Structure-function relationships in rat brainstem subnucleus interpolaris: III. Local circuit neurons

Intracellular recording, electrical stimulation, receptive field mapping, and intracellular injection of horseradish peroxidase were used to assess the response properties, collateral projections, and morphology of 44 local circuit (LC) neurons in the subnucleus interpolaris (Sp Vi) of the trigeminal brainstem complex of the rat. LC neurons were defined as those with axons restricted to brainstem areas receiving trigeminal primary afferent fibers. Thus, none were antidromically activated from the thalamus, tectum, or cerebellum, and their axons could be seen terminating exclusively within the trigeminal brainstem complex or reticular formation. All neurons sampled were discharged by innocuous or noxious mechanical stimulation of a restricted portion of the face or mouth. They were classified functionally as sensitive to vibrissae (N = 22), nociceptors (N = 9), guard hairs (N = 7), hairy skin (N = 3), or periodontia (N = 3). Fifty percent of the stained neurons were vibrissa sensitive. Twenty-one of these 22 responded to deflection of only one vibrissa. The remaining functional groups also had small receptive fields. Intracellular staining revealed a consistency in vibrissa-sensitive LC morphology. Somata were small to medium in size and multipolar. Their axons had an initial transverse trajectory and gave off recurrent collaterals which arborized extensively in the region of the soma. The parent axon then bifurcated. One branch traveled rostrally to subnucleus principalis while the other branch traveled caudally to subnucleus caudalis. The branches periodically sent collaterals into regions of the trigeminal complex corresponding to the transverse position of the soma. Dendrites extended 440 +/- 140 microns rostrocaudally, forming a tree with a transverse perimeter of 459 +/- 226 microns. Distal dendrites were thin and sinuous, had few spines, and extensively arborized adjacent to the soma. They ended in multiple swellings connected by slender processes. The stereotyped morphology of vibrissa-sensitive LC neurons differed from the variable morphologies of LC neurons activated by nociceptors, guard hairs, hairy skin, or periodontia. Although no group of neurons in one of these categories displayed a distinguishing morphological characteristic, they collectively had features which distinguished them from the vibrissa-sensitive neurons. Non-vibrissa-responsive neurons generally had more expansive, but less circular, dendritic and recurrent axonal arbors; dendrites had more spines, and axons often sent endings into the reticular formation.(ABSTRACT TRUNCATED AT 400 WORDS)