The Innervation of the Muscle-Spindle

Abstract

A study of the morphology and innervation of muscle-spindles from the quadriceps of the rabbit and cat has shown that: 1. The intrafusal muscle-fibres do not subdivide in their course through the spindle, as is maintained in some descriptions, but retain their individuality from pole to pole. 2. There is no constant feature which is characteristic of one pole of a spindle and not the other. A distinction can be made between the proximal and distal ends only when it is possible to orientate the spindle according to the proximal and distal ends of the muscle. The extreme ends of the spindle are attached indifferently to extrafusal endomysium, tendon, or perimysial connective tissue. 3. In the equatorial region each muscle-fibre of the spindle contains a dense aggregation of spherical central nuclei (‘nuclear bag’). On either side of this aggregation oval nuclei are disposed in the form of a chain within a central core of protoplasm (‘myotube region’). The nuclear bag is devoid of cross-striations and presumably non-contractile. The two polar portions of the muscle-fibre on either side of the bag are striated and each receives a motor innervation; hence they are presumed to function as independent contractile units. 4. The number of end-plates possessed by a spindle is approximately double its number of intrafusal muscle-fibres, with half the total number of end-plates situated at each pole. The ratio is rarely exact, since one polar half of an intrafusal fibre frequently bears two end-plates; these are innervated by nerve-fibres which retain their individuality as far as they can be traced back from the spindle. Both small nerve-fibres (3-4 µ in gold chloride preparations) and relatively large nerve-fibres (6-7 µ in gold chloride preparations) take part in the motor innervation of muscle-spindles, as was deduced on physiological grounds by Leksell (1945). 5. An analysis of the sensory innervation has confirmed many of Ruffini's (1898) observations. Primary or ‘annulo-spiral’ and secondary or ‘flowerspray’ endings occur and they are innervated by independent nerve-fibres; it is suggested that Ruffini's terms ‘primary’ and ‘secondary’ be adopted since the descriptive terms cannot always be applied. In the rabbit the secondary ending is ‘annulo-spiral’ in form and differs little from the primary ending; in the cat it is more irregular and could be termed ‘flower-spray’. The primary ending is always present and is associated with the nuclear bags of the intrafusal muscle-fibres; in some instances its ramifications are more extensive and also entwine the myotube regions. The primary ending may be the only sensory termination present, or it may be accompanied by one or by two secondary endings. These are borne by the myotube regions of the musclefibres. In the rabbit's quadriceps and interossei, spindles with one primary and one secondary ending were the most frequent in the samples taken; in the cat's quadriceps spindles with one primary and two secondary endings were the most numerous. Both the primary and secondary nerve-fibres invariably ramify so as to innervate each intrafusal fibre in the muscle-bundle. The two sensory terminations are often closely intercalated but do not overlap with one another to any great extent. As estimated from measurements made on fresh, silver, and gold chloride preparations the total diameter of the primary fibre lies between 8 and 12 µ, that of the secondary fibre between 6 and 9 µ. 6. Apart from small sympathetic fibres innervating the vascular supply of the spindle, other finer fibres may occasionally be seen ramifying within the walls of the capsule and over the polar regions. It is possible that they are somatic sensory fibres subserving the sensation of pain. 7. The nature of the reflex effects of the afferent impulses discharged by the muscle-spindle and tendon-organ is considered, and it is concluded that the balance of evidence indicates that the afferent discharge from the spindle is excitatory and that from the tendon-organ inhibitory to the motor neurones of the same muscle. However, the identification of the spindle as the receptor which excites the stretch reflex is found to rest largely upon equivocal evidence, its acceptance depending ultimately upon Matthews's finding (1933) of a considerable difference-in threshold between the spindle and tendon-organ in response to stretch. It is suggested that the large primary fibre innervating the spindle should be identified as the ‘stretch afferent’ rather than the smaller secondary fibre specified by Matthews, for the rapid con duction rate of the afferent discharge exciting the stretch reflex (Lloyd, 1943) indicates that sensory fibres of the largest diameter are employed. The functional significance of the secondary fibres is obscure and the specific reflex functions of the sensory fibres innervating both the spindle and the tendon organ clearly require further elucidation.