Crossed reflexes evoked by selective activation of muscle spindle primary endings in the decerebrate cat

Crossed reflexes evoked by selective activation of muscle spindle primary endings in the decerebrate cat

324 Brain Research, 115 (1976) 324-32? '( , Elsevier Scmntlhc Pubhshlng Company, Amsterdam - Printed m The Netherland~ Crossed reflexes evoked by se...

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324

Brain Research, 115 (1976) 324-32? '( , Elsevier Scmntlhc Pubhshlng Company, Amsterdam - Printed m The Netherland~

Crossed reflexes evoked by selective activation of muscle spindle primary endings in the decerebrate cat

RONALD H. BAXENDALE and JAY R ROSENBERG htmtute of Physiology, Umverstty oJ Glasgow, Glasgow GI2 8QQ (Great Britain)

(Accepted June 2nd, 1976)

Sherrmgton 5 showed that lengthening and shortening reactions were frequently accompanied by reflexes in the contralateral limb. Shortemng of an extensor muscle was frequently accompanied by a lengthening of the equivalent contralateral extensor. Conversely, ipsilateral lengthening of an extensor was regularly accompanied by a shortening of the eqmvalent contralateral extensor. He went on to show that both the ipsilateral and contralateral reactions depend on receptors lying within the muscle. However, the question of whmh receptors were responsible for each of the crossed reflexes was left unanswered. More recently the queshon of the receptors responsible for the crossed reflexes was taken up by PerP ,6 and Holmqvist 4. They used graded electrical stimulation of muscle nerves 4,5 or applied graded loads to the muscle tendon 6 in an attempt to separate out the effects of each of the group I components of muscle nerves on the contralateral limb reflexes. These studies gave conflicting results. PerP ,6 beheved that the activahon of Ia axons produced an inhibition of the contralateral equivalent muscle. Holmqvist 4, in most cases, was unable to separate out the contralateral effects of the Ia and lb axons. However, m the few instances where she was able to effect a separation, the la axons were assigned a crossed facilitatory action. These conflmting reports may in part be a consequence of the threshold dJscrimmatmn techniques used to selectively activate the la axons. Techniques have now been developed which allow unambiguous selective activation of the group 1 components. Brown et al.2 demonstrated that low amplitude, high frequency vibration applied to the muscle tendon could be used to selectively generate a pure la discharge; and C o p p m et al. a outlined a procedure for selectwely raising the la threshold to electrical stimulation, and thereby allowing the lb axons to be electrically stimulated in ~solat~on. In a prehminary study 1 we used these threshold discriminatmn techmques to investigate the crossed reflexes arising from muscle spindle primary afferents and tendon organ afferents onto the contralateral soleus muscle. The Ia afferents exerted an inhibitory influence on the contralateral soleus muscle, whereas the Ib afferents were facihtatory to the same muscle. The present experiments extend our previous study by considering the crossed Ia reflexes arising from soleus onto both extensors and flexors acting at the knee and ankle in the contralateral hindlimb.

325 These experiments were carried out on cats decerebrated under deep N 2 0 - O 2 halothane anaesthesia by transecting the midbrain at an mtercollicular level. The forebrain rostral to the transection was removed, and the anaesthetic discontinued. The left hindlimb was denervated, with the exception of soleus which was de-efferented by cutting ventral roots L6 to $1. The soleus tendon was d~ssected free and connected to the vibrator with a stout linen thread. The Ia axons were selectively activated by longitudinal vibration of the muscle tendon at frequencies between 100-200 Hz, at amplitudes below 50 # m peak-to-peak. The crossed reflex effects were assessed in two ways. The test muscles were isotonically loaded with weights between 50 and 500 g, and their responses to stimulation of the contralateral Ia axons were recorded as changes in muscle length. Alternatively, the effect of contralateral Ia axon activation on the averaged monosynaptm ventral root potential was examined. In this case several muscle nerves were prepared for stimulation, and the ventral roots supplying the contralateral hindlimb were cut. The monosynaptic responses of the motoneurone pool conditioned by contralateral Ia stimulation were compared with control responses taken before and after the conditioning sUmulus. The size of the contralateral responses was measured as the area under the curve of the averaged monosynaptic response. In all cases where contralateral reflexes were obtained, selective Ia activation produced lengthenings in both the contralateral soleus and tibiahs anterior muscles. In 217 crossed reflexes from soleus Ia axons, lengthenings of the contralateral soleus occurred in all cases. In 62 observations of crossed reflexes from soleus Ia axons onto the contralateral tibialis anterior muscle, lengthening occurred in all cases. In no observation of a crossed reflex generated by soleus Ia axons was a contralateral shortening observed. However, there were differences in the form of the response of soleus and tibialis anterior to selectwe actwation of Ia axons from the contralateral soleus. Fig. 1 illustrates the type of crossed reflexes obtained from soleus and tibialis anterior SOLEUS

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Fig. 1. Length changes recorded from an lsotomcallyloaded ankle extensor (soleus) and flexor (tibialis anterior) during periods of vibration of the contralateral soleus muscle tendon. Vibration: 50 pm peak-to-peak, 100-200 Hz The lengthening in soleus persists after the vibration has stopped, while that in tibialis antermr is limited to the duration of the wbratlon.

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FJg. 2. A comparison of the averaged monosynaptic ventral root potentml recorded w~tb and wJtbou t vibration of the contralateral soleus muscle. Each trace represents the average of 32 monosynapt~c potentials evoked by stimulation of muscle nerves indicated m the figure, and recorded m the central stumps of the cut L7 or $1 ventral root bundles The size of the ventral root potential is reduced during periods of vibration of the contralateral soleus The periods of vibration are indicated by black bars under the recorded potentml. The control monosynapt~c potentials recorded before and after wbrat~on are shown for comparison

in response to selective activation of the soleus la axons. Low amplitude, high frequency vibration of the contralateral soleus muscle tendon produced a lengthening in the soleus which persisted beyond the time that the vibratory stimulus was applied. In some instances the lengthening persisted for several minutes. Subsequent periods of vibration produced further sustained lengthenings of the contralateral soleus, indicating that the muscle was still reflexly actwe at each new sustained length. On the other hand the lengthening which occurred in tibialis anterior as a consequence of vibration of the contralateral soleus muscle was limited to the duration of the vibration. Once the vibration had stopped tibialis anterior returned to its original length. Crossed reflex changes in length were often difficult to elicit, and every test vibration of soleus &d not

327 produce a crossed reflex, with those onto tibialis anterior occurring less frequently than those onto soleus. To facihtate examination o f several muscles in the same preparation, vibration o f the soleus tendon was used as a conditioning stimulus, and its effect on the contralateral monosynaptic reflex elicited f r o m several muscle nerves assessed. The control and conditioned contralateral monosynaptic reflexes from four different muscle nerves are dlustrated in Fig. 2. In each case the monosynaptlc reflex elicited during contralateral vibration was smaller than the control responses which preceded and followed the test reflex. In some cases vibration reduced the averaged evoked monosynaptic response by as m u c h as 40 o~, o f its control value. In no case did the size o f the m o n o synapt~c reflex initiated during contralateral vibration exceed the control values preceding and following vibration. Control experiments showed that electrical stimulation o f the cut central end of L7 or S1 ventral roots did not effect contralateral averaged monosynaptic potentials. Thus crossed reflex effects seen during vibration must be due to excitation o f the Ia axons by vibration, and do not arise from activation of the recurrent collaterals which are stimulated by motoneurones autogenically excited by the Ia axons. Several cats were made acutely spinal by transection o f the spinal cord at C1. Subsequent vibration o f the soleus muscle tendon produced lengthenings in the contralateral soleus muscle similar m size and latency to those observed in decerebrate cats. This result implies that the crossed reflexes do not necessarily depend on midbrain or cerebellar structures. The present results clearly demonstrate that Ia axons from soleus exert an inhibitory influence on both flexors and extensors acting at the contralateral knee and ankle. The f o r m o f the crossed reflexes onto flexors and extensors confirms Sherrington's 7 observations that the crossed reflexes were stronger and more easily observed in extensors, and often difficult to discern in flexors. However, his 'impression' (cf. ref. 3, p. 112) was that a weak flexor contraction a c c o m p a m e d the extensor inhibition, whereas our results show that there is a relaxation o f both flexors and extensors. Thus it appears that the crossed Ia reflexes are not reciprocally orgamzed, as is the case for the ipsilateral | a reflexes.

1 Baxendale, R. H. and Rosenberg, J. R, Crossed reflex actions of group I muscle afferents, J. PhysioL (Lond.), 251 (1975) 53P. 2 Brown, M C, Engberg, I. and Matthews, P. B. C., The relative sensitivity to wbrat~on of muscle receptors of the cat, J Physiol. (Lond.), 192 (1976) 773-800. 3 Coppm, C. M. L., Jack, J. J. B. and McLennan, C. R., A method for the selective activation of tendon organ afferent fibres from the cat soleus muscle, J. PhysioL (Lond.), 219 (1970) 20P. 4 Holmqwst, B., Crossed spinal reflex actions evoked by volleys m somatic afferents, Acta physiol. scand., 52, Suppl. 181 (1961) 1-66. 5 Perl, E. R, Crossed reflex effects evoked by actwlty m myehnated afferent fibres of muscle, J. NeurophysioL, 21 (1958) 101-112. 6 Perl, E. R , Effects of muscle stretch on exc~tabdity of contralateral motoneurones, J Phystol. (Lond.), 145 (1959) 193-203 7 Sherrmgton, C. S., On plastic tonus and proprioceptive reflexes, Quart. J. exp. PhysioL, 2 (1909) 109-156.