Neuroscience Letters, 19 (1980) 213-217 213 © Elsevier/North-Holland Scientific Publishers Ltd.

SEGMENTATION OF H U M A N SPINDLE A N D EMG RESPONSES TO SUDDEN MUSCLE STRETCH

K.-E. HAGBARTH, R.R. YOUNG, J.V. HAGGLUND and E.U. WALLIN

Department of Clinical Neurophysiology, University Hospital, S-750 14 Uppsala (Sweden)

(Received May 5th, 1980) (Revised version received May 27th, 1980) (Accepted May 28th, 1980)

SUMMARY

Grouping of the EMG response produced by quick stretches of contracting muscles has been thought to reflect 'long loop reflexes' through cerebral cortex adding to the segmental stretch reflex. Our recordings from human muscle spindle afferents responding to such stretches show that these discharges also tend to be grouped. EMG grouping may therefore be a consequence of successive segmental reflexes rather than of additional delays in long loop reflex arcs.

Sudden displacements at a primate or cat limb joint produce segmentation of ongoing electromyographic (EMG) activity in stretched muscles provided there is voluntary background drive on the motoneuron pool. All investigators assume that the initial burst represents the segmental spinal stretch reflex, but the origin of the later responses is less clear-cut. On the basis of indirect evidence, the second EMG burst, with a latency shorter than the reaction time, has been assumed to be reflexly mediated by a loop through cerebral sensorimotor cortex [4, 12, 13]. A third burst, with latency close to the reaction time, has also been denoted a 'long loop cortical reflex' by some authors, but by others is called a 'voluntary' or ' intended' response [5, 10, 14]. Latencies of these EMG bursts are always measured from the start of the stretch movement; the main effective stimulus is implicitly assumed to be a simple one occurring at the beginning of the dynamic change.

In cats, Ghez and Shinoda [6] found that segmentation of EMG response could be elicited by sudden limb displacements in decerebrate and spinal preparations. They

concluded: 'receptor properties and /or spinal mechanisms involved in the stretch reflex are sufficient to produce a segmented (EMG) response similar to that observed in intact animals.'

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The present study recorded for the first time the afferent input required to elicit 'long loop reflexes'. In 3 healthy human subjects, different methods produce rapid angular displacements at the wrist, while afferent stretch responses were recorded with microelectrodes inserted in median (or radial) nerve fascicles [17]. In some experiments, a hydraulic motor, its drive-axis attached to the splinted hand, produced ramp extension movements, the speed and amplitude of which could be varied [11]. Flexion movements were produced when recordings were made from radial nerve fascicles supplying wrist extensors. A low inertia goniometer, containing a conductive-plastic-element potentiometer with an essentially infinite resolution, was Used to monitor wrist position; a strain gauge monitored force between hand and motor. As a rule, the sudden extension movements had speeds of 100-200°/sec and amplitudes of 10-20 °. Such movements always caused grouped discharges in muscle afferents, two or three bursts of afferent impulses occurring during stretching (Fig. 1A, F). One or two additional bursts often occurred when the movement was suddenly arrested. With quick discrete movements, final decelerative forces may be high and one is not surprised to find afferent bursts at the sudden stop of a fast movement, where overshoots in length with 'bouncing' appear to be inevitable.

Grouping of afferent neural discharge was most pronounced when subjects maintained a weak or moderate contraction in wrist flexors, but was also seen during relaxation. Multiunit afferent bursts during the stretch phase, recurring at intervals of 20-30 msec and separated by periods of relative neural silence, were closely time-locked to mechanical oscillations sensed by the strain gauge (Fig. 1A). It was initially assumed that these 'vibrations' arose in the mechanical system attached to the hand. However, with the stretch movements employed, it was not possible to eliminate the vibrations or the grouping of neural discharges either by altering the mass or spring-constant of this system. Neither could one significantly alter their frequency or the repetition rate of neural bursts during stretching.

In other experiments, similar muscle stretches were produced by a brisk voluntary twitch of antagonist muscle groups (Fig. 1B), by suddenly increased manual forces delivered to the hand through a spring (Fig. 1C), by a weight dropped into the palm of the hand (Fig. 1D), or by acceleration due to gravity during relaxation after an electrically induced twitch of wrist flexors (Fig. 1E). No matter how wrist displacements were produced, grouped afferent discharge was regularly seen during stretch with at least two neural bursts separated by an interval of 20-30 msec. With highly amplified goniometer and accelerometer signals, these neural bursts were often correlated with small irregularities in speed of movement. Especially prominent 'notches' or 'angles' in the goniometer trace were seen following very

sudden increments in force, such as those caused by weights dropped onto a shock- absorbing material placed in the palm of the hand to avoid 'bouncing' of the weight (Fig. 1D). Segmentation of neural discharge during stretching could be avoided only if actual muscle lengthening was very small.

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A B C D E

F G H

50ms

Fig. 1. Grouping of muscle spindle afferent responses (upper trace) from wrist flexors during fast extension movements of the wrist, produced in different ways (E, an exception, shows spindle response from wrist extensors during a wrist flexion movement). Angular displacement shown by goniometer signal on second trace in A - E and third trace in F-H; stretch movement downwards. All, except E, are rectified nerve signals from multi-unit recordings. F - H (second trace) also show corresponding grouping of rectified EMG from flexor muscles during moderate voluntary contraction (F) or almost complete relaxation (G and H). A, D, F and H are superimpositions of 3-5 individual recordings; B, C and G are single recordings. A and F: ramp-stretch by hydraulic machine; note the relatively smooth ramp movement with marked oscillations in the torque signal (bottom trace) which correlate with grouping of afferent discharges. Also note the multiple EMG bursts in F follow nerve discharges with an approximate delay of 25 msec (arrow). B: voluntary fast extension of wrist. C and G: extension produced by sudden pull on spring attached to the hand. D and H: extension produced by falling weight striking the palm of the outstretched hand. The notch in the goniometer trace, corresponding to a pause in the spindle discharge, is attributable to high viscous resistance following an initial phase of low elastic resistance [8]. E: single-unit spindle discharges in radial nerve during the stretch phase after an electrically induced twitch of the forearm extensor muscles. This afferent unit fired during one or both of two discrete periods on the falling phase of tension; in 20/25 of these superimposed successive twitches it fired twice. Certain spindle primary endings may respond to mechanical fluctuations later during stretch than responses caused by the beginning of stretch. Vertical goniometer calibration is 20 ° in A, B, E and F and 10 ° in C, D, G and H.

Provided there was background contraction in wrist flexor muscle, EMG responses to stretches such as those illustrated in Fig. 1A-E were likewise grouped (Fig. 1F-H). Allowing for a minimum 20-25 msec monosynaptic stretch reflex delay in human forearm muscles, correspondence between afferent and efferent bursts was often observed (Fig. IF). Individual EMG bursts were sometimes missing; when flexor muscles were relaxed, there was generally only one EMG burst present (Fig. 1G).

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Techniques for identifying primary spindle afferents in single unit recordings have been described [17]. An advantage with multiunit recording techniques (as compared to single unit recordings) is information about synchrony of discharges in group Ia fibers. Following is evidence that the multiunit afferent bursts described are dominated by discharge from primary muscle spindle endings: (i) similar groupings of afferent impulses were seen in both multiunit and single unit records from group 1A afferents (Fig. 1E). As with single unit group Ia impulses, multiunit discharges appeared during the falling phase of electrically induced extrafusal twitches and not during the initial phase of rising tension; (ii) weak mechanical taps on the muscle itself or its tendon were always sufficient to evoke distinct multiunit afferent bursts, increasing in strength during evolving muscle stretch. Primary muscle spindle endings are known to be very sensitive to minute mechanical perturbations (e.g. vibration), especially when the muscle is being stretched [2].

Though grouping of spindle responses during sudden angular displacements may appear to be artifactual, its occurrence with each stretching technique employed suggests that grouping depends on some inherent mechanical property within the limb. Grouping must be unrelated to reflex activity since, for the stretches employed, reflex torque changes did not start before the stretch movement ended. Step changes in compliance, unrelated to reflex activity, are known to occur when an isometrically contracting muscle is suddenly lengthened [8] and similar non- linearities in muscular compliance have also been demonstrated in relaxed muscle [9]. Neither we (Fig. 1) nor others, to judge by published figures [3], have succeeded in eliminating these mechanical irregularities during stretching.

In conclusion, brisk angular displacements of hand at wrist produce bursts of grouped spindle impulses. This grouping should be considered in framing hypotheses to explain segmentation of the EMG responses. Primary spindle endings, with non-linear dynamic sensitivity [7, 15, 16], respond with particular accuracy to those minute fluctuations in speed and force that occur during fast stretch movements. These 'vibrations' may arise in part because of non-linearities in joint or muscle compliance, even with stretches produced by smoothly increasing torque. In addition to groups of afferent spindle discharge, which appear to result in successive segmental stretch reflexes, other segmental mechanisms may facilitate synchronized oscillatory activity of motoneurons. Inhibitory input from Golgi tendon organs responding to stretch of an already contracting muscle, after- hyperpolarization caused by synchronous firing and recurrent inhibition all tend to produce hypoexcitable periods in the motoneuron pool following synchronous discharge. There is also recent evidence that sequential EMG bursts may result from reflex excitation of separately responding motoneuron 'subpopulations' [1].

Our findings do not exclude the operation of 'long loop reflexes' but such reflexes are probably not the main source of successive EMG responses to an apparently simple stretch stimulus.

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ACKNOWLEDGEMENTS

S u p p o r t w a s p r o v i d e d b y t h e S w e d i s h M e d i c a l R e s e a r c h C o u n c i l ( P r o j e c t s

B 7 9 - 1 4 X - 0 2 8 8 1 - 1 0 B , K 7 9 - 1 4 V - 5 5 3 2 - 0 1 ) . T h i s r e s e a r c h w a s c a r r i e d o u t w h i l e R . R .

Y o u n g was o n s a b b a t i c a l l eave f r o m t h e c l in ica l N e u r o p h y s i o l o g y L a b o r a t o r y ,

D e p a r t m e n t o f N e u r o l o g y , M a s s a c h u s e t t s G e n e r a l H o s p i t a l a n d H a r v a r d M e d i c a l

S c h o o l , B o s t o n , as a F a c u l t y S c h o l a r , J o s i a h M a c y , J r . F o u n d a t i o n , N e w Y o r k

C i ty .

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