Correlated histological and physiological observations on a case of common sensory output and motor input of the bag₁ fibre and a chain fibre in a cat tenuissimus spindle

Abstract

In muscle spindles of the cat, independent control of dynamic and static components of the response of the primary sensory ending to stretch is provided by separate motor inputs to the various kinds of intrafusal muscle fibre: dynamic axons (γ or β) to the bag₁ fibres and static axons to the bag₂ (typically γ only) and chain (γ or β) fibres. Nonlinear summation of separately evoked effects during combined stimulation of dynamic and static motor axons appears to be due to mutual resetting by antidromic invasion of separate encoding sites, leading to partial occlusion of the momentarily lesser response by the greater. The encoding sites are thought to be located within the primary ending's preterminal branches which from first-order level are normally segregated to the bag₁ fibre and to the bag₂ and chain fibres. Here we describe the analysis of a special case that arose in a histophysiological study which had shown that the degree of occlusion was related to the minimum number of nodes between the putative encoding sites. Three-dimensional reconstruction of the primary ending revealed that the terminals of one chain fibre were derived entirely from the first-order branch that supplied the bag₁ fibre, including one terminal that was shared directly with the bag₁ (sensory cross-terminal). The other first-order branch supplied the bag₂ and remaining chain fibres as normal. The degree of occlusion seen during simultaneous stimulation of a dynamic β axon and a static γ axon indicated that the encoding sites were separated by both first-order branches. Schematic reconstruction of the motor innervation revealed that the static γ axon was most unlikely to have supplied the chain fibre which shared sensory terminals with the bag₁, but that these fibres also shared a motor input with histological characteristics of β type. Ramp-frequency stimulation of the dynamic β axon at constant length evoked a driving effect which persisted after fatiguing the extrafusal component and was therefore explicable on the basis of the observed pattern of motor innervation, though the identity of the axon could not be conclusively proved. Individually, instances of shared sensory terminals and motor input of bag₁ and chain fibres are rare in the cat; their combination in a single spindle with correlated physiology is described here for the first time. The observation is considered in relation to the importance of dynamic and static segregation in motor control, since it may imply that there is a lower limit to the degree of segregation that the developmental programme can provide.