Brain Research, 160 (1979) 529-532 © Elsevier/North-Holland Biomedical Press
Excitation of dynamic fusimotor neurones of the cat triceps surae by contralateral joint afferents
B. APPELBERG, M. HULLIGER, H. JOHANSSON and P. SOJKA Department of Physiology, University of Umed, S-901 87 Umed (Sweden)
(Accepted October 5th, 1978)
In recent experiments the reflex inputs from peripheral nerves to gamma motoneurones were investigated. The cells were classified as static or dynamic using weak electrical stimulation in a mesencephalic region known to selectively control dynamic spindle sensitivity 2. Electrically evoked reflex effects were studied in these cells with extra- or intracellular recording. It was found that group II (but only rarely group I) fibres and also low threshold skin and joint afferents exerted a potent excitatory influence on dynamic gamma cells innervating extensor muscles 3. With regard to the mechanisms concerned in the control of normal movements it seemed desirable to examine whether natural stimulation of these afferents could also excite dynamic fusimotor neurones to the triceps surae. The present experiments were performed on cats which were lightly anaesthetized, usually with chloralose (50-55 mg/kg). Gastrocnemius-soleus (GS) (occasionally soleus (S) alone) and posterior biceps semitendinosus (PBSt) muscles were prepared with intact nerve supply. The muscles were connected to two separate electromagnetic pullers for the application of controlled stretches. The hip and the hind limb, particularly the tibia, were rigidly fixed in a metal frame. Apart from GS and PBSt the whole limb was extensively denervated. Functionally single units were isolated from thin filaments of otherwise intact L7 and $1 dorsal roots and classified as primary or secondary afferents on the basis of their conduction velocity (division line at 72 m/sec). The ventral roots were not interfered with. The possible excitation ofextrafusal motor units was assessed by recording gross E M G activity with surface electrodes placed on the muscle bellies (GS or S). Any alteration of fusimotor activity was assessed indirectly by monitoring the responses of spindle afferents to large amplitude ramp (8 mm at 10 mm/sec) and sinusoidal (1 or 2 mm at 1 Hz) stretching. The responses to a number of successive stimuli (5 or 10) were averaged on line by constructing cycle histograms with the aid of an averaging computer (Didac 800, lntertechnique). The numerical analysis was also performed on line with a desk calculator (HP 9810A) which was linked to the averaging device. Ramp responses were quantified by measuring the dynamic index and the mean rate of firing 1°. The averaged responses to sinusoidal stretching were assessed by
530 fitting a simple sinusoid using a least square algorithm which ignored periods of afferent silence 8. Based on earlier investigations with controlled electrical stimulation of functionally single gamma fibres 1,6,s-]° the occurrence of predominantly dynamic fusimotor reflex activation was inferred when the following criteria were met: (1) increase of the dynamic sensitivity of primary afferents, with the dynamic index of ramp responses and/or the depth of modulation of responses to sinusoidal stretching clearly raised above the levels of the control responses; (2) moderate increase of the maintained rate of firing during the static phase of the ramp and hold stretches and/or moderate increase of the means fitted to the sinusoidal responses; (3) occurrence of afferent silence during the release phase of both ramp and sinusoidal stretching; and (4) manifestation of spindle excitation with primary but not with secondary afferentsl, 1°. Relying on these criteria the occurrence of appreciable dynamic fusimotor excitation could be demonstrated during static stretching of the ipsilateral PBSt muscles. Given the intracellular findings this excitation can be attributed to secondary spindle afferents, as will be argued in a more detailed report on these findings (present authors, in preparation). Using the same method of sensitivity testing it was incidentally discovered that full extension of the contralateral hind limb also increased the dynamic sensitivity of primary afferents from the ipsilateral triceps or soleus. The effects were both consistent and large, since it was regularly found that the parameters of dynamic sensitivity easily could be doubled. This is illustrated with the ramp responses of Fig. 1, when extension of the contralateral joints increased the dynamic index by a factor of about two. Similarly, the depth of modulation of the responses to sinusoidal stretching (Fig. 2A) was approximately doubled when the contralateral hind limb was fully extended. The effects were found both before and after spinalization at L3 (cf. Fig. 2A) and they were mainly studied in spinal preparations (5 animals). Routine checks of the EMG record
ANTAGONIST RELEASED 150
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Fig. 1. Cycle histograms with averaged responses (5 cycles) of a primary spindle afferent to ramp stretches applied to triceps muscle (bottom row). Left: contralateral hind limb in resting position. Right: full extension of the contralateral hip, knee and ankle. Spinal preparation.
TEST: JOINTS EXTENDED
EFFECTOF PRESSURE ON KNEEJOINT TEST
KNEE JOINT \ / ~ UNANAES- ) ( ~ THETIZED
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Fig. 2. Responses of primary spindle afferent to sinusoidal stretching (1 mm at 1 Hz) of triceps (same unit as in Fig. 1). A: cycle histograms with averaged responses (10 cycles). Left, contalateral hind limb in resting position. Right, full extension of contralateral hip, knee and ankle. Top row, prior to spinalization, with PBSt released. Bottom row, after spinalization at L3, now with PBSt stretched in order to obtain tonic inhibition (cf. Fig. 1) leading to comparable control responses. B: scatter diagram of controls versus test responses for both mean (circles) and modulation (triangles) of the best fitting sinusoid (responses averaged over 10 cycles). For each pair of responses mean and modulation are connected by a straight line. Same unit as in A, after spinalization. For further details see text.
showed that these effects were not accompanied by extrafusal activity. The excitation observed with contralateral limb stretching cannot be attributed to some accidental mechanical coupling, since it disappeared with contralateral denervation, during deep anaesthesia, or sometimes with postoperative deterioration of the spinal cord. The fusimotor excitation from the contralateral hind limb was largely confined to primary afferents. Of 42 primary afferents, 25 exhibited effects which fulfilled the criteria of predominant dynamic fusimotor excitation (cf. above). Only 1 out of 9 secondary afferents showed weak excitation affecting the mean rate of discharge rather than the depth of modulation of sinusoidal responses. In contrast to the ipsilateral side, the contralateral hind limb was normally not denervated. The observed effects might therefore have been mediated by either skin, muscle or joint afferents, or they might have been due to convergence of excitatory inputs from these categories. Evidence could be obtained suggesting that joint afferents are certainly contributing to the dynamic fusimotor excitation elicited from the contralateral hind limb. Fusimotor excitation could be obtained in separate experiments with two kinds of tests: firm pressure was applied to the joint capsule of either the knee (cf. Fig. 2B) or the ankle. This procedure was chosen since capsular strain has been shown to excite joint afferents effectively~. It was ensured that these manoeuvres were not accompanied by joint movements which might have caused muscle stretch. With either test the pressure-induced excitation disappeared when joint afferents could no longer be excited. In the case of the knee (Fig. 2B) this was achieved
532 by intra-articular injection of local anaesthetic (20 mg Xylocard). This abolition was not attributable to any non-specific reduction of reflex excitability, since plantar flexion of the contralateral foot still evoked an equally large increase in dynamic sensitivity as before anaesthesia of the knee. In the case of the ankle any contribution from cutaneous afferents had been excluded from the beginning by completely removing the skin from the contralateral hind limb. The pressure induced reflex excitation was abolished by denervation of the ankle joint. Again, this was not due to a non-specific reduction of excitability of fusimotor neurones, since the dynamic sensitivity of primary afferents could still be increased by vibration of the contralateral hind limb in the popliteal area, the size of the effect being the same as prior to denervation. The present findings show that proprioceptive afferents, for which readily understandable spinal functions so far have been missing, exert powerful excitatory effects on dynamic fusimotor neurones. The excitation from ipsilateral secondary spindle afferents may well help to achieve a high gain in the stretch reflex loop when this is desirable, e.g. when large or unexpected loads have to be overcome. The excitation from contralateral joint afferents may be particularly valuable for the coordination of bilateral motor activity, as e.g. in locomotion. This fits in with the well known properties of joint afferents, which are mainly excited at extreme joint angles 4 and during contraction of muscles straining the joint capsule 7. This work was supported by the Swedish Medical Research Council, Project 03873, by Gunvor and Josef An6rs Stiftelse and by the Swiss National Foundation (M.H., Grant 831.445.76). We wish to thank Mrs Gerdy Kristr6m and Mr G6ran Westling for valuable technical assistance. 1 Appelberg, B., Bessou, P. and Laporte, Y., Action of static and dynamic fusimotor fibres on secondary endings of cat's spindles, J. Physiol. (Lond.), 185 (1966) 160-171. 2 Appelberg, B. and Jeneskog, T., Mesencephalic fusimotor control, Exp. Brain Res., 15 (1972) 97-112. 3 Appelberg, B., Johansson, H. and Kalistratov, G., The influence of Group II muscle afferents and low threshold skin afferents on dynamic fusimotor neurones to the triceps surae of the cat, Brain Research, 132 (1977) 153-158. 4 Burgess, P. R. and Clark, F. J., Characteristics of knee joint receptors in the cat, J. PhysioL (Lond.), 203 (1969) 317-335. 5 Clark, F. J., Information signalled by sensory fibres in medial articular nerve, J. Neurophysiol., 38 (1975) 1464-1472. 6 Emonet-Denand, F., Laporte, Y., Matthews, P. B. C. and Petit, J., On the subdivision of static and dynamic fusimotor actions on the primary ending of the cat muscle spindle, J. Physiol. (Lond.), 268 (1977) 827-861. 7 Grigg, P., Mechanical factors influencing response of joint afferent neurones from cat knee, J. Neurophysiol., 38 (1975) 1473-1484. 8 Hulliger, M., Matthews, P. B. C. and Noth, J., Static and dynamic fusimotor action on the response of Ia fibres to low frequency sinusoidal stretching of widely ranging amplitude, J. Physiol. (Lond.), 267 (1977) 811-838. 9 Hulliger, M., Matthews, P. B. C. and Noth, J., Effects of combining static and dynamic fusimotor stimulation on the response of the muscle spindle primary ending to sinusoidal stretching, J. Physiol. (Lond.), 267 (1977) 839-856. 10 Matthews, P. B. C., Mammalian Muscle Receptors and Their Central Actions, Arnold, London, 1972, Chapt. 5.