Relation between intrafusal and extrafusal activity in triceps surae muscles of the decerebrate cat: Evidence for β action

In an attempt to assess the relative influence of γ and β innervation on muscle spindles, the discharge patterns of 105 normally innervated medial gastrocnemius and soleus spindle receptor afferents were compared in resting and reflexively activated muscles of the decerebrate cat. Our premise was that increases in afferent discharge rate arising above extrafusal threshold could result, in some degree, from β (skeletofusimotor) activity superimposed on a background of γ efferent discharge. In isometric muscles, primary and secondary spindle receptors responded to low-intensity mechanical or electrical stimulation of the contralateral limb with acceleration of discharge rate. This acceleration occurred at stimulus intensities insufficient to activate extrafusal fibers, and was therefore of γ origin. Approximately half of the endings generated further rate increases when simulation of the contralateral limb was sufficient to induce substantial increases in isometric force and EMG activity. Eight of 105 receptors were activated only at high force levels, and 3 of these showed abrupt discontinuities consistent with recruitment of a new efferent (γ and β) fiber. For many spindles, a continuing increase in efferent excitation, extending well beyond extrafusal threshold, must have occurred. Both primary and secondary spindle afferents showed significant alterations in their response to constant velocity stretch during contralateral limb stimulation; the responses were classiffied as 'static type,' 'dynamic type,' and 'mixed,' depending on their resemblance to the known patterns observed during stimulation of single static and/or dynamic γ-fibers. Eleven of 65 units showed unexpected additions to the dynamic response at intermediate or high forces. A fourth pattern, 'unloading,' was identified when receptor discharge decreased with increasing force. The general features of the dynamic response suggest that both static and dynamic γ-fibers were often active in our preparations, although β-fibers could also have influenced afferent discharge above extrafusal threshold. Since γ-motoneurons are neither recruited nor strongly excited by muscle stretch, the unexpected additions to the dynamic response probably resulted from recruitment of a β-fiber. Muscle spindle receptors that showed continuing rate increases with contralateral limb stimulation usually increased their average discharge during isotonic muscle shortening; other spindle afferents showed substantial rate reductions. The former rate increases imply that motor excitation of the muscle spindle must have continued to increase during crossed-extensor stimulation. Recordings from 61 γ-fibers isolated from teased filaments of the medial gastrocnemius nerve in similar preparations showed activation thresholds lower than those of extrafusal fibers from the same muscle. Most significantly, there was no evidence of γ recruitment or continuing rate modulation at intermediate or high force levels, and the γ-fibers were largerly unresponsive to stretch. Modifications of spindle receptor discharge arising at substantial levels of excitation of the motoneuron pool could result from recruitment or rate modulation of either γ- or β-motoneurons. However, the finding of consistently lower thresholds for γ-fiber activation, the apparent saturation of γ-fiber discharge near extrafusal threshold, and our failure to demonstrate significant additional γ-fiber recruitment or rate modulation above extrafusal threshold support the hypothesis of β-motoneuronal influence on muscle spindles.