Nitric oxide synthase in the adult and developing thalamus: Histochemical and immunohistochemical study in the rat

Journal of Comparative Neurology

Volumn 388, Issue 1, 1997, Pages 89-105

  Bertini, Giuseppe ^a,b   Bentivoglio, Marina ^a  

^a UNIVERSITY OF VERONA   (Italy)

^b NATIONAL INSTITUTE OF MENTAL HEALTH   (United States)

Author keywords

Development; NADPH diaphorase; Nitrinergic transmission; Thalamic cholinergic innervation; Thalamocortical

Indexed keywords

NITRIC OXIDE; NITRIC OXIDE SYNTHASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE DEHYDROGENASE;

ADOLESCENT; ANIMAL TISSUE; ARTICLE; BRAIN DEVELOPMENT; IMMUNOHISTOCHEMISTRY; MALE; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; THALAMUS;

AGING; ANIMALS; ANIMALS, NEWBORN; DIHYDROLIPOAMIDE DEHYDROGENASE; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENICULATE BODIES; HISTOCYTOCHEMISTRY; IMMUNOHISTOCHEMISTRY; MALE; NEURONS; NITRIC OXIDE SYNTHASE; RATS; RATS, WISTAR; THALAMIC NUCLEI; THALAMUS;

EID: 0030684790     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1096-9861(19971110)388:1<89::AID-CNE6>3.0.CO;2-K     Document Type: Article

References (59)

1. Arai, R., D.M. Jacobowitz, and S. Deura (1994) Distribution of calretinin, calbindin-D28k, and parvalbumin in the rat thalamus. Brain Res. Bull. 33:595-614.
2. Arcelli, P., C. Frassoni, M.C. Regondi, S. De Biasi, and R. Spreafico (1997) GABAergic neurons in mammalian thalamus: A marker of thalamic complexity? Brain Res. Bull. 42:27-37.
3. Arnt-Ramos, L.R., W.E. O'Brien, and S.R. Vincent (1992) Immunohistochemical localization of argininosuccinate synthetase in the rat brain in relation to nitric oxide synthase-containing neurons. Neuroscience 51:773-789.
4. Bentivoglio, M., K. Kultas-Ilinsky, and I.A. Ilinsky (1993) The limbic thalamus. Structure, intrinsic organization, and connections. In B.A. Vogt and M. Gabriel (eds): Neurobiology of the Cingulate Cortex and Limbic Thalamus. Boston: Birkhauser, pp. 71-122.
5. Bentivoglio, M., M. Mishkin, and J.P. Aggleton (1997) Thalamus and memory formation. In M. Steriade, E.G. Jones, and D.A. McCormick (eds): Handbook on Thalamus. Amsterdam: Elsevier (in press).
6. Bertini, G., Z.-C. Peng, and M. Bentivoglio (1996a) The chemical heterogeneity of cortical interneurons: Nitric oxide synthase vs. calbindin and parvalbumin immunoreactivity in the rat. Brain Res. Bull. 39:261-266.
7. Bertini, G., T. Savio, D. Zaccheo, H.H.H.W. Schmidt, and M. Bentivoglio (1996b) NADPH-diaphorase activity in brain macrophages during postnatal development in the rat. Neuroscience 70:287-293.
8. Bickford, M.E., A.E. Günlük, W. Guido, and S.M. Sherman (1993) Evidence that cholinergic axons from the parabrachial region of the brainstem are the exclusive source of nitric oxide in the lateral geniculate nucleus of the cat. J. Comp. Neurol. 334:410-430.
9. Bredt, D.S., C.E. Glatt, P.M. Hwang, M. Fotuhi, T.M. Dawson, and S.H. Snyder (1991) Nitric oxide synthase protein and mRNA are discretely localized in neuronal populations of the mammalian CNS together with NADPH-diaphorase. Neuron 7:615-624.
10. Catania, M.V., T.R. Tolle, and H. Monyer (1995) Differential expression of AMPA receptor subunits in NOS-positive neurons of cortex, striatum, and hippocampus. J. Neurosci. 15:7046-7061.
11. Cramer, K.S., C.I. Moore, and M. Sur (1995) Transient expression of NADPH-diaphorase in the lateral geniculate nucleus of the ferret during early postnatal development. J. Comp. Neurol. 353:306-316.
12. Cudeiro, J., C. Rivadulla, R. Rodriguez, S. Martinez-Conde, L. Martinez, K.L. Grieve, and C. Acuña (1996) Further observations on the role of nitric oxide in the feline lateral geniculate nucleus. Eur. J. Neurosci. 8:144-152.
13. Dawson, T.M., and S.H. Snyder (1994) Gases as biological messengers: Nitric oxide and carbon monoxide in the brain. J. Neurosci. 14:5147-5159.
14. Do, K.Q., K.E. Binns, and T.E. Salt (1994) Release of the nitric oxide precursor, arginine, from the thalamus upon sensory afferent stimulation, and its effect on thalamic neurons in vivo. Neuroscience 60:581-586.
15. Dun, N.J., R. Huang, S.L. Dun, and U. Forstermann (1994) Infrequent co-localization of nitric oxide synthase and calcium binding proteins immunoreactivity in rat neocortical neurons. Brain Res. 666:289-294.
16. Frassoni, C., M. Bentivoglio, R. Spreafico, M.P. Sanchez, A. Fairen, and L. Puelles (1991) Postnatal development of calbindin and parvalbumin immunoreactivity in the thalamus of the rat. Dev. Brain Res. 58:243-249.
17. Frassoni, C., R. Spreafico, and M. Bentivoglio (1997) Glutamate, aspartate and co-localization with calbindin in the medial thalamus: An immunohistochemical study in the rat. Exp. Brain Res. 115:95-104.
18. Gabbott, P.L., and S.J. Bacon (1994) Two types of interneuron in the dorsal lateral geniculate nucleus of the rat: A combined NADPH diaphorase histochemical and GABA immunocytochemical study. J. Comp. Neurol. 350:281-301.
19. Gally, J.A., P.R. Montague, G.N. Reeke, Jr., and G.M. Edelmann (1990) The NO hypothesis: Possible effects of a short lived, rapidly diffusible signal in the development and function of the nervous system. Proc. Natl. Acad. Sci. USA 87:3547-3551.
20. Garthwaite, J., and C.L. Boulton (1995) Nitric oxide signaling in the central nervous system. Annu. Rev. Physiol. 57:683-706.
21. Gonzalez-Hernandez, T., M. Conde-Sendin, B. Gonzalez-Gonzalez, B. Mantolan-Sarmiento, H. Perez-Gonzalez, and G. Meyer (1993) Postnatal development of NADPH-diaphorase activity in the superior colliculus and the ventral lateral geniculate nucleus of the rat. Dev. Brain Res. 76:141-145.
22. Gonzalez-Hernandez, T., B. Mantolan-Sarmiento, B. Gonzalez-Gonzalez, R. Ferres-Torres, and G. Meyer (1994) NADPH-d (dihydronicotinamide adenine dinucleotide phosphate diaphorase) activity in geniculo-tectal neurons of the rat. Neurosci. Lett. 167:77-80.
23. Haley, J.E., G.L. Wilcox, and P.F. Chapman (1992) The role of nitric oxide in hippocampal long-term potentiation. Neuron 8:211-216.
24. Hope, B.T, and S.R. Vincent (1989) Histochemical characterization of neuronal NADPH-diaphorase. J. Histochem. Cytochem. 37:653-661.
25. Hope, B.T., G.J. Michael, K.M. Knigge, and S.R. Vincent (1991) Neuronal NADPH diaphorase is a nitric oxide synthase. Proc. Natl. Acad. Sci. USA 88:2811-2814.
26. Jones, E.G. (1985) The Thalamus. New York: Plenum Press.
27. Kharazia, V.N., P. Petrusz, K. Usunoff, R.J. Weinberg, and A. Rustioni (1997) Arginine and NADPH diaphorase in the rat ventroposterior thalamic nucleus. Brain Res. 744:151-155.
28. Krekelberg, B., and J.G. Taylor (1996) Nitric oxide in cortical map formation. J. Chem. Neuroanat. 10:191-196.
29. Leigh, P.N., J.H. Connick, and T. W. Stone (1990) Distribution of NADPH-diaphorase positive cells in the rat brain. Comp. Biochem. Physiol. 97C:259-264.
30. Matsumoto, T., M. Nakane, J.S. Pollock, J.E. Kuk, and U. Forstermann (1993) A correlation between soluble brain nitric oxide synthase and NADPH-diaphorase activity is only seen after exposure of the tissue to fixative. Neurosci. Lett. 155:61-64.
31. Meng, X.-W., P.T. Ohara, and H.J. Ralston (1996) Nitric oxide synthase immunoreactivity distinguishes a sub-population of GABA-immunoreactive neurons in the ventrobasal complex of the cat. Brain Res. 728:111-115.
32. Mengual, E., J.L. Velayos, and F. Reinoso-Suarez (1993) Nicotinamide-adenine dinucleotide phosphate diaphorase activity matches acetylcholinesterase-rich patches in the medial thalamic nuclei of the cat. Brain Res. 625:165-168.
33. Milligan, C.E., T.J. Cunningham, and P. Levitt (1991) Differential immunochemical markers reveal the normal distribution of brain macrophages and microglia in the developing rat brain. J. Comp. Neurol. 314:125-135.
34. Mitrofanis, J. (1992) NADPH-diaphorase reactivity in the ventral and dorsal lateral geniculate nuclei of rats. Visual Neurosci. 9:211-216.
35. Miyazaki, M., Y. Kayama, T. Kihara, K. Kawasaki, E. Yamaguchi, Y. Wada, and M. Ikeda (1996) Possible release of nitric oxide from cholinergic axons in the thalamus by stimulation of the rat laterodorsal tegmental nucleus as measured with voltammetry. J. Chem. Neuroanat. 10:203-207.
36. Nakamura, H., T. Saheki, H. Ichiki, K. Nakata, and S. Nakagawa (1991) Immunocytochemical localization of argininosuccinate synthetase in the rat brain. J. Comp. Neurol. 312:652-679.
37. O'Dell, T.J., R.D. Hawkins, E.R. Kandel, and O. Arancio (1991) Tests of the roles of two diffusible substances in long-term potentiation: Evidence for nitric oxide as a possible early retrograde messenger. Proc. Natl. Acad. Sci. USA 88:11285-11289.
38. Otake, K., and D.A. Ruggiero (1995) Monoamines and nitric oxide are employed by afferents engaged in midline thalamic regulation. J. Neurosci. 15:1891-1911.
39. Pape, H.-C., and R. Mager (1992) Nitric oxide controls oscillatory activity in thalamocortical neurons. Neuron 9:441-448.
40. Paxinos, G., and C. Watson (1986) The rat brain in stereotaxic coordinates. Sydney: Academic Press.
41. Paxinos, G., K.W.S. Ashwell, and I. Törk (1994) Atlas of the developing rat nervous system. San Diego: Academic Press.
42. Rivadulla, C., R. Rodriguez, S. Martinez-Conde, C. Acuña, and J. Cudeiro (1996) The influence of nitric oxide on perigeniculate GABAergic cell activity in the anaesthetized cat. Eur. J. Neurosci. 8:2459-2466.
43. Scherer-Singler, U., S.R. Vincent, H. Kimura, and E.G. McGeer (1983) Demonstration of a unique population of neurons with NADPH-diaphorase histochemistry. J. Neurosci. Methods 9:229-234.
44. Schilling, K., H.H.H.W. Schmidt, and S.L. Baader (1994) Nitric oxide synthase expression reveals compartments of cerebellar granule cells and suggests a role for mossy fibers in their development. Neuroscience 59:893-903.
45. Schmidt, H.H.H.W., and U. Walter (1994) NO at work. Cell 78:919-925.
46. Schmidt, H.H.H.W., G.D. Gagne, M. Nakane, J.S. Pollock, M.F. Miller, and F. Murad (1992) Mapping of neural nitric oxide synthase in the rat suggests frequent co-localization with NADPH diaphorase but not with soluble guanylyl cyclase, and novel paraneural functions for nitrinergic signal transduction. J. Histochem. Cytochem. 40:1439-1456.
47. Shibata, H. (1992) Topographic organization of subcortical projections to the anterior thalamic nuclei in the rat. J. Comp. Neurol. 323:117-127.
48. Sikes, R.W., and B.A. Vogt (1987) Afferent connections of anterior thalamus in rats: Sources and association with muscarinic acetylcholine receptors. J. Comp. Neurol. 256:538-551.
49. Skinner, R.D., C. Conrad, V. Henderson, S.A. Gilmore, and E. Garcia-Rill (1989) Development of NADPH diaphorase-positive pedunculopontine nucleus neurons. Exp. Neurol. 134:15-21.
50. Spreafico, R., C. Frassoni, P. Arcelli, G. Battaglia, R.J. Wenthold, and S. De Biasi (1994) Distribution of AMPA selective glutamate receptors in the thalamus of adult rats and during postnatal development. A light and ultrastructural immunocytochemical study. Dev. Brain Res. 82:231-244.
51. Spreafico, R., C. Frassoni, P. Arcelli, M. Selvaggio, and S. De Biasi (1995) In situ labeling of apoptotic cell death in the cerebral cortex and thalamus of rats during development. J. Comp. Neurol. 363:281-295.
52. Steriade, M., E.G. Jones, and R.R. Llinas (1990) Thalamic oscillations and signaling. New York: Wiley & Sons.
53. Thomas, E., and A.G.E. Pearse (1961) The fine localization of dehydrogenases in the nervous system. Histochemie 2:266-282.
54. Valtschanoff, J.G., R.J. Weinberg, V.N. Kharazia, H.H.H.W. Schmidt, M. Nakane, and A. Rustioni (1993) Neurons in the rat cerebral cortex that synthesize nitric oxide: NADPH diaphorase histochemistry, NOS immunocytochemistry, and colocalization with GABA. Neurosci. Lett. 157:157-161.
55. Vincent, S.R. (1994) Nitric oxide: A radical neurotransmitter in the central nervous system. Prog. Neurobiol. 42:129-160.
56. Vincent, S.R., and H. Kimura (1992) Histochemical mapping of nitric oxide synthase in the rat brain. Neuroscience 46:755-784.
57. Williams, C.V., D. Nordquist, and S.C. McLoon (1994) Correlation of nitric oxide synthase expression with changing patterns of axonal projections in the developing visual system. J. Neurosci. 14:1746-1755.
58. Williams, J.A., S.R. Vincent, and P.B. Reiner (1997) Nitric oxide production in rat thalamus changes with behavioral state, local depolarization, and brainstem stimulation. J. Neurosci. 17:420-427.
59. Wu, H.H., C.V. Williams, and S.C. McLoon (1994) Involvement of nitric oxide in the elimination of a transient retinotectal projection in development. Science 265:1593-1596.