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Nuclear chain fibres are classically regarded as being much shorter and thinner than bag fibres, either bag1 or bag2. However, Barker et al. (1976) noticed that some spindles possessed one or more chain fibres with unusually long poles, often of similar length to the bag fibres. As an estimate of the incidence of these ‘long chain’ fibres they assessed the proportion of spindles containing at least one chain fibre pole that extended for more than 1mm beyond the end of the capsule. Kucera (1980) formalised this practical criterion as a definition of a class of long chain fibres each of which possessed at least one long pole. Since that time, long chain fibres have often been treated as though they formed a distinct type of intrafusal fibre with a specific static beta (βs) innervation (Kucera, 1982, 1984; Barker & Banks, 1986). Here we give evidence in detail of both static β and static γ innervation of long chain fibres.

The abductor digiti quinti medius (adqm) is an intrinsic muscle of the foot which abducts the fifth digit. Despite its small size (about 30mg) it contains all the elements of a complete skeletomotor and fusimotor system. It may therefore provide a practical model for studying integrated fusimotor and skeletomotor activity under a variety of conditions. Morphological investigation of the innervation of the adqm muscle of the cat hind limb was carried out as an adjunct to electrophysiological studies.

It is clear from even a cursory examination of the literature on muscle spindles that these are receptors of great sophistication and functional versatility. But a simple textbook ‘role’ for them in the serious business of motor control cannot be formulated realistically without taking into account that some information they signal is inconsequential to motor control, as for example when spindle afferents are influenced by the arterial pulse (Ellaway & Furness, 1977), and γ-motoneurones are influenced by laughing and mental arithmetic (Ribot, Roll & Vedel, 1986). Clearly their involvement is detachable, which presumes there are rules for engaging and disengaging them. Their participation is context specific; information from spindles must not only be interpreted in the context of any current motor act, but also be set against the gamut of information continually flowing into the spinal cord from other receptors — joint, cutaneous and all. The high stretch sensitivity of primary sensory endings sometimes must be essential to motor control, and at other times irrelevant and even dangerous, and will need to be excluded. This is not new (e.g. Graham Brown, 1911; Forssberg, Grillner & Rossignol, 1975; Taylor & Gottlieb, 1985).

Histophysiological experiments using the superficial lumbrical muscle of the cat have provided the opportunity to analyse the structure of a large number of spindles (Decorte, Emonet-Denand, Ginape & Laporte, 1986). This muscle was initially chosen because of its small size, spindle content and known motor-unit properties (Emonet-Denand, Hunt, Petit & Pollin, 1988).

Areas in the midbrain where stimulation preferentially affects γs- and γd-motoneurones have been reported (see Appelberg, 1981; Fowle, Taylor, Rodgers & Durbaba, 1992; Taylor, Durbaba, Rodgers & Fowle, 1993). In the tenuissimus muscle of anaesthetised animals we also found these effects in experiments in which the responses of Ia afferents to standard ramp and hold stretches were monitored during midbrain stimulation (Dickson & Gladden, 1990). Static effects tended to predominate. This was also the case in separate experiments in which activity of γ-motoneurones was detected by observing the contractions of the types of intrafusal fibre they control in spindles exteriorised under anaesthesia. Chain and/or bag2 contractions indicate active γs-motoneurones, whereas active γd-motoneurones cause bag1 contractions. In confirmation of Fowle et al. (1992) chain fibres could regularly be recruited with bag2 (pure γs- activation), and these fibres were also recruited together with bag1 (mixed γs- and γd-activation) in 14 experiments, including several in which more than one spindle was isolated. It proved difficult to recruit bag1 fibres alone (pure γd- activation). Spontaneous γs-activity could also be inhibited. Here we document an example in which some γs-motoneurones were activated while others were inhibited.

The muscles used in these two studies, the masseter of the rabbit (Saed et al.) and the first lumbrical of the human hand (Thornell et al.) would seem to have very little in common. The first lumbrical has been intimately involved in some of the highest cultural achievements of human beings, since it is the muscle needed to apply pressure by the tip of the index finger against the thumb when holding a pen or paintbrush. However, one cannot be homocentrically dismissive about a muscle merely dedicated to lagomorph nutrition after reading the paper by Saed et al. The control of both these muscles must be closely coordinated not only with the control of several other muscles, but also with sensory information from the skin and joints of the hand in the lumbrical case, and from the buccal cavity and mandibular joints in the masseter case. But the rabbit masseter has an impressive versatility in addition, due to its internal organisation. As Saed et al explain it is divided by partitions into multiple compartments, from superficial to deep, capable of being activated successively, and possibly differentially even within each compartment. Surprisingly, however, this peripheral anatomical order was not reflected in a topographical organisation of the motoneurone cell bodies, which occur in two groups, in the trigeminal motor nucleus, and in cell group k, a separate collection of small fusiform neurones.

The facility to isolate muscle spindles continues to provide new insights into their physiology, but the rationale for the heterogeneous composition of γs-fusimotor units is still unknown. A fusimotor unit consists of a γs- or γd -motoneurone and all the intrafusal fibres that neurone innervates, though these fibres are distributed among several spindles, γd-motoneurones have one effector, the bag 1 fibre, but γs-motoneurones have two, bag2 and chain fibres. Boyd’s view was that there are two types of fusimotor unit whose principal component was either bag2 or chain fibres. The reasons why this attractively simple hypothesis cannot be accepted now unequivocably are explained.

When an isolated cat muscle spindle is subjected to a ramp and hold stretch the primary sensory annulo-spiral round the dynamic bag1 (Db1) fibre is extended and then creeps back part way towards its original state over several seconds since the poles of the fibre give way (Boyd, 1976). This ‘creep’ at the final length is small, or absent, when the fibre is inactive, and is greatly enhanced by activation of the fibre (Fig. 1; Boyd, Gladden & Ward, 1981). The length sensitivity of the primary sensory ending is greatly increased during the dynamic phase of stretching, but the static length sensitivity is little increased because the creep causes pronounced slow adaptation of the Ia discharge (Fig. 2).

The work presented in this report forms part of a larger research programme in which the behaviour of the muscle spindle is described under conditions when several fusimotor inputs, and length changes are applied simultaneously to the spindle while recording simultaneously from its primary (Ia) and secondary (II) sensory endings. We restrict the current presentation to a discussion of the strength of coupling or association and time delay between the responses of primary and secondary endings from the same tenuissimus muscle spindle during activation of single and multiple fusimotor inputs. A description of this interaction is particularly interesting in the light of a recent study by Edgley and Jankowska (1987) which demonstrated the convergence of group Ia and II afferent axons onto the same interneurones in the midlumbar segment of the spinal cord.

In neonatal kittens an appreciable number of soleus spindle afferents did not respond when the ventral root filaments were stimulated at strengths sufficient to recruit fusimotor axons (Gregory and Proske, 1986). This may imply that the fusimotor innervation is not yet functionally developed, as Gregory and Proske suggest. However, Milburn (1984) did find some fusimotor endings in peroneal muscles of newborn kittens which had some of the post-synaptic features of fusimotor endings in adult cats (see Boyd and Gladden, 1985, Part 1 review). We are presently engaged in a more systematic review of the development of fusimotor innervation, using the tenuissimus muscle. By birth in these muscles also post-junctional elaboration was already well advanced at some fusimotor endings, while post-junctional folding was absent or rudimentary at extrafusai motor endings.