Morphology and topography of identified primary afferents in trigeminal subnuclei principalis and oralis

1. Intra-axonal recording, receptive field mapping, horseradish peroxidase injection, cytochrome oxidase staining, and computer-assisted reconstruction/morphometric methods were used to elucidate the structure and topography of trigeminal primary afferent collaterals in the normal adult rat. Prior studies focused on trigeminal brain stem subnuclei interpolaris and caudalis. This work is extended here to the remaining 2 subnuclei, principalis (PrV) and oralis (SpVo), where collaterals from 66 axons in 37 adult rats were studied. In nine rats, three to five axons were stained for within-nucleus comparisons of different fibers. Quantitative analyses were restricted to vibrissa sensitive fibers. 2. All of the axons conducted rapidly with small, low-threshold receptive fields. The majority responded to vibrissa deflection (n = 47); the remainder responded to guard hair deflection; gentle pressure applied to hairy skin, glabrous skin, lingual mucosa, or an incisor; or jaw movement. All descended in the trigeminal sensory root where some bifurcated into ascending and descending branches. Each well-stained fiber gave rise to transversely oriented collaterals in PrV and SpVo. 3. Within PrV and SpVo, fibers with differing adaptation properties and receptive fields had indistinguishable collateral morphologies. Arbors from single axons were rostrocaudally discontinuous, small relative to collaterals in subnuclei interpolaris and caudalis, circumscribed and topographically organized in a manner consistent with cytochrome oxidase and bulk-labeled primary afferent staining patterns. In SpVo and caudal PrV, the map is inverted with the nose pointing medially. In rostral PrV, the map turns 90° such that the nose points dorsally. 4. Axons had different quantitative properties along the rostrocaudal axis of the trigeminal brain stem complex. Whereas arbors subtended similar transverse areas throughout PrV and SpVo, collaterals in the rostral third of PrV had a relatively low bouton density. Arbors in the caudal two thirds of PrV had the highest bouton density. Arbors in SpVo tended to be more variable in size and shape than those of caudal PrV, and their bouton numbers were significantly lower than in PrV. 5. In PrV, arbors were largely confined to somatotopically corresponding cytochrome oxidase patches, precluding significant overlap of neighboring whisker projections. In SpVo, termination sites were not as strictly confined and numerous examples of within- and between-row overlap were obtained for whisker afferents in cases where multiple axons were stained. 6. These and prior data suggest that peripheral and central target factors influence collateral morphology in the rat trigeminal brain stem complex, and that physiological distinctions between cells in PrV and SpVo reflect different primary afferent arborization patterns in these two regions. These and other data on the geometry of PrV dendritic trees suggest an anatomic substrate for receptive field size in PrV second-order neurons.