STATIC A N D D Y N A M I C F U S I M O T O R ACTIVITY D U R I N G L O C O M O T O R M O V E M E N T S IN T H E CAT
c . P E R R E T AND P.
Laboratoire de Neurophysiologie comparde, Universitd de Paris VI, Paris 5 (France)
The participation of fusimotor activity in organized movements has now been explored in the cat in at least two particular cases: (1) spontaneous respiration (see e.g. ref. 4) and (2) locomotion elicited through electrical stimulation of the brain stem 6. The present study of fusimotor activity was also performed using locomotor movements. However, in order to avoid a possible artificial activation of gamma efferents through central electrical stimulation, we have analyzed movements which develop spontaneously or which occur upon natural stimulation in the acute decorticate cat. The movements consisted of sequences, of variable duration, of successive flexions and extensions alternating in both hindlimbs. In previous experiments 5 performed on the same type of preparation we have shown that after deep curare paralysis, blocking both extra- and intrafusal transmission, efferent discharges persist in motor nerves with almost exactly the same pattern as observed in the locomotor movements. Thus it could be concluded that these movements are programmed centrally and that the reafferent feedback, and so the gamma loop, is not essential for their development. Despite this finding, a definite participation of fusimotor innervation in stepping movements can be demonstrated, as will be shown herein. Cats were fully decorticated under brief barbiturate anaesthesia (Brietal, 10 mg/kg). One hindlimb was left intact and its movements were recorded through a strain gauge. The opposite hindlimb was completely denervated except for the muscle(s) selected for study (tibialis anterior, tenuissimus, gastrocnemius, soleus). It was immobilized through rigid fixation of the knee and ankle joints, of the pelvis and of the spines in order to avoid possible artefactual transmission of movements to the muscle. Muscle contractions were also recorded with a strain gauge of sufficient sensitivity to detect any contraction. The limb was deafferented by section of the dorsal roots, thus suppressing possible ipsilateral reflex activation of gamma or alpha motoneurones. The activity in single afferents from the muscle was recorded from filaments in the distal cut end of the dorsal roots. They were identified following the classical criteria as being either tendon organ or primary or secondary muscle spindle afferents. The unit discharges were controlled on the oscilloscope and fed into frequency-tovoltage converters displaying analog curves with ordinates proportional to the input Brain Research, 40 (1972) 165--169
C. PERRET AND P. BUSER
TA IaTA II TA Ec
Fig. 1. Activity of two spindle afferent fibres from tibialis anterior during rhythmic movements of the opposite limb. TA, strain gauge recording of tibialis anterior contractions (contraction upwards); la TA, 1I TA, frequency curves of primary and secondary endings (increase upwards); F_c, strain gauge recording of opposite limb movements (extension upwards). Note: spindle endings discharge even in absence of TA contraction; absence of pause during TA contraction; la and I1 frequency curves closely similar.
frequency. Records were taken either from a Brush 6 channel ink-writer or from the oscilloscope. (A) Evidence ~?Ffusimotor activity in[texors. Fig. I shows a typical example obtained from tibialis anterior. Contractions of this flexor muscle follow a stereotyped pattern of alternation, i.e., they occur during contralateral extension ('Ec'). But probably beca'.Tse of deafferentation, these contractions do not appear at each Ec. However inspection of the frequency curve of spindle la and 11 afferents shows rhythmic increases occurring at each Ec whether or not there is activity in the corresponding muscle: when the latter does contract, the increase in afferent discharge begins before and persists during and after the contraction period, even for strong contractions in isotonic conditions. In only a few cases did the spindle discharge stop during spontaneous contractions, although it always stopped when an electrical stimulation of the muscle nerve was delivered in order to identify the afferent as being of spindle origin. The conclusion to be drawn is that rhythmic gamma activity occnrs in the nerve to tibialis anterior during movements of the contralateral intact limb. The activity either occurs alone or preceding the alpha discharge and so it fully compensates for the pause that would otherwise occur due to contraction of the muscle. That these effects are not due to some incidental repercussion of the contralateral movements on proprioceptors of the muscle is indicated by the following facts: (a) no increased discharge was ever observed in tendon afferents from the muscle when it did not contract; (b) direct recordings of efferent activity in a filament from the proximal cut end of the motor nerve (the main part of the nerve remaining intact) showed small spikes accelerating together with Ec, even when the muscle itself did not contract; large spikes appeared precisely when contractions occurred: it is very likely that the small spikes were g a m m a and the large ones alpha: (c) through direct recording from the surface of the tenuissimus muscle, small potentials can be obtained e which have been identified as being intrafusal potentials due to fusimotor activity. We could Brain Research, 40 (1972) 165 169
FUSIMOTORACTIVITYIN LOCOMOTORMOVEMENTSIN CA7
NP NP ,o
E c - - ~
, , , v "
Fig. 2. 'Muscle potentials' recorded from the surface of tenuissimus (upper trace) during movements of the opposite limb (Ec, extension upwards). A, Oscillographic identification. Upper picture: polyphasic propagated intrafusal potentials (static, P) and extrafusal discharge. Lower picture! monophasic, non propagated intrafusal potentials (NP) and extrafusal discharge. B, Ink-writer recording of P potentials (upper picture) and NP potentials (lower picture, filtering used for adequate pen recording). Note: both types of potentials show increased frequency during Ec; NPs have a lower range of frequency than Ps.
Fig. 3. Activity of a primary spindle afferent from gastrocnemius medialis at the end o1 a sequence of movements of the opposite limb. GM, strain gauge recording of gastrocnemius contractions (contraction upwards); Ia GM, frequency curve of spindle ending (increase upwards); Fc, strain gauge recording of opposite limb movements (flexion upwards). Note: spindle ending discharge even in absence of GM contraction (on the right); between two successive arrows, frequency curve shows an increase which is soon partly interrupted by a decrease during GM contraction; no such cornplexity exists when contractions are absent (right end of picture). observe these potentials (cJ~ *) and record their rhythmic increases in frequency during Ec, either when they occurred alone or when they preceded large spikes which appeared only when a contraction occurred (extrafusal potentials). (B) Identification of the type of fusimotor activity in flexors. These findings raise the question whether the observed fusimotor activity is of the static or o f the dynamic type. Several data indicate that we are actually dealing with static activity: (a) Fig. 1 shows the simultaneous recording o f a primary and of a secondary spindle afferent o f tibialis anterior. Since secondary endings are devoid of dynamic control (see e.g. ref. 1) we may assume that the g a m m a action which is responsible for variations in spontaneous frequency and for the absence of the pause as described above is o f the static type in secondary endings. This is probably also the case in primary endings, for it can be seen that they behave in exactly the same way. (b) Fig. 2A illustrates the two types of intrafusal potentials obtained by a systematic point to point surface recording from the tenuissimus: polyphasic propagated
Brain Research, 40 (1972) 165-169
C. PERRETAND P. BUSER
ones (P) due to static fusimotor fibres* and small monophasic non-propagated ones (NP) due either to static or to dynamic fibres ~. Both types of potentials showed rhythmic accelerations during Ec as mentioned above, thus indicating at least a participation of static fusimotor fibres. Concerning NP potentials, the fact that they show a much lower frequency of discharge than P potentials (Fig. 2B) suggests (but does not demonstrate) that they are of a different nature than P potentials, i.e., dynamic. (C) Evidence offusimotor activity in extensors. Fig. 3 is a typical example of recordings performed with gastrocnemius medialis using the same methods as for tibialis anterior. Similarities and differences are evident: (a) even in the absence of contraction, an activation of the spindle ending can be observed that is synchronous with contralatera[ flexion, as expected from the alternation pattern; (b) this activation is presumably of static origin as, here again, primary and secondary (not shown) endings behave in the same way; (c) when the muscle contracts, the spindle frequency curve displays a complex and variable shape; the initial acceleration is interrupted by a decrease. This is presumably due to only partial compensation of the pause by gamma activity even when the contraction is weak. The same is true in isometric conditions. (D) Further stud)' of dynamic fushnotor activiO'. In order to search for a possible dynamic action, we compared the amplitudes of the velocity response of primary afferents to sinusoidal stretch 3 of the muscle at a frequency of 5/sec, at rest and during movements of the opposite limb**. With this method it could be shown that an important dynamic fusimotor action takes place in gastrocnemius, together with the static one, during contralateral flexion, whereas this dynamic effect appears unimportant for tibialis.
Conclusion Using spontaneous locomotor activity of a deafferented hindlimb in decorticate cats, we could show that: (a) in flexors (tibialis anterior and tenuissimus) and in extensors (gastrocnemius and soleus), there is an alpha-gamma linkage; (b) gamma activation usually precedes alpha activation in time; (c) in our experimental conditions, gamma activation can occur alone in the absence of alpha activation; (d) there are indications of simultaneous static and dynamic fusimotor activity: (e) quantitative differences appear, however, between the two functional types of muscles; the static action is important, and possibly occludes the dynamic one, in flexors whereas a strong dynamic action occurs in extensors in addition to a weak static effect. * These potentials were identified as efferent potentials: (I) because they did not respond to passive stretch of the muscle; (2) because identical potentials could be elicited at the same muscle point by stimulating isolated gamma fibres identified as such in the distal cut end of the ventral roots at the end of the experiment. ** These experiments, carried out with Dr. Berthoz, will be described elsewhere.
Brain Research, 40 (1972) 165-169
FUSIMOTOR ACTIVITY IN LOCOMOTOR MOVEMENTS IN CAT
I APPELBERG, B., BESSOU, P., AND LAPORTE, Y., Effects of dynamic and static fusimotor gamma fibers on the responses of primary and secondary ending belonging to the same spindle, d. PhysioL (Lond.), 177 (1965) 29-30 P. 2 BESSOU, P., ET LAPORTE, Y., Potentiels fusoriaux provoqu6s par la stimulation de fibres fusimotrices chez le Chat, C.R. Acad. Sci. (Paris), 260 (1965) 4827-4830. 3 CROWE, A., AND MATTHEWS, P. B. C., Further studies of static and dynamic fusimotor fibres. J. Physiol. (Lond.), 174 (1964) 132-151. 4 EULER, C. VON, AND PERE'I~I, G., Dynamic and static contributions to the rhythmic gamma activation of primary and secondary spindle endings in external intercostal muscles, J. PhysioL (Lond.), 187 (1966) 501-516. 5 PERRET, C., Relations entre activit6s eff6rentes spontan&s de nerfs moteurs de la patte posterieure et activit6s de neurones du tronc c6r~bral chez le chat d6cortiqu6, J. Physiol. (Paris), 60, SuppL 2 (1968) 511-512. 6 SEVERIN, F. V., ORLOVSKII, G. N., AND SHIK, M. L., Work of the muscle receptors during controlled locomotion, Biophysics, 12 (1967) 575-586. (Translated from Russian.)
Brain Research, 40 (1972) 165-169