory (E) neurons to stimulation (S) of intercostal and abdominal muscle afferents. A: tonic firing E neuron relative to phrenic efferent activity (PHR). B and C: two different neurons, left record is control cycle and right record is during intercostal nerve stimulation (INS).

From Shannon and Lindsey 101


Figure 9.

Inhibitory effect of internal intercostal muscle contraction elicited by ventral root stimulation (VRS) on inspiratory (phrenic) activity. Stimulation occurred during ongoing phrenic activity. A: control. B: test (VRS) cycle. (D. C. Bolser, B. G. Lindsey, and R. Shannon, unpublished observations.)



Figure 10.

Reduction in dorsal respiratory group inspiratory (I) neuron and phrenic (PHR) motor activity with vibration of single intercostal space. Vibration applied to rib during ongoing inspiratory activity. (D. C. Bolser, B. G. Lindsey, and R. Shannon, unpublished observations.)



Figure 11.

Effects of rib vibration on respiratory pattern. Vibrator (300 Hz) applied to 7th rib between arrows. Intercostal electromyogram (EMG) was recorded from 6th interspace. BP, blood pressure.

From Remmers 80


Figure 12.

Sample polygraph tracings of 2 animals breathing room air, showing effects of thoracic dorsal rhizotomies on breathing pattern. dV/dt, airflow; Vt, spirogram; BP, arterial blood pressure. Top panel: intact (Int.) after thoracic dorsal roots section (DR) and after secondary vagotomy (DRX). Bottom panel: intact (Int.) after vagotomy (X) and after secondary dorsal root section (XDR). Bars, 1 s each.

From Gautier 54


Figure 13.

One type of response to chest compression in vagotomized dog. End‐tidal CO2 () above records represents average over a few breaths at points denoted. V, volume; V, airflow; BP, arterial blood pressure.

From Shannon 96


Figure 14.

Second type of response to chest compression in vagotomized dogs. A and B are records from 2 dogs. PHR, phrenic efferent activity; V, airflow; BP, blood pressure.

From Shannon 96


Figure 15.

Phrenic efferent activity changes during costovertebral joint movement, on, Joints moved; off, joints returned to resting position; INT PHR, integrated (moving average) phrenic activity; , end‐tidal CO2. A: manual manipulation of neurally isolated costovertebral joints had inhibitory effect on inspiratory activity (phrenic motor discharge) and prolonged expiratory time. B: respiratory rate could be paced by moving joints in synchrony with PHR.

From Shannon 98
References
 1. Agostoni, E., E. d'Angelo, G. Torri, and L. Ravenna. Effects of uneven elastic loads on breathing pattern of anesthetized and conscious men. Respir. Physiol. 30: 153–168, 1977.
 2. Altose, M. D., N. N. Stanley, N. S. Cherniack, and A. P. Fishman. Effects of mechanical loading and hypercapnia on inspiratory muscle EMG. J. Appl. Physiol. 38: 467–473, 1975.
 3. Aminoff, M. J., and T. A. Sears. Spinal integration of segmental, cortical and breathing inputs to thoracic respiratory motoneurones. J. Physiol. London 215: 557–575, 1971.
 4. Bainton, C. R., P. A. Kirkwood, and T. A. Sears. On the transmission of the stimulating effects of carbon dioxide to the muscles of respiration. J. Physiol. London 280: 249–272, 1978.
 5. Baker, J. P., D. T. Frazier, M. Hanley, and F. W. Zechman, Jr. Behavior of expiratory neurons in response to mechanical and chemical loading. Respir. Physiol. 36: 337–351, 1979.
 6. Banzett, R. B., G. F. Inbar, R. Brown, M. Goldman, A. Rossier, and J. Mead. Diaphragm electrical activity during negative lower torso pressure in quadriplegic men. J. Appl. Physiol.: Respirat. Environ. Exercise Physiol. 51: 654–659, 1981.
 7. Barillot, J. C., and M. Dussardier. Activité des motoneurones laryngés expiratoires. J. Physiol. Paris 72: 311–343, 1976.
 8. Barron, W., and J. H. Coote. The contribution of articular receptors to cardiovascular reflexes elicited by passive limb movement. J. Physiol. London 235: 423–436, 1973.
 9. Bartoli, A., E. Bystrzycka, A. Guz, S. K. Jain, M. I. M. Noble, and D. Trenchard. Studies of the pulmonary vagal control of central respiratory rhythm in the absence of breathing movements. J. Physiol. London 230: 449–465, 1973.
 10. Bianchi, A. L., and J. C. Barillot. Activity of medullary respiratory neurones during reflexes from the lungs in cats. Respir. Physiol. 25: 335–352, 1975.
 11. Bianconi, R., and J. P. van der Meulen. The response to vibration of the end organs of mammalian muscle spindles. J. Neurophysiol. 26: 177–190, 1963.
 12. Bishop, B. Reflex control of abdominal muscles during positive‐pressure breathing. J. Appl. Physiol. 19: 224–232, 1964.
 13. Bland, S., L. Lazerou, G. Dyck, and R. M. Cherniack. The influence of the “chest wall” on respiratory rate and depth. Respir. Physiol. 3: 47–54, 1967.
 14. Bolser, D. C., B. G. Lindsey, and R. Shannon. Inhibition of medullary inspiratory drive by intercostal muscle tendon organs. Soc. Neurosci. Abstr. 9: 1160, 1983.
 15. Bolser, D. C., B. G. Lindsey, and R. Shannon. Evidence that intercostal muscle spindle endings do not reflexly modulate medullary inspiratory drive (Abstract). Federation Proc. 43: 433, 1984.
 16. Bradley, G. W. The response of the respiratory system to elastic loading in cats. Respir. Physiol. 16: 142–160, 1972.
 17. Brown, M. C., I. Engberg, and P. B. C. Matthews. The relative sensitivity to vibration of muscle receptors of the cat. J. Physiol. London 192: 773–800, 1967.
 18. Bruce, E. N., J. D. Smith, and F. S. Grodins. Chemical and reflex drives to breathing during resistance loading in cats. J. Appl. Physiol. 37: 176–182, 1974.
 19. Clark, F. J., and C. von Euler. On the regulation of depth and rate of breathing. J. Physiol. London 222: 267–295, 1972.
 20. Cleland, C. L., W. Z. Rymer, and F. R. Edwards. Force‐sensitive interneurons in the spinal cord of the cat. Science 217: 652–655, 1982.
 21. Colebatch, J., S. Gandevia, and D. McCloskey. Reduction in inspiratory activity in response to sternal vibration. Respir. Physiol. 29: 327–338, 1977.
 22. Comroe, J. H., Jr., and C. F. Schmidt. Reflexes from the limbs as a factor in the hyperpnea of muscular exercise. Am. J. Physiol. 138: 536–547, 1943.
 23. Coombs, H. C. The relation of the dorsal roots of the spinal nerves and the mesencephalon to the control of the respiratory movements. Am. J. Physiol. 46: 459–471, 1918.
 24. Corda, M., G. Eklund, and C. von Euler. External intercostal and phrenic α‐motor responses to changes in respiratory load. Acta Physiol. Scand. 63: 391–400, 1965.
 25. Corda, M., C. von Euler, and G. Lennerstrand. Proprioceptive innervation of the diaphragm. J. Physiol. London 178: 161–177, 1965.
 26. Critchlow, V., and C. von Euler. Intercostal muscle spindle activity and its γ‐motor control. J. Physiol. London 168: 820–847, 1963.
 27. Cuénod, M. Réflexes proprioceptifs du diaphragm chez le lapin. Helv. Physiol. Pharmacol. Acta 19: 360–372, 1961.
 28. Culver, G. A., and H. Rahn. Reflex respiratory stimulation by chest compression in the dog. Am. J. Physiol. 168: 686–693, 1952.
 29. d'angelo, E., and E. Agostoni. Immediate response to expiratory threshold load. Respir. Physiol. 25: 269–284, 1975.
 30. d'angelo, E., G. Miserocchi, and E. Agostoni. Effect of rib cage or abdomen compression at iso‐lung volume on breathing patterns. Respir. Physiol. 28: 161–177, 1976.
 31. Decima, E., C. von Euler, and U. Thoden. Intercostal‐to‐phrenic reflexes in the spinal cat. Acta Physiol. Scand. 75: 568–579, 1969.
 32. Downman, C. B. B. Skeletal muscle reflexes of splanchnic and intercostal nerve origin in acute spinal and decerebrate cats. J. Neurophysiol. 18: 217–235, 1955.
 33. Duron, B. Postural and ventilatory functions of intercostal muscles. Acta Neurobiol. Exp. 33: 355–380, 1973.
 34. Duron, B., and M. C. Jung‐Caillol. Investigation of afferent activity in the intact phrenic nerve with bipolar electrodes. Acta Neurobiol. Exp. 33: 427–432, 1973.
 35. Duron, B., M. C. Jung‐Caillol, and D. Marlot. Réflexe inhibiteur phrenico‐phrénique. In: Respiratory Centres and Afferent Systems, edited by B. Duron. Paris: INSERM, 1976, vol. 59, p. 193–197.
 36. Duron, B., and D. Marlot. Intercostal and diaphragmatic electrical activity during wakefulness and sleep in normal unrestrained adult cats. Sleep 3: 269–280, 1980.
 37. Duron, B., and D. Marlot. The non‐myelinated fibers of the phrenic and intercostal nerves in the cat. Z. Mikrosk. Anat. Forsch. 94: 257–268, 1980.
 38. Eklund, G., C. von Euler, and S. Rutkowski. Spontaneous and reflex activity of intercostal gamma motoneurones. J. Physiol. London 171: 139–163, 1964.
 39. Eldridge, F. L., P. Gill‐Kumar, D. E. Millhorn, and T. G. Waldrop. Spinal inhibition of phrenic motoneurones by stimulation of afferents from peripheral muscles. J. Physiol. London 311: 67–79, 1981.
 40. Euler, C. von. The control of respiratory movement. In: Breathlessness, edited by J. B. L. Howell and E. J. M. Campbell. Oxford, UK: Blackwell, 1966, p. 19–32.
 41. Euler, C. von. Proprioceptive control in respiration. In: Muscular Afferents and Motor Control, edited by R. Granit. Stockholm: Almqvist & Wiksell, 1966, p. 193–207. (Nobel Symp. 1.).
 42. Euler, C. von. Fusimotor activity in spindle control of natural movements with special reference to respiration. In: Excitatory Synaptic Mechanisms, edited by P. Andersen and J. K. S. Jansen. Oslo: Universitetsforlaget, 1970, p. 341–349.
 43. Euler, C. von. The role of proprioceptive afferents in the control of respiratory muscles. Acta Neurobiol. Exp. 33: 329–341, 1973.
 44. Euler, C. von. On the role of proprioceptors in perception and execution of motor acts with special references to breathing. In: Loaded Breathing, edited by L. D. Pengelly, A. S. Rebuck, and E. J. M. Campbell. Don Mills, Ontario: Longman Canada, 1974, p. 139–150.
 45. Euler, C. von, and G. Peretti. Dynamic and static contributions to the rhythmic γ‐activation of primary and secondary spindle endings in external intercostal muscle. J. Physiol. London 187: 501–516, 1966.
 46. Flandrois, R., J. R. Lacour, J. Islas‐Maroquin, and J. Charlot. Limb mechanoreceptors inducing the reflex hyperpnea of exercise. Respir. Physiol. 2: 335–343, 1967.
 47. Fleisch, A., E. Grandjean, and R. Crausaz. Contribution à l'étude de la fonction des fibres afférentes du phrénique. Helv. Physiol. Pharmacol. Acta 4: 134–167, 1946.
 48. Fleisch, A., and J. Tripod. Die afferente Komponente der Atmungssteurerung. Pfluegers Arch. Gesamte Physiol. Menschen Tiere 240: 676–679, 1938.
 49. Frazier, D. T., R. Shannon, and F. W. Zechman. Response of medullary respiratory neurones to mechanical loads. In: Loaded Breathing, edited by L. D. Pengelly, A. S. Rebuck, and E. J. M. Campbell. Don Mills, Ontario: Longman Canada, 1974, p. 163–171.
 50. Fryman, D., and D. T. Frazier. Modulation of diaphragm activity by phrenic afferents (Abstract). Federation Proc. 42: 1014, 1983.
 51. Gandevia, S. C., and D. I. McCloskey. Changes in the pattern of breathing caused by chest vibration. Respir. Physiol. 26: 163–171, 1976.
 52. Garcia Ramos, J. On the integration of respiratory movements. Acta Physiol. Lat. Am. 9: 246–256, 1959.
 53. Garcia Ramos, J., and E. Lopez Mendoza. On the integration of respiratory movements. II. The integration at spinal level. Acta Physiol. Lat. Am. 9: 257–266, 1959.
 54. Gautier, H. Respiratory responses of the anesthetized rabbit to vagotomy and thoracic dorsal rhizotomy. Respir. Physiol. 17: 238–247, 1973.
 55. Gill, P. K., and M. Kuno. Excitatory and inhibitory actions on phrenic motoneurones. J. Physiol. London 168: 274–289, 1963.
 56. Gill, P. K., and M. Kuno. Properties of phrenic motoneurons and their responses to some synaptic inputs. Am. Rev. Respir. Dis. 119: 51–55, 1979.
 57. Godwin‐Austen, R. B. The mechanoreceptors of the costovertebral joints. J. Physiol. London 202: 737–753, 1969.
 58. Grandjean, E. Atmungsveränderungen bei Reizung der afferenten Phrenicusfasern. Helv. Physiol. Pharmacol. Acta 1: 205–220, 1943.
 59. Hagan, R., A. C. Bryan, M. H. Bryan, and G. Gulston. Neonatal chest wall afferents and regulation of respiration. J. Appl. Physiol.: Respirat. Environ. Exercise Physiol. 42: 362–367, 1977.
 60. Holmes, R., and R. W. Torrance. Afferent fibers of the stellate ganglion. Q. J. Exp. Physiol. 44: 271–281, 1959.
 61. Homma, I. Inspiratory inhibitory reflex caused by the chest wall vibration in man. Respir. Physiol. 39: 345–353, 1980.
 62. Homma, I., G. Eklund, and K. E. Hagbarth. Respiration in man affected by TVR contractions elicited in inspiratory and expiratory intercostal muscles. Respir. Physiol. 35: 335–348, 1978.
 63. Irani, B., D. Megirian, and J. H. Sherrey. An analysis of reflex changes in excitability of phrenic, laryngeal, and intercostal motoneurons. Exp. Neurol. 36: 1–13, 1972.
 64. Iscoe, S., and C. Polosa. Synchronization of respiratory frequency by somatic afferent stimulation. J. Appl. Physiol. 40: 138–148, 1976.
 65. Jung‐Caillol, M. C, and B. Duron. Number of neuromuscular spindles and electrical activity of the respiratory muscles. In: Respiratory Centres and Afferent Systems, edited by B. Duron. Paris: INSERM, 1976, vol. 59, p. 165–174.
 66. Kalia, M., J. M. Senapati, B. Parida, and A. Panda. Reflex increase in ventilation by muscle receptors with nonmedullated fibers (C fibers). J. Appl. Physiol. 32: 189–193, 1972.
 67. Kirkwood, P. A., and T. A. Sears. Monosynaptic excitation of motoneurones from secondary endings of muscle spindles. Nature London 252: 243–244, 1974.
 68. Kirkwood, P. A., and T. A. Sears. Excitatory post‐synaptic potentials from single muscle spindle afferents in external intercostal motoneurones of the cat. J. Physiol. London 322: 287–314, 1982.
 69. Kirkwood, P. A., and T. A. Sears. The effects of single afferent impulses on the probability of firing of external intercostal motoneurones in the cat. J. Physiol. London 322: 315–336, 1982.
 70. Knill, R., and A. C. Bryan. An intercostal‐phrenic inhibitory reflex in human newborn infants. J. Appl. Physiol. 40: 352–356, 1976.
 71. Kostreva, D. R., F. A. Hopp, E. J. Zuperku, F. O. Igler, R. L. Coon, and J. P. Kampine. Respiratory inhibition with sympathetic afferent stimulation in the canine and primate. J. Appl. Physiol.: Respirat. Environ. Exercise Physiol. 44: 718–724, 1978.
 72. Kostreva, D. R., E. J. Zuperku, G. L. Hess, R. L. Coon, and J. P. Kampine. Pulmonary afferent activity recorded from sympathetic nerves. J. Appl. Physiol. 39: 37–40, 1975.
 73. Kugelberg, E., and K. E. Hagbarth. Spinal mechanism of the abdominal and erector spinae skin reflexes. Brain 81: 290–304, 1958.
 74. Massion, J. Postural function of respiratory muscles. In: Respiratory Centres and Afferent Systems, edited by D. Duron. Paris: INSERM, 1976, vol. 59, p. 175–181.
 75. Matthews, P. B. C. The relative unimportance of the temporal pattern of the primary afferent input in determining the mean level of motor firing in the tonic vibration reflex. J. Physiol. London 251: 333–361, 1975.
 76. McCloskey, D. I., and J. H. Mitchell. Reflex cardiovascular and respiratory responses originating in exercising muscle. J. Physiol. London 224: 173–176, 1972.
 77. Newsom Davis, J. Spinal control. In: The Respiratory Muscles, edited by E. J. M. Campbell, E. Agostoni, and J. Newsom Davis. Philadelphia, PA: Saunders, 1970, p. 205–233.
 78. Newsom Davis, J. Control of the muscles of breathing. In: Respiratory Physiology, edited by J. G. Widdicombe. Baltimore, MD: University Park, 1974, p. 221–245.
 79. Newsom Davis, J., and T. A. Sears. The proprioceptive reflex control of the intercostal muscles during their voluntary activation. J. Physiol. London 209: 711–738, 1970.
 80. Remmers, J. E. Inhibition of inspiratory activity by intercostal muscle afferents. Respir. Physiol. 10: 358–383, 1970.
 81. Remmers, J. E. Extra‐segmental reflexes derived from intercostal afferents: phrenic and laryngeal responses. J. Physiol. London 233: 45–62, 1973.
 82. Remmers, J. E. Functional role of the inspiratory terminating reflex from intercostal muscle spindles. In: Respiratory Centres and Afferent Systems, edited by B. Duron. Paris: INSERM, 1976, vol. 59, p. 183–191.
 83. Remmers, J. E., and I. Marttila. Action of intercostal muscle afferents on the respiratory rhythm of anesthetized cats. Respir. Physiol. 24: 31–41, 1975.
 84. Remmers, J. E., and W. G. Tsiaras. Effect of lateral cervical cord lesions on the respiratory rhythm of anaesthetized decerebrate cats after vagotomy. J. Physiol. London 233: 63–74, 1973.
 85. Rijlant, P. Contribution à l'étude du contrôle reflex de la respiration. Bull. Acad. R. Med. Belg. 7: 58–107, 1942.
 86. Russell, J. A., and B. Bishop. Vagal afferents essential for abdominal muscle activity during lung inflation in cats. J. Appl. Physiol. 41: 310–315, 1976.
 87. Sant'Ambrogio, G., and J. G. Widdicombe. Respiratory reflexes acting on the diaphragm and inspiratory intercostal muscles of the rabbit. J. Physiol. London 180: 766–779, 1965.
 88. Sant'Ambrogio, G., M. F. Wilson, and D. T. Frazier. Somatic afferent activity in reflex regulation of diaphragmatic function in the cat. J. Appl. Physiol. 17: 829–832, 1962.
 89. Sears, T. A. Electrical activity in expiratory muscles of the cat during inflation of the chest (Abstract). J. Physiol. London 142: 35P, 1958.
 90. Sears, T. A. The fibre calibre spectra of sensory and motor fibres in the intercostal nerves of cat. J. Physiol. London 172: 150–161, 1964.
 91. Sears, T. A. Investigations on respiratory motoneurones of the thoracic spinal cord. In: Progress in Brain Research. Physiology of Spiral Neurons, edited by J. C. Eccles and J. P. Schadé. Amsterdam: Elsevier, 1964, vol. 12, p. 259–274.
 92. Sears, T. A. Some properties and reflex connexions of respiratory motoneurones of the cat's thoracic spinal cord. J. Physiol. London 175: 386–403, 1964.
 93. Sears, T. A. The respiratory motoneurone: integration at spinal segmental level. In: Breathlessness, edited by J. B. L. Howell and E. J. M. Campbell. Oxford, UK: Blackwell, 1966, p. 33–47.
 94. Shannon, R. Respiratory frequency control during external elastic loading and chest compression. Respir. Physiol. 23: 11–22, 1975.
 95. Shannon, R. Effects of thoracic dorsal rhizotomies on the respiratory pattern in anesthetized cats. J. Appl. Physiol.: Respirat. Environ. Exercise Physiol. 43: 20–26, 1977.
 96. Shannon, R. Involvement of thoracic nerve afferents in the respiratory response to chest compression. Respir. Physiol. 36: 65–76, 1979.
 97. Shannon, R. Intercostal and abdominal muscle afferent influence on medullary dorsal respiratory group neurons. Respir. Physiol. 39: 73–94, 1980.
 98. Shannon, R. Respiratory pattern changes during costovertebral joint movement. J. Appl. Physiol.: Respirat. Environ. Exercise Physiol. 48: 862–867, 1980.
 99. Shannon, R., and D. L. Freeman. Nucleus retroambigualis respiratory neurons: responses to intercostal and abdominal muscle afferents. Respir. Physiol. 45: 357–375, 1981.
 100. Shannon, R., and B. G. Lindsey. Brainstem interneurons transmitting respiratory proprioceptor afferent information (Abstract). Federation Proc. 42: 333, 1983.
 101. Shannon, R., and B. G. Lindsey. Intercostal and abdominal muscle afferent influence on pneumotaxic center respiratory neurons. Respir. Physiol. 52: 85–98, 1983.
 102. Shannon, R., S. Saporta, and B. G. Lindsey. Transmission of intercostal muscle proprioceptor afferent information to medullary respiratory areas. Exp. Neurol. 78: 222–225, 1982.
 103. Shannon, R., W. T. Shear, A. R. Mercak, D. C. Bolser, and B. G. Lindsey. Influence of cervical and thoracic dorsal root afferent information on inspiratory neuron activity during mechanical loading (Abstract). Physiologist 26: A46, 1983.
 104. Shannon, R., F. W. Zechman, and D. T. Frazier. First‐breath response of medullary inspiratory neurones to the mechanical loading of inspiration. Respir. Physiol. 16: 70–78, 1972.
 105. Speck, D. F., and C. L. Webber, Jr. Thoracic dorsal rhizotomy in the anesthetized cat: maintenance of eupnic breathing. Respir. Physiol. 38: 347–357, 1979.
 106. Speck, D. F., and C. L. Webber, Jr. Time course of intercostal afferent termination of the inspiratory process. Respir. Physiol. 43: 133–145, 1981.
 107. Speck, D. F., and C. L. Webber, Jr. Cerebellar influence on the termination of inspiration by intercostal nerve stimulation. Respir. Physiol. 47: 231–238, 1982.
 108. Speck, D. F., and C. L. Webber, Jr. Baroreceptor modulation of inspiratory termination by intercostal nerve stimulation. Respir. Physiol. 52: 387–395, 1983.
 109. Stella, G. On the mechanism of production and the physiological significance of “apneusis.” J. Physiol. London 93: 10–23, 1938.
 110. Sumi, T., and S. Kotani. Excitatory and inhibitory reflexogenic skin areas for the intercostal respiratory neurons in the dog. Acta Med. Okayama 13: 301–313, 1959.
 111. Whitehead, R. W., and W. B. Draper. A respiratory reflex originating from the thoracic wall of the dog. Anesthesiology 8: 159–165, 1947.
 112. Whitelaw, W. A., J.‐P. Derenne, J. Couture, and J. Milic‐Emili. Adaptation of anesthetized men to breathing through an inspiratory resistor. J. Appl. Physiol. 41: 285–291, 1976.
 113. Widdicombe, J. G. Respiratory reflexes in man and other mammalian species. Clin. Sci. 21: 163–170, 1961.
 114. Widdicombe, J. G. Respiratory reflexes. In: Handbook of Physiology. Respiration, edited by W. O. Fenn and H. Rahn. Bethesda, MD: Am. Physiol. Soc., 1964, sect. 3, vol. I, chapt. 24, p. 585–630.
 115. Yamamoto, S., M. Miyajima, and M. Urabe. Respiratory neuronal activities in spinal afferents of cat. Jpn. J. Physiol. 10: 509–517, 1960.
 116. Zechman, F. W., and J. Taylor. Respiratory response to forward acceleration compared with chest compression in dogs. J. Appl. Physiol. 17: 410–412, 1962.

Contact Editor

Submit a note to the editor about this article by filling in the form below.

* Required Field

How to Cite

Roger Shannon. Reflexes from Respiratory Muscles and Costovertebral Joints. Compr Physiol 2011, Supplement 11: Handbook of Physiology, The Respiratory System, Control of Breathing: 431-447. First published in print 1986. doi: 10.1002/cphy.cp030213