Golgi and immunocytochemical analysis of neurons in trigeminal subnucleus interpolaris: correlations with cellular localization of enkephalin.

Abstract Recent electrophysiological evidence shows that rostral levels of the trigeminal spinal complex are concerned with pain processing from receptive fields in the face and oral cavity. The ventrolateral quadrant of the subnucleus interpolaris contains concentrations of enkephalin, dynorphin, serotonin, substance P and GABA [Matthews M.A. Hernandez T.V. and Liles S.L. (1987) Synapse1, 512–529; Matthews M.A., McDonald G.K. and Hernandez T.V. (1988) Somatosensory Res.5, 205–217]. These transmitters have also been localized to the fusiform and stalked cells in Laminae I and II of the subnucleus caudalis [Basbaum A.I. and Fields H.L. (1984) A. Rev. Neurosci.7, 309–338]. The present study compares Golgi impregnations of the subnucleus interpolaris with sections at the same levels immunoreacted against enkephalin to determine if comparable cells exist in the subnucleus interpolaris and if they occur predominantly in the ventrolateral quadrant of the subnucleus. Twelve, young adult cats were killed by perfusion, the brainstems removed and either processed for rapid Golgi impregnation or sectioned and immunoreacted for enkephalin using the avidin-biotin Vectastain method. Golgi impregnated tissue was sectioned in the coronal, transverse or sagittal plane to insure the most advantageous visualization of cells with a directional bias in their dendritic arbors. The subnucleus interpolaris contained several distinctive cell types. The predominant neuron throughout the subnucleus was the smooth pyramidal cell or multipolar cell, characterized by a large round soma (15–25 μm diameter) and a spherical dendritic arborization which allowed its identification in all planes of section. The second cell type was the fusiform cell which had a smaller ovoid soma (10–15μm) with narrow, less ramified, dendritic arbors oriented dorsoventrally, thus giving a bipolar appearance. Fusiform cells were most concentrated along the lateral margin of the subnucleus interpolaris. Examination of sections at the same level reacted for enkephalin revealed cells with a bipolar appearance in these same locations. An additional cell population which tended to predominate in the lateral zone was the stalked cell. These displayed a rounded soma (12–20 μm) and were evident only in the transverse or sagittal plane. Two to four primary dendrites arose from the soma and extensively ramified into a dense spiny arbor directed into the body of the subnucleus interpolaris. Many examples contained enkephalin. Islet cells, characterized by a very small oval soma (6–12 μm) and dense, rostrocaudally oriented dendrites, were less common than stalked cells and were located deeper in the nucleus. These cells displayed recurrent dendritic branches in common with the spiny pyramidal cell, which was noted by Gobel [Gobel S. (1978) J. comp. Neurol.180, 378–394; Gobel S. (1978) J. comp. Neurol.180, 395–414] in the subnucleus caudalis and which was occasionally seen in our preparations. Spiny pyramidal cells had a triangular and distinctive basal and apical dendrites. Arboreal cells represented the last neuronal category noted in the subnucleus interpolaris. These were only infrequently encountered and displayed an extensively branched, laterally directed, dendritic arbor. Occasional arboreal cells were found to contain enkephalin. Finally, an extensive axonal plexus was observed along the lateral margin of the subnucleus interpolaris throughout its length. Axons arising from fusiform, stalked and arboreal cells had branches which either ramified in this plexus, recurred into the dendritic arbor of the parent cell or coursed into the spinal V tract. In conclusion, these findings indicate that the ventrolateral quadrant and lateral margin of the subnucleus interpolaris contains populations of neurons comparable in structure and enkephalin affinity to those neurons located in the superficial laminae of the subnucleus caudalis. These data provide additional support for a functional subdivision of the subnucleus interpolaris involved principally in pain processing.