Ultrastructural basis for synaptic transmission between jaw-muscle spindle afferents and trigeminothalamic neurons in the rostral trigeminal sensory nuclei of the rat.

Abstract

Trigeminothalamic neurons were retrogradely labeled by injection of horseradish peroxidase into the ventroposteromedial nucleus of the thalamus in rats. Jaw-muscle spindle afferent axons were then physiologically identified and intracellularly stained with biotinamide. The ultrastructure of labeled spindle afferent boutons was then studied in the caudolateral supratrigeminal region (Vsup) and dorsomedial trigeminal principal sensory nucleus (Vpdm). A total of 418 stained spindle afferent boutons were identified in Vsup and Vpdm; approximately 75% of these synapsed with dendrites, 10% synapsed with somata, and 15% synapsed with axons. Most jaw-muscle spindle afferent boutons were postsynaptic to unlabeled P-type boutons. Reciprocal synapses between spindle afferent boutons and unlabeled boutons were occasionally observed. A few dendrites in Vsup and Vpdm received synapses from multiple spindle afferent boutons. Conversely, some large (from 3 x 6 to 4 x 8 microns) and giant (from > 4 x 8 to 5 x 10 microns) spindle afferent boutons simultaneously contacted two to five dendrites and/or somata. Jaw-muscle spindle afferent boutons also formed synapses with retrogradely labeled trigeminothalamic neurons in Vsup and Vpdm. Numerous unlabeled S-and F-type boutons converged onto the same trigeminothalamic dendrite or soma contacted by a spindle afferent bouton. A small number of synaptic triads consisting of an unlabeled P-type bouton, a spindle afferent bouton, and either a dendrite or soma were also encountered. These data indicate that sensory feedback from the masticatory muscles is subject to presynaptic inhibition and integration prior to reaching the thalamus. This pathway is likely to be important in the relay of proprioceptive and kinesthetic information from the muscles of mastication to the thalamus.