The trigeminal ganglion (TrG) and mesencephalic trigeminal nucleus (MTN) neurons are involved in the transmission of orofacial sensory information. The presence of nitric oxide (NO), a putative neurotransmitter substance in the nervous system, was examined in the cat TrG and MTN using nicotinamide adenine dinucleotide phosphate diaphorase (NADPH-d) histochemistry and nitric oxide synthase (NOS) immunohistochemistry. In the TrG, where the majority of the trigeminal primary afferent perikarya are located, most of the intensely NADPH-d/ NOS-stained cells were small in size and distributed randomly throughout the ganglion. The medium-sized neurons were moderately stained. A plexus of pericellular varicose arborizations around large unstained ganglion cells and densely stained fibers in-between could also be observed. In the caudal part of the MTN, both NADPH-d activity and NOS immunoreactivity was present in MTN neurons. In addition, a few scattered NADPH-d/NOS-containing neurons were found in the mesencephalic-pontine junction part of the nucleus. In contrast, only nerve fibers and their terminals were present at a more rostral level in the mid- and rostral MTN. MTN neuronal perikarya were enveloped in fine basket-like NADPH-d/ NOS-positive networks. Differential expression patterns of NOS and its marker NADPH-d suggest that trigeminal sensory information processing in the cat MTN is controlled by nitrergic input through different mechanisms. We introduce the concept that NO can act as a neurotransmitter in mediating nociceptive and proprioceptive information from periodontal mechanoreceptors but may also participate in modulating the activity of jaw-closing muscle afferent MTN neurons.

1.
Aimi, Y., M. Fujimura, S.R. Vincent, H. Kimura (1991) Localization of NADPH-diaphorase-containing neurons in sensory ganglia of the rat. J Comp Neurol 306: 382–392.
2.
Alm, P., B. Uvelius, J. Ekström, B. Holmqvist, B. Larsson, K.E. Andersson (1995) Nitric oxide synthase-containing neurons in rat parasympathetic, sympathetic and sensory ganglia: A comparative study. Histochem J 27: 819–831.
3.
Alvarado-Mallart, M.R., C. Batini, C. Buisseret-Delmas, J. Corvisier (1975) Trigeminal representations of the masticatory and extraocular proprioceptors as revealed by horseradish peroxidase retrograde transport. Exp Brain Res 23: 167–179.
4.
Bredt, D.S., P.M. Hwang, S.H. Snyder (1990) Localization of nitric oxide synthase indicating a neural role for nitric oxide. Nature 347: 768–770.
5.
Bredt, D.S., C.E. Glatt, P.M. Hwang, M. Fotuhi, T.M. Dawson, S.H. Snyder (1991a) Nitric oxide synthase protein and mRNA are discretely localized in neuronal populations of the mammalian CNS together with NADPH diaphorase. Neuron 7: 615–624.
6.
Bredt, D.S., P.M. Hwang, C.E. Glatt, C. Lowenstein, R.R. Reed, S.H. Snyder (1991b) Cloned and expressed nitric oxide synthase structurally resembles cytochrome P-450. Nature 351: 714–718.
7.
Brodal, A. (1981) Neurological Anatomy, ed 3. New York, Oxford University Press.
8.
Brüning, G. (1993) Localization of NADPH-diaphorase in the brain of the chicken. J Comp Neurol 334: 192–208.
9.
Brüning, G., U. Funk, B. Mayer (1994a) Immunocytochemical localization of nitric oxide synthase in the brain of the chicken. NeuroReport 5: 2425–2428.
10.
Brüning, G., S. Wiese, B. Mayer (1994b) Nitric oxide synthase in the brain of the turtle Pseudemys scripta elegans. J Comp Neurol 348: 183–206.
11.
Byers, M.R., T.A. O’Connor, R.F. Martin, W.K. Dong (1986) Mesencephalic trigeminal sensory neurons of cat: Axon pathways and structure of mechanoreceptive endings in periodontal ligament. J Comp Neurol 250: 181–191.
12.
Cajal, S.R. (1909) Histologie du Système Nerveux de l’Homme et des Vertébrés. Maloine, Paris.
13.
Capra, N.F., K.V. Anderson, R.C. Atkinson, III (1985) Localization and morphometric analysis of masticatory muscle afferent neurons in the nucleus of the mesencephalic root of the trigeminal nerve in the cat. Acta Anat 122: 115–125.
14.
Chouchkov, C., N. Lazarov (1989) Neuropeptide immunoreactivity in the cat trigeminal ganglion. Anat Anz 164(suppl): 207–208.
15.
Christova, T., A. Paloff, W. Ovtscharoff, D. Hinova-Palova, Z. Nicolova (1997) NADPH-diaphorase enzyme activity and tyrosine hydroxylase immunoreactivity in the locus coeruleus of the cat. Eur J Morphol 35: 58–59.
16.
Davies, A.M. (1988) The trigeminal system: An advantageous experimental model for studying neuronal development. Development 103 (suppl): 175–183.
17.
Dawson, T.M., D.S. Bredt, M. Fotuhi, P.M. Hwang, S.H. Snyder (1991) Nitric oxide synthase and neuronal NADPH diaphorase are identical in brain and peripheral tissues. Proc Natl Acad Sci USA 88: 7797–7801.
18.
Dohrn, C.S., M.A. Mullett, R.H. Price, A.J. Beitz (1994) Distribution of nitric oxide synthase-immunoreactive interneurons in the spinal trigeminal nucleus. J Comp Neurol 346: 449– 460.
19.
Elphick, M.R. (1996) Localization of nitric oxide synthase using NADPH diaphorase histochemistry; in Rayne RC (ed): Methods in Molecular Biology. Neurotransmitter Methods. Totowa, Humana Press, vol 72, pp 153–158.
20.
Hope, B.T., G.J. Michael, K.M. Knigge, S.R. Vincent (1991) Neuronal NADPH diaphorase is a nitric oxide synthase. Proc Natl Acad Sci USA 88: 2811–2814.
21.
Hsu, S.M., L. Raine, H. Fanger (1981) Use of avidin-biotin-peroxidase complex (ABC) in immunoperoxidase techniques: A comparison between ABC and unlabeled antibody (PAP) procedures. J Histochem Cytochem 29: 577– 580.
22.
Jiang, P.-J., S. Terashima (1996) Distribution of NADPH-diaphorase in the central nervous system of an infrared-sensitive snake, Trimeresurus flavoviridis. Brain Res 713: 168–177.
23.
Kalina, M., J.J. Bubis (1969) Ultrastructural localization of acetylcholine esterase in neurones of rat trigeminal ganglion. Experientia 25: 388–389.
24.
Lazarov, N. (1994) Primary trigeminal afferent neuron of the cat. II. Neuropeptide- and serotonin-like immunoreactivity. J Brain Res 35: 373–389.
25.
Lazarov, N. (1995) Distribution of calcitonin gene-related peptide- and neuropeptide Y-like immunoreactivity in the trigeminal ganglion and mesencephalic trigeminal nucleus of the cat. Acta Histochem 97: 213–223.
26.
Lieberman, A.R. (1976) Sensory ganglia; in Landon DN (ed): The Peripheral Nerve. London, Chapman & Hall, pp 188–278.
27.
Light, A.R. (1992) The Initial Processing of Pain and Its Descending Control: Spinal and Trigeminal Systems. Basel, Karger.
28.
Linden, R.W.A., B.J. Millar, Z. Halata (1994) A comparative physiological and morphological study of periodontal ligament mechanoreceptors represented in the trigeminal ganglion and the mesencephalic nucleus of the cat. Anat Embryol 190: 127–135.
29.
Lohinai, Z., A.D. Székely, P. Benedek, A. Csillag (1997) Nitric oxide synthase containing nerves in the cat and dog dental pulp and gingiva. Neurosci Lett 227: 91–94.
30.
Mizukawa, K., S.R. Vincent, P.L. McGeer, E.G. McGeer (1989) Distribution of reduced-nicotinamide-adenine-dinucleotide-phosphate diaphorase-positive cells and fibers in the cat central nervous system. J Comp Neurol 279: 281–311.
31.
Nomura, S., N. Mizuno (1985) Differential distribution of cell bodies and central axons of mesencephalic trigeminal nucleus neurons supplying the jaw-closing muscles and periodontal tissue: A transganglionic tracer study in the cat. Brain Res 359: 311–319.
32.
Panzica, G.C., R. Arévalo, F. Sánchez, J.R. Alonso, N. Aste, C. Viglietti-Panzica, J. Aijón, R. Vázquez (1994) Topographical distribution of reduced nicotinamide adenine dinucleotide phosphate (NADPH)-diaphorase in the brain of the Japanese quail. J Comp Neurol 342: 97–114.
33.
Rodrigo, J., D.R. Springall, O. Uttenthal, M.L. Bentura, F. Abadia-Molina, V. Riveros-Moreno, R. Martínez-Murillo, J.M. Polak, S. Moncada (1994) Localization of nitric oxide synthase in the adult rat brain. Phil Trans R Soc Lond [B] 345: 175–221.
34.
Ryall, R.W. (1982) Modulation of cholinergic transmission by substance P; in: Substance P in the Nervous System. Ciba Foundation Symp 91. London, Pitman, pp 267–280.
35.
Scherer-Singler, U., S.R. Vincent, H. Kimura, E.G. McGeer (1983) Demonstration of a unique population of neurons with NADPH-diaphorase histochemistry. J Neurosci Methods 9: 229–234.
36.
Schmidt, H.H.H.W., G.D. Gagne, M. Nakane, J.S. Pollock, M.F. Miller, F. Murad (1992) Mapping of neural nitric oxide synthase in the rat suggests frequent colocalization with NADPH diaphorase but not with soluble guanylyl cyclase, and novel paraneural functions for nitrinergic signal transduction. J Histochem Cytochem 40: 1439–1456.
37.
Schuman, E.M., D.V. Madison (1994) Nitric oxide and synaptic function. Annu Rev Neurosci 17: 153–183.
38.
Sienkiewicz W., J. Kaleczyc, M. Majewski, M. Lakomy (1995) NADPH-diaphorase-containing cerebrovascular nerve fibres and their possible origin in the pig. J Hirnforsch 36: 353– 363.
39.
Snyder, S.H. (1992) Nitric oxide: First in a new class of neurotransmitters? Science 257: 494– 496.
40.
Weinberg, R.J., J.G. Valtschanoff, H.H.H.W. Schmidt (1996) The NADPH diaphorase histochemical stain; in Feelisch, M., J.S. Stamler (eds): Methods in Nitric Oxide Research. New York, Wiley, pp 237–248.
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