Fusimotor-sensor and fusimotor-trigger functions: A re-interpretation of the dual control of mammalian muscle spindles

Fusimotor-sensor and fusimotor-trigger functions: A re-interpretation of the dual control of mammalian muscle spindles

385 SHORT COMMUNICATIONS Fusimotor-sensor and fusimotor-trigger functions: A re-interpretation of the dual control of mammalian muscle spindles Pres...

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Fusimotor-sensor and fusimotor-trigger functions: A re-interpretation of the dual control of mammalian muscle spindles Present concepts of the dual fusimotor control of mammalian muscle spindles are mainly based upon functional criteria, as observable, for instance, with the different spindle responses to ramp stretches of the muscle. From the effects of stimulation of individual fusimotor fibres, Matthews and his coworkers have claimed that there are two fibre types: 'dynamic' fusimotor fibres which predominantly enhance the dynamic or rate-dependent sensitivity of primary spindle endings, and 'static' fusimotor fibres which markedly increase their static discharges at constant muscle lengthZ,6,1°-12. Most subsequent workers have agreed upon this classificationt,3,7, 9. It is now also generally accepted that Matthews' 'dynamic' fibres terminate in Barker's 'v-trail' endings, and the 'static' fibres in the '7-plate' endings 2-4. We have recently submitted the experimental data, as presented by the Matthews and Laporte groups, to a careful re-analysislL This has convinced us that the differentiation of dynamic and static fusimotor fibres is not correct in a strict sense. What is open for discussion is not the recorded facts themselves, but rather their evaluation and interpretation. In previous studies, it has been common practice to estimate the stretch sensitivities in terms of absolute frequency values of the spindle discharge, independent of whether or not a 'spontaneous' or basic activity was already present before the testing stretch. However, if a testing stretch is superimposed upon an existing basic activity, only that amount of spindle discharge exceeding it can be taken as the true response to the stretch. Consequently, the static response must be obtained by subtracting the underlying basic discharge frequency from the total average frequency value after adaptation to the new muscle length. The same holds for the so-called acceleration response, usually visible after the start of a ramp stretch (for its nature, see Sch~fer14). No correction is needed for the conventional dynamic response (or 'index'), thanks to its definition as a difference of two frequency values. The proposed correction of the calculation procedure seems to be but a minor point. Its application leads, however, to a quite different picture of the effects of TABLE

I

EFFECTS OF FUSIMOTOR STIMULATION UPON DISCHARGE PATTERNS OF PRIMARY MUSCLE SPINDLE ENDING == e n h a n c e d ; - - - r e d u c e d .

Type o f stimulated fusimotor fibre

Responses to ramp stretch

Proposed new name

Recent terminol,

Acceler. response

Fusimot. sensor

v-trail (dynamic)

÷

Fusimot. trigger

7-plate (static)

Dynamic response

+

Static response

Basic activity (due to fusimot. tone)

.

(!) i+

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fusimotor stimulation. For a full discussion, we refer to the detailed study by Sch~ifer and Henatsch 15. Here we need only summarize the results obtained in this analysis in a tabulated form (Table I). It will be noted that Matthews' so-called 'dynamic" fusimotor fibre type not only enhances the dynamic but also the acceleration and static response; in other words, it sensitizes, in all three respects, the spindle against external disturbances. In contrast, the so-called 'static' fusimotor fibre type reduces all three response components, including the static response; in other words, it desensitizes the spindle against such disturbances. Additionally, but independent of this, the spindle's basic activity increases in both instances, due to the enhanced fusimotor tone. The increase is only moderate with the first but marked with the latter fibre type. All these events can be clearly recognized in many of the original records of the formerly mentioned authors, provided that the occurring changes in the basic discharge frequency are taken into account as described above. They need no further proof by new own recording examples. From this revised point of view, the functional roles of the two fusimotor control components appear in a new light. In previous interpretations, their effects were thought to be restricted to the spindle's function as a measuring instrument or sensor device. Regarding the muscle spindle as the main sensor of a length-stabilizing feedback system, it would indeed be advantageous if it possesses independently adjustable static (or proportional) and dynamic (or differential) sensitivities 12,13. But the muscle spindles are not only sensor devices playing an important but passive role i n a feedback or servo system. They are as well powerful afferent input sources for their own alpha motoneurones, privileged among other inputs by the la-monosynaptic contact. Thus, by means of appropriate central fusimotor command, the spindle primaries may act as executor or trtgger organs for centrally induced motor acts. It has repeatedly been pointed out that this indirect way of throwing the alpha motoneurones into action (Granit's peripheral 'gamma-spindle loop') may be preferred in vivo under many circumstances. Quite recently, Granit et al. 8 have proved that gamma-induced afferent spindle volleys can indeed trigger, without support from other sources, alpha motor unit discharges. For this task it would be an undesired complication if the spindles were too sensitive to peripheral mechanical disturbances. The less they were influenced by external events, the closer they could follow descending fusimotor orders. It is obvious that the two types of fusimotor action described above will serve exactly the two different purposes for which the spindles may be used. If the situation calls for a precise and fast-working stabilization of the peripheral muscle length, this will be supported by one fusimotor component (the previous 'dynamic" or 'y-trail" fibres): it turns the spindles into highly efficient measuring devices or "sensors'. improving their proportional and differential sensitivities towards optimum feedback performance. If, on the other hand, the spindles ought to be turned into motor trigger organs, the other fusimotor component (the previous "static' or "7,-plate' fibres) takes action: it forces the spindles into strong intrafusal contractions that will determine their basic afferent discharges while at the same time it reduces their sensitivity to unwanted interfering disturbances. There is no room to discuss here in detail the intrafusal events causing either one or the other behaviour. For a satisfying Brain Research, 6 (1967) 385-387

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anatomical model of the spindle which incorporates the new knowledge about the distribution and electrical operation of y-trail and y-plate endings, respectively, and which may well account for the functions described above, reference is again given to our detailed paper 15. In conclusion, we have once more reached a point where a change of adopted terminology seems inevitable. The terms 'dynamic' and 'static' may still be useful to describe the two main sensing properties of the spindles; however, they are not at all adequate for characterizing the contrasting functions of the dual fusimotor control. We suggest that unless better terminology is found, one component could be called the 'fusimotor-sensor' system and the other the 'fusimotor-trigger' system. This work was supported by the Deutsche Forschungsgemeinschaft. Physiologisches lnstitut der Universitiit G6ttingen, 34 G6ttingen (Germany)

H.-D. HENATSCH SONJA S. SCH,~FER

I APPELBERG,B., AND EMONET-DI~NAND,F., Central control of static and dynamic sensitivity of muscle spindle primary endings, Acta physiol, scand., 63 (1965) 487-494. 2 BARKER, D., The motor innervation of the mammalian muscle spindle. In R. GRANIT (Ed.), Nobel Symposium I, Muscular Afferents and Motor Control, Almquist and Wiksell, Stockholm, 1966, pp. 51-58. 3 BESSOU,P., LAPORTE Y., ET PAG/~S, B., Similitude des effets (statiques ou dynamiques) exerc6s par des fibres fusimotrices uniques sur les terminaisons primaires de plusieurs fuseaux chez le chat, J. Physiol. (ParisJ, 58 (1966) 31-39. 4 Bovo, I. A., Signed contributions to the discussion on muscle spindles. In R. GRANIT (Ed.), Nobel Symposium I, Muscular Afferents and Motor Control, Almquist and Wiksell, Stockholm, 1966, pp. 115-119. 5 CROWE, A., AND MATTHEWS,P. B. C., The effects of stimulation of static and dynamic fusimotor fibres on the response to stretching of the primary endings of muscle spindles, J. Physiol. (Lond.), 174 (1964) 109 131. 6 CROWE, A., AND MATTHEWS, P. B. C., Further studies of static and dynamic fusimotor fibre, J. Physiol. (Lond.), 174 (1964) 132-151. 7 EMONET-DI~NAND,F., LAPORTE, Y., ET PAGI~S, B., Fibres fusimotrices statiques et fibres fusimotrices dynamiques, chez le lapin, Arch. ital. BioL, 104 (1966) 195-213. 8 GRANIT,R., KELLERTH, G.-O., AND SZUMSKI,A. J., Intracellular recording from extensor motoneurons activated across the gamma loop, J. Neurophysiol., 29 (1966) 530-544. 9 JANSEN,J. K. S., On fusimotor reflex activity. In R. GRANIT (Ed.), Nobel Symposium 1, Muscular Afferents andMotor Control, Almquist and Wiksell, Stockholm, 1966, pp. 91-105. 10 JANSEN,J. K. S., AND MATTHEWS,P. B. C., The central control of the dynamic response of muscle spindle receptors, J. Physiol. (Lond.), 161 (1962) 357-378. 11 JANSEN,J. K. S., AND MATTHEWS, P. B. C., The effects of fusimotor activity on the static responsiveness of primary and secondary endings of muscle spindles in the decerebrate cat, Acta physiol, scand., 55 (1962) 376-386. 12 MATTHEWS,P. B. C., Muscle spindles and their motor control, Physiol. Rev., 44 (1964) 219-288. 13 MILHORN, H. T., The Application of Control Theory to Physiological Systems, Saunders, Philadelphia, 1966, pp. 283-316. 14 SCH~EER, S. S., The acceleration response of a muscle spindle primary ending to ramp stretch of the extrafusal muscle, Eaperientia (Basel), in press. 15 SCH~IFER,S.S., eND HENATSCH,H.-D., Dehnungs-Antworten der primfiren Muskelspindelafferenz bei elektrischer Reizung und nattirlicher lnnervation der beiden fusimotorischen Fasertypen, Exp. Brain Res., in press (1967). (Accepted July 18th, 1967)

Brain Research, 6 (1967) 385-387