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. 1989 Mar;410:463–477. doi: 10.1113/jphysiol.1989.sp017544

The organization of heterogenic reflexes among muscles crossing the ankle joint in the decerebrate cat.

T R Nichols 1
PMCID: PMC1190490  PMID: 2795487

Abstract

1. Mechanical actions of heterogenic (intermuscular) reflexes arising from proprioceptors in flexor and extensor ankle muscles were measured in intercollicular and premammillary decerebrate cats. Length inputs were applied to the freed tendons of one of a pair of muscles crossing the ankle joint and resulting changes in force in both muscles were measured. Interactions between autogenic and heterogenic reflexes were studied by applying length changes to both muscles. 2. A consistent asymmetry was observed in the heterogenic inhibition between the single-joint antagonists soleus and tibialis anterior (TA). Inhibition from soleus to TA was weak or absent during the reflex activation of TA. In contrast, a strong heterogenic inhibition was consistently observed from TA to soleus during the activation of soleus by a crossed-extension reflex. The effect of this inhibition in the intact joint is to increase the apparent mechanical stiffness of soleus. 3. Mutual synergism among soleus, medial gastrocnemius (MG) and lateral gastrocnemius (LG) was demonstrated only at low to moderate forces by the observation of excitatory reflexes among them. During a naturally or electrically evoked crossed-extension reflex, however, a unidirectional inhibitory reflex from MG and LG to soleus was observed. This inhibition increased with force in MG or LG. These results suggest that the knee and ankle joints become more tightly linked mechanically at high forces since the stiffness of the biarticular gastrocnemius muscle predominates over that of the uniarticular soleus. 4. Under quiescent conditions (no resting muscle activation), mutual synergism was obeyed among the ankle extensors soleus, LG and MG and also between the pretibial flexors TA and extensor digitorum longus (EDL). Moreover, inhibition was generally observed between a pretibial flexor and an ankle extensor. Departures from this expected pattern of heterogenic reflexes occurred when the muscle groups were activated by crossed-extension and flexion reflexes. Reflexes onto soleus, TA and EDL reversed in sign or increased in magnitude. 5. The observed patterns of reflex connectivity among the ankle flexors and extensors were similar in both intercollicular and premammillary preparations, although changes in reflex strength were sometimes noted in cases where a second, lower transection was performed during the experiment. 6. It is argued from the large magnitudes of certain heterogenic reflexes that the mechanical response properties of muscles crossing the ankle joint in the intact animal are not dominated by autogenic reflexes and intrinsic mechanical properties.(ABSTRACT TRUNCATED AT 400 WORDS)

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Abraham L. D., Loeb G. E. The distal hindlimb musculature of the cat. Patterns of normal use. Exp Brain Res. 1985;58(3):583–593. [PubMed] [Google Scholar]
  2. Binder M. D., Houk J. C., Nichols T. R., Rymer W. Z., Stuart D. G. Properties and segmental actions of mammalian muscle receptors: an update. Fed Proc. 1982 Nov;41(13):2907–2918. [PubMed] [Google Scholar]
  3. Capaday C., Cooke J. D. Vibration-induced changes in movement-related EMG activity in humans. Exp Brain Res. 1983;52(1):139–146. doi: 10.1007/BF00237158. [DOI] [PubMed] [Google Scholar]
  4. Crago P. E., Houk J. C., Rymer W. Z. Sampling of total muscle force by tendon organs. J Neurophysiol. 1982 Jun;47(6):1069–1083. doi: 10.1152/jn.1982.47.6.1069. [DOI] [PubMed] [Google Scholar]
  5. Duysens J. Reflex control of locomotion as revealed by stimulation of cutaneous afferents in spontaneously walking premammillary cats. J Neurophysiol. 1977 Jul;40(4):737–751. doi: 10.1152/jn.1977.40.4.737. [DOI] [PubMed] [Google Scholar]
  6. ECCLES J. C., ECCLES R. M., IGGO A., ITO M. Distribution of recurrent inhibition among motoneurones. J Physiol. 1961 Dec;159:479–499. doi: 10.1113/jphysiol.1961.sp006822. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. ECCLES J. C., ECCLES R. M., LUNDBERG A. The convergence of monosynaptic excitatory afferents on to many different species of alpha motoneurones. J Physiol. 1957 Jun 18;137(1):22–50. doi: 10.1113/jphysiol.1957.sp005794. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. ECCLES J. C., ECCLES R. M., MAGNI F. Central inhibitory action attributable to presynaptic depolarization produced by muscle afferent volleys. J Physiol. 1961 Nov;159:147–166. doi: 10.1113/jphysiol.1961.sp006798. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. ECCLES J. C. PRESYNAPTIC INHIBITION IN THE SPINAL CORD. Prog Brain Res. 1964;12:65–91. doi: 10.1016/s0079-6123(08)60618-4. [DOI] [PubMed] [Google Scholar]
  10. Fu T. C., Hultborn H., Larsson R., Lundberg A. Reciprocal inhibition during the tonic stretch reflex in the decerebrate cat. J Physiol. 1978 Nov;284:345–369. doi: 10.1113/jphysiol.1978.sp012544. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. GRANIT R., PASCOE J. E., STEG G. The behaviour of tonic alpha and gamma motoneurones during stimulation of recurrent collaterals. J Physiol. 1957 Oct 30;138(3):381–400. doi: 10.1113/jphysiol.1957.sp005857. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Goslow G. E., Jr, Reinking R. M., Stuart D. G. The cat step cycle: hind limb joint angles and muscle lengths during unrestrained locomotion. J Morphol. 1973 Sep;141(1):1–41. doi: 10.1002/jmor.1051410102. [DOI] [PubMed] [Google Scholar]
  13. Grillner S. The role of muscle stiffness in meeting the changing postural and locomotor requirements for force development by the ankle extensors. Acta Physiol Scand. 1972 Sep;86(1):92–108. doi: 10.1111/j.1748-1716.1972.tb00227.x. [DOI] [PubMed] [Google Scholar]
  14. Hoffer J. A., Andreassen S. Regulation of soleus muscle stiffness in premammillary cats: intrinsic and reflex components. J Neurophysiol. 1981 Feb;45(2):267–285. doi: 10.1152/jn.1981.45.2.267. [DOI] [PubMed] [Google Scholar]
  15. Houk J., Henneman E. Responses of Golgi tendon organs to active contractions of the soleus muscle of the cat. J Neurophysiol. 1967 May;30(3):466–481. doi: 10.1152/jn.1967.30.3.466. [DOI] [PubMed] [Google Scholar]
  16. Hultborn H., Illert M., Santini M. Convergence on interneurones mediating the reciprocal Ia inhibition of motoneurones. III. Effects from supraspinal pathways. Acta Physiol Scand. 1976 Mar;96(3):368–391. doi: 10.1111/j.1748-1716.1976.tb10206.x. [DOI] [PubMed] [Google Scholar]
  17. Hutton R. S., Enoka R. M. Kinematic assessment of a functional role for recurrent inhibition and selective recruitment. Exp Neurol. 1986 Aug;93(2):369–379. doi: 10.1016/0014-4886(86)90197-4. [DOI] [PubMed] [Google Scholar]
  18. Macpherson J. M., Rushmer D. S., Dunbar D. C. Postural responses in the cat to unexpected rotations of the supporting surface: evidence for a centrally generated synergic organization. Exp Brain Res. 1986;62(1):152–160. doi: 10.1007/BF00237411. [DOI] [PubMed] [Google Scholar]
  19. Matthews P. B., Watson J. D. Effect of vibrating agonist or antagonist muscle of the reflex response to sinusoidal displacement of the human forearm. J Physiol. 1981 Dec;321:297–316. doi: 10.1113/jphysiol.1981.sp013985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Nichols T. R. A technique for measuring the mechanical actions of heterogenic (intermuscular) reflexes in the decerebrate cat. J Neurosci Methods. 1987 Oct;21(2-4):265–273. doi: 10.1016/0165-0270(87)90121-x. [DOI] [PubMed] [Google Scholar]
  21. Nichols T. R., Houk J. C. Improvement in linearity and regulation of stiffness that results from actions of stretch reflex. J Neurophysiol. 1976 Jan;39(1):119–142. doi: 10.1152/jn.1976.39.1.119. [DOI] [PubMed] [Google Scholar]
  22. Nichols T. R., Steeves J. D. Resetting of resultant stiffness in ankle flexor and extensor muscles in the decerebrate cat. Exp Brain Res. 1986;62(2):401–410. doi: 10.1007/BF00238859. [DOI] [PubMed] [Google Scholar]
  23. Smith J. L., Betts B., Edgerton V. R., Zernicke R. F. Rapid ankle extension during paw shakes: selective recruitment of fast ankle extensors. J Neurophysiol. 1980 Mar;43(3):612–620. doi: 10.1152/jn.1980.43.3.612. [DOI] [PubMed] [Google Scholar]

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