J. Physiol. (1977), 268, pp. 827-861 With 17 text-figures Printed in Great Britain

827

ON THE SUBDIVISION OF STATIC AND

DYNAMIC FUSIMOTOR ACTIONS ON THE PRIMARY ENDING OF THE CAT MUSCLE SPINDLE BY F. EMONET-DIRINAND, Y. LAPORTE, P. B. C. MATTHEWS AND J. PETIT From the Laboratoire de Neurophy8iologie, College de France, 75231 Paris Cedex 05, France

(Received 14 October 1976) SUMMRY

1. Using large ramp and triangular stretches a survey has been made of the effect of stimulating single y fusimotor fibres on primary endings of muscle spindles in the peroneus brevis to see whether 'intermediate' types of fusimotor action could be recognized, falling between the well known static and dynamic types. 2. Responses were classified into six groups, as detailed on pp. 844-846, ranging from apparently 'pure' dynamic action (category I) to apparently 'pure' static action (category VI). Models for a putative mixed action were produced by combining the stimulation of a static and of a dynamic fibre to the same spindle. The clearest sign of static action was firing on the releasing phase of the stretch. The essential sign of dynamic action, which survived combination with the more dominant static action, was the slow adaptive decay of firing with a time constant of about 05 sec that occurs on the plateau of the ramp stretch. 3. Out of 153 responses, each elicited from a primary ending on stimulation of a single fusimotor fibre, 67 % were apparently 'pure' examples of dynamic and static action. The remaining 33 % of responses were to some degree suggestive of an admixture, in various proportions, of static and dynamic actions. For only 18 % of them was there firm indication of such admixture. 4. When a given fibre was tested on more than one ending then, with one exception out of thirty-six instances, its action always proved to be either predominantly static or predominantly dynamic. There was no special tendency for an axon with a mixed action on one spindle to have a similarly mixed action on other endings so that individual fusimotor fibres were best classified as static or dynamic without intermediate grades.

828 F. EMONET-DJ9NAND AND OTHERS 5. Simultaneous stimulation of two fusimotor fibres eliciting apparently 'pure' static and dynamic actions, could mimic all the intermediate types of action. 6. The results are discussed in relation to recent studies, especially those based on glycogen depletion. It was concluded that dynamic action arises from activation of the bag, intrafusal muscle fibre, and that static action arises from the bag2 and chain fibres, whether acting individually or collaboratively. The intermediate actions are suggested to arise from an overlap of motor innervation to contrasting types of intrafusal muscle fibre. 7. On the basis of effects on the regularity of the afferent discharge the findings support the view that a given static action axon can innervate bag2 and chain fibres in various proportions in different spindles, so that they do not provide separable effector pathways. 8. Responses to large amplitude sinusoidal stretching were also studied in relation to our classification. INTRODUCTION

For the last 15 years it has been generally agreed that y motor fibres may be usefully classified on functional grounds into static and dynamic fibres by virtue of the effects of their stimulation on the response of spindle primary endings to various mechanical stimuli. This functional classification followed immediately upon the structural classification of intrafusal muscle fibres into nuclear-chain and nuclear-bag fibres along with the suggestion that these two anatomical entities received an independent motor innervation. On the balance of indirect evidence many adopted the hypothesis that the dynamic fibres achieve their specialized action through the nuclear-bag fibres and conversely that the static fibres act via the nuclear-chain fibres (Matthews, 1972). However, the simplest view of such a one to one correspondence between structure and function has been progressively eroded by experiments which combine experimental and histological approaches (Barker, Emonet-D6nand, Laporte, Proske & Stacey, 1970, 1973; Barker, Bessou, Jankowska, Pages & Stacey, 1972; Bessou & Pages, 1975; Brown & Butler, 1973, 1975). Dynamic fibres are indeed found to supply nuclear-bag fibres almost exclusively, but static fibres commonly supply nuclear-bag fibres as well as, or even instead of, nuclear-chain fibres. However, in experiments on isolated spindles a given individual nuclear-bag fibre has never yet been seen to be supplied by both functional types of axon (Bessou & Pages, 1975; Boyd, Gladden, McWilliam & Ward, 1977). This bears emphasis since nuclear-bag fibres are now being divided into two types

829 STATIC AND DYNAMIC SUBDIVISIONS with the suggestion that one type is responsible for the characteristic 'dynamic' action of some fusimotor fibres, whereas the'other type of bag fibre is held responsible for a 'static' action similar in many ways to that arising from contraction of nuclear-chain fibres. Thus, on the basis of observation of living isolated spindles Boyd et al. (1977) distinguish between 'static nuclear-bag fibres' and 'dynamic nuclear-bag fibres' depending upon the type of fusimotor fibre that activated them; these fibres also differ in certain mechanical aspects of their contraction, in their passive behaviour after step-stretch, and in their sensitivity to topically applied acetylcholine (Boyd, 1976; Gladden, 1976). Again, on the basis of combined histochemical and ultrastructural observations on single fixed spindles Banks, Barker, Harker & Stacey (1975) distinguish between bag, and bag2 fibres, with the bag2 fibres much closer to the chain fibres in their histochemical profile and ultrastructure than they are to the bag, fibres. There appears every prospect that these two modes of classification will shortly be consolidated with the equation that bag, fibres = dynamic bag fibres and are responsible for dynamic actions, while bag2 fibres = static bag fibres and are responsible for static actions along with the chain fibres. Thus the matter of the correspondence between functional and anatomical classifications appears close to resolution, but before this can be achieved various difficulties require to be dealt with. In particular, in recent work on tenuissimus spindles, stimulation of single static fibres has been found to deplete the glycogen, indicating neural activation, as much in bag1 fibres as in the expected bag2 fibres (Barker, EmonetDenand, Harker, Jami & Laporte 1976); this is in line with earlier work in which the two kinds of bag fibre were not distinguished (Brown & Butler, 1973). In addition, preliminary work on the response of spindles to small sinusoidal stretches suggested that a given fusimotor fibre may commonly change its action from dynamic to static on increasing the frequency of its stimulation (Emonet-Denand, Joffroy & Laporte, 1972). However, it is now recognized that there are considerable difficulties in interpreting such observations in terms of conventional static and dynamic actions, as defined on using ramp stretching (Hulliger, Matthews & Noth, 1976) so that on their own these preliminary sinusoidal findings can no longer be considered especially cogent. This uncertainty led us to use large amplitude ramp stretches to look again at the classification of a number of fusimotor fibres, chosen randomly with respect to their function, to see how clearly they all fell into the conventional 'static' and 'dynamic' classes and whether any would be better classified as 'intermediate' in their actions. We were also concerned that histological and micro-electrode work are being pushed to a

F. EMONET-DENAND AND OTHERS 830 degree of refinement far above that being employed in the classification of the individual fusimotor fibres being studied, or indeed that used at the inception of the static-dynamic classification itself (cf. Brown, Crowe & Matthews, 1965, p. 156). The outcome of the present experimental reevaluation, as already briefly noted (Emonet-Denand, Laporte, Matthews & Petit, 1976), has been that on the majority of occasions the action of a fusimotor fibre on a given primary ending has lent itself to classification as purely static or as purely dynamic. However a certain number of actions that are predominantly of one kind appeared to have been 'modified' by the other type of action and a few could not be classified either way. This had not led us to jettison the classification, since virtually every individual fusimotor fibre was consistent in being largely static or largely dynamic on all the spindles that it influenced. The present findings serve to soften any conceptual difficulty experienced on finding histologically that a given fusimotor fibre includes the unexpected kind of intrafusal fibre in the distribution of its innervation, provided that it primarily supplies the expected kind of fibre. In other words, the distribution of motor innervation to the different intrafusal muscle fibres shows a degree of overlap, rather than a complete dichotomy. In view of the difficulty of 'wiring up' a spindle correctly during ontogenesis this seems hardly surprising, but it may also be that a degree of non-specificity serves some definite function. METHODS Preparation. The experiments were performed on thirteen cats anaesthetized with pentobarbitone sodium using techniques similar to those described earlier (EmonetD6nand, Jami & Laporte, 1975). The right hind limb was widely denervated except for the peroneus brevis muscle which was connected to an electromagnetic stretcher. Functionally single afferent fibres from this muscle were isolated in dorsal root filaments and single y motor fibres in ventral root filaments. The afferents were judged to supply primary endings on the basis of their conduction velocity and on their dynamic responsiveness. The y fibres were characterized by their conduction velocity and by their failure to produce observable electromyographic activity. The various action potentials and any e.m.g. were recorded by a unipolar electrode placed under the nerve close to the muscle. The detection of such single fibre potentials, their characterization as all-or-none responses, and the ease of obtaining matched afferent-efferent pairs were all aided by restricting the nerve supply to the muscle to a single fine branch. The signal to noise ratio was then good enough for it to be guaranteed that stimulation of the filament with a 'single y fibre' did indeed excite only a single y fibre. In a typical experiment up to half a dozen primary endings would be isolated first, followed by a series of y fibres detected by their conduction velocity. Immediately after it was isolated each y fibre was tested on each afferent; when an effect was found it was studied forthwith using a ramp stretch and a standard range of frequencies of stimulation (20, 35, 50, 75, 100 and 150/sec). The various afferent responses were observed at the time of the experiment on a storage oscilloscope using an instantaneous frequency display and also recorded on magnetic tape for

STATIC AND DYNAMIC SUBDIVISIONS

831

subsequent production of photographic records to allow closer inspection and measurement. 153 examples of the action of a fusimotor fibre on a primary ending were studied. They should not have been biased towards those with particularly strong effects on the spindle, as tends to happen when fusimotor fibres are initially sought by stimulating thick ventral root filaments (containing many a fibres) to find a filament containing a y fibre influencing a particular primary ending, and then subdividing the filament. There may perhaps have been a slight biasing of the population studied, as compared with the whole population of y efferents, towards those with a dynamic action since when there was not time to isolate and study every gamma potentially available we tended to prefer 'good' dynamic actions, while occasionally passing over those with an apparently 'ordinary' static action; this was simply because it is harder to find dynamic y fibres, of which there are only usually one or two per spindle, than static fibres, of which there are always several. Altogether fifty primary endings were studied with eighty-two y axons, of which twentyfive were dynamic and fifty-four were static in their over-all action. In thirty cases the effect was studied of combining the stimulation, nearly always at several frequencies for each, of a static and of a dynamic axon acting on the same ending. Stretching. The ramp stretch was usually 2 mm, but was varied between 1P5 and 3 mm in different experiments; these may all be considered 'large' for peroneus brevis since its total range of movement is 4-5 mm. The final extension was normally 1-1-5 mm short of maximal length. The rising phase of the ramp was set to last about 0-3 sec, to give a velocity of about 6 mm/sec. Its falling phase was made deliberately slower (fall time about 1 sec, velocity about 2 mm/sec) to make it relatively easy for an ending to fire during release. Observations were also made with fusimotor stimulation at 100/sec on the response to triangular and sinusoidal stretching of the same amplitude as the ramp and between the same limits. The velocity of the triangular stretching was made the same as that of the ramp, so that its frequency became about 1-5 Hz. In any particular experiment the sinusoidal stretching was set at the same frequency, which meant that the peak velocity of movement was then x7 times that of the triangular stretching. RESULTS

Using ramp and triangular stretching we have systematically studied the action of a fusiniotor fibre on a primary ending on 153 occasions. Taking account of several features of the responses these actions have been classified into one of six categories ranging progressively from apparently 'pure' dynamic action (category I) to apparently 'pure' static action (category VI). In essence, the exercise consisted in making a qualitative survey of various features of a population to identify the extremes, in this case static and dynamic actions, and then interposing a graduated scale in order to assess the extent to which other members of the population lay in between. Category I. Apparently 'pure' dynamic action As illustrated in Fig. 1, what we regard as a purely dynamic action leads to a remarkably uniform and uncomplicated response of the primary ending to a ramp stretch. The excitatory effect at the initial length is usually comparatively week, but during the dynamic phase of the ramp

F. EMONET-DJ9NAND AND OTHERS stretch the firing increases to a high level, in this case to above 200/sec. When the final length is reached the frequency of firing falls precipitously with the removal of the dynamic component of the stimulus. The fall apparently occurs in two phases. The first is too fast to be followed with the present type of display. The second is approximately exponential with a time constant of about 0-5 sec (Crowe & Matthews, 1964a), and is an invariable characteristic of dynamic action. Some primary endings may

832

A

B

.

~

~

C

~

~

~ _

~

-200

I

f*

'

'

E

I sec 100/sec 100/sec Fig. 1. Apparently 'pure' dynamic fusimotor action (category I) characterized by the behaviour of a primary ending during ramp and during triangular stretching. A, 'passive' response of ending to ramp. B, response to ramp during fusimotor stimulation at 100 sec-'. C, response to triangular stretching before and during fusimotor stimulation at 100 see-' (ramp, 2 mm extent, applied at 6 mm see-', released at 2 mm see-. Same amplitude triangles at 15 Hz, corresponding to 6 mm see-; note expanded time scale in C.) 2 sec

show a muted form of such slow decay of firing when they are passive and this appears to be favoured by increase of the initial length; but many show no sign of it when studied within the physiological range. In contrast, passive secondary endings quite commonly show such a slow component of adaptation (cf. Matthews, 1963; Cheney & Preston, 1976). At all times, though particularly prominently during the slow decay of firing on the ramp plateau, dynamic action is associated with a very regular rhythm of afferent firing; this is shown here by the close packing of the successive values of instantaneous frequency which persists even when the frequency of stimulation is lowered (cf. Fig. 11). Such regularity of afferent discharge is quite distinct from that seen during the 'driving' of some afferents by some static fibres. During 'driving' the firing is restricted to the stimulus frequency or its subharmonics, while during dynamic action the firing varies smoothly and continuously. The regularity of the discharge during dynamic action is another facet of the underlying behaviour which equally expresses itself as 'fusion' in the frequencygram, or as lack of modulation in the post-stimulus histogram (Bessou, Laporte & Pages, 1968; Goodwin, Hulliger & Matthews, 1975). On the release of the ramp stretch, which was deliberately made slower

833 STATIC AND DYNAMIC SUBDIVISIONS than the application of the stretch, the passive primary ending almost always falls silent (cf. Harvey & Matthews, 1961); however Fig. 2D shows an exception. Likewise, during purely dynamic action the ending usually still falls silent during the release in spite of the continued fusimotor stimulation, as in Fig. 1. Some endings, however, then continued to fire weakly during this slow release though they had not done so when passive; whether or not this occurred appeared to be related to the particular spindle in question and was commoner when the initial length of the muscle was greater. If any such firing occurred there was always an abrupt drop in its frequency at the beginning of the release. A more rigorous test of the ability of the fusimotor action to evoke firing during release was provided by triangular stretching (Fig. 1 C). This was made of the same amplitude as the ramp stretching and of the same velocity of rise, so that the symmetrical release was at about 6 mm/sec rather than at about 2 mm/sec (note that the time scale differs in B and C of Fig. 1). Triangular stretching provides a convenient way of repetitively testing the effects of release, but the response is not necessarily the same as that observed during the falling phase of a ramp of the same velocity since the holding phase of the ramp permits adaptation of the system. During the fast releases of the triangles our examples of purely dynamic action never elicited significant firing on release, although during the slower releases after the ramps they did so on about a sixth of occasions. Thus purely dynamic action is largely ineffective at overcoming the depressing effects of release, but whether the silence on release is absolute depends upon the precise conditions (cf. Crowe & Matthews, 1964b; Lennerstrand & Thoden,

1968).

Category VI. Apparently 'pure' static action Purely static fusimotor actions form a relatively heterogeneous group. Their characterizing feature is that the response of the ending to the dynamic stimulus of the rising phase of a ramp stretch is diminished in relation to the passive, or at any rate not appreciably increased, in spite of definite excitation of the ending under static conditions; the dynamic sensitivity of the ending is conveniently assessed by the arbitrary 'dynamic index', namely the fall in firing in 0.5 see on completion of the dynamic phase of stretching (Crowe & Matthews, 1964a). Likewise, during static action the ending is relatively unaffected by release of stretch, whether slowly as with the ramps or more rapidly as with the triangles, and almost always continues to fire while the muscle is shortening. These features may be seen in Fig. 2 for two separate primary endings. It can also be noted in records E and F that that ending showed an abrupt diminution in the rate of discharge at the beginning of the release. Such behaviour 29

PHY 268

Air_., hi;~ ~ ~10

834 F. EMONET-DJ9NAND AND OTHERS was commonly seen when the afferent rhythm remained regular during static action. The heterogeneity of static action arises in large part from variation in the effect on the regularity of the afferent discharge. Sometimes, as in Fig. 2E, the discharge remains as regular as it does during purely dynamic action. In other cases the fusimotor stimulation causes the afferent firing to become grossly irregular, as in Fig. 2 B. Both frequencygrams and poststimulus histograms (Bessou et al. 1968; Goodwin et al. 1975) show that A 8 C '. ~~~~~~~~~~~~~~~A

_~~~~~~~~~~~~~~

I 00/sec

1 00/sec

E

D

E

F -100

_~~~2 sec

e

-0f

__

100/sec

I sec

100/sec

Fig. 2. Two examples both of apparently 'pure' station fusimotor action (category VI), but differing in their effect on the regularity of the afferent rhythm. Pattern of ramp and triangular stretching as in Fig. 1. A, B, C, responses of one primary ending; D, E, F, responses of another primary ending in the same preparation. In spite of the differences between them, the actions on the two endings were produced by stimulation of one and the same fusimotor fibre (amplitude of movement, 2 mm in all cases).

the irregularity arises from the tendency for the ending to fire at certain particular times with regard to the stimulus and to tend to avoid firing at other times, suggesting that the ending is being influenced by the residual mechanical ripple of an unfused intrafusal muscle fibre contraction. In the extreme, such phased intrafusal action manifests itself not as irregularity of the afferent discharge but as the extreme regularity of 1:1 driving; but that was not the case in Fig. 2E, since the regular firing there seen varies continuously with time rather than in the discrete steps that are found when the driving ratio changes. Under static conditions, the increase in mean firing elicited by static fibres causing variable firing could be of any extent, whereas that elicited by those maintaining regular firing was only moderate, as in Fig. 2E.

STATIC AND DYNAMIC SUBDIVISIONS

835

Category II. Dynamic action with suspected static modification Fig. 3 shows what we judge to be a dynamic action modified by a weak static action. The classification of this effect as predominantly dynamic rests upon the observation of a large increase, relative to the passive, in the firing during the dynamic phase of stretching above the corresponding static levels, coupled with the characteristic component of slow decay of firing on completion of the dynamic phase of the ramp stretching. However, the effect differs in two respects from the purely dynamic action of A

C .

~

t ,4

*

200

a-00 -i E

100/sec I sec 100/sec Fig. 3. Stimulation of a single y fibre producing on this primary ending a slight static modification of dynamic action (category II). Arrangement as in Fig. 1 (movement, 2 mm). 2 sec

Fig. 1. Firstly, during the fusimotor stimulation the ending continues to fire during release, both with the slow ramp and with the more rapid triangles. Secondly, the afferent discharge is appreciably more irregular in Fig. 3 B. Another consideration, is that the excitatory effect of the fusimotor stimulation at the initial length is relatively strong in relation to the effect on the dynamic sensitivity of the ending, as assessed by the dynamic index. Fig. 4 shows that a purely dynamic action elicited by stimulating a single fibre may indeed be modified in these various ways by simultaneously stimulating a second fusimotor fibre that elicits a purely static action on its own. Such a correspondence between the action of a single fibre with that of the combined stimulation of a pair of fibres shows that the effect of the single fibre is compatible with its having activated separate static and dynamic mechanisms within the spindle, but of course this does not provide a proof that it has actually done so. Our category II subdivision has consisted of such actions which on classical criteria, notably measurement of the dynamic index, would have been classified unhesitatingly as dynamic, but which on detailed scrutiny gave grounds for suspicion that they had been somewhat modified by a super-added static action. It is here worth emphasizing that the combined action of a pair of 29-2

F. EMONET-D19NAND AND OTHERS 836 fusimotor fibres never leads, at any stage of a stretch, to a reduction in the firing of the ending below the maximal level it has on stimulating one or other fibre on its own (Crowe & Matthews, 1964a; Lennerstrand, 1968); the particular present example is the persistence of the static-elicited firing on release during dynamic action. Such absence of a peripheral 'inhibitory' effect on the afferent discharge might seem unremarkable, except that it could conceivably have arisen from the mechanical unloading of one intrafusal fibre by the contraction of another. A

B

-200

t

>

2 sec

~~~~~~-100

Ys 50/secC, E

C CS

D D

X

-200 -100 -0

YD 1 00/s YD 1 00/s + ys 50/sec Fig. 4. Deliberate static modification of dynamic action by stimulating simultaneously a powerful dynamic gamma and a static gamma. A, passive response; B, during static stimulation (category VI response); a, during dynamic stimulation (category I response); D, during combined stimulation (movement, 2 umn).

Category IV. Static action with 8u8pected dynamic modification Fig. 5 shows an example of the suspected modification of static action by dynamic action. The classification of the response as predominantly static is based on the very considerable excitation at the initial length, the approximate constancy of the dynamic index in relation to the passive, the considerable firing during release, and the irregularity of the afferent firing. The suspicion of dynamic admixture arises from the distinctive slow decay of firing seen on completion of the dynamic phase of stretching. As may be seen in Fig. 6 this is a characteristic of dynamic action which survives with remarkable persistence when combined with quite considerable static action, and when the other familiar signs of dynamic

837 STATIC AND DYNAMIC SUBDIVISIONS action have been obliterated. Such mimicking of the single fibre effects of Fig. 5 by the double fibre effects of Fig. 6 allows significance to be attached to the slow adaptation observed during the action of the single fibre, and which might not otherwise have attracted attention. A

B

C Is

i

D

I -300

I4

t,I, 1i ti' -200 I., -i a i_ .1 X0 VV -100 X i

a

.

0 V

,.

V

.

0.~~~

-0

2sec

50/sec

75/sec

100/sec Fig. 5. Suspected dynamic modification of static action (category IV). Arrangement as in Fig. 1, but with ramp responses for two frequencies of single fibre fusimotor stimulation (movement, 2 mm).

A

I

sec

C

B

iK

-

-No

100

-

2 sec

200

ys 75/sec

ys 100/sec

0

V

V

4 D

~-300 X

IE

i

.

KK A.; AA

_

~- 200E *,-

,,^.

.1

100

-

YD 1 OO/SeC YD 1 00/sec + ys 75/sec YD 1 00/sec + ys 1 00/sec Fig. 6. Deliberate dynamic modification of static action by stimulating a pair of single fibres simultaneously. A, passive response to ramp; B, C, responses during static stimulation at 75 and 100/sec; D, response during dynamic stimulation; E, F, responses during combined stimulation (movement, 2 mm). One proviso is that it is essential to compare the fusimotor action with the appro. priate passive response. Any slow fall in the passive response usually persisted more or less unchanged during an otherwise apparently pure static action, but its occurrence can then no longer be taken to provide evidence for the neural activation of a dynamic intrafusal process in addition to a static one. Moreover, we felt that to be attributed significance any slow fall during fusimotor stimulation should be

838

F. EMONET-DINAND AND OTHERS of appreciable amplitude, arbitrarily taken as 50 impulses/sec measured over 1 sec. Suspicion of a super-added dynamic action was fortified when the dynamic index was definitively above its passive value. In measuring the dynamic index we did not include any high frequency points associated with an 'initial burst' at the beginning of the stretching (of. Matthews, 1963), as was the case in Fig. 5.

Category V. Static action with conceivable dynamic participation Category IV static action, for which we were reasonably confident of dynamic modification, shades off into category V static action, for which we felt unable to exclude dynamic participation but where any signs were too faint for us to feel confident that it must have been occurring. Sometimes the reason for the uncertainty arose from the weakness of the dynamic action that would be required to be added to a purely static A

B ....

C _

A

200

.~1

~

...

; -IOn Z. 0

2 sec

1 00/sec

1 sec

1 00/sec 0.

E

D

E

F - 200 ~~.*

,:

-~100

-0 YD 75/sec

YD 75/sec + ys 1 00/sec

ys 100/sec Fig. 7. Static action with conceivable dynamic participation (category V), compared with deliberately introduced such participation. In this case the static action was too weak to have obscured a major dynamic contribution. A, B, C, category V action produced by stimulation of a single y fibre. D, purely dynamic response of another primary ending during stimulation of a single fusimotor fibre; F, purely static response of this ending during stimulation of another single y fibre; E, response to combined stimulation mimicking that seen in B on stimulating a single fibre (movement, 2 mm).

response in order to mimic the type of response seen. Fig. 7 shows an example of this; the effect of the static component of the action in increasing the absolute frequency of firing of the ending should have left scope for a powerful dynamic action to have manifested itself in the usual way (cf. Figs. 3 and 4). In other cases, however, the uncertainty arose

839 STATIC AND DYNAMIC SUBDIVISIONS because the static component of action was so powerful that it could be expected to have largely submerged even quite an appreciable dynamic component of action. Fig. 8 B shows such a case where the slight component of slow fall might, by virtue of comparison with the combined response of Fig. 8E, indicate dynamic participation in the response, but it is hardly large enough or of sufficiently characteristic time course to indicate that this must have been so. A

C6

B

C

__

~P; *'; _t. ;

' ?

;r;P411i -,S.'

200

a 4. -0

2 sec

1 00/sec

1 sec

u W

100/sec

4,

E

D

/ ..

E

F

-200

A

N

,

-

100

__

e

-0

YD 75/sec YD 75/sec + ys 50/sec ys 50/sec Fig. 8. Another example of static action with conceivable dynamic par. ticipation (category V) compared with known participation. In this case the static action is sufficiently powerful to obscure the dynamic action almost completely. A, B, C, stimulation of single y fibre. E, mimic of B, produced in another experiment by combining the actions seen in D and F each due to single y fibre stimulation (movement, 2 mm in A, B and C and 3 mm in D, E and F).

Thus category V contains examples covering a wide range of strengths of static action. In contrast, category VI (our presumed pure static action) never included those static actions that were so strong that they might have completely occluded a significant dynamic action. But, of course, both here and for category I (apparently pure dynamic) there must have been a threshold for our ability to recognize signs of admixture. Thus there is no guarantee that the two ends of our spectrum are indeed totally pure, rather that under the conditions of our experiment they give no sign of having a functionally significant contribution from the other type of action.

840

F.

EMONET-D19NAND AND OTHERS

Category III. Uncldasifiable After classifying the majority of apparently mixed actions as predominantly dynamic (category II) or as predominantly static (categories IV and V) there remained a few examples (eight cases) which defied us. Sometimes our various criteria seemed to point in different directions and we could not decide between their relative merits. On other occasions, the difficulty arose because the appropriate classification changed on varying the frequency of stimulation (which was tested invariably) or the initial length of the muscle (which was tested on about 20 % of occasions). Fig. 9 illustrates one of the difficult cases in which the frequency of stimulation had a material effect. For frequencies of 35 and 50/sec (B, C) we would A

a

*

/_,

I¢>>

2 sec

Cc

Q

-100 -0

50/secu

35/sec

E

D

.

E

-200

F _ _

Hi m

~

t

-100 -0

75/sec

100/sec 150/sec Fig. 9. Example of single fusimotor action which could not be properly classified either as primarily static or as primarily dynamic (category III, unclassifiable). With intermediate frequencies of stimulation features of both types of action are present, and the balance shifts from static to dynamic with increase of the frequency (movement, 2 mm).

have classified the action as predominantly static, either as V or VI. For frequencies of 100 and 150/sec (E, F) we should just have classified the effect as predominantly dynamic, in category II, since the dynamic index was slightly increased and there is a prominent slow fall. For a frequency of 75/sec (D) it seemed improper to allocate the action to either static or dynamic categories. Fig. 10 shows another difficult example, in this case affected by changing the initial length of the muscle. With the muscle well stretched (E, F) the fusimotor action contained a clear dynamic component as well as a marked static component and does not lend itself to ready categorization. On

841 STATIC AND DYNAMIC SUBDIVISIONS starting from a rather short initial length (A, D) the dynamic fusimotor component had disappeared although the response of the passive ending showed that the spindle as a whole was still being somewhat influenced by the stretch; possibly the intrafusal fibre responsible for the dynamic action had fallen slack. Apart from these few examples which we have allocated to category III the fusimotor actions that we observed remained true to type, that is with approximately constant proportions of static and dynamic components, on varying the frequency of stimulation, or the length of the muscle when it was tested.

L.+1 5mm A

B

C

i

L.+25 mm fi

-100

I*1 -

~

~

-

-

0

2 sec Zr

-$

E

D

F

i J..

i

11

P

1.

L.-e ir.W.

I j$;
75/sec). Calculation on individual samples shows that the splay in instantaneous frequency increases progressively with increase in the variance of the inter-spike interval distribution. If the coefficient of variation of the interval distribution is approximately constant with changing mean interval (Matthews & Stein, 1969) then the splay is relatively independent of the mean level of firing at which it is measured. Thus, Fig. 15 shows that a particular primary ending may have a regular discharge or an irregular discharge depending upon which fusimotor fibre is activating it, including when it is activated by two different fibres each with a purely static category VI action. This latter is to be expected if different static fibres can activate intrafusal fibres with different contractile properties, as have the chain fibres and the static bag fibres of

851 STATIC AND DYNAMIC SUBDIVISIONS Boyd et al. (1977). Fig. 14 shows that the activation of a given static fusimotor fibre quite often leads to a regular discharge of one spindle and to irregular firing of another, as already illustrated in the particular in Fig. 2 (cf. Crowe & Matthews, 1964b, Fig. 3, and Bessou, Laporte & Pages, 1966, Fig. 1). This is entirely compatible with the suggestion that in different spindles a given static fibre might innervate fibres with different contractile properties, say chain fibres in one spindle and a static bag fibre in another.

Responses to sinusoidal stretching We initially hoped to classify intermediate types of fusimotor action by using sinusoidal stretching, but in the event we came to prefer the classical ramp stimuli. None the less, the findings with sinusoidal stretching merit attention since this is still used for fusimotor classification and the difficulties involved may not always be appreciated. In the first place, consideration must be given to the frequency and amplitude of stretching since these may influence the findings. We used a frequency of about 1-5 Hz with the expectation that the findings would apply approximately to the range of low frequencies which are commonly employed for classification (say 0 5-4 Hz). The choice of amplitude is more problematical. For small movements, below about 200 aum peak to peak for the soleus muscle, the primary ending usually fires at all phases of the cycle while activated by either type of fusimotor fibre; thus fusimotor classification cannot then be based upon whether or not the ending falls silent. Moreover, in this range the receptor sensitivity (expressed as impulses/sec firing per unit stretching) is decreased by dynamic as well as by static action and there is no sign of the characteristic dynamic effect seen with large stretches (Goodwin et al. 1975). We therefore chose to use 'large' stretches of about 2 mm peak to peak amplitude and of the same extent as the ramps employed in each case. The responses to sinusoidal stretching have been analysed qualitatively by inspection and simple measurements of instantaneous frequency, rather than by fitting a sine curve to them (cf. Hulliger et al. 1976). On cursory inspection, records of the sine responses taken on our relatively slow time base differ only slightly from those elicited by triangular stretching and which have already been amply illustrated. However, as may be readily seen in Fig. 16A, B during dynamic activation the peak firing elicited by triangular stretching occurs at the point of maximum exten. sion, whereas the peak firing elicited by the sine is shifted part of the way towards the point of maximum velocity (900 phase advance). The same tended to be true during predominantly static type action, but in this case the most prominent feature of the sine response, like that to the triangle, was the continued firing during release. In the aggregate, for equivalent frequencies and amplitudes of stretching, the peak

F. EMONET-DEJNAND AND OTHERS

852

frequencies of firing were remarkably similar in the two cases; apparently, the if times greater peak velocity of the sinusoidal stretch is approximately offset by its occurrence at the point of half-stretch, so that in comparing their peak firing the greater velocity response with the sine is combined with a smaller position response than with the triangle. However, the correspondence in the peak firing elicited by the two modes of stretching was not exact in all cases.

A

B -100 *

*

-so

0

E

C

D

~100 .

*de.V

50

-0

0*4 sec Fig. 16. Comparison of the responses to triangular and to sinusoidal stretching. A, B, for a fusimotor action classified as purely dynamic (category I) on the ramp response. C, D for another ending a fusimotor action classified as purely static (category VI). 2 mm stretching at 1-5 Hz. Rate of stimulation, 1O0/sec.

The effect of category I or purely dynamic actions on the response to the sinusoidal stretching was uniformly simple. The maximum frequency of firing during the stretching phase was considerably increased, but the ending still fell silent during the releasing phase (cf. Crowe & Matthews, 1964b, Fig. 6). Thus there was a large increase in the peak to peak modulation of firing, measured from zero to the maximum value, as shown in Fig. 17. With category II actions the peak firing was greater than with category I actions, but since the endings usually fired somewhat on release, the net effect of these opposing tendencies was that the increase in the modulation was about the same as that for category I. For accidental reasons only two category II responses were studied with sinusoidal stretch; since Fig. 16 shows that triangle stretching elicits generally similar modulation, five examples of this have been included in Fig. 17.

STATIC AND DYNAMIC SUBDIVISIONS 853 Category VI actions varied, though most were associated with wellmarked firing on release. Generally the changes in modulation were small but with increases commoner than decreases. The precise value of the 'active' modulation in relation to the passive modulation is, however, without significance. This is because the active modulation usually occurs +300 I I

,

III, IV

V, VI

EA

_ +200-

A. 100 0

0

A0 0 A

0

iA4

E

O+100 A

A

&A

AA~~~~~~~~~~~~

Increase in static firing (impulses/sec)

Fig. 17. The change in peak to peak modulation elicited by sinusoidal stretch relative to the passive value found for the various categories of fulsimotor action. The abscissa gives the strength of static action in each case assessed by the increase in afferent firing at the initial length used for the ramp stretching, corresponding to the minimum length for the sines. The peak to peak modulation was obtained simply by substracting the minimum from the maximum value on the frequency display, irrespective of whether or not the ending fell silent during the release (see text). The categories have been plotted in pairs, as indicated. Filled triangles (AVT) used for categories I, III, V, open triangles ( A V) for categories II, IV, VI. Upwards pointing triangles indicate stretch was 2 mm, downwards triangles indicate that amplitude was slightly different, usually 1-5 or 2-5 mm. In category II, the five open circles ( O) were obtained with 2 mm triangular stretches (see text) (frequency of stretching, 1-5 Hz; rate of stimulation always 100/sec).

between two measurable positive frequencies, whereas the passive modulation takes place between a positive value and zero when zero is an indeterminate value since it equally represents all negative frequencies. Fig. 17 also shows changes in modulation found for the remaining categories of fusimotor action. Increases of varying amount were observed for all of them., including the predominantly static category V, but they

F. EMONET-D19NAND AND OTHERS 854 were generally smaller than those found in categories I and II. Comparison with Fig. 13 which illustrates changes in dynamic index for a larger population of endings, but including all those whose sine responses were studied, shows that measurement of the dynamic index is appreciably better at emphasizing the 'static' contribution to the response and thus at separating static and dynamic action. It might be suggested, however, that the sinusoidal stretching (this applies also to triangle stretch) serves to emphasize any 'dynamic' contribution to the responses in categories IV and V and so scores in this respect over the ramp. This may be partly true, but as discussed in detail below the situation is too complex to allow any categorical statement in this respect since other factors undoubtedly contribute to the modulation seen during both purely static and pre-

dominantly static actions. Factor leading to modulation. The deepness of the modulation with category I action arises partly from the increase in the maximum frequency of firing during the stretching above the steady level elicited by fusimotor stimulation on its own, and partly from the silence during release. The weak modulation with category VI action arises equally from the smallness of the increase in firing during the stretching phase of the cycle and fromn the maintenance of the discharge of the ending during the falling phase. When by stimulating two y fibres together a category VI action is combined with a category I, then the modulation is decreased in comparison with that found for the dynamic action alone. This is because of the firing on release which occurs with the combined stimulation. However, as with ramp stretching, the combined stimulation increases the maximum frequency of firing during the stretching phase above that found for the dynamic action alone (partial summation, q.v.) thus helping to preserve an appreciable modulation (see especially Hulliger et al. 1976). Thus the occurrence of a moderate degree of modulation should provide a valid sign of dynamic admixture with static action. Unfortunately, however, it is not a unequivocal sign since quite considerable modulation may occur with otherwise clear-cut category VI actions for unrelated reasons as follows. (1) When the positional sensitivity of the ending is high (large increase in static firing per unit extension) then an appreciable modulation follows automatically. Quite possibly such modulation associated with a high position sensitivity would show less 'phase advance' on the stretching than that associated with dynamic admixture, and so might be potentially distinguishable; this has not been currently

attempted. (2) When an ending has a tendency to be 'driven' by a static fibre it may abruptly change its driving regime from 1: 2 to 1: 1 during the stretching phase of the cycle and revert to the lower value on the releasing phase, with consequent large changes in its mean frequency of firing at various phases of the cycle. This can occur even when the driving is not absolutely secure at any particular driving ratio. (3) Measurement of modulation per se does not distinguish a stretch-elicited increase of firing above the steady level occurring at constant length, which is characteristic of dynamic effects mixed with static effects, from a releasing-elicited fall in firing below the steady level which may be seen on occasions with pure but weak static action. In other words, any increase in static firing level with fusimotor stimulation which fails to be reflected by an equivalent increase in firing on the falling phase of the cycle leads to increased modulation. Such effects might well be rather

STATIC AND DYNAMIC SUBDIVISIONS

855 sensitive to the amplitude of stretching. Thus when using sinusoidal stretching to characterize fusimotor action it is also desirable to measure the static firing of the ending at the two extremes of stretching, partly in order to assess the positional sensitivity, and partly to distinguish between stretch-evoked excitation and releaseevoked depression. This is perhaps most expeditiously done by applying a ramp stretch, thus somewhat obviating the need for sinusoidal stretching.

The value of sinusoidal stretching is that it approximates to certain physiological movements where it may be relevant that it simultaneously takes into account the effects of both stretching and releasing. But it should be emphasized that the present measurements apply only to one arbitrarily chosen pattern of stretching (2 mm at 1-5 Hz). The advantage of ramp stretching is that it permits ready visualization of the 'slow fall' of firing on completion of the dynamic phase of stretching, for which there is no immediate counterpart in the sinusoidal responses. It is this slow component of adaptation that emerges from the mixing experiments as the most constant and characteristic feature of dynamic fusimotor action. DISCUSSION

The present findings reaffirm the validity of the broad subdivision of fusimotor actions into separate static and dynamic categories. Even when signs of intermediate action are assiduously sought some two thirds of the total of observed actions appear to be functionally pure with no sign of effective modification by the alternative action. There is, however, inevitably a limit to our ability to recognize a slight degree of modification so that the absolute frequency of occurrence of such overlap may well be slightly higher. More important, when individual fusimotor fibres are considered, taking into account their actions on more than one primary ending, there is virtually complete separation into two distinct groups. The dynamic fibres form a particularly well defined entity with little tendency for their actions to be modified by static action. Static fibres more commonly show dynamic modification of their action on some of the endings they influence, but not to a consistent extent for any particular fusimotor fibre. Looked at on their own rather than as part of a continuum, some of our intermediate effects might not be felt to provide any problem of classification and to be compatible with a complete dichotomy of fusimotor action. Most previous studies have indeed been content with such a simple complete bimodal separation. Relation to structure with special regard to glycogen depletion evidence 'Pure' responses. The classical hypothesis that dynamic action arises from the activation of bag fibres has been amply validated during the

F. EMONET-DJ9NAND AND OTHERS 856 past few years (cf. Matthews, 1972), but at the same time it has become clear that only certain bag fibres can be held responsible. In particular, the most recent glycogen depletion work shows that dynamic axons, whether specifically fusimotor or skeleto-fusimotor (fi), almost exclusively supply the histologically distinct bag, fibre (Barker et al. 1976, 1977). There seems little doubt, moreover, that these bag, fibres correspond to those with a slow localized contraction that have been studied cine-photographically on stimulating single axons; in some experiments these were identified as dynamic y axons (Bessou & Pages, 1973, 1975; Boyd et al. 1977) though in others that was not possible (Boyd, 1976). Especially noteworthy, is Boyd's (1976) observation, in the single case studied, of a very pronounced slow equatorial creep following the dynamic phase of ramp stretch applied during fusimotor activation of such a slow fibre; this creep then partially restores the length of the primary innervated region to its resting value. In passive conditions smaller similar effects were regularly seen for this type of fibre but not for the remaining intrafusal fibres. Such creep provides the obvious basis for the slow fall of afferent firing at the end of the dynamic phase of the ramp which is such an essential characteristic of dynamic action. Thus there seems very little doubt that our category I responses with their regular firing and slow adaptation are due to the exclusive activation of a bag1 fibre. On the other hand static action per se cannot originate from the bag1 fibre for these seem never to be depleted on their own by static y axons; Barker et al. (1976, p. 66) were unable to exclude chain activation in their only three possible such cases. Rather, all evidence suggests that the essentials of static action must be attributed to chain fibres and bag2 fibres whether acting individually or

collaboratively. 'Mixed' responses. Our category II responses can be easily accounted for by assuming they result from the concomitant activation of a bag1 fibre and of a different functional type of intrafusal fibre, whether a bag2 or a chain fibre. As shown in Fig. 12 we found that of forty-four examples of predominantly dynamic action, thirty-four were category I and ten were category II responses. This gives a figure of 77 % of dynamic actions being apparently 'pure', which agrees closely with the corresponding value of 81 % for the proportion of the occasions in a glycogen depletion study (Barker et al. 1976) in which dynamic y stimulation depleted a bag1 fibre on its own rather than along with a bag2 or a chain fibre. Barker et al. (1976) did not correlate patterns of glycogen depletion with categories of responses largely because these had yet to be fully delimited. But there were also technical reasons; the tenuissimus muscle on which their histophysiological study was carried out is very compliant and even when a fraction of that muscle is used, its various spindles are not evenly

857 STATIC AND DYNAMIC SUBDIVISIONS stretched with consequent variation in their responses. Correlation of such responses with patterns of depletion appeared to be too hazardous to be systematically attempted. However, more recently when studying the distribution off? skeleto-fusimotor fibres in peroneus brevis Barker et al. (1977) made a relevant observation. Stimulation of a dynamic f axon elicited a category I response from two spindles and a category III or IV response from a third (the full tests required for categorization were not applied). The muscle was then studied for glycogen depletion and depletion was observed in just three spindles. In two of them the bag, fibre was the only fibre depleted, whereas in the third spindle a chain fibre was depleted in addition to the bag, fibre. It seems highly probable that the two spindles with exclusive bag, innervation were responsible for the two category I responses and that the spindle with the mixed bag1 and chain innervation gave the mixed type of response. Since it appears that a purely dynamic response to ramp stretch with its typical slow decay can be attributed to the exclusive activation of a bag1 fibre, it follows that whenever a complex response shows an appreciable slow decay it is logical to attribute it to the action of a bag1 fibre adding its effect to those of muscle fibres of other types. Such an assumption is supported by the features of the responses obtained when a single dynamic y axon giving a category I response is stimulated concomitantly with a static axon. As shown in Figs. 4, 6, 7, 8 all intermediate categories of responses can be readily so matched. This is particularly striking in experiments such as that illustrated by Fig. 11 in which altering the rate of stimulation of each of the two fusimotor axons, and consequently the relative degree of activation of different types of muscle fibre, allowed all intermediate responses to be observed. Of course, the matching of effects elicited by individual gamma motor fibres with those produced by stimulating a pair of fibres of contrasting 'pure' action does not provide direct evidence that the individual supposedly 'mixed' actions arose from the simultaneous activation of separate static and dynamic elements within the spindles, but we find this the most natural explanation. On this interpretation the predominantly static responses of category IV, and possibly also those of category V, are due to axons which in addition to bag2 and/or chain fibres supply a bag1 fibre. Of 102 examples of predominantly static action (categories IV, V, VI) 11 were category IV and 23 were category V responses giving about 33 % of occasions in which bag1 activation might be expected in addition to chain and/or bag2 activation. The proportion rises to 38 % if category III actions are also included. This may be compared with the occurrence of some bag1 glycogen depletion in just below half of the tenuissimus spindles supplied by static axons (Barker et al. 1976). Perhaps this difference can be accounted for by

858

8F. EMONET-DtNAND AND OTHERS

the inability of a slight dynamic action to manifest itself, at least under our conditions, when there is concomitantly a strong activation of 'static' intrafusal muscle fibres. However, it is equally possible that the distribution of static axons is not the same in peroneus brevis spindles and in tenuissimus spindles; the two muscles differ in many respects, including the relative length changes they undergo in natural conditions and the greater average number of y fibres per spindle for the peroneus (Boyd & Davey, 1968). It may be urged against the view that bag, fibre are activated by some static axons that direct observation has yet to show fibres of contrasting types (i.e. dynamic bag versus static bag or chain) contracting simultaneously on stimulating a single motor fibre (Bessou & Pages, 1975; Boyd et al. 1977). But this essentially negative finding requires wider validation before it can be regarded as compelling. There is, for example, the risk that a weak contraction in one intrafusal fibre might be masked by the occurrence of a strong contraction of a nearby intrafusal fibre. Moreover, the dynamic effects seen with a large stretch need not be associated with appreciable frank shortening of the relevant intrafusal fibres but rather may depend upon localized changes in its mechanical properties; micro-electrode probing might provide a more searching test of neural activation than does simple observation. In the reverse, it may be noted that the considerable agreement between the present findings and the related glycogen studies has enhanced our confidence in both types of approach. Neither, however, would seem to provide quantitatively precise figures for the detailed pattern of the distribution of fueimotor axons to the various intrafusal fibres. For example, for a given degree of intrafusal activation glycogen depletion is perhaps more readily shown by the bag, fibres, whose glycogen content is relatively lower than that of bag2 or chain fibres (see Barker et al. 1976, p. 63). Similarly, the relative inaccuracy of the present figures should be obvious. Relation to fusimotor function An acute question is why static action per se, which is currently considered as a functional unity, should be apparently mediated by two separate types of intrafusal muscle fibre (chain and bag2) as shown both by glycogen depletion experiments (Barker et al. 1976) and by observations on isolated spindles (Bessou & Pages, 1975; Boyd, 1976). Since chain fibres show much more propensity to give 'unfused' contractions than do the static bag fibres (Bessou & Pages, 1975; Boyd, 1976) our static actions associated with high afferent variability or with 'driving' may be reasonably associated with chain action. Equally, our static action accompanied by a regular smoothly varying afferent discharge may well be associated

STATIC AND DYNAMIC SUBDIVISIONS

859 with bag2 action. But a high degree of regularity, as we have measured it, may not be a specific indication of bag2 action entirely unaccompanied by chain action since we have seen it for a much higher proportion of static actions, than would be expected from the glycogen studies (Barker et al. 1976). None the less, the finding that a given fusimotor axon may have very different effects on the afferent rhythm of different primary endings (see Fig. 14) provides some support for the view that a given static fibre may distribute itself between bag2 and chain fibres in widely varying proportions in different spindles, as also shown by other lines of evidence (Barker et al. 1976; Boyd et al. 1977). In other words, on the statistical average the static bag and the chain fibres act in a complementary role rather than providing alternative affector pathways, and this presumably confers some functional advantage upon the system. The apparent failure of certain individual fusimotor fibres to restrict their innervation to the 'right' kind of intrafusal muscle fibres (dynamic to bag,, and static to bag2 and chain) has no immediate explanation. To some extent this non-selectivity may simply represent an ontogenetic accident, but for the static axons it occurs on such a scale that it seems more likely to achieve some desirable functional consequence. For instance, during strong activation of the static fusimotor system it could help to preserve the responsiveness of the bag, terminals of individual primary endings by preventing slackness, without the need for activation of the dynamic system. This might be particularly appropriate during gross muscle shortening and help to prepare the spindle for whatever awaits it at the new muscle length. Also, it should be remembered that in so far as the chain fibres are arranged in series with the polar part of bag1, as well as of bag2 fibres, then the avoidance of polar yielding by activation of bag1 fibres might be important for static action. Be that as it may, both ontogenetically and functionally it is interesting that the dynamic fibres apparently achieve an appreciably higher degree of specificity in the distribution of their innervation than do the static fibres. Perhaps this asymmetrical arrangement relates to our finding that dynamic action requires to be kept separate if it is to avoid being largely submerged by a powerful static action (cf. Fig. 8). Such occlusive action is particularly marked when the amplitude of stretching is small (Hulliger et al. 1976). The general conclusion of the present re-evaluation of the static/ dynamic classification is that it holds firm for all broad functional purposes, but there is apparently a certain lack of rigidity in the detailed wiring up of individual fusimotor nerve fibres with individual intrafusal muscle fibres. This needs to be taken into account in making detailed morphological correlations with static and dynamic actions, but it remains

860 F. EMONET-D.9NAND AND OTHERS an open question as to whether and how far any such overlap matters for motor function. This investigation was supported by grants from the Fondation pour la Recherche M6dicale Frangaise. REFERENCES BANKs, R. W., BARKER, D., HARKER, D. W. & STACEY, M. J. (1975). Correlation between ultrastructure and histochemistry of mammalian intrafusal muscle fibres. J. Physiol. 252, 16-17P. BARKER, D., BEssou, P., JANKowsKA, E., PAGkS, B. & STACEY, M. (1972). Distribu. tion des axones fusimoteurs statiques et dynamiques aux fibres musculaires intrafusales, chez le Chat. C. r. hebd. Seanc. Acad. Sci., Paris 275, s6rie D, 25272530. BARKER, D., EMONET-D]iNAND, F., HARKER, D., 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. Physiol. 261, 49-69. BARKER, D., EMONET-DANAND, F., HARKER, D., JAmi, L. & LAPORTE, Y. (1977). Types of intra and extrafusal muscle fibre innervated by dynamic skeleto-fusimotor axons in cat peroneus brevis and tenuissimus muscles as determined by the glycogen depletion method. J. Physiol. 266, 713-726. BARKER, D., EMONET-DANAND, F., LAPORTE, Y., PROSKE, U. & STACEY, M. (1970). Identification des terminaisons motrices des fibres fusimotrices statiques chez le Chat. C. r. hebd. Seanc. Acad. Sci., Pari 271, s6rie D, 1203-1206. BARKER, D., EMONET-DANAND, F., LAPORTE, Y., PROsKE, U. & STACEY, M. (1973). Morphological identification and intrafusal distribution of the endings of static fusimotor axons in the cat. J. Physiol. 230, 405-427. BEssou, P., LAPORTE, Y. & PAGfrS, B. (1966). Similitude des effets statiques ou dynamiques exerc6s par des fibres fusimotrices unique sur les terminaisons primaires de plusieurs fuseaux chez le Chat. J. Physiol., Paris 58, 31-39. BEssou, P., LAPORTE, Y. & PAGiS, B. (1968). Frequencygrams of spindle primary endings elicited by stimulation of static and dynamic fusimotor fibres. J. Physiol. 196, 47-63. BEssou, P. & PAGoS, B. (1973). Nature des fibres musculaires fusales activ6es par des axones fusimoteurs unique statiques ou dynamiques chez le Chat. C. r. hebd. Seanc. Acad. Sci., Paris 277, s6rie D, 89-91. BEssou, P. & PAGkS, B. (1975). Cinematographic analysis of contractile events produced in intrafusal muscle fibres by stimulation of static and dynamic fusi. motor axons. J. Physiol. 252, 397-427. BOYD, I. A. (1976). The response of fast and slow nuclear bag fibres and nuclear chain fibres in isolated cat muscle spindles to fusimotor stimulation, and the effect of intrafusal contraction on the sensory endings. Q. Ji exp. Physiol. 61, 203-254. BOYD, I. A. & DAVEY, M. R. (1968). Composition of Peripheral Nerves. Edinburgh and London: Livingstone. BOYD, I. A., GLADDEN, M., MCWILaLIAM, P. N. & WARD, J. (1977). Control of dynamic and static nuclear bag fibres and nuclear chain fibres by y and ,f axons in isolated cat muscle spindles. J. Physiol. 265, 133-162. BROWN, M. C. & BuTLER, R. C. (1973). Studies on the site of termination of static and dynamic fusimotor fibres within muscle spindles of the tenuissimus muscle of the cat. J. Physiol. 233, 553-573.

STATIC AND DYNAMIC SUBDIVISIONS

861

BROWN, M. C. & BuTLER, R. G. (1975). An investigation into the site of termination of static gamma fibres within muscle spindles of the cat peroneus longus muscle. J. Physiol. 247, 131-143. BROWN, M. C., CROWE, A. & MATTHEWS, P. B. C. (1965). Observations on the fusimotor fibres of the tibiahis posterior muscle of the cat. J. Physwil. 177, 140-159. CHENEY, P. D. & PRESTON, J. B. (1976). Classification and response characteristics of muscle spindle afferents in the primate. J. Neurophysiol. 39, 1-8. CROWE, A. & MATTHEWs, 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. Physiol. 174, 109-131. CROWE, A. & MATTHEWS, P. B. C. (1964b). Further studies of static and dynamic fusimotor fibres. J. Physiol. 175, 132-151. EMONET-D1NAND, F., JAm, L. & LAPORTE, Y. (1975). Skeleto-fusimotor axons in hind-limb muscles of the cat. J. Physiol. 249, 153-156. EMONET-DkENAND, F., JOFFROY, M. & LAPORTE, Y. (1972). Fibres fusimotrices dont l'action sur la sensibility phasique des terminaisons primaires depend de leur fr6quence de stimulation. C. r. hebd. Acad. Sci., Paris 275, s6rie D, 89-91. EMONET-D1hNAND, F., LAPORTE, Y., MATTHEws, P. B. C. & PETIT, J. (1976). Experimental observations on the sharpness of classification of fusimotor fibre into static and dynamic types. J. Physiol. 260, 68-69P. GLADDEN, M. (1976). Structural features relative to the function of intrafusal muscle fibres in the cat. In Understanding the Stretch Reflex, vol. 44, ed. HoMMA, S., Progress in Brain Research, pp. 51-59. Amsterdam: Elsevier. GOODwIN, G. M., HULIGER, 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. Physiol. 253, 175-206. HARVEY, R. J. & MATTHEws, P. B. C. (1961). The response of de-efferented muscle spindle endings in the cat's soleus to slow extension in the muscle. J. Physiol. 157, 370-392. HULIGER, M., MATTHrWS, P. B. C. & NOTH, J. (1976). The response of spindle primary afferents to 1 Hz sinusoidal stretching during paired fusimotor stimulation. J. Physiol. 263, 182-183P. 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 physiol. scand. 74, 257-273. LENNERSTRAND, G. & THODEN, U. (1968). Position and velocity sensitivity of muscle spindles in the cat. II. Dynamic fusimotor single-fibre activation of primary endings. Acta physiol. scand. 74, 30-49. MATrTHwS, P. B. C. (1963). The response of de-efferented muscle spindle receptors to stretching at different velocities. J. Physiol. 168, 660-678. MATTHEWS, P. B. C. & STEIN, R. B. (1969). The regularity of primary and secondary muscle spindle afferent discharges. J. Physiol. 202, 59-82. MATTHEWs, P. B. C. (1972). Mammalian Muscle Receptors and their Central Actions. London: Arnold. SCHAFER, S. S. (1974). The discharge frequencies of primary muscle spindle endings during simultaneous stimulation of two fusimotorfibres. Pflugers Arch. gms. Physiol. 350, 359-372.