Muscle
Spindle
Behavior
K. Sllcrrirlgfolz
Scl~ool
S.
during Active in Amphibia
PC. MUKTIIY
AXI)
A.
Muscle
TAYLOR
of Physiology, St. Tho~ms’s Hospiful Loldo~, SE1 7,511, l31glmd Kcccizwd
October
Contraction
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The effects of different mechanical loads on discharge of frog and toad muscle spindles were studied during active contraction of twitch muscles. Intrafusal driving, which accompanies extrafusal contraction, was found to maintain spindle discharge to a degree dependent on the compliance of the load. Intrafusal contraction alone could not drive afi’erent discharge to maximum frequencies, which were reached only with muscle stretch following a period of tetanic stimulation. Maximal intrafusal driving effects were reached at low rates of stimulation (5 to 10/s). E ven with a very compliant load, which caused silencing during a developed tetanic contraction, there was an initial burst of activity from the spindle afferents. There was also a prominent burst at the end of stimulation. The consequences of these properties of amphibian spindles are discussed and the potential existence of a positive feedback loop is indicated. The results provide some basis for understanding the significance of the separation of intrafusal and estrafusal motor pathways in mammals.
INTKODUCTION The significance of intrafusal muscle contraction in the regulation of movement by muscle spindles has heen considered almost exclusively in mammalian species. Granit [see (9) for review] favored the idea of a close linkage between skeletomotor and fusimotor driving from the central nervous system, acting principally to ensure that spindle discharge is maintained during active muscle shortening. As pointed out by Matthews (17), this hardly seems to provide an adequate explanation in terms of evolutionary advantages for the emergence of a dual, independent fusimotor Abbreviations : L,,--irz sift length ; VK-ventral roots. r This work was supported by the Wellcome Trust. Dr. and address for reprint requests is Division of Neurosurgery, Medical School, Houston,, Texas 77030.
Murthy’s present address University of Texas,
175 00144886/78/060.?-0175$02.00/O All
Copyright Q 1978 rights Iof reproduction
by Academic Press, Inc. in any form reserved.
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system. The servo hypothesis of Merton (18) implied that special advantages arose from driving movement via the fusimotor route. This now seems much less attractive on fundamental grounds (17, 25, 27) and in the light of more recent direct observations on mammalian spindles (28-30). In any case, the existence of separate static and dynamic fusimotor systems has become clear only since the formulation of this hypothesis, and there is a lack of any comprehensive theory to incorporate the newly recognized complexities of the mammalian spindle in a general scheme of motor control. In Amphibia, on the other hand, it appears that intrafusal innervation arises by way of branches from the extrafusal skeletomotor innervation (7, 8, 10, 14). Such a situation represents the simplest and most rigid form of “q linkage.” It would therefore seem appropriate to attempt to understand the amphibian arrangement and its limitations as a background to mammalian studies. Accordingly, in the present work a study is made of muscle spindle behavior in frogs and toads when length changes are caused by active contraction against a variety of spring loads (20) as an approximation to the natural situation. The amphibian motor system consists of fast-contracting “twitch” muscle fibers and slow-contracting “tonic” muscle fibers (26), both of which feature common intra- and extrafusal motor innervation (10). These experiments are restricted to single and repetitive stimulation of twitch muscles in the hind limbs of Bufo and Rana. METHODS To study spindle behavior during repeated motor stimulation, a preparation was needed in which a good circualtion could be maintained for long periods. This was possible with large (300-g) specimens of Bufo vnarinus and Rana tigrina. Urethane (1.5 g/kg) was injected as a 15% solution into a lymph sac with supplements, when necessary, injected at lo-fold dilution. All the muscles of one hind limb, except the muscle under investigation, were denervated and the animal was mounted in a specially designed frame (19, 22). Laminectomy was done to expose the cord and nerve roots from the fourth to tenth laminae. The spinal roots are usually 10 pairs, the hind limb muscles being innervated from spinal roots 8, 9, and 10. These were cut, dorsal and ventral, close to the cord near the third and fourth laminae, making available a maximum length of approximately 3 cm of the roots. A paraffin-filled pool was built up using 4% agar gel and gauze packing. A total of 28 toads and 110 frogs were used in this investigation. Spindles in a pure fast-twitch muscle (sartorius) and in a mixed muscle (gastrocnemius) were studied. Both are innervated mainly from spinal
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roots 9 and 10. Functionally single spindle afferents were isolated from either root by progressive splitting, a process which is much easier in Rana than in Bufo. Spindle afferents are said to be characterized in frogs by being the only muscle stretch receptors respondin, v to passive stretch of the inert muscle (13). We have not found this entirely dependable because receptors identified as tendon organs in all other respects sometimes behaved in this way. The usual test for spindles, silencing during the rising phase of a twitch, is confused by the intrafusal excitation and it was found best to rely on (a) tonic response to passive stretch, (b) tendency to silencing in relatively isometric contraction, and (c) increased discharge during relaxation after a tetanic contraction. Ventral roots 9 and 10 (VR9 and 10) were placed on separate pairs of chlorided silver wire electrodes for stimulation from isolated stimulators. Unless otherwise stated, stimulus intensity was adjusted to be just maximal for fast motor fibers, as indicated by the muscle twitch. By selective blocking of fast motor fibers and increasing stimulation strength to involve any slow fibers present (15, 16), it was confirmed that sartorius in the frog was purely twitch muscle and had no slow motor system effects on its spindle. For testing responses to stretch, the muscle tendon was attached to an electromechanical vibrator (Goodman, Type V50) driven by a DC power amplifier (AIM Electronics, WPA 116). Variable compliance was arranged by attaching the tendon to a strain gauge by means of various coiled steel springs. The force recorded was converted to length changes of the muscle by scaling with the spring compliance. Muscle length was set to be optimal for twitch tension development. Experiments were carried out at room temperature (18 to 22°C). Because of the irregularity of firing of amphibian spindles, instantaneous frequency plots were not very satisfactory. Instead, a reasonable degree of smoothness and reliability was achieved by producing ensemble averages of firing frequency across a number of stimulus presentations, using an averaging computer (Medelec, AVM3) or a general purpose digital computer (Varian 620L). RESULTS Ejfects of Ventral Root StilrLlrlation. In both frogs and toads it was usually found that any given spindle afferent showed evidence of intrafusal excitation predominantly from one ventral root. Figure 1 shows typical behavior recorded from a gastorcnemius spindle in Rana. Stimulation of VR9 caused silencing during a twitch (Fig. la) and VRIO stimulation (b) caused a brief burst in contraction and a second, more prolonged
MURTHY
FoRCE
lkg for 1 Zkgfor
AND
b-f a
FIG. 1. Responses of spindle afferent from to VR9(a) and VRlO(b). c-f-Repetitive 20/s, respectively. Isometric force recording.
TAYLOR
I
8
0.5 set gastrocnemius stimulation of
of frog to single stimuli VRlO at 5, 10, 15, and
discharge during relaxation. Figures lc-f show responses to tetanic stimulation of VRlO at increasing frequencies. It is noticeable that the first stimulus of each train elicited several afferent impulses, whereas subsequently only a single impulse was generally produced immediately following each stimulus. Considering the single-twitch response (b) it is clear that two factors are concerned in initiating spikes: first the activation of intrafusal muscle fibers and second the stretching of the spindle during the extrafusal relaxation. Consequently, the afferent activity actually seen during a contraction must depend not only on the motor nerve firing frequency and the degree of unloading, but also on the smoothness or degree of fusion of the intra- and extrafusal contractions. However, leaving aside effects of incomplete fusion, it would be expected that the afferent discharge frequency should depend on the difference between intrafusal and extrafusal muscle shortening. If this were so, then adding to the series elastic ,element by interposing a spring between the
AMPHIBIAN
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tendon and the strain gauge should reduce the discharge during active shortening. In principle this is the case, as shown in Fig. 2, in which tetanic contractions are excited at various frequencies and against various load compliances. Column A with 10/s stimulation shows that increasing compliance leads to almost-total elimination of the sustained firing for compliances greater than 16 pm/g. Expressed in terms of maximal tetanic force for stimulation of VRlO (PO) this is 9.6 mm/PO. At any given compliance, increasing stimulus frequency from 10 to 20/s also substantially reduces the afferent discharge, both shortening the initial burst and reducing any tendency to fire in the plateau of contraction. The obvious implication that shortening reaches a maximmii in intrafusal fibers at lower frequencies than in extrafusal fibers must be reserved because propagated intrafusal activity may break clown at high frequencies. At the same time, the initial burst remains prominent, and this suggests that initially the intrafusal muscle fibers shorten faster than the extrafusal fibers. Note particularly that the timing of the afferent spikes in tetani at 10/s is such that they appear to be generated after each stimulus during the onset of increased muscle shortening rather than durin g the ensuing relaxation. The possibility that there might have been some involvement of the tonic motor system was checked by additional studies made on sartorius in Rana, which in R. tcn~j~~~ria. and R. ~ijicns appears to be purely fast [ (2), and above Methods section].
b
d
TBllBlOll 170 p for for d I 353g
il.b&C
I
spikes 40 pv
FIG. 2. Responses of spindle afferent from gastrocnemius of toad during tetanic contraction against a variety of loads. A-C-Stimulation of VRlO at 10, 15, and 20/s,
respectively. a-c--Spring Resting length constant.
compliances of 3.5, 16.1, 32.3, and 90.9 pm/g, respectively. Horizontal bars indicate timing of l-s duration tetani.
180
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0’
-ii?
HSEC
FIG. 3. Tetanic stimulation of frog sartorius through VRIO at 10, 15, and 20/s (from above, downward). Left-hand column, isometric conditions ; right-hand column, spring load compliance 25 pm/g. Spindle response (dotted) is the instantaneous frequency averaged at 75ms intervals for 10 consecutive stimulus presentations (see Methods).
Figure 3 shows that the results of normal tetanic stimulation of the sartorius at 10, 15, and 20/s are essentially the same as in the gastrocnemius, but the display has been made more quantitative and reliable by showing firing frequency averaged for 10 stimulus presentations, with less complete fusion at the lower frequencies. It is evident that in this case some sign of incomplete fusion of the effects of stimulation persists to as much as 20/s, particularly in the isometric records in the left-hand column. At the same time, while the peak firing frequency changes very little with increased stimulus frequency, the mean firing rate does rise. It is quite clear that the peaks of frequency are due to intrafusal activity rather than to extrafusal relaxation because there is a well-marked delay after the last stimulus of each train before the onset of the relaxation burst, in line with the observed slow onset of extrafusal relaxation. Contractions against
AMPHIBIAiX
SPINDLES
IN
ACTIVE
181
CONTRACTION
a compliant load (right-hand column) show evidence of progressive LIIIloading of the spindle at stimulus rates above 15/s, confirming the view expressed above that extrafusal contraction can continue to increase to higher frequencies than can intrafusal contraction. Some further insight into the relationship of intrafusal and extrafusal contraction is given by reference to Fig. 4, showing the effects of critical curarization (14). In (a) the stimulation of normal muscle at 5/s gives a very incompletely fused tetanus against a load of compliance of 25 pm/g, and the afferent spikes occur mostly in relation to the extrafusal relaxation (which 1s thus presumably faster than the intrafusal). Close arterial infusion of 200 pg curare completely blocked extrafusal contraction (b) but left an afferent discharge reaching 50/s very abruptly, due to intrafusal contraction. The “frequencygram” showed only slight modulation in time with stimulation so that even at this frequency intrafusal contraction must be reasonably completely fused ( 1). I ncreasing stimulus frequency
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FIG. 4. Effect on spindle discharge from gastrocnemius of frog of progressive curarization. Stimulation of VRlO at 5/s (a) before and (b) after intra-arterial injection of 200 pg d-tubocurarine chloride; c-stimulation at 15/s ; and d-stimulation repeated after a further dose (600 pg) of curare. Spring load of compliance, 25 pm/g. Spindle firing shown as two superimposed traces of instantaneous frequency.
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to 15/s (c) caused some extrafusal contraction to appear slowly such that shortening by about 1 mm cancelled the effect of intrafusal contraction. It is notable that the the initial response to 15/s stimulation is only very little greater than that to 5/s stimulation. Finally, increasing the dose of curare so as to practically eliminate extrafusal shortening with stimulation at 15/s (d) showed a firing pattern very much like that in (b). One may conclude that intrafusal effects are of rapid onset, tend to fuse at low frequencies, and virtually saturate at stimulus rates of 5/s and afferent firing rates of 50 to 60/s. The highest afferent frequencies (120/s) are achieved only with the addition of extrafusal lengthening. Recordings made with a compliant load (Figs. 2, 3) show a very marked discharge at the end of tetani. This must be due to extra force transmitted to the innervation zone of the intrafusal fibers when the extrafusal muscle relaxes while some intrafusal contraction still persists. That intrafusal activation can outlast the stimulation is demonstrated by Figs. 4b and d where the afferent firing does not diminish appreciably for some 300 ms after the end of stimulation. Thus the realxation firing seen in Fig. 2 and in Figs. 4a and c may be closely related to the initial burst sometimes seen during ramp stretches of mammalian spindles (4). Another feature of these records which should be noticed is that adaptation of the afferent discharge is small and slow in the absence of extrafusal shortening. In Figs. 4b and d there is very little diminution of firing during the first 0.5 s of tetanic stimulation. Dynamic Properties. The time course of the spindle firing is best studied in records smoothed by averaging across a number of stimulus presentations. Also, because we wish to derive data generally representative of the ensemble of muscle spindles, there is some advantage in examining multiunit spindle afferent records. In Figs. 5a and b, a four-unit record has been averaged for 10 sweeps and the firing expressed in arbitrary units of frequency estimated in 20-ms time bins. The maximum firing is reached very soon after the stimulus onset and thereafter decays with a time course resembling that of extrafusal muscle shortening. Indeed, normalized semilogarithmic plots of firing frequency and muscle shortening from the records of Fig. 5, seen in Fig. 6, reveal that both are reasonably well described in the first 0.5 s as simple exponentials, with essentially similar time constants (in the range 0.25 to 0.16 s). Thus, it appears that most of the adaptation of sensory discharge seen in tetanic contractions against spring loads can be accounted for by the mechanical unloading due to extrafusal shortening. This is consistent with the findings illustrated in Fig. 4 that very little adaptation of afferent discharge during the first 0.5 s of a tetanus occurs when extrafusal contraction is blocked by curare.
AMI’HIIIIAN
Si’INI)LES
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FIG. 5. Ensemble response of four spindle afferents from gastrocnemius of toad. Sl)indle firing averaged for 10 cycles of stimulus presentation for 1 s at 15/s (horizontal bar) and sho\vn as puststimulus histograms representing arbitarary units of frequency estimated in ZO-ms time bins. a-Load compliance, 4.29 pm/g; b-compliance, 1.02 pm/g.
Such behavior is in contrast to the well-known passive stretch properties of frog spindles, as illustrated in Fig. 7,4. Here a ranq) stretch gives a nlarkedly atlapting afferent discharge. As seen in Fig. 7B the effect of nlotor stimulation is evidently to increase the background discharge frequency and to reduce the static and dynamic incremental sensitivities to stretch. Motor stimulation was also found to reduce considerably the effect of controlled passive shortening. These findings are consistent with those of Brown (2, 3). The contrary results of Smith and Kales (24), who found that isolated Xe~op~s spindles showed high sensitivity to stretch only when intrafusal fibers were active, nlay have been due to different conditions, in that Smith and Kales used small, slow movements [approximately 1 R inaxiniun~ it2 sits length (L,,) at 0.25s L,,/s], whereas we were concerned with movements within the likely normal physiologic range of as 171nch as S7& L, stretch and 20% L,,/ s velocity. In the light of the reduction of sensitivity to such length changes seen here during background niotor stimulation, it is evident that part of the conipensation for active shortening of muscle is due to this and part to the shortening of intrafusal fibers.
DISCUSSION The primary purpose of this work was to examine the behavior of muscle spindles in active contractions against a variety of tnechanical loads. Aqhibia were studied because the inbuilt rigid “fry coactivation” which
MURTHY
AND
TAYLOR
025 TIME
05
bed
FIG. 6. Semilogarithmic plots of spindle frequency and muscle length in the first 0.5 s of tetanic stimulation of toad gastrocnemius at 15/s. Data of Fig. 5. Time constants (seconds) shown estimated from linear regressions. A, B-Load compliance, 1.5 am/g; C, D-compliance, 5 pm/g.
they display seemedto place them in the position of a simple model of one hypothesis for mammalian spindle function. Attention was restricted to the twitch or fast motor system. This could be stimulated through ventral roots apparently in isolation in the gastrocnemius by using shock strengths just maximal for twitch responses. The sartorius in Rana tigrina is apparently entirely fast muscle and we were unable to find any evidence of slow motor innervation of intrafusal fibers. This agrees with Brown (2), who found in Rana tenzporaria and Rana pipiens that no sartorius spindles were excited by succinylcholine. No qualitative differences were apparent between spindle afferent units in gastrocnemius and sartorius in Bufo marinus or Rana tigrina.
AMPHTRTAN
1 x,5
SPTNDLES TX ACTIVE CONTRACTTON
A difficulty in setting up these experiments to deduce how amphibian spindles behave in normal movement was uncertainty about the appropriate frequency of stimulation. Electronlyogram recordings from gastrocnetnius in normal Bzffo shavings (19) showed units firing at 15 to 30/s when the leg was passively flexed. In the present experiments, frequencies were generally limited to 20/s to avoid fatigue, but it would be interesting to repeat some of the observations with short bursts of much higher frequencies. This is more likely to be the way the muscles are used in jumping. It is also recognized that the synchronous volleys used here in single ventral roots are likely to have effects different from those of natural asynchronous discharge of motor neurons [see Rack and Westbury (23) 1. The incompletenessof tetanic fusion which contributed to spindle discharge at low-frequency stimulation might in future experiments be avoided by rotational stimulation of a number of ventral root filaments as introduced by Rack and Westbury. Nevertheless, the general expectations of the experiments were realized in that the tendency for a spindle to be silenced during shortening is counteracted, at least in part, by simultaneous intrafusal activation. The amount of afferent discharge during an active muscle contraction de-
[
lmm
FIG. 7. Effects of VRlO stimulationon response of frog sartoriusafferent to ramp stretch. A-No stimulation; B-stimulation at threshold for spindleactivation at 20/s; C-fast fibers blocked and stimulation strength increasedsevenfoldand to SO/s; D-stimulation at twice threshold,20/s. Heavy dots in B and D indicatemean frequencyestimatedat 100-msintervals.
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pended on the compliance of the spring load, being greatest with loads of lowest compliance. This behavior would be quite appropriate for a motor control system using load compensation via the spindles, especially to improve the speed of response at the onset of a movement. However, it is not possible from the present experiments to say how effective such a load compensation would be in practice because we do not know the strength of the reflex connections. Remarkably little work has been reported specifically on muscle afferent spindle reflex connections in Amphibia (6) but it is known that the spindles do give excitatory monosynaptic input to homonymous motor neurons (11). This being so, the motor control system in such animals is remarkable in incorporating a positive feedback loop. Thus, a-motor neuron activity will excite spindles which will in turn add further excitation to the motor neurons (21). Positive feedback inherently leads toward instability, but evidently such an effect would be offset by the negative feedback contributed by the spindle unloading during active muscle shortening. It is possible to show that such a system can be perfectly stable given the proper choice of dynamic properties for the components and that the positive feedback could help to speed up muscle shortening. Houk (12) has also considered the consequences of the positive feedback situation in Amphibia and in a theoretical study indicated that stability could actually be improved by this feature. It also appears that if the characteristics of the muscle-load combination are matched by those of the intrafusal muscle fiber, then the system becomes insensitive to changes in spindle transducing properties. It should be emphasized, however, that the change in sensitivity of the spindle to stretch which occurs during active contraction represents a nonlinearity which is difficult to incorporate in such a theoretical analysis, and it is not possible at present to say whether or not it would have an important effect. In addition to the striking burst of activity at the onset of tetanic stimulation, there is another prolonged discharge in the relaxation phase. Taken with the behavior after curarization, these effects imply that the intrafusal muscle fibers shorten more rapidly than the extrafusal fibers and that subsequently the extrafusal fibers relax more quickly. It is also necessary to explain why the sensory response to motor stimulation (with extrafusal contraction blocked by curare) adapts so much less than does the response to passive stretch. It may be that contraction of the nonsensory parts of the intrafusal fibers stretches the sensory regions rapidly and holds them in this condition. If activation then spreads to the sensory region and increases its stiffness relative to that of the nonsensitive region, then this would explain why the active spindle has a reduced incremental sensitivity to stretch. Then the high dynamic sensitivity of the resting spindle would reflect the differential viscoelastic properties of the sensory and nonsensory
AMPIIJRTAN
SPINDLES
TN
ACTIVE
CONTRACTION
1x7
parts of the fibers (17) and the loss of the dynamic sensitivity during contraction would again imply activation of the sensory region to make it more viscous as well as stiffer than normal. Finally, in relaxation, the conspiciuous afferent burst would result if the sensory region were the first to lose its enhanced stiffness and viscosity. Leaving aside these conjectures regarding the biophysics of the amphibian spindle, it appears that the inbuilt rigid or-y coactivation in Amphibia may limit the utility of the spindles as linear feedback elements in active contractions. By contrast, such evidence as we have regarding normal movements in manmals (5, 28) shows that their independent fusimotor system permits some spindles to continue to act as linear length transducers with incremental sensitivity adapted to the type of movement being performed. REFERENCES 1. BESSOU, P., Y. LAPORTE, AND B. PAGES. 1968. A method of analysing the responses of spindle primary endings to fusimotor stimulation. J. Physiol. (London) 196: 37-45. 2. BROWN, M. C. 1971. A comparison of the spindles in two different muscles of the frog. J. Physiol. (London) 216 : 553-563. 3. BROWN, M. C. 1971. The response of frog muscle spindles and fast and slow muscle fibers to a variety of mechanical inputs. J. Pllysiol. (London) 218: 1-17. 3. BROWN, M. C., G. M. GOODWIN, AND P. B. C. MATHHEWS. 1969. After effects of fusimotor stimulation on the response of muscle spindle primary afferent endings. J. Physiol. (Lmrdou) 205 : 677-694. 5. CODY, F. W. J., L. M. HAKRISOK, AKD A. TAYLOR. 1975. Analysis of the activity of muscle spindles of the jaw-closing muscles during normal movements in the cat. J. Physiol. (LO&HZ) 253 : 565-582. 6. EBISESSON, S. 0. E. 1976. Morphology of the spinal cord. In R. LIJNAS ANI) W. PRECHT, Eds., Nczrvobioloyy nf tl~e Frog. Springer, Berlin. 7. E~ZAGUIRRE, C. 1957. Functional organisation of neuromuscular spindle in the toad. J. Nenrophgsiol. 20 : 523-542. 8. EYZAGURRE, C. 1958. Xodulntion of sensory discharges by efferent spindle cxcitation. J. Ncz~~~~hysiol. 21 : 465-480. 9. GRANIT, R. 1970. ?‘kc Zjasis of n’lrjtor C‘ollfrol. Academic Press, London. 10. GRAY, E. G. 1957. The spindle and extrafusal innervation of a frog muscle.
Proc. K. Sue. Lad.
[Biol.]
146 : 416-430.
11. HOL~IAN, K. C., H. S. MEIJ, AND B. J. MEYER. 1966. The existence of a monosynaptic reflex arc in the spinal cord of the frog. Exp. Nrwol. 14: 175-186. 12. HOUK, J. C. 1972. The phylogeny of muscular control configurations. Pages 125144 in H. DRISCIIEI, AND P. DEFIXAR, Eds., Biorybrtwctirs, 1’01. J. Gustav Fischer Verlag VEB, Jena. 13. ITO, F. 1968. Functional properties of tendon receptors in the frog. Jap. J. Pllysiol. 18 : 576-589. 14. KATZ, B. 1949. The efferent regulation of the muscle spindle in the frog. J. Exp. Z?io/. 26 : 201-217. 15. KUPFLER, S. W., AND R. W. GERAIID. 1947. The small nerve motor system to skeletal muscle. J. Nc~tropl~ysiol. 10 : 383-394.
188 16. 17. 18. 19. 20. 21. 22. 23. 24. 25. 26. 27. 28. 29. 30.
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S. W., Y. LAPORTE, AND R. E. RANSILZEIER. 1947. The function of the frog’s small nerve motor system. /. Ncurophysiol. 10 : 395-408. MATTHEWS, P. B. C. 1972. Marrmaliau Muscle Receptors cmd their Central Actions. Edward Arnold, London. MERMN, P. A. 1953. Speculations on the servo control of movement. Pages 247255 in J. L. MALCOLM, J. A. B. GRAY, AND G. E. W. WOLSTENHOLME, Eds., The Spinal Cord. Little, Brown, Boston. MURTHY, K. S. K. 1970. Studies on Transfer Fwzctions Comerncd in Voluntary Muscle Control. Ph.D. thesis. University of London. MURTHY, K. S. Ii., AND A. TAYLOR. 1971. Muscle spindle response to active muscle shortening in Bufo marinus. J. Physiol. (London) 213: 28P-29P. MURTHY, K. S. K., AND A. TAYLOR. 1971. The nature of the sensory feedback in the stretch reflex of the toad. Digest of the 9th International Conference on Medical and Biological Engineering, p. 31. MURTHY, K. S. K., AND A. TAYLOR. 1973. The use of Rana tig&zu for experiments on dorsal and ventral spinal nerve roots. J. Physiol. (Lolzdon) 234: 3P. RACK, P. M. H., AND D. R. WESTBURY. 1969. The effects of length and stimulus rate on tension in the isometric cat soleus muscle. J. Physiol. (London) 204: 443460. SMITH, R. S., AND Z. J. KOLES. 1974. Mechanical properties of muscle spindles in Xelzopzu laevis. Kybemetic 15 : 91-98. STEIN, R. B. 1974. Peripheral control of movement. Physiol. Rrv. 54: 215-243. TASAICI, I., AND K. MIZUTANI. 1944. Comparative studies of the activities of the muscle evoked by two kinds of motor nerve fibres. I. Myographic studies. Jap. J. Med. Sci. 10 : 237-244. TAYLOR, A. 1972. Muscle receptors in the control of voluntary movement. Paraplegia 9 : 167-172. TAYLOR, A., AND F. W. J. CODY. 1974. Jaw muscle spindle activity in the cat during normal movements of eating and drinking. Braift Res. 71: 523-530. VALLBO, A. B. 1971. Muscle spindle response at the onset of isometric voluntary contractions in man. Time difference between fusimotor and skeletomotor effects. J. Physiol. (London) 218 : 405432. VALLBO, A. B. 1974. Human muscle spindle discharge during isometric voluntary contractions. Amplitude relations between spindle frequency and torque. Acta Physiol. Stand. 90 : 319-336. KUFFLER,
Spindle
Behavior
K. Sllcrrirlgfolz
Scl~ool
S.
during Active in Amphibia
PC. MUKTIIY
AXI)
A.
Muscle
TAYLOR
of Physiology, St. Tho~ms’s Hospiful Loldo~, SE1 7,511, l31glmd Kcccizwd
October
Contraction
r Mcdicnl
Sclronl,
5, 192
The effects of different mechanical loads on discharge of frog and toad muscle spindles were studied during active contraction of twitch muscles. Intrafusal driving, which accompanies extrafusal contraction, was found to maintain spindle discharge to a degree dependent on the compliance of the load. Intrafusal contraction alone could not drive afi’erent discharge to maximum frequencies, which were reached only with muscle stretch following a period of tetanic stimulation. Maximal intrafusal driving effects were reached at low rates of stimulation (5 to 10/s). E ven with a very compliant load, which caused silencing during a developed tetanic contraction, there was an initial burst of activity from the spindle afferents. There was also a prominent burst at the end of stimulation. The consequences of these properties of amphibian spindles are discussed and the potential existence of a positive feedback loop is indicated. The results provide some basis for understanding the significance of the separation of intrafusal and estrafusal motor pathways in mammals.
INTKODUCTION The significance of intrafusal muscle contraction in the regulation of movement by muscle spindles has heen considered almost exclusively in mammalian species. Granit [see (9) for review] favored the idea of a close linkage between skeletomotor and fusimotor driving from the central nervous system, acting principally to ensure that spindle discharge is maintained during active muscle shortening. As pointed out by Matthews (17), this hardly seems to provide an adequate explanation in terms of evolutionary advantages for the emergence of a dual, independent fusimotor Abbreviations : L,,--irz sift length ; VK-ventral roots. r This work was supported by the Wellcome Trust. Dr. and address for reprint requests is Division of Neurosurgery, Medical School, Houston,, Texas 77030.
Murthy’s present address University of Texas,
175 00144886/78/060.?-0175$02.00/O All
Copyright Q 1978 rights Iof reproduction
by Academic Press, Inc. in any form reserved.
176
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system. The servo hypothesis of Merton (18) implied that special advantages arose from driving movement via the fusimotor route. This now seems much less attractive on fundamental grounds (17, 25, 27) and in the light of more recent direct observations on mammalian spindles (28-30). In any case, the existence of separate static and dynamic fusimotor systems has become clear only since the formulation of this hypothesis, and there is a lack of any comprehensive theory to incorporate the newly recognized complexities of the mammalian spindle in a general scheme of motor control. In Amphibia, on the other hand, it appears that intrafusal innervation arises by way of branches from the extrafusal skeletomotor innervation (7, 8, 10, 14). Such a situation represents the simplest and most rigid form of “q linkage.” It would therefore seem appropriate to attempt to understand the amphibian arrangement and its limitations as a background to mammalian studies. Accordingly, in the present work a study is made of muscle spindle behavior in frogs and toads when length changes are caused by active contraction against a variety of spring loads (20) as an approximation to the natural situation. The amphibian motor system consists of fast-contracting “twitch” muscle fibers and slow-contracting “tonic” muscle fibers (26), both of which feature common intra- and extrafusal motor innervation (10). These experiments are restricted to single and repetitive stimulation of twitch muscles in the hind limbs of Bufo and Rana. METHODS To study spindle behavior during repeated motor stimulation, a preparation was needed in which a good circualtion could be maintained for long periods. This was possible with large (300-g) specimens of Bufo vnarinus and Rana tigrina. Urethane (1.5 g/kg) was injected as a 15% solution into a lymph sac with supplements, when necessary, injected at lo-fold dilution. All the muscles of one hind limb, except the muscle under investigation, were denervated and the animal was mounted in a specially designed frame (19, 22). Laminectomy was done to expose the cord and nerve roots from the fourth to tenth laminae. The spinal roots are usually 10 pairs, the hind limb muscles being innervated from spinal roots 8, 9, and 10. These were cut, dorsal and ventral, close to the cord near the third and fourth laminae, making available a maximum length of approximately 3 cm of the roots. A paraffin-filled pool was built up using 4% agar gel and gauze packing. A total of 28 toads and 110 frogs were used in this investigation. Spindles in a pure fast-twitch muscle (sartorius) and in a mixed muscle (gastrocnemius) were studied. Both are innervated mainly from spinal
AMPHIBIAN
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177
roots 9 and 10. Functionally single spindle afferents were isolated from either root by progressive splitting, a process which is much easier in Rana than in Bufo. Spindle afferents are said to be characterized in frogs by being the only muscle stretch receptors respondin, v to passive stretch of the inert muscle (13). We have not found this entirely dependable because receptors identified as tendon organs in all other respects sometimes behaved in this way. The usual test for spindles, silencing during the rising phase of a twitch, is confused by the intrafusal excitation and it was found best to rely on (a) tonic response to passive stretch, (b) tendency to silencing in relatively isometric contraction, and (c) increased discharge during relaxation after a tetanic contraction. Ventral roots 9 and 10 (VR9 and 10) were placed on separate pairs of chlorided silver wire electrodes for stimulation from isolated stimulators. Unless otherwise stated, stimulus intensity was adjusted to be just maximal for fast motor fibers, as indicated by the muscle twitch. By selective blocking of fast motor fibers and increasing stimulation strength to involve any slow fibers present (15, 16), it was confirmed that sartorius in the frog was purely twitch muscle and had no slow motor system effects on its spindle. For testing responses to stretch, the muscle tendon was attached to an electromechanical vibrator (Goodman, Type V50) driven by a DC power amplifier (AIM Electronics, WPA 116). Variable compliance was arranged by attaching the tendon to a strain gauge by means of various coiled steel springs. The force recorded was converted to length changes of the muscle by scaling with the spring compliance. Muscle length was set to be optimal for twitch tension development. Experiments were carried out at room temperature (18 to 22°C). Because of the irregularity of firing of amphibian spindles, instantaneous frequency plots were not very satisfactory. Instead, a reasonable degree of smoothness and reliability was achieved by producing ensemble averages of firing frequency across a number of stimulus presentations, using an averaging computer (Medelec, AVM3) or a general purpose digital computer (Varian 620L). RESULTS Ejfects of Ventral Root StilrLlrlation. In both frogs and toads it was usually found that any given spindle afferent showed evidence of intrafusal excitation predominantly from one ventral root. Figure 1 shows typical behavior recorded from a gastorcnemius spindle in Rana. Stimulation of VR9 caused silencing during a twitch (Fig. la) and VRIO stimulation (b) caused a brief burst in contraction and a second, more prolonged
MURTHY
FoRCE
lkg for 1 Zkgfor
AND
b-f a
FIG. 1. Responses of spindle afferent from to VR9(a) and VRlO(b). c-f-Repetitive 20/s, respectively. Isometric force recording.
TAYLOR
I
8
0.5 set gastrocnemius stimulation of
of frog to single stimuli VRlO at 5, 10, 15, and
discharge during relaxation. Figures lc-f show responses to tetanic stimulation of VRlO at increasing frequencies. It is noticeable that the first stimulus of each train elicited several afferent impulses, whereas subsequently only a single impulse was generally produced immediately following each stimulus. Considering the single-twitch response (b) it is clear that two factors are concerned in initiating spikes: first the activation of intrafusal muscle fibers and second the stretching of the spindle during the extrafusal relaxation. Consequently, the afferent activity actually seen during a contraction must depend not only on the motor nerve firing frequency and the degree of unloading, but also on the smoothness or degree of fusion of the intra- and extrafusal contractions. However, leaving aside effects of incomplete fusion, it would be expected that the afferent discharge frequency should depend on the difference between intrafusal and extrafusal muscle shortening. If this were so, then adding to the series elastic ,element by interposing a spring between the
AMPHIBIAN
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tendon and the strain gauge should reduce the discharge during active shortening. In principle this is the case, as shown in Fig. 2, in which tetanic contractions are excited at various frequencies and against various load compliances. Column A with 10/s stimulation shows that increasing compliance leads to almost-total elimination of the sustained firing for compliances greater than 16 pm/g. Expressed in terms of maximal tetanic force for stimulation of VRlO (PO) this is 9.6 mm/PO. At any given compliance, increasing stimulus frequency from 10 to 20/s also substantially reduces the afferent discharge, both shortening the initial burst and reducing any tendency to fire in the plateau of contraction. The obvious implication that shortening reaches a maximmii in intrafusal fibers at lower frequencies than in extrafusal fibers must be reserved because propagated intrafusal activity may break clown at high frequencies. At the same time, the initial burst remains prominent, and this suggests that initially the intrafusal muscle fibers shorten faster than the extrafusal fibers. Note particularly that the timing of the afferent spikes in tetani at 10/s is such that they appear to be generated after each stimulus during the onset of increased muscle shortening rather than durin g the ensuing relaxation. The possibility that there might have been some involvement of the tonic motor system was checked by additional studies made on sartorius in Rana, which in R. tcn~j~~~ria. and R. ~ijicns appears to be purely fast [ (2), and above Methods section].
b
d
TBllBlOll 170 p for for d I 353g
il.b&C
I
spikes 40 pv
FIG. 2. Responses of spindle afferent from gastrocnemius of toad during tetanic contraction against a variety of loads. A-C-Stimulation of VRlO at 10, 15, and 20/s,
respectively. a-c--Spring Resting length constant.
compliances of 3.5, 16.1, 32.3, and 90.9 pm/g, respectively. Horizontal bars indicate timing of l-s duration tetani.
180
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0’
-ii?
HSEC
FIG. 3. Tetanic stimulation of frog sartorius through VRIO at 10, 15, and 20/s (from above, downward). Left-hand column, isometric conditions ; right-hand column, spring load compliance 25 pm/g. Spindle response (dotted) is the instantaneous frequency averaged at 75ms intervals for 10 consecutive stimulus presentations (see Methods).
Figure 3 shows that the results of normal tetanic stimulation of the sartorius at 10, 15, and 20/s are essentially the same as in the gastrocnemius, but the display has been made more quantitative and reliable by showing firing frequency averaged for 10 stimulus presentations, with less complete fusion at the lower frequencies. It is evident that in this case some sign of incomplete fusion of the effects of stimulation persists to as much as 20/s, particularly in the isometric records in the left-hand column. At the same time, while the peak firing frequency changes very little with increased stimulus frequency, the mean firing rate does rise. It is quite clear that the peaks of frequency are due to intrafusal activity rather than to extrafusal relaxation because there is a well-marked delay after the last stimulus of each train before the onset of the relaxation burst, in line with the observed slow onset of extrafusal relaxation. Contractions against
AMPHIBIAiX
SPINDLES
IN
ACTIVE
181
CONTRACTION
a compliant load (right-hand column) show evidence of progressive LIIIloading of the spindle at stimulus rates above 15/s, confirming the view expressed above that extrafusal contraction can continue to increase to higher frequencies than can intrafusal contraction. Some further insight into the relationship of intrafusal and extrafusal contraction is given by reference to Fig. 4, showing the effects of critical curarization (14). In (a) the stimulation of normal muscle at 5/s gives a very incompletely fused tetanus against a load of compliance of 25 pm/g, and the afferent spikes occur mostly in relation to the extrafusal relaxation (which 1s thus presumably faster than the intrafusal). Close arterial infusion of 200 pg curare completely blocked extrafusal contraction (b) but left an afferent discharge reaching 50/s very abruptly, due to intrafusal contraction. The “frequencygram” showed only slight modulation in time with stimulation so that even at this frequency intrafusal contraction must be reasonably completely fused ( 1). I ncreasing stimulus frequency
0 50cn
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FIG. 4. Effect on spindle discharge from gastrocnemius of frog of progressive curarization. Stimulation of VRlO at 5/s (a) before and (b) after intra-arterial injection of 200 pg d-tubocurarine chloride; c-stimulation at 15/s ; and d-stimulation repeated after a further dose (600 pg) of curare. Spring load of compliance, 25 pm/g. Spindle firing shown as two superimposed traces of instantaneous frequency.
182
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to 15/s (c) caused some extrafusal contraction to appear slowly such that shortening by about 1 mm cancelled the effect of intrafusal contraction. It is notable that the the initial response to 15/s stimulation is only very little greater than that to 5/s stimulation. Finally, increasing the dose of curare so as to practically eliminate extrafusal shortening with stimulation at 15/s (d) showed a firing pattern very much like that in (b). One may conclude that intrafusal effects are of rapid onset, tend to fuse at low frequencies, and virtually saturate at stimulus rates of 5/s and afferent firing rates of 50 to 60/s. The highest afferent frequencies (120/s) are achieved only with the addition of extrafusal lengthening. Recordings made with a compliant load (Figs. 2, 3) show a very marked discharge at the end of tetani. This must be due to extra force transmitted to the innervation zone of the intrafusal fibers when the extrafusal muscle relaxes while some intrafusal contraction still persists. That intrafusal activation can outlast the stimulation is demonstrated by Figs. 4b and d where the afferent firing does not diminish appreciably for some 300 ms after the end of stimulation. Thus the realxation firing seen in Fig. 2 and in Figs. 4a and c may be closely related to the initial burst sometimes seen during ramp stretches of mammalian spindles (4). Another feature of these records which should be noticed is that adaptation of the afferent discharge is small and slow in the absence of extrafusal shortening. In Figs. 4b and d there is very little diminution of firing during the first 0.5 s of tetanic stimulation. Dynamic Properties. The time course of the spindle firing is best studied in records smoothed by averaging across a number of stimulus presentations. Also, because we wish to derive data generally representative of the ensemble of muscle spindles, there is some advantage in examining multiunit spindle afferent records. In Figs. 5a and b, a four-unit record has been averaged for 10 sweeps and the firing expressed in arbitrary units of frequency estimated in 20-ms time bins. The maximum firing is reached very soon after the stimulus onset and thereafter decays with a time course resembling that of extrafusal muscle shortening. Indeed, normalized semilogarithmic plots of firing frequency and muscle shortening from the records of Fig. 5, seen in Fig. 6, reveal that both are reasonably well described in the first 0.5 s as simple exponentials, with essentially similar time constants (in the range 0.25 to 0.16 s). Thus, it appears that most of the adaptation of sensory discharge seen in tetanic contractions against spring loads can be accounted for by the mechanical unloading due to extrafusal shortening. This is consistent with the findings illustrated in Fig. 4 that very little adaptation of afferent discharge during the first 0.5 s of a tetanus occurs when extrafusal contraction is blocked by curare.
AMI’HIIIIAN
Si’INI)LES
IN
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CONTKACTION
183
FIG. 5. Ensemble response of four spindle afferents from gastrocnemius of toad. Sl)indle firing averaged for 10 cycles of stimulus presentation for 1 s at 15/s (horizontal bar) and sho\vn as puststimulus histograms representing arbitarary units of frequency estimated in ZO-ms time bins. a-Load compliance, 4.29 pm/g; b-compliance, 1.02 pm/g.
Such behavior is in contrast to the well-known passive stretch properties of frog spindles, as illustrated in Fig. 7,4. Here a ranq) stretch gives a nlarkedly atlapting afferent discharge. As seen in Fig. 7B the effect of nlotor stimulation is evidently to increase the background discharge frequency and to reduce the static and dynamic incremental sensitivities to stretch. Motor stimulation was also found to reduce considerably the effect of controlled passive shortening. These findings are consistent with those of Brown (2, 3). The contrary results of Smith and Kales (24), who found that isolated Xe~op~s spindles showed high sensitivity to stretch only when intrafusal fibers were active, nlay have been due to different conditions, in that Smith and Kales used small, slow movements [approximately 1 R inaxiniun~ it2 sits length (L,,) at 0.25s L,,/s], whereas we were concerned with movements within the likely normal physiologic range of as 171nch as S7& L, stretch and 20% L,,/ s velocity. In the light of the reduction of sensitivity to such length changes seen here during background niotor stimulation, it is evident that part of the conipensation for active shortening of muscle is due to this and part to the shortening of intrafusal fibers.
DISCUSSION The primary purpose of this work was to examine the behavior of muscle spindles in active contractions against a variety of tnechanical loads. Aqhibia were studied because the inbuilt rigid “fry coactivation” which
MURTHY
AND
TAYLOR
025 TIME
05
bed
FIG. 6. Semilogarithmic plots of spindle frequency and muscle length in the first 0.5 s of tetanic stimulation of toad gastrocnemius at 15/s. Data of Fig. 5. Time constants (seconds) shown estimated from linear regressions. A, B-Load compliance, 1.5 am/g; C, D-compliance, 5 pm/g.
they display seemedto place them in the position of a simple model of one hypothesis for mammalian spindle function. Attention was restricted to the twitch or fast motor system. This could be stimulated through ventral roots apparently in isolation in the gastrocnemius by using shock strengths just maximal for twitch responses. The sartorius in Rana tigrina is apparently entirely fast muscle and we were unable to find any evidence of slow motor innervation of intrafusal fibers. This agrees with Brown (2), who found in Rana tenzporaria and Rana pipiens that no sartorius spindles were excited by succinylcholine. No qualitative differences were apparent between spindle afferent units in gastrocnemius and sartorius in Bufo marinus or Rana tigrina.
AMPHTRTAN
1 x,5
SPTNDLES TX ACTIVE CONTRACTTON
A difficulty in setting up these experiments to deduce how amphibian spindles behave in normal movement was uncertainty about the appropriate frequency of stimulation. Electronlyogram recordings from gastrocnetnius in normal Bzffo shavings (19) showed units firing at 15 to 30/s when the leg was passively flexed. In the present experiments, frequencies were generally limited to 20/s to avoid fatigue, but it would be interesting to repeat some of the observations with short bursts of much higher frequencies. This is more likely to be the way the muscles are used in jumping. It is also recognized that the synchronous volleys used here in single ventral roots are likely to have effects different from those of natural asynchronous discharge of motor neurons [see Rack and Westbury (23) 1. The incompletenessof tetanic fusion which contributed to spindle discharge at low-frequency stimulation might in future experiments be avoided by rotational stimulation of a number of ventral root filaments as introduced by Rack and Westbury. Nevertheless, the general expectations of the experiments were realized in that the tendency for a spindle to be silenced during shortening is counteracted, at least in part, by simultaneous intrafusal activation. The amount of afferent discharge during an active muscle contraction de-
[
lmm
FIG. 7. Effects of VRlO stimulationon response of frog sartoriusafferent to ramp stretch. A-No stimulation; B-stimulation at threshold for spindleactivation at 20/s; C-fast fibers blocked and stimulation strength increasedsevenfoldand to SO/s; D-stimulation at twice threshold,20/s. Heavy dots in B and D indicatemean frequencyestimatedat 100-msintervals.
186
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pended on the compliance of the spring load, being greatest with loads of lowest compliance. This behavior would be quite appropriate for a motor control system using load compensation via the spindles, especially to improve the speed of response at the onset of a movement. However, it is not possible from the present experiments to say how effective such a load compensation would be in practice because we do not know the strength of the reflex connections. Remarkably little work has been reported specifically on muscle afferent spindle reflex connections in Amphibia (6) but it is known that the spindles do give excitatory monosynaptic input to homonymous motor neurons (11). This being so, the motor control system in such animals is remarkable in incorporating a positive feedback loop. Thus, a-motor neuron activity will excite spindles which will in turn add further excitation to the motor neurons (21). Positive feedback inherently leads toward instability, but evidently such an effect would be offset by the negative feedback contributed by the spindle unloading during active muscle shortening. It is possible to show that such a system can be perfectly stable given the proper choice of dynamic properties for the components and that the positive feedback could help to speed up muscle shortening. Houk (12) has also considered the consequences of the positive feedback situation in Amphibia and in a theoretical study indicated that stability could actually be improved by this feature. It also appears that if the characteristics of the muscle-load combination are matched by those of the intrafusal muscle fiber, then the system becomes insensitive to changes in spindle transducing properties. It should be emphasized, however, that the change in sensitivity of the spindle to stretch which occurs during active contraction represents a nonlinearity which is difficult to incorporate in such a theoretical analysis, and it is not possible at present to say whether or not it would have an important effect. In addition to the striking burst of activity at the onset of tetanic stimulation, there is another prolonged discharge in the relaxation phase. Taken with the behavior after curarization, these effects imply that the intrafusal muscle fibers shorten more rapidly than the extrafusal fibers and that subsequently the extrafusal fibers relax more quickly. It is also necessary to explain why the sensory response to motor stimulation (with extrafusal contraction blocked by curare) adapts so much less than does the response to passive stretch. It may be that contraction of the nonsensory parts of the intrafusal fibers stretches the sensory regions rapidly and holds them in this condition. If activation then spreads to the sensory region and increases its stiffness relative to that of the nonsensitive region, then this would explain why the active spindle has a reduced incremental sensitivity to stretch. Then the high dynamic sensitivity of the resting spindle would reflect the differential viscoelastic properties of the sensory and nonsensory
AMPIIJRTAN
SPINDLES
TN
ACTIVE
CONTRACTION
1x7
parts of the fibers (17) and the loss of the dynamic sensitivity during contraction would again imply activation of the sensory region to make it more viscous as well as stiffer than normal. Finally, in relaxation, the conspiciuous afferent burst would result if the sensory region were the first to lose its enhanced stiffness and viscosity. Leaving aside these conjectures regarding the biophysics of the amphibian spindle, it appears that the inbuilt rigid or-y coactivation in Amphibia may limit the utility of the spindles as linear feedback elements in active contractions. By contrast, such evidence as we have regarding normal movements in manmals (5, 28) shows that their independent fusimotor system permits some spindles to continue to act as linear length transducers with incremental sensitivity adapted to the type of movement being performed. REFERENCES 1. BESSOU, P., Y. LAPORTE, AND B. PAGES. 1968. A method of analysing the responses of spindle primary endings to fusimotor stimulation. J. Physiol. (London) 196: 37-45. 2. BROWN, M. C. 1971. A comparison of the spindles in two different muscles of the frog. J. Physiol. (London) 216 : 553-563. 3. BROWN, M. C. 1971. The response of frog muscle spindles and fast and slow muscle fibers to a variety of mechanical inputs. J. Pllysiol. (London) 218: 1-17. 3. BROWN, M. C., G. M. GOODWIN, AND P. B. C. MATHHEWS. 1969. After effects of fusimotor stimulation on the response of muscle spindle primary afferent endings. J. Physiol. (Lmrdou) 205 : 677-694. 5. CODY, F. W. J., L. M. HAKRISOK, AKD A. TAYLOR. 1975. Analysis of the activity of muscle spindles of the jaw-closing muscles during normal movements in the cat. J. Physiol. (LO&HZ) 253 : 565-582. 6. EBISESSON, S. 0. E. 1976. Morphology of the spinal cord. In R. LIJNAS ANI) W. PRECHT, Eds., Nczrvobioloyy nf tl~e Frog. Springer, Berlin. 7. E~ZAGUIRRE, C. 1957. Functional organisation of neuromuscular spindle in the toad. J. Nenrophgsiol. 20 : 523-542. 8. EYZAGURRE, C. 1958. Xodulntion of sensory discharges by efferent spindle cxcitation. J. Ncz~~~~hysiol. 21 : 465-480. 9. GRANIT, R. 1970. ?‘kc Zjasis of n’lrjtor C‘ollfrol. Academic Press, London. 10. GRAY, E. G. 1957. The spindle and extrafusal innervation of a frog muscle.
Proc. K. Sue. Lad.
[Biol.]
146 : 416-430.
11. HOL~IAN, K. C., H. S. MEIJ, AND B. J. MEYER. 1966. The existence of a monosynaptic reflex arc in the spinal cord of the frog. Exp. Nrwol. 14: 175-186. 12. HOUK, J. C. 1972. The phylogeny of muscular control configurations. Pages 125144 in H. DRISCIIEI, AND P. DEFIXAR, Eds., Biorybrtwctirs, 1’01. J. Gustav Fischer Verlag VEB, Jena. 13. ITO, F. 1968. Functional properties of tendon receptors in the frog. Jap. J. Pllysiol. 18 : 576-589. 14. KATZ, B. 1949. The efferent regulation of the muscle spindle in the frog. J. Exp. Z?io/. 26 : 201-217. 15. KUPFLER, S. W., AND R. W. GERAIID. 1947. The small nerve motor system to skeletal muscle. J. Nc~tropl~ysiol. 10 : 383-394.
188 16. 17. 18. 19. 20. 21. 22. 23. 24. 25. 26. 27. 28. 29. 30.
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S. W., Y. LAPORTE, AND R. E. RANSILZEIER. 1947. The function of the frog’s small nerve motor system. /. Ncurophysiol. 10 : 395-408. MATTHEWS, P. B. C. 1972. Marrmaliau Muscle Receptors cmd their Central Actions. Edward Arnold, London. MERMN, P. A. 1953. Speculations on the servo control of movement. Pages 247255 in J. L. MALCOLM, J. A. B. GRAY, AND G. E. W. WOLSTENHOLME, Eds., The Spinal Cord. Little, Brown, Boston. MURTHY, K. S. K. 1970. Studies on Transfer Fwzctions Comerncd in Voluntary Muscle Control. Ph.D. thesis. University of London. MURTHY, K. S. Ii., AND A. TAYLOR. 1971. Muscle spindle response to active muscle shortening in Bufo marinus. J. Physiol. (London) 213: 28P-29P. MURTHY, K. S. K., AND A. TAYLOR. 1971. The nature of the sensory feedback in the stretch reflex of the toad. Digest of the 9th International Conference on Medical and Biological Engineering, p. 31. MURTHY, K. S. K., AND A. TAYLOR. 1973. The use of Rana tig&zu for experiments on dorsal and ventral spinal nerve roots. J. Physiol. (Lolzdon) 234: 3P. RACK, P. M. H., AND D. R. WESTBURY. 1969. The effects of length and stimulus rate on tension in the isometric cat soleus muscle. J. Physiol. (London) 204: 443460. SMITH, R. S., AND Z. J. KOLES. 1974. Mechanical properties of muscle spindles in Xelzopzu laevis. Kybemetic 15 : 91-98. STEIN, R. B. 1974. Peripheral control of movement. Physiol. Rrv. 54: 215-243. TASAICI, I., AND K. MIZUTANI. 1944. Comparative studies of the activities of the muscle evoked by two kinds of motor nerve fibres. I. Myographic studies. Jap. J. Med. Sci. 10 : 237-244. TAYLOR, A. 1972. Muscle receptors in the control of voluntary movement. Paraplegia 9 : 167-172. TAYLOR, A., AND F. W. J. CODY. 1974. Jaw muscle spindle activity in the cat during normal movements of eating and drinking. Braift Res. 71: 523-530. VALLBO, A. B. 1971. Muscle spindle response at the onset of isometric voluntary contractions in man. Time difference between fusimotor and skeletomotor effects. J. Physiol. (London) 218 : 405432. VALLBO, A. B. 1974. Human muscle spindle discharge during isometric voluntary contractions. Amplitude relations between spindle frequency and torque. Acta Physiol. Stand. 90 : 319-336. KUFFLER,
