Abstract
We described the distribution of NADPH-diaphorase-containing neurons in relation to tyrosine hydroxylase immunoreactivity in the diencephalon and mesencephalon of the chicken. In the diencephalon, both markers were found in the lateral hypothalamus, dorsal hypothalamic area, hypothalamic periventricular nucleus, paraventricular nucleus and mamillary area. A close examination showed that the fine distribution of these markers differed slightly, so that they were never observed in the same neurons. In the mesencephalon, NADPH-diaphorase and tyrosine hydroxylase immunoreactivity were found in the ventral pedunculopontine area (nucleus tegmenti pedunculopontinus pars compacta, adjacent areas surrounding the quintofrontal tract and the nucleus mesencephalicus profundus ventralis), the coeruleus complex (locus coeruleus, ventral and dorsal subcoeruleus nuclei), the ventral tegmental area and the central gray. The majority of these neurons contained either diaphorase or tyrosine hydroxylase. Nevertheless, in a few cases both markers appeared to colocalize in the same neuron, typically in large perikarya of the ventral pedunculopontine area.
Similar content being viewed by others
Abbreviations
- AVT :
-
Ventral tegmental area of Tsai
- DAB :
-
diaminobenzidine
- DHA :
-
dorsal hypothalamic area
- DMA :
-
anterior dorsomedial thalamic nucleus
- DMP :
-
posterior dorsomedial thalamic nucleus
- DSV :
-
ventral supraoptic decussation
- GCt :
-
central gray
- ICH :
-
intercalated hypothalamic nucleus
- IH :
-
inferior hypothalamic nucleus
- LHy :
-
lateral hypothalamic area
- LoC :
-
locus coeruleus
- ML :
-
lateral mamillary nucleus
- MM :
-
medial mamillary nucleus
- MPv :
-
ventral part of the deep mesencephalic nucleus
- nI :
-
interstitial nucleus of Rendahl
- NADPH-d :
-
NADPH-diaphorase
- NGS :
-
normal
References
Agulló L, Garcia A (1991) Norepinephrine increases cyclic GMP in astrocytes by a mechanism dependent on nitric oxide synthesis. Eur J Pharmacol 206: 343–346
Akil H, Liebeskind JC (1975) Monoaminergic mechanisms of stimulation-produced analgesia. Brain Res 94: 279–296
Artero C, Masucci A, Mazzi V, Barale E, Franzoni MF (1994) NADPH-diaphorase (and its relationships with NOS and some neuroactive molecules) in the brain of the crested newt. 17th Ann Meeting Eur Neurose Assoc Abs in Eur J Neurose [Suppl] 7: 23
Bailhache T, Balthazart J (1993) The catecholaminergic system of the quail brain: immunocytochemical studies of dopamine βhydroxylase and tyrosine hydroxylase. J Comp Neurol 329: 230–256
Bartheld CS von, Bothwell M (1992) Development and distribution of noradrenergic and cholinergic neurons and their trophic phenotypes in the avian ceruleus complex and midbrain tegmentum. J Comp Neurol 320: 479–500
Böhme GA, Bon C, Stutzmann JM, Doble A, Blanchard JC (1991) Possible involvement of nitric oxide in long-term potentiation. Eur J Pharmacol 199: 379–381
Bottjer SW (1993) The distribution of tyrosine hydroxylase immunoreactivity in the brains of male and female zebra finches. J Neurobiol 24: 51–69
Brauth S, Ferguson JL, Kitt CA (1978) Prosencephalic pathways related to the paleostriatum of the pigeon (Columba livia). Brain Res 147: 205–221
Bredt DS, Hwang PM, Snyder SH (1990) Localization of nitric oxide synthase indicating a neural role for nitric oxide. Nature 347: 768–770
Bredt DS, Glatt CE, Hwang PM, Fotuhi M, Dawson TM, Snyder SH (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
Brüning G (1993a) Localization of NADPH-diaphorase in the brain of the chicken. J Comp Neurol 334: 192–208
Brüning G (1993b) NADPH-diaphorase histochemistry in the postnatal mouse cerebellum suggests specific developmental functions for nitric oxide. J Neurosci Res 36: 580–587
Brüning G, Funk U, Mayer B (1994) Immunocytochemical localization of the nitric oxide synthase in the brain of the chicken. Neuroreport 5: 2425–2428
Cozzi B, Viglietti-Panzica C, Aste N, Panzica GC (1991) The serotoninergic system in the brain of the Japanese quail. An immunohistochemical study. Cell Tissue Res 263: 271–284
Dawson TM, Bredt DS, Fotuhi M, Hwang PM, Snyder SH (1991) Nitric oxide synthase and neuronal NADPH diaphorase are identical in brain and peripheral tissues. Proc Natl Acad Sci USA 88: 7797–7801
Dun NJ, Dun SL, Wu SY, Forstermann U, Schmidt HH, Tseng FF(1993) Nitric oxide synthase immunoreactivity in the rat, mouse, cat and squirrel monkey spinal cord. Neuroscience 54: 845–857
Garthwaite J, Charles SL, Chess-Williams R (1988) Endothelium derived relaxing factor release on activation of NMDA receptors suggests role as intercellular messenger in the brain. Nature 336: 385–388
Grozdanovic Z, Baumgarten HG, Brüning G (1992) Histochemistry of NADPH-diaphorase, a marker for neuronal nitric oxide synthase, in the peripheral autonomic nervous system of the mouse. Neuroscience 48: 225–235
Haglund L, Köhler C, Haaparanta T, Goldstein M, Gustafsson JA (1984) Presence of NADPH-cytochrome P-450 reductase in central catecholaminergic neurons. Nature 307: 259–262
Haley JE, Wilcox GL, Chapman PF (1992) The role of nitric oxide in hippocampal long-term potentiation. Neuron 8: 211–216
Hirunagi K, Hasegawa M, Vigh B, Vigh-Teichmann I (1992) Immunocytochemical demonstration of serotonin-immunoreactive cerebrospinal fluid-contacting neurons in the paraventricular organ of the pigeons and domestic chickens. Prog Brain Res 91: 327–330
Hope BT, Michael GJ, Knigge KM, Vincent SR (1991) Neuronal NADPH-diaphorase is a nitric oxide synthase. Proc Natl Acad Sci USA 88: 2811–2814
Iadecola C (1993) Regulation of the cerebral microcirculation during neural activity: is nitric oxide the missing link? Trends Neurosci 16: 206–214
Johnson MD, Ma PM (1993) Localization of NADPH diaphorase activity in monoaminergic neurons of the rat brain. J Comp Neurol 332: 391–406
Karten HJ, Dubbeldam JL (1973) The organization and projections of the paleostriatal complex in the pigeon (Columba livia). J Comp Neurol 148: 61–90
Kishimoto J, Keverne EB, Hardwick J, Emson PC (1993) Localization of nitric oxide synthase in the mouse olfactory and vomeronasal system: a histochemical, immunological and in situ hybridization study. Eur J Neurosci 5: 1684–1694
Kiss JZ, Péczely P (1987) Distribution of tyrosine hydroxylase (TH)-immunoreactive neurons in the diencephalon of the pigeon (Columba livia domestica). J Comp Neurol 257: 333–346
Kitt CA, Brauth SE (1986) Telencephalic projections from midbrain and isthmal cell groups in the pigeon. II. The nigral complex. J Comp Neurol 247: 92–110
Koyama Y, Kayama Y (1993) Mutual interactions among cholinergic, noradrenergic and serotoninergic neurons studied by ionophoresis of these transmitters in rat brainstem nuclei. Neuroscience 55: 1117–1126
Kuenzel WJ, Masson M (1988) A stereotaxic atlas of the brain of the chick (Gallus domesticus) The Johns Hopkins University Press, Baltimore London
Kuenzel WJ, Tienhoven A van (1982) Nomenclature and location of avian hypothalamic nuclei and associated circumventricular organs. J Comp Neurol 206: 293–313
Kuonen DR, Kemp MC, Roberts PJ (1988) Demonstration and biochemical characterisation of the rat brain NADPH-dependent diaphorase. J Neurochem 50: 1017–1025
Luebke JI, Weider JM, McCarley RW, Greene RW (1992) Distribution of NADPH-diaphorase positive somata in the brain stem of the monitor lizard Varanus exanthematicus. Neurosci Lett 148: 129–132
Matsumoto T, Nakane M, Pollock JS, Kuk JE, Forstermann U (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
Medina L, Reiner A (1994) Distribution of choline acetyltransferase immunoreactivity in the pigeon brain. J Comp Neurol 342: 497–537
Meek J, Joosten HW (1993) Tyrosine hydroxylase-immunoreactive cell groups in the brain of the teleost fish Gnathonemus petersii. J Chem Neuroanat 6: 431–446
Meek J, Joosten HW, Steinbush HW (1989) Distribution of dopamine immunoreactivity in the brain of the mormyrid teleost Gnathonemus petersii. J Comp Neurol 281: 362–383
Mizukawa K, McGeer PL, Vincent SR, McGeer EG (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
Moons L, Vangils J, Ghisels E, Vandesande F (1994) Immunocytochemical localization of L-DOPA and dopamine in the brain of the chicken (Gallus domesticus). J Comp Neurol 346: 97–118
Morgan IG, Miethke P, Li ZK (1994) Is nitric oxide a transmitter of the centrifugal projection to the avian retina? Neurosci Lett 168: 5–7
Moro MA, Michelena P, Sánchez-Garcia P, Palmer S, Garcia AG, Moncada S (1991) Nitric oxide in the adrenal medulla. 3rd IBRO World Congress of Neuroscience. Montreal Canada Abs P57-23
Moro MA, Michelena P, Sánchez-Garcia P, Palmer S, Moncada S, and Garcia AG (1993) Activation of adrenal medullary l-arginine: nitric oxide pathway by stimuli which induce the release of catecholamines. Eur J Pharmacol 246: 213–218
Ohta A, Takagi H, Matsui T, Hamai Y, Iida S, Esumi H (1993) Localization of nitric oxide synthase-immunoreactive neurons in the solitary nucleus and ventrolateral medulla oblongata of the rat: their relation to catecholaminergic neurons. Neurosci Lett 158: 33–35
O'Sullivan AJ, Burgoyne RD (1990) Cyclic GMP regulates nicotine-induced secretion from cultured bovine adrenal chromaffin cells: effects of 8-bromo-cyclic GMP, atrial natriuretic peptide, and nitroprusside (nitric oxide). J Neurochem 54: 1805–1808
Otake K, Ruggiero DA (1995) Monoamines and nitric oxide are employed by afferents engaged in midline thalamic regulation. J Neurosci 15: 1891–1911
Panzica GC, Arévalo R, Sánchez F, Alonso JR, Aste N, VigliettiPanzica C, Aijón J, Vázquez R (1994) Topographical distribution of reduced nicotinamide adenine dinucleotide phosphatediaphorase in the brain of the Japanese quail. J Comp Neurol 342: 97–114
Petko M, Ihionven M (1989) Distribution of Substance P, vasoactive intestinal polypeptide and serotonin immunoreactive structures in the central nervous system of the lizard Lacerta agilis. J Hirnforsch 30: 415–423
Pogun S, Baumann MH, Kuhar MJ (1994) Nitric oxide inhibits [3H]dopamine uptake. Brain Res 641: 83–91
Reiner A, Anderson KD (1990) The patterns of neurotransmitter and neuropeptide co-occurrence among striatal projection neurons: conclusions based on recent findings. Brain Res Rev 15: 251–265
Reiner A, Brauth SE, Karten HJ (1984) Evolution of the amniote basal ganglia. Trends Neurosci 7: 320–325
Schober A, Malz CR, Meyer DL (1993) Enzyme histochemical demonstration of nitric oxide synthase in the diencephalon of the rainbow trout (Oncorhynthus mickiss). Neurosci Lett 151: 67–70
Shibuki K, Okada D (1991) Endogenous nitric oxide release required for long-term synaptic depression in the cerebellum. Nature 349: 326–328
Sorenson EM, Parkinson P, Dahl JL, Chiappinelli VA (1989) Immunohistochemical localization of choline acetyltransferase in the chicken mesencephalon. J Comp Neurol 281: 641–657
Székely AD, Boxer MI, Stewart MG, Csillag A (1994) Connectivity of the lobus parolfactorius of the domestic chicken (Gallus domesticus): An anterograde and retrograde pathway tracing study. J Comp Neurol 348: 374–393
Terenghi G, Riveros-Moreno V, Hudson LD, Ibrahim NB, Polak JM (1993) Immunocytochemistry of nitric oxide synthase demonstrates immunoreactive neurons in spinal cord of the dorsal root ganglia of men and rat. J Neurol Sci 118: 34–37
Thatikunta P, Chakder S, Rattan S (1993) Nitric oxide synthase inhibitor inhibits catecholamines release caused by hypogastric sympathetic nerve stimulation. J Pharmacol Exp Ther 267: 1363–1368
Thomas E, Pearse AGE (1961) The fine localisation of dehydrogenase in the nervous system. Histochimie 2: 266–282
Tracey WR, Nakane M, Pollock JS, Forstermann U (1993) Nitric oxide synthases in neuronal cells, macrophages and endothelium are NADPH diaphorases, but represent only a fraction of total cellular NADPH diaphorase activity. Biochem Biophys Res Commun 195: 1035–1040
Vincent SR, Hope BT (1992) Neurons that say NO. Trends Neurosci 15: 108–113
Vincent SR, Kimura H (1992) Histochemical mapping of nitric oxide synthase in the rat brain. Neuroscience 46: 755–784
Wang ZZ, Bredt DS, Fidone SJ, Stensaas LJ (1993) Neurons synthesizing nitric oxide innervate the mammalian carotid body. J Comp Neurol 336: 419–432
Wetts R, Vaughn JE (1993) Transient expression of beta-NADPH diaphorase in developing rat dorsal root ganglia neurons. Brain Res Dev Brain Res 76: 278–282
Wiklund CU, Olgart C, Wiklund NP, Gustafsson LE (1993) Modulation of cholinergic and substance P-like neurotransmission by nitric oxide in the guinea-pig ileum. Br J Pharmacol 110: 833–839
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Montagnese, C.M., Csillag, A. Comparative distribution of NADPH-diaphorase activity and tyrosine hydroxylase immunoreactivity in the diencephalon and mesencephalon of the domestic chicken (Gallus domesticus). Anat Embryol 193, 427–439 (1996). https://doi.org/10.1007/BF00185874
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00185874