Ultrastructural anatomy of physiologically identified jaw-muscle spindle afferent terminations onto retrogradely labeled jaw-elevator motoneurons in the rat.

Abstract

Neuronal microcircuits involving jaw-muscle spindle afferents and jaw-elevator motoneurons were studied via retrograde and intracellular labeling in rats. Initially, trigeminal motoneurons were retrogradely labeled from horseradish peroxidase (HRP) injections into the temporalis and masseter muscles. The intracellular response of jaw-muscle spindle afferent neurons was then characterized during palpation, ramp and hold, and sinusoidal stretching of the jaw-closing muscles. Biotinamide was injected into these neurons, and the tissue was processed for the visualization of HRP and biotinamide. The ultrastructure of 243 intracellularly stained jaw-muscle spindle afferent boutons located within the trigeminal motor nucleus (Vmo) was examined. Eighty-five of these boutons synapsed with motoneurons retrogradely labeled with HRP, and 158 boutons synapsed with unlabeled structures within the Vmo. All spindle afferent boutons contained clear, spherical synaptic vesicles. Although the majority of boutons were S type, a few labeled jaw-muscle spindle afferent boutons possessed a long, narrow cleft, with a subsynaptic cistern comparable to previous descriptions of C-type boutons. Sixty-eight percent of spindle afferent boutons synapsed with large or medium-sized, retrogradely labeled motoneuron dendrites, and 32% synapsed with retrogradely labeled somata. In numerous instances, spindle afferent boutons synapsed with trigeminal motoneuron dendritic or somatic spines. Most of the synapses between spindle afferent boutons and trigeminal motoneuron dendrites were asymmetric, and the greatest percentage of axosomatic synapses between spindle afferents and trigeminal motoneurons were symmetric. Approximately 24% of spindle afferent boutons constituted the intermediate element of a axoaxodendritic or axoaxosomatic assemblage, implying that some jaw-muscle spindle afferent synapses with trigeminal motoneurons are presynaptically modulated.