Distribution and morphology of nitrergic neurons across functional domains of the rat primary somatosensory cortex

Frontiers in Neural Circuits

Volumn , Issue NOV, 2012, Pages

  Nogueira Campos, Anaelli A ^a,b   Finamore, Deborah M ^a   Imbiriba, Luis A ^a   Houzel, Jean C ^a   Franca, João G ^a  

^a FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

^b FEDERAL UNIVERSITY OF JUIZ DE FORA   (Brazil)

Author keywords

Barrel cortex; Dendritic morphometry; Inhibitory neurons; NADPH diaphorase; Nitric oxide; Rat cortical area S1

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL DENSITY; CELL STRUCTURE; CONTROLLED STUDY; COUPLING FACTOR; DENDRITE; DENDRITIC CELL; GABAERGIC TRANSMISSION; HISTOCHEMISTRY; HYPEREMIA; INTERNEURON; MALE; NERVE CELL PLASTICITY; NITRERGIC NERVE; NONHUMAN; PHENOTYPE; PRIMARY SOMATOSENSORY CORTEX; PROTEIN DOMAIN; PROTEIN FUNCTION; RAT; SIGNAL TRANSDUCTION; STEREOLOGY; SYNAPTIC TRANSMISSION; WHITE MATTER;

EID: 84871390390     PISSN: 16625110     EISSN: None     Source Type: Journal    
DOI: 10.3389/fncir.2012.00057     Document Type: Article

References (71)

1. Abercrombie, M. (1946). Estimation of nuclear population from microtome sections. Anat. Rec. 94, 239-247.
2. Aoki, C., Fenstemaker, S., Lubin, M., and Go, C.-G. (1993). Nitric oxide synthase in the visual cortex of monocular monkeys as revealed by light and electron microscopic immunocytochemistry. Brain Res. 620, 97-113.
3. Beijamini, V., and Guimaraes, F. S. (2006). Activation of neurons containing the enzyme nitric oxide synthase following exposure to an elevated plus maze. Brain Res. Bull. 69, 347-355.
4. Bohme, G. A., Bon, C., Stutzmann, J. M., Doble, A., and Blanchard, J. C. (1991). Possible involvement of nitric oxide in long-term potentiation. Eur. J. Pharmacol. 199, 379-381.
5. Bredt, D. S., Glatt, C. E., Hwang, P. M., Fotuhi, M., Dawson, T. M., and Snyder, S. H. (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.
6. Bredt, D. S., Huang, P. M., and Snyder, S. H. (1990). Localization of nitric oxide sythase indicating a neural role for nitric oxide. Nature 347, 768-770.
7. Bredt, D. S., and Snyder, S. H. (1992). Nitric oxide, a novel neuronal messenger. Neuron 8, 3-11.
8. Calabrese, V., Mancuso, C., Calvani, M., Rizzarelli, E., Butterfield, D. A., and Stella, A. M. (2007). Nitric oxide in the central nervous system: neuroprotection versus neurotoxicity. Nat. Rev. Neurosci. 8, 766-775.
9. Catania, K. C. (2002). Barrels, stripes, and fingerprints in the brain - implications for theories of cortical organization. J. Neurocytol. 31, 347-358.
10. Cauli, B., and Hamel, E. (2010). Revisiting the role of neurons in neurovascular coupling. Front. Neuroenerg. 2:9. doi: 10.3389/fnene.2010.00009
11. Cauli, B., Tong, X. K., Rancillac, A., Serluca, N., Lambolez, B., Rossier, J., et al. (2004). Cortical GABA interneurons in neurovascular coupling: relays for subcortical vasoactive pathways. J. Neurosci. 24, 8940-8949.
12. Chen, B., So, K. F., Yu, E., and Tay, D. K. Expression of nicotinamide adenine dinucleotide phosphate- diaphorase in the retina of postnatal golden hamsters deprived of light stimulation. Neurosci. Lett. 405, 74-78.
13. Cruz-Rizzolo, R. J., Horta-Junior, J. A., Bittencourt, J. C., Ervolino, E., de Oliveira, J. A., and Casatti, C. A. (2006). Distribution of NADPH-diaphorase-positive neurons in the prefrontal cortex of the Cebus monkey. Brain Res. 1083, 118-133.
14. Dawson, T. M., Bredt, D. S., Fotuhi, M., Hwang, P. M., and Snyder, S. H. (1991). Nitric oxide synthase and neuronal NADPH diaphorase are identical in brain and peripheral tissues. Proc. Natl. Acad. Sci. U.S.A. 88, 7797-7801.
15. Dawson, T. M., and Snyder, S. H., Gases as biological messengers: nitric oxide and carbon monoxide in the brain. J. Neurosci. 14, 5147-5159.
16. Douglas, R. J., and Martin, K. A. (2004). Neuronal circuits of the neocortex. Annu. Rev. Neurosci. 27, 419-451.
17. Drake, C. T., and Iadecola, C. (2007). The role of neuronal signaling in controlling cerebral blood flow. Brain Lang. 102, 141-152.
18. Estevez, A. G., Spear, N., Manuel, S. M., Radi, R., Henderson, C., Barbeito, L., et al. (1998). Nitric oxide and superoxide contribute to motor neuron apoptosis induced by trophic factor deprivation. J. Neurosci. 18, 923-931.
19. Estrada, C., and DeFelipe, J. (1998). Nitric oxide-neurons in the neocortex: morphological and functional relationship with intraparechymal microvasculature. Cereb. Cortex 8, 193-203.
20. Franca, J. G., do-Nascimento, J. L. M., Picanço-Diniz, C. W., Quaresma, J. A. S., and Silva, A. L. C. (1997). NADPH-diaphorase activity in area 17 of the squirrel monkey visual cortex: neuropil pattern, cell morphology and laminar distribution. Braz. J. Med. Biol. Res. 30, 1093-1105.
21. Franca, J. G., and Volchan, E. (1995). NADPH diaphorase histochemistry as a marker for barrels in rat somatosensory cortex. Braz. J. Med. Biol. Res. 28, 787-790.
22. Franca, J. G., Volchan, E., Jain, N., Catania, K. C., Oliveira, R. L. S., Hess, F. F., et al. (2000). Distribution of NADPH-diaphorase cells in visual and somatosensory cortex in four mammalian species. Brain Res. 864, 163-175.
23. Freire, M. A., Faber, J., Picanco-Diniz, C. W., Franca, J. G., and Pereira, A. (2012). Morphometric variability of nicotinamide adenine dinucleotide phosphate diaphorase neurons in the primary sensory areas of the rat. Neuroscience 205, 140-153.
24. Freire, M. A., Franca, J. G., Picanco- Diniz, C. W., and Pereira, A. Jr. (2005). Neuropil reactivity, distribution and morphology of NADPH diaphorase type I neurons in the barrel cortex of the adult mouse. J. Chem. Neuroanat. 30, 71-81.
25. Freire, M. A., Gomes-Leal, W., Carvalho, W. A., Guimaraes, J. S., Franca, J. G., Picanco-Diniz, C. W., et al. (2004). A morphometric study of the progressive changes on NADPH diaphorase activity in the developing rat's barrel field. Neurosci. Res. 50, 55-66.
26. Gabbott, P. L. A., and Bacon, S. J. (1995). Co-localisation of NADPH diaphorase activity and GABA immunoreactivity in local circuit neurones in the medial prefrontal cortex (mPFC) of the rat. Brain Res. 699, 321-328.
27. Garthwaite, J. (2008). Concepts of neural nitric oxide-mediated transmission. Eur. J. Neurosci. 27,2783-2802.
28. Garthwaite, J., and Boulton, C. L., Nitric oxide signaling in the central nervous system. Ann. Rev. Neurosci. 57, 683-706.
29. Gundersen, H. J., Bendtsen, T. F., Korbo, L., Marcussen, N., Moller, A., Nielsen, K., et al. (1988). Some new, simple and efficient stereo- logical methods and their use in pathological research and diagnosis. APMIS 96, 379-394.
30. Hilbig, H., and Punkt, K. (1997). 24-hour rhythmicity of NADPH- diaphorase activity in the neuropil of rat visual cortex. Brain Res. Bull. 43, 337-340.
31. Hope, B. T., Michael, G. J., Knigge, K. M., and Vincent, S. R. (1991). Neuronal NADPH diaphorase is a nitric oxide synthase. Proc. Natl. Acad. Sci. U.S.A. 88, 2811-2814.
32. Horton, J. C., and Adams, D. L. (2005). The cortical column: a structure without a function. Philos. Trans. R. Soc. Lond B Biol. Sci. 360, 837-862.
33. Hubener, M., and Bolz, J. (1992). Relationships between dendritic morphology and cytochrome oxidase compartments in monkey striate cortex. J. Comp. Neurol. 324, 67-80.
34. Iadecola, C. (1993). Regulation of the cerebral microcirculation during neural activity: is nitric oxide the missing link? Trends Neurosci. 16, 206-214.
35. Iwase, K., Takemura, M., Shimada, T., Wakisawa, S., Nobuki, T., and Shigenaga, Y. (1998). Ontogeny of NADPH-diaphorase in rat forebrain and midbrain. Anat. Embryol. 197, 229-247.
36. Izumi, Y., Clifford, D. B., and Zorumski, C. F. (1992). Inhibition of long-term potentiation by NMDA-mediated nitric oxide release. Science 257, 1273-1276.
37. Kubota, Y., Shigematsu, N., Karube, F., Sekigawa, A., Kato, S., Yamaguchi, N., et al. (2011). Selective coexpression of multiple chemical markers defines discrete populations of neocortical GABAergic neurons. Cereb. Cortex 21, 1803-1817.
38. Lubke, J., and Feldmeyer, D. (2007). Excitatory signal flow and connectivity in a cortical column: focus on barrel cortex. Brain Struct. Funct. 212, 3-17.
39. Lüth, H.-J., Hedlich, A., Heidegard, H., Winkelmann, E., and Mayer, B. (1994). Morphological analyses of NADPH-diaphorase/nitric oxide synthase positive structures in human visual cortex. J. Neurocytol. 23, 770-782.
40. Malach, R. (1992). Dendritic sampling across processing streams in monkey striate cortex. J. Comp. Neurol. 315, 303-312.
41. Malinski, T., Taha, Z., Grunfeld, S., Patton, S., Kapturczak, M., and Tomboulian, P. (1993). Diffusion of nitric oxide in the aorta wall monitored in situ by porphyrinic microsensors. Biochem. Biophys. Res. Commun. 193, 1076-1082.
42. Matsumoto, T., Nakane, M., Pollock, J. S., Kuk, J. E., and 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.
43. Meulemans, A. (1994). Diffusion coefficients and half-lives of nitric oxide and N-nitroso-L-arginine in rat cortex. Neurosci. Lett. 171, 89-93.
44. Mountcastle, V. B. (1997). The columnar organization of the neocortex. Brain 120, 701-722.
45. Pereira, A. Jr., Freire, M. A., Bahia, C. P., Franca, J. G., and Picanco-Diniz, W. (2000). The barrel field of the adult mouse SmI cortex as revealed by NADPH-diaphorase histochemistry. Neuroreport 11, 1889-1892.
46. Petersen, C. C. (2007). The functional organization of the barrel cortex. Neuron 56, 339-355.
47. Rice, F. L. (1995). Comparative aspects of barrel structure and development, in The Barrel Cortex of Rodents, eds E. G. Jones and I. T. Diamond (New York, NY: Plenum Publishing Corporation), 1-75.
48. Riddle, D. R., Gutierrez, G., Zheng, White, L.E., Richards, A., and Purves, D. (1993). Differential metabolic and electrical activity in the somatic sensory cortex of juvenile and adult rats. J. Neurosci. 13, 4193-4213.
49. Rocha, E. G., Freire, M. A. M., Bahia, C. P., Pereira, A., Sossthenes, M. C. K., Silveira, L. C. L., et al. (2012). Dendritic structure varies as a function of eccentricity in V1, a quantitative study of NAPDH diaphorase neurons in the diurnal south american roden Agouti, Dasyprocta prymnolopha. Neuroscience 216, 94-102.
50. Rockland, K. S. (2010). Five points on columns. Front. Neuroanat. 4:22. doi: 10.3389/fnana.2010.00022
51. Romanelli, P., Di Matteo, L., Cobellis, G., Varriale, B., Menegazzi, M., Gironi Carnevale, U. A., et al. Transcription factor expression, RNA synthesis and NADPH- diaphorase across the rat brain and exposure to spatial novelty. Behav. Brain Res. 184, 91-100.
52. Sandell, J. H. (1986). NADPH diaphorase histochemistry in the macaque striate cortex. J. Comp. Neurol. 251, 388-397.
53. Santiago, L. F., Rocha, E. G., Freire, M. A., Dias, I. A., Lent, R., Houzel, J. C., et al. (2007). The organizational variability of the rodent somatosensory cortex. Rev. Neurosci. 18, 283-294.
54. Scherer-Singler, U., Vincent, S. R., Kimura, H., and McGeer, E. G. (1983). Demonstration of a unique population of neurons with NADPH-diaphorase histochemistry. J. Neurosci. Meth. 9, 229-234.
55. Schubert, D., Kotter, R., and Staiger, J. (2007). Mapping functional connectivity in barrel-related columns reveals layer- and cell type-specific microcircuits. Brain Struct. Funct. 212, 107-119.
56. Schuz, A., and Palm, G. (1989). Density of neurons and synapses in the cerebral cortex of the mouse. J. Comp. Neurol. 286, 442-455.
57. Swindale, N. V. (1990). Is the cerebral cortex modular? Trends Neurosci. 13, 487-492.
58. Tenorio, F., Giraldi-Guimaraes, A., Santos, H. R., Cintra, W. M., and Mendez-Otero, R. (1998). Eye enucleation alters intracellular distribution of NO synthase in the superior colliculus. Neuroreport 9, 145-148.
59. Torres, J. B., Assuncao, J., Farias, J. A., Kahwage, R., Lins, N., Passos, A., et al. (2006). NADPH-diaphorase histochemical changes in the hippocampus, cerebellum and striatum are correlated with different modalities of exercise and water- maze performances. Exp. Brain Res. 175, 292-304.
60. Valtschanoff, J. G., Weinberg, R. J., Kharazia, V. N., Schmidt, H. H., Nakane, M., and Rustioni, A. (1993). Neurons in rat cerebral cortex that synthesize nitric oxide: NADPH diaphorase histochemistry, NOS immunocytochemistry, and colocalization with GABA. Neurosci. Lett. 157, 157-161.
61. Vincent, S. R., and Kimura, H. (1992). Histochemical mapping of nitric oxide synthase in the rat brain. Neuroscience 46, 755-784.
62. Wallace, M. N. (1987). Histochemical demonstration of sensory maps in the rat and mouse cerebral cortex. Brain Res. 418, 178-182.
63. Wallace, M. N., Tayebjee, M. H., Rana, F. S., Farquhar, D. A., and Nyong'o, A. O. (1996). Pyramidal neurones in pathological human motor cortex express nitric oxide synthase. Neurosci. Lett. 212, 187-190.
64. Wässle, H., and Boycott, B. B. (1991). Functional architecture of the mammalian retina. Physiol. Rev. 71, 447-480.
65. Wester, J. C., and Contreras, D. (2012). Columnar interactions determine horizontal propagation of recurrent network activity in neocortex. J. Neurosci. 32, 5454-5471.
66. Wong-Riley, M. T. T., Anderson, B., Liebl, W., and Huang, Z. (1998). Neurochemical organization of the macaque striate cortex: correlation of cytochrome oxidase with Na+K+ ATPase, NAD PH - diaphorase, nitric oxide synthase, and N-methyl-D-aspartate receptor subunit 1. Neuroscience 83, 1025-1045.
67. Wong-Riley, M. T. T., and Welt, C. (1980). Histochemical changes in cytochrome oxidase of cortical barrels after vibrissal removal in neonatal and adult mice. Proc. Natl. Acad. Sci. U.S.A. 77, 2333-2337.
68. Wood, J., and Garthwaite, J. (1994). Models of the diffusional spread of nitric oxide: implications for neural nitric oxide signalling and its pharmacological properties. Neuropharmacology 33, 1235-1244.
69. Woolsey, T. A., and Van der Loos, H. (1970). The structural organization of layer IV in the somatosensory region (S1) of mouse cerebral cortex. The description of a cortical field composed of discrete cytoar- chitectonic units. Brain Res. 17, 205-242.
70. Yan, X. X., and Garey, L. J. (1997). Morphological diversity of nitric oxide synthesising neurons in mammalian cerebral cortex. J. Hirnforsch. 38, 165-172.
71. Zilles, K., andWree, A. (1985). "Cortex: areal and laminar structure," in Forebrain and Midbrain, ed G. Paxinos (Sydney, Orlando, San Diego, New York: Academic Press, Harcourt Brace Janovich), 375-415