J. Physiol. (1977), 267, pp. 839-856 With 9 text-figure8 Printed in Great Britain

839

EFFECTS OF COMBINING STATIC AND DYNAMIC FUSIMOTOR STIMULATION ON THE RESPONSE OF THE MUSCLE SPINDLE PRIMARY ENDING TO SINUSOIDAL STRETCHING

BY M. HULLIGER,* P. B. C. MATTHEWS AND J. NOTHt From the University Laboratory of Physiology, Parks Road, Oxford OX1 3PT

(Received 27 October 1976) SUMMARY

1. A pair of fusimotor fibres, one static and the other dynamic, were stimulated simultaneously to test their combined action on the response of muscle spindle primary endings in the cat soleus to sinusoidal stretching. A frequency of 1 Hz was chiefly used, with a wide range of amplitudes (10 ,um-2 mm). The response of the ending was assessed from the parameters of the sine fitted to its firing averaged throughout the course of the cycle; this was felt useful even though the responses to the larger stretches showed certain non-linear features. 2. With small stretches (up to about 50 dm amplitude) static action dominated, and the modulation of firing during combined stimulation was little or no larger than that found during the static stimulation on its own, and much smaller than that found during the dynamic stimulation. The phase of the response was, however, much the same for all three

conditions. 3. With larger stretches the modulation with combined stimulation was intermediate between the values found on stimulating either fusimotor fibre on its own; the dynamic contribution increased progressively with the amplitude of stretching. 4. With larger stretches the phase of the response during combined stimulation was appreciably closer to that for static action than to that for dynamic action. But the differences between the various conditions were small (below 200) and seem attributable to various distortions of the response wave form away from a true sinusoid, rather than betokening a * Present address: Department of Physiology, UmeA University, S-90187 UmeA, Sweden. t Present address: Neurologische Klinik Mit, Abtellung fur Hansastr. 9, D-78 Freiburg, W. Germany.

Neurophysiologie,

840 M. HULLICER, P. B. C. MATTHEWS AND J. NOTH difference in the ratio of velocity to length sensitivity under the various conditions. This view was supported by the effects on phase of grading the rate of stimulation of one fusimotor fibre while holding that of the other constant. 5. Detailed comparison of the cycle histograms obtained under different conditions showed an interestingly asymmetrical pattern of summation and occlusion of the effects of the two kinds of fusimotor fibre. At the peak of the response to a large stretch static action summed with dynamic action, which was here the stronger, so that at this phase of the cycle the firing was greater with the combined stimulation than with either fibre on its own. But, in the trough of the response to the same stretch static action occluded any dynamic action, which was now the weaker, so that at this phase of the cycle the firing with combined stimulation was virtually the same as that with static stimulation on its own. With a small stretch, static action normally occluded dynamic action throughout the cycle; this is in line with the firing during static action now usually being greater than that during dynamic action for all phases of the cycle. INTRODUCTION

The preceding paper (Hulliger, Matthews & Noth, 1977) describes the effects of stimulating single fusimotor fibres on the response of muscle spindle primary endings to low-frequency sinusoidal stretching of a wide range of amplitude. In spite of complexities introduced by the non-linear behaviour of the ending with the larger stretches the findings supported the view that static and dynamic fusimotor action differ principally in their effect on the absolute value of the sensitivity of the ending to such stretching (i.e. gain), rather than in any small differences they produce in the relative value of velocity- and/or acceleration-sensitivity to length sensitivity (i.e. phase). Since under physiological conditions fusimotor fibres must often fire in combination it seemed desirable to extend the previous study by simultaneously stimulating a pair of fusimotor fibres, one static and the other dynamic. This has provided further support for the above view, and at the same time has demonstrated an interestingly asymmetrical pattern of summation and occlusion of static and dynamic effects at different phases of the sinuosidal cycle for large amplitude (cf. Lennerstrand, 1968). All this bears on the general question as to how far fusimotor interaction produces an intermediate effect or whether one or other type of action can dominate.

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841

METHODS

The methods have been fully described in a preceding paper based upon the same series of experiments (Hulliger et al. 1977). Twelve pairs of fusimotor fibres, each consisting of a typical static and a typical dynamic fibre operating on the same ending, have been studied in twelve anaesthetized cats using the soleus muscle; one of the dynamic fibres was a fi fibre rather than a y fibre. Each fusimotor fibre was activated by its own stimulator and care was taken to avoid cross-stimulation. Each member of a pair was stimulated both alone and with its partner while the muscle was stretched sinusoidally at amplitudes up to 2 mm. The resulting response of the primary afferent was analysed with a PDP 12 computer by constructing a cycle histogram, giving the average number of spikes throughout the course of the sinusoidal cycle, and fitting this with a sine of the same period; the parameters of this sine were taken as the measure of the response. As before, the empty bins corresponding to a period of afferent silence on the falling phase of the stretch were ignored in the fitting procedure. The majority of observations were taken with 1 Hz stretching (amplitude of 10 ,um-2 mm), but additional observations have been made commonly using frequencies down to 0.1 Hz and sporadically up to 4 Hz. The rates of stimulation of the two fibres were in the range 40-130/sec, and were adjusted relative to each other so that the mean increase of firing should not be too unequally matched in the two cases. On average, the dynamic fibres were stimulated at a slightly higher rate than the static fibres. In obtaining systematic data the frequency of stretching was set first and the amplitude increased in steps from zero upwards; this was done separately for each mode of activation in the order: passive, dynamic, static, combined. At the end of such a full run at a given frequency the responses at a few amplitudes were checked to ensure consistency; the superimposed histograms of Figs. 7-9 were obtained from such constant-amplitude controls.

RESULTS

Fig. 1 shows the characteristic effect of combining the stimulation of a static and of a dynamic fibre on the response of a primary ending to large amplitude stretching. During the combined stimulation the static action dominates during the falling phase of the stretch, corresponding to the trough of the response, and so prevents the ending falling silent, while the dynamic action dominates during the rising phase. Thus the depth of modulation of firing during the combined stimulation is greater than that during static stimulation. But equally it is below that found during dynamic stimulation alone, because in comparison with the latter the trough of the histogram is shifted up more than the peak. The amplitude of the fitted sinusoid provides an acceptable measure of these changes in modulation, even though the various histograms are not strictly sinusoidal (Hulliger et al. 1977). Fig. 2A shows the effect of a range of amplitudes of stretching on the depth of modulation. At amplitudes above 250 sum the curve obtained with the combined stimulation runs between the two curves for the individual fusimotor actions, in parallel with the dynamic.

842

M. HULLIGER, P. B. C. MATTHEWS AND J. NOTH A Static

B Both static and dynamic

C Dynamic

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Fig. 1. Cycle histograms showing the effect of combining the stimulation of a static and of a dynamic fibre on the response of a primary ending to 1 Hz sinusoidal stretching of large amplitude (700 ,um, half peak to peak). A, during stimulation of a single static fibre at 100/sec. C, during stimulation of a single dynamic fibre at 87/sec. B, during their combined stimulation at the same rates. The sinusoids are fitted to the data by the method of least squares. 360° on the abscissa corresponds to the point of maximum extension.

But at amplitudes below 100 ,um the combined curve is virtually the same as the static curve, and there is little sign of any extra contribution from the dynamic fibre. In the phase plots of Fig. 2B, the combined action is similar to the static action throughout the whole range studied. Fig. 3 emphasizes that for larger stretches the ending behaved nonlinearly, particularly during dynamic and combined stimulation. As detailed earlier (Hulliger et al. 1977), non-linearity is shown by the increase with amplitude of the R.M.S. deviation of the fitted sine from the cycle histogram, and by the increasing value of the mean level of the fitted sine. The effects during the combined stimulation can be seen to be broadly comparable to those found during dynamic stimulation. In this case, as was usual, the R.M.S. deviation was just greater for the dynamic stimulation than for the combined stimulation (mean values of twelve experiments with 1 Hz, 1 mm stretching 11-8 + 3-5 S.D. and 10-4 + 5.7 impulses/sec respectively). The similarity is notable because on cursory inspection the characteristic flattening of the trough of the histogram for combined action presents such an obviously non-linear feature; but in quantitative terms it would appear to be no worse than the usual asymmetry between rising and falling phases of the response during dynamic stimulation which no longer manifests itself to the same extent during combined stimulation. The rise of the mean level of the fitted sine with amplitude for the combined action is unsurprising, for it indicates that with increasing amplitude of movement the peak of the histogram continues to rise, as it does for dynamic stimulation on its own, whereas the trough remains at a nearly constant level, as it does during static stimulation on its own. Fig. 4 systematizes these findings by displaying the mean values for

843 COMBINED FUSIMOTOR STIMULATION twelve pairs of endings with 1 Hz stretching. With restriction of the stretching to the linear range essentially similar results were obtained for frequencies of 03, 4 and 15 Hz on four occasions for each. The collective amplitude-response curves of Fig. 4A again show the essential features noted for the example of Fig. 2A. In addition, the mean curve for modulation during combined stimulation can be seen to be appreciably more linear than either of the curves for individual stimulation, but such apparent linearization of the spindle was not supported by the other parameters of the response. Fig. 4B emphasizes the way in which the combined response starts, at small amplitudes, by being virtually the same as the response 75 I--U

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Fig. 2. The effect of the amplitude of stretching (at 1 Hz) on the depth of modulation and on the phase of the afferent response, as given by the parameters of the fitted sine, for combined fusimotor stimulation in comparison with the effect of stimulating either fibre on its owa. Same experiment as Fig. 1 (same symbols in A and B for corresponding modes of

activation).

844 M. HULLIGER, P. B. C. MATTHEWS AND J. NOTH during static stimulation and then, with increasing amplitude, progressively rises above the static curve and eventually attains some 2/3 of the dynamic value. It should be noted, however, that occasionally the small amplitude response during combined stimulation was actually slightly below the static value (this appeared to have arisen from adventitious effects associated with a tendency to 'driving' of the afferent by the fusimotor stimulation which became more secure during the combined stimulation). The static curve for relative modulation (0, Fig. 4B) also shows that irrespective of the amplitude of stretching the average modulation during static stimulation was always about a quarter of the modulation during dynamic stimulation. This suggests that the two mean curves of absolute modulation (Fig. 4A, 0, LI) for static and dynamic action have 15

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Fig. 3. Manifestations of non-linearity. The effect of the amplitude of stretching, A, on the root mean square (R.M.S.) deviation of the fitted sine from the histogram and, B, on the mean level of the fitted sine, both for the experiment of Fig. 2. See text.

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Fig. 4. Averaged results to illustrate the consistency of the progression, during combined stimulation, from a static domination for small amplitudes of stretching to an intermediate pattern for large amplitudes of stretching. Data from 12 primary endings for each of which a static and a dynamic fibre were stimulated both separately and in combination during 1 Hz stretching. A, amplitude-response curves. B, depth of modulation at each amplitude expressed relative to that during dynamic fusimotor stimulation; this ratio was determined for each individual ending before the averaging. C, phase of the response in relation to that seen during dynamic stimulation, determined by subtracting each individual value before the averaging; the negative sign signifies that the response during dynamic stimulation was always in advance of the other two. The vertical bars show the standard deviation: those for A have been omitted for clarity. (Four static responses missing at 30 Kim, and 1 combined response absent up to 250 /Sm. Same symbols in B and C for corresponding modes of activation.)

845

846 M. HULLIGER, P. B. C. MATTHEWS AND J. NOTH the same shape and differ simply in their scaling. But this was not a regular finding for the individual examples; nor were the cycle histograms at a given amplitude simply scaled versions of each other during static and during dynamic stimulation. The phase plot in Fig. 4C re-affirms the similarity of the phase during static and during combined stimulation in comparison with the greater phase advance at large amplitude during dynamic stimulation, as already noted for Fig. 2. In addition, the phase during combined stimulation can now be seen to be very slightly in advance of that during static stimulation. It may finally be noted that on 4 occasions Bode plots for the linear range during combined stimulation showed the sensitivity in the range 03-5 Hz to be uniformly just above that for static action, and far below that for dynamic action.

Varying relative rate of stimulation Large amplitude. With large amplitude the characteristic blending of static and of dynamic action occurred for a wide range of relative rates of stimulation. In Fig. 5A the addition of a constant dynamic activation increased the modulation, above its value with static activation alone, by about the same amount whatever the rate of static stimulation. Rather similarly, in Fig. 5B the addition of a constant static activation produced about the same reduction of modulation from its value during dynamic activation alone, irrespective of the rate of dynamic stimulation. However, on the other occasions when this was tested (three more for each, but only once more with the rates of both efferents varied in the same preparation) the two curves of a pair did not usually run quite so parallel so that this may be a fortuituous feature of Fig. 5. Of equal interest is the effect on the phase of the responses of altering the relative strength of static and dynamic action. In Fig. 5A the addition of dynamic action produced no change in the phase relative to its value for the same rate of static stimulation on its own, although it markedly enhanced the modulation. In Fig. 5B the phase advance during combined stimulation was always less than that during dynamic stimulation on its own; but as the filled circles (@) show when the static action was present (and so filling in the trough of the histogram) there was no appreciable shift of phase on adding progressively greater amounts of dynamic action, although this was manifestly influencing the modulation. It is concluded that with large amplitude stretching, altering the relative amounts of static and dynamic activation has large effects on the depth of afferent modulation but is without systematic effect on the phase of the response. Small amplitude. Fig. 6 shows curves for small amplitude stretching based on a similar procedure to that used for Fig. 5. The amplitude-

847 COMBINED FUSIMOTOR STIMULATION response curves conform to and support the principle that during combined stimulation static action dominates the response when the amplitude of movement is small. The details of the graphs are, however, somewhat complex and are dealt with below; the complexity arises because with small amplitudes of movement both static and dynamic action produce the same effect, namely a reduction in the modulation from its passive value without change of phase (Goodwin, Hulliger & Matthews, 1975). As expected from this, in Fig. 6 alterations in the balance between static and dynamic action were without effect on the phase. Similar results were obtained in other experiments (three more of each). Large amplitude

A

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Fig. 5. Progressive shift in the balance between the static and dynamic contributions to the response seen during large amplitude stretching (700 #tm, 1 Hz). Each set of curves shows the effect of changing the rate of stimula-

tion of one of the fusimotor fibres while that for the other is held constant. A, *, dynamic stimulation constant at 125/sec while static stimulation varied; 0, static stimulation on its own. B, *, static stimulation constant at 70/sec while dynamic stimulation varied; 0I, dynamic stimulation alone. All data from same ending and fusimotor fibres.

Details of curves. The open circles (0) in Fig. 6 A show the usual progressive reduction in the modulation, from the passive level, with increase in the rate of static fusimotor stimulation. The filled circle (-) lying precisely on the ordinate corresponds to dynamic stimulation on its own and is quite properly below the corresponding open circle representing the passive response, since dynamic action reduces the afferent responsiveness below its passive value (Goodwin et al. 1975; Hulliger et al. 1977). This reduction is shown, inter alia, more fully in the top curve of Fig. 6B for dynamic stimulation on its own, and in this case becomes progressively greater with increasing rate of stimulation. Returning to Fig. 6A it can be seen that as soon as the

M. HULLIGER, P. B. C. MATTHEWS AND J. NOTH

848

static action was strong enough to reduce the modulation appreciably below the value with the dynamic stimulation, so the static effect became dominant and progressively reduced the response during the combined stimulation to an intermediate value. In Fig. 6B increasing the strength of dynamic action on its own progressively reduced the modulation below the passive value, but when it was added to the static action it slightly increased the modulation above the value for static action on its own. The former effect is well known, as already noted. The latter increase indicates that a sufficiently strong dynamic action can begin to match the normally dominant static action at small amplitude, so that the combined response is intermediate between the two individual responses as it is for large amplitudes. Such

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Fig. 6. Alteration, as in Fig. 5, in the relative strengths of static and dynamic actions now seen during 8ma~ll amplitude stretching. A, *, dynamic stimulation constant at 125/sec while static stimulation varied; 0, static stimulation alone. B, *, static stimulation constant at 87/sec while dynamic stimulation varied; 0I, dynamic stimulation alone. Stretching: A, 50 jam at 1 Hz (same expt. as Fig. 5); B, 30 jsm at 1 Hz (different expt.). At the maximum rate of stimulation in each graph the mean rates of firing during static and dynamic action on their own were in A, 126 and 64 impulses/sec, and in B, 65 and 75 impulses/sec.

matching of action was associated not so much with the absolute depth of modulation, but occurred rather when the mean level of response during dynamic activation approaches that during static activation on its own. This suggests that the normal static dominance of the small-amplitude sensitivity is related to its greater excitatory effect on the mean rate of firing, as seen both in the presence and absence of small amplit~ude stretching. For the twelve pairs of fibres of Fig. 4 the static fibres produced a mean increase of firing of 54+± 16 S.D. impulses/sec and the dynamic fibres of 23±+ 6 irnpulses/sec, with the particular rates of stimulation which were chosen.

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849

Occlusion versus summation of effects at different phases of the stretch

cycle Peak summation with large amplitudes. The quantitative relations illustrated in Figs. 2-6 have their basis in the asymmetrical way in which static and dynamic action sum at different phases of the sinusoidal cycle. With large stretches a degree of summation between static and dynamic effects was virtually always seen for the peak of the histogram, corresponding to the last half of the rising phase of stretch. As illustrated in Fig. 7D the firing during the combined stimulation was, at this phase of the cycle, very appreciably above that seen for both static and dynamic stimulation on their own. Fig. 8 C shows that the amount of the increase became greater with increasing amounts of static activation, since the peaks of the histograms are progressively moved upwards with increasing rate of static stimulation. Such peak summation would appear, however, usually to fall short of arithmetical addition, with equal weighting of the effects of each fibre on its own (taking the corresponding passive response as the reference); but the matter has not been given systematic attention. Trough occlusion with large amplitudes. In complete contrast, during the trough of the histogram static action typically occluded any signs of dynamic action. As shown in Fig. 7D the rate of firing in the trough of the histogram for combined stimulation was virtually the same as that occurring with static stimulation on its own. Fig. 8D shows that the occlusion can occur for varying strengths of dynamic action. Moreover, comparison of Fig. 8B with D shows that the occlusion persists when the progressive dynamic action is strong enough to increase the trough firing appreciably; thus the occlusion does not arise merely from a total inability of the dynamic fibre to exert itself during the course of a release when it is acting on its own. Nor did the occlusion result solely from 1:1 driving of the afferent by the static stimulation as may have been tending to occur in Fig. 8, but not in Fig. 7. The occlusion, however, only occurred for phases of the cycle for which dynamic stimulation on its own elicited less firing than did static stimulation on its own. Thus there is an interesting asymmetry between the summation of static and dynamic action. For phases of the cycle for which the firing is greater during dynamic than during static stimulation the static action can none the less manifest itself during the combined stimulation and increase the average firing above the level for dynamic stimulation on its own. But when with the dynamic stimulation on its own less firing occurs than with static stimulation, then the dynamic action fails to influence the response during combined stimulation. It should be noted that all these statements are based upon the average rate of firing determined bin by bin and we have not attempted to

850 M. HULLIWER, P. B. C. MATTHEWS AND J. NOTH study the related inter-spike interval distributions during sinusoidal stretching, or the instantaneous frequencies, to see whether there is any overlap in the moment to moment firing in the various cases. Uniform occlusion with small amplitudes. When the amplitude of stretching was small static action normally dominated dynamic action at all phases of the cycle, as illustrated in Fig. 9. Again, as with the large 700 lim 1 Hz stretching

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3600 Fig. 7. Cycle histograms showing the asymmetrical pattern of summation and occlusion of static and dynamic actions during large amplitude stretching. A, stimulation of static fibre at 56/sec. B, stimulation of dynamic fibre at 100/sec. C, combined stimulation. D, superposition of histograms from A, B, and C each drawn in a separate manner.

amplitude stretching, the pre-requisite for occlusion to occur was that the firing during static stimulation should always be somewhat above that during the dynamic stimulation on its own, as it was for Fig. 9. When the rate of firing approximated in the two individual cases then a degree of summation could occur for small amplitude stretching. As the amplitude

COMBINED FUSIMOTOR STIMULATION 851 of stretching was increased, for constant amounts of fusimotor activation, and the peak firing during dynamic stimulation reached and then exceeded the more constant static level so occlusion was replaced by summation. These statements are based on serial comparison by superposition of numerous histograms, but we have not attempted a quantitative survey to establish the precise conditions for the transition from occlusion to summation. A

Static alone at different stimulation rates

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Fig. 8. Asymmetry of trough occlusion and peak summation. Sets of superosed histograms for large amplitude stretching (700dt m at 1 Hz) to show the progressive interaction between static and dynamic effects on changing the rate of stimulation of one while holding that of the other constant. All results from the same experiment (same as Fig. 5). A, B, effect of static and of dynamic stimulation on their own. C, constant dynamic stimulation with increasing rates of static stimulation. D, constant static stimulation with increasing rates of dynamic stimulation. (For clarity, alternate histograms in each set have been marked with dots. Equivalent histograms in different sets - for example the two passive responses without stimulation in A and B - are not identical because they were obtained at different times, as controls for the other histograms in its set.) Note especially, constancy of trough in spite of increasing dynamic action (B, D), and the static-evoked increase in the peak during constant dynamic action (A, C).

M. HULLIGER, P. B.C. MATTHEWS AND J. NOTH

852

DISCUSSION

The present results with large amplitude sinusoidal stretching complement and extend those of Lennerstrand (1968) with large triangular stretches, also applied during combined static and dynamic stimulation. During the stretching phase of the cycle the firing is dominated by the dynamic action, but there is a definite contribution from the static action so that the firing is appreciably greater than with dynamic stimulation on its own. Likewise, such summation has been seen on the rising phase of a 50 pm 1 Hz stretching

A

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Fig. 9. Cycle histograms showing the occlusion of dynamically induced modulation by static action during *mall amplitude stretching. A, stimulation of static fibre at 56/sec. B, stimulation of dynamic fibre at 100/sec. C, combined stimulation. D, superposition of histograms from A, B and C. Same experiment as Fig. 7.

large ramp stretch, and also normally occurs on the subsequent plateau (Crowe & Matthews, 1964b; Emonet-Denand, Laporte, Matthews & Petit, 1977; Schaifer, 1974). In contrast, on the falling phase of the sinusoidal stretch static action dominates and, moreover, any dynamic action on the firing level is largely occluded by static action so that the firing at this phase of the cycle is virtually the same as with static stimulation alone. Lennerstrand (1968) also noted the equivalence of the firing on the falling phase for mixed and for static stimulation, but he did not apparently pay

853 COMBINED FUSIMOTOR STIMULATION any particular attention as to whether or not firing occurred at this phase of the cycle with dynamic stimulation on its own, and if so whether the firing was greater than the corresponding passive value. We have indeed seen occlusion of such positive dynamic effects, which would seem of interest for understanding the underlying mechanisms. The essential thing determining whether occlusion or summation occurred at a given phase of the cycle seemed to be the absolute level of firing during the individual fusimotor actions. When dynamic stimulation alone led to the higher firing then a degree of summation was found, but when static stimulation alone gave the higher firing then occlusion occurred. The interaction between static and dynamic effects was thus asymmetrical. When the amplitude of stretching was small the firing during static stimulation was usually above the level during dynamic stimulation throughout the cycle, and the normal dynamic modulation was largely abolished during combined stimulation. The virtual suppression of dynamic action for the small stretches is thus entirely in line with the principle suggested by the large amplitude findings. With increasing amplitude of stretching the dynamic action begins to make itself felt when the peak firing with dynamic stimulation alone begins to surpass that for static stimulation alone, and the modulation of firing during combined stimulation then becomes progressively more intermediate between the values for static and for dynamic stimulation. When the muscle is at a constant length varying mixtures of occlusion and summation have been reported for combined stimulation (Crowe & Matthews, 1964b; Lennerstrand, 1968; Schafer, 1974); some of this variability may prove explicable in terms of the asymmetrical interaction that we have observed. It will be of interest to have the quantitative extent of summation and the precise conditions for its occurrence defined yet more exactly, particularly with reference to interspike interval distributions. Possible intrafusal mechanisms. The intrafusal mechanisms underlying the asymmetry of interaction of static and dynamic effects remain to be elucidated, but certain possibilities may be outlined. Summation of firing presents no special conceptual problem since it presumably arises from direct electrical addition, after electrotonic spread to some common site for spike initiation (pace-maker), of the receptor potentials arising in functionally separate branches of the afferent terminal. It should be noted in support of this that for the plateau of a ramp stretch the summation process can elicit an elevation of the whole band of instantaneousfrequency points, so that during combined stimulation all values lie above the highest individual values found with either fusimotor fibre stimulated alone (Emonet-D6nand et al. 1977). Thus, in this case the summation cannot arise simply from the 'probabilistic mixing' of two or more separate streams

854 M. HULLIGER, P. B. C. MATTHEWS AND J. NOTH of impulses, each with a finite variability and initiated at its own pacemaker, which in turn is activated selectively by a particular fusimotor fibre. If each pace-maker can reset the others, the interaction ofthe impulse trains at a branching point lying centrally to the individual pace-makers could evoke some increase in the mean level of firing (Eagles & Purple, 1974), but it could not shift the whole band of instantaneous frequencies beyond the peak values obtained with single fibre stimulation. A further possibility for summation is that a given static axon might send a branch to an intrafusal muscle fibre that was specialized for dynamic action and predominantly supplied by the dynamic axon (cross-innervation); the intrafusal fibre could then contract more forcibly with the combined stimulation and so augment the dynamic effect of the dynamic axon. This may perhaps have contributed on occasion, but it is unsatisfactory as a universal explanation of the summation: peak summation has been seen almost invariably with 'typical' static fibres, whereas all evidence suggests that any overlap of innervation from static axon to 'dynamic' intrafusal muscle fibre cannot be above 50 % (Barker, Emonet-D6nand, Harker, Jami & Laporte, 1976; Emonet-D6nand et al. 1977). Thus electrotonic spread to a common site seems the likely basis of peak summation, irrespective of the number of pace-makers in the spindle. The origin of the occlusion is more controversial (Crowe & Matthews, 1964a, b; Lennerstrand, 1968; Schafer, 1974). It might arise from a mechanical unloading of one intrafusal fibre, with its afferent terminals, by the contraction of another fibre which is arranged in parallel. Any such contraction-induced unloading might be additive with the stretch-induced unloading occurring on the release phase, with the consequence that dynamic action was debarred from manifesting itself throughout the trough of the histogram obtained during combined stimulation, even though it had done so when acting on its own. An alternative type of explanation, which we find the more attractive, is that the occlusion arises from a switching, by virtue of their relative discharge frequencies, between pace-makers, thus, between the sites, determining the stream of impulses which is finally discharged along the main afferent axon (cf. Crowe & Matthews, 1964a; Lennerstrand, 1968; Brokensha & Westbury, 1974); the particular pacemaker with the highest instantaneous frequency is then the only one whose behaviour is momentarily open to observation in the present type of experiment. But the observed asymmetry can then only be explained in terms of further assumptions on the number, site and properties of the various pace-makers involved, and two alone would appear insufficient. We hope to develop this theme in a later paper in the light of certain additional indirect observations. For the moment no final decision can be reached between the alternatives of mechanical unloading and pace-

855 COMBINED FUSIMOTOR STIMULATION maker switching as the origin of the present occlusion, nor need they be entirely exclusive. Functional implications. Irrespective of their detailed mechanism several aspects of the present findings are also of interest in relation to motor function, although in view of various limitations none of the conclusions should be regarded as final. Firstly, the occlusion of the dynamic effects by static action means that the high sensitivity of the spindle seen for small amplitude stretching applied during dynamic fusimotor activity can only manifest itself when the static fusimotor system is largely quiescent. This is particularly so because individual static fibres commonly produce a greater increase in mean firing than do individual dynamic fibres and, moreover, the static y fibres outnumber the dynamic y fibres by some 2-3 to 1. Thus if the dynamic system is to be used to set low-frequency reflex gain at a high level to resist small perturbations during some postural task, then the dynamic system must be used largely on its own without the co-operation of the static system. Likewise, in so far as some static axons may have a degree of dynamic action along with their main static action (Barker et al. 1976; Emonet-D6nand et al. 1977) this is unlikely to manifest itself when the amplitude of movement is small. Secondly, the summation of static and dynamic actions, once a stretching movement is of appreciable size, means that under many physiological conditions they can act co-operatively and so can usefully be employed together. In this respect it may be noted that the occlusion of dynamic by static action seen on the falling phase of stretch is partly offset by the summation that occurs between them on the rising phase, so that the depth of modulation during combined action is intermediate between that seen with either alone. Thus varying the relative strengths of action of the two systems provides a continuous regulation of the sensitivity of the spindle to large movements. Thirdly, as discussed elsewhere (Hulliger et al. 1977) the lack of any systematic effect on the phase of the response on shifting the relative strengths of static and dynamic action (Figs. 5 and 6) supports the view that both dynamic and static fusimotor action primarily control the overall sensitivity (gain) of the primary ending and not its relative sensitivities to length and its higher derivatives. But the dynamic system would appear to play slightly different roles when acting alone, and when acting co-operatively with the static system. On its own, it equally effects the response to both small and large movements, whereas when acting cooperatively it can only control the response to larger movements. How far the occlusion of dynamic action during a large release fulfils a functional role is open to debate. Perhaps it is immaterial for central action, since the spinal centres will continuously receive information from opposing muscles, so that on joint movement the release of one muscle will always be balanced

856 M. HULLIGER, P. B. C. MATTHEWS AND J. NOTH by the stretch of another with subsequent opportunity for the provision of dynamic information. The Medical Research Council and the Deutsche Forshungsgemeinschaft are thanked for support. REFERENCES

BARKER, D., EMONET-DE'NAND, F., HARKER, D. W., JAMI, L. & LAPORTE, Y. (1976). Distribution of fusimotor axons to intrafusal muscle fibres in cat tenuissimus spindles as determined by the glycogen-depletion method. J. Phy8iol. 261, 49-69. BROKENSHA, G. & WESTBURY, D. R. (1974). Adaptation of the discharge of frog muscle spindles following a stretch. J. Phy8iol. 242, 383-403. CROWE, A. & MArTTEws, P. B. C. (1964a). The effects of stimulation of static and dynamic fusimotor fibres on the response to stretching of the primary endings of muscle spindles. J. Phy8iol. 174, 109-131. CROWE, A. & MATTHEWS, P. B. C. (1964b). Further studies of static and dynamic fusimotor fibres. J. Phy8iol. 175, 132-151. EAGLES, J. P. & PURPLE, R. L. (1974). Afferent fibres with multiple encoding sites. Brain Re8. 77, 182-193. EMONET-DIPNAND, F., LAPORTE, Y., MATTHEWS, P. B. C. & PETIT, J. (1977). On the sub-division of static and dynamic fusimotor actions on the primary ending of the cat muscle spindle. J. Phy8iol. In the Press. GOODWIN, G. M., HULLIGER, M. & MATTHEWS, P. B. C. (1975). The effects of fusimotor stimulation during small amplitude stretching on the frequency-response of the primary ending of the mammalian muscle spindle. J. Phy8iol. 253, 175-206. HULLIGER, M., MATTHEWS, P. B. C. & NOTH, J. (1977). Effects of static and of dynamic fusimotor stimulation on the response of Ia fibres to low frequency sinusoidal stretching covering a wide range of amplitudes. J. Phy8iol. 267, 811838. LENNERSTRAND, G. (1968). Position and velocity sensitivity of muscle spindles in the cat. IV. Interaction between two fusimotor fibres converging on the same spindle ending. Acta phy8iol. 8cand. 74, 257-273. SCHIFER, S. S. (1974). The discharge frequencies of primary muscle spindle endings during simultaneous stimulation of two fusimotor fibres. Pfliuger Arch. ge8. Phyaiol. 350, 359-372.