Morphological variability of NADPH diaphorase neurons across areas V1, V2, and V3 of the common agouti

Brain Research

Volumn 1318, Issue , 2010, Pages 52-63

  Freire, Marco Aurélio M ^a,b   Rocha, Emiliana G ^a   Oliveira, Jorge Luiz F ^a   Guimarães, Joanilson S ^a,c   Silveira, Luiz Carlos L ^a   Elston, Guy N ^d   Pereira, Antonio ^a,c   Picanço Diniz, Cristovam W ^a  

^a FEDERAL UNIVERSITY OF PARÁ   (Brazil)

^b POTIGUAR UNIVERSITY   (Brazil)

^c Edmond and Lily Safra International Institute of Neuroscience of Natal   (Brazil)

^d Centre for Cognitive Neuroscience   (Australia)

Author keywords

Area 17; Area 18; Extrastriate; Interneuron; Rodent; Striate

Indexed keywords

REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE DEHYDROGENASE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; CELL STRUCTURE; CONTROLLED STUDY; DIURNAL ANIMAL; MALE; MORPHOLOGICAL TRAIT; MORPHOMETRICS; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PYRAMIDAL NERVE CELL; RODENT; VISUAL CORTEX;

ANIMALS; CELL SIZE; CLUSTER ANALYSIS; DENDRITES; IMAGING, THREE-DIMENSIONAL; MALE; NADPH DEHYDROGENASE; NEURONS; PHOTOMICROGRAPHY; RODENTIA; VISUAL CORTEX;

AGOUTI; DASYPROCTA; HYSTRICOGNATHI; RODENTIA;

EID: 76449107362     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainres.2009.12.045     Document Type: Article

References (85)

1. Aoki C., Fenstemaker S., Lubin M., and Go C.G. Nitric oxide synthase in the visual cortex of monocular monkeys as revealed by light and electron microscopic immunocytochemistry. Brain Res. 620 (1993) 97-113
2. Barone P., and Kennedy H. Non-uniformity of neocortex: areal heterogeneity of NADPH-diaphorase reactive neurons in adult macaque monkeys. Cereb. Cortex 10 (2000) 160-174
3. Benavides-Piccione R., Hamzei-Sichani F., Ballesteros-Yanez I., DeFelipe J., and Yuste R. Dendritic size of pyramidal neurons differs among mouse cortical regions. Cereb. Cortex 16 (2006) 990-1001
4. Binzegger T., Douglas R.J., and Martin K.A. A quantitative map of the circuit of cat primary visual cortex. J. Neurosci. 24 (2004) 8441-8453
5. Calabrese V., Mancuso C., Calvani M., Rizzarelli E., Butterfield D.A., and Stella A.M. Nitric oxide in the central nervous system: neuroprotection versus neurotoxicity. Nat. Rev. Neurosci. 8 (2007) 766-775
6. Costa E.T., do-Nascimento J.L., Picanço-Diniz C.W., Quaresma J.A., and Silva-Filho M. Histochemical characterization of NADPH-diaphorase activity in area 17 of diurnal and nocturnal primates and rodents. Braz. J. Med. Biol. Res. 29 (1996) 1355-1362
7. Dawson T.M., Bredt D.S., Fotuhi M., Hwang P.M., and Snyder S.H. Nitric oxide synthase and neuronal NADPH diaphorase are identical in brain and peripheral tissues. Proc. Natl. Acad. Sci. U. S. A. 88 (1991) 7797-7801
8. DeFelipe J., and Farinas I. The pyramidal neuron of the cerebral cortex: morphological and chemical characteristics of the synaptic inputs. Prog. Neurobiol. 39 (1992) 563-607
9. DeFelipe J., Gonzalez-Albo M.C., Del Rio M.R., and Elston G.N. Distribution and patterns of connectivity of interneurons containing calbindin, calretinin, and parvalbumin in visual areas of the occipital and temporal lobes of the macaque monkey. J. Comp. Neurol. 412 (1999) 515-526
10. de Lima S.M., Ahnelt P.K., Carvalho T.O., Silveira J.S., Rocha F.A., Saito C.A., and Silveira L.C.L. Horizontal cells in the retina of a diurnal rodent, the agouti (Dasyprocta aguti). Vis. Neurosci. 22 (2005) 707-720
11. Douglas R.J., Martin K.A., and Whitteridge D. A canonical microcircuit for neocortex. Neural Comput. 1 (1989) 480-488
12. Elston G.N. Cortical heterogeneity: implications for visual processing and polysensory integration. J. Neurocytol. 31 (2002) 317-335
13. Elston G.N. Cortex, cognition and the cell: new insights into the pyramidal neuron and prefrontal function. Cereb. Cortex 13 (2003) 1124-1138
14. Elston G.N. Pyramidal cell heterogeneity in the visual cortex of the nocturnal New World owl monkey (Aotus trivirgatus). Neuroscience 117 (2003) 213-219
15. Elston G.N. Specializations in pyramidal cell structure during primate evolution. In: Kaas J.H., and Preuss T. (Eds). Evolution of Nervous Systems 4 (2007), Academic Press, Oxford 191-242
16. Elston G.N., and DeFelipe J. Spine distribution in neocortical pyramidal cells: a common organizational principle across species. In: Azmitia E.C., DeFelipe J., Jones E.G., Rakic P., and Ribak C.E. (Eds). Prog. Brain Res. 136 (2002), Elsevier 109-133
17. Elston G.N., and Rockland K.S. The pyramidal cell of the sensorimotor cortex of the macaque monkey: phenotypic variation. Cereb. Cortex 12 (2002) 1071-1078
18. Elston G.N., and Rosa M.G.P. Morphological variation of layer III pyramidal neurones in the occipitotemporal pathway of the macaque monkey visual cortex. Cereb. Cortex 8 (1998) 278-294
19. Elston G.N., and Rosa M.G.P. Ipsilateral corticocortical projections to the primary and middle temporal visual areas of the primate cerebral cortex: area-specific variations in the morphology of connectionally identified pyramidal cells. Eur. J. Neurosci. 23 (2006) 3337-3345
20. Elston G.N., Tweedale R., and Rosa M.G. Cellular heterogeneity in cerebral cortex: a study of the morphology of pyramidal neurones in visual areas of the marmoset monkey. J. Comp. Neurol. 415 (1999) 33-51
21. Elston G.N., Tweedale R., and Rosa M.G. Cortical integration in the visual system of the macaque monkey: large-scale morphological differences in the pyramidal neurons in the occipital, parietal and temporal lobes. Proc. Biol. Sci. 266 (1999) 1367-1374
22. Elston G.N., Benavides-Piccione R., Elston A., DeFelipe J., and Manger P. Pyramidal cell specialization in the occipitotemporal cortex of the Chacma baboon (Papio ursinus). Exp. Brain Res. 167 (2005) 496-503
23. Elston G.N., Benavides-Piccione R., Elston A., Manger P., and DeFelipe J. Pyramidal cell specialization in the occipitotemporal cortex of the vervet monkey (Cercopithecus pygerythrus). NeuroReport 16 (2005) 967-970
24. Elston G.N., Elston A., Casagrande V.A., and Kaas J. Areal specialization in pyramidal cell structure in the visual cortex of the tree shrew: a new twist revealed in the evolution of cortical circuitry. Exp. Brain Res. 163 (2005) 13-20
25. Elston G.N., Elston A., Freire M.A.M., Gomes-Leal W., Pereira Jr. A., Silveira L.C.L., and Picanço-Diniz C.W. Specialization of pyramidal cell structure in the visual areas V1, V2 and V3 of the South American rodent, Dasyprocta primnolopha. Brain Res. 1106 (2006) 99-110
26. Estrada C., and DeFelipe J. Nitric oxide-producing neurons in the neocortex: morphological and functional relationship with intraparenchymal microvasculature. Cereb. Cortex 8 (1998) 193-203
27. Franca J.G., do-Nascimento J.L., Picanço-Diniz C.W., Quaresma J.A., and Silva A.L. 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 (1997) 1093-1105
28. Franca J.G., Volchan E., Jain N., Catania K.C., Oliveira R.L., Hess F.F., Jablonka M., Rocha-Miranda C.E., and Kaas J.H. Distribution of NADPH-diaphorase cells in visual and somatosensory cortex in four mammalian species. Brain Res. 864 (2000) 163-175
29. Freire M.A.M., Gomes-Leal W., Carvalho W.A., Guimarães J.S., Franca J.G., Picanço-Diniz C.W., and Pereira Jr. A. A morphometric study of the progressive changes on NADPH diaphorase activity in the developing rat's barrel field. Neurosci. Res. 50 (2004) 55-66
30. Freire M.A.M., Franca J.G., Picanço-Diniz C.W., and Pereira Jr. A. Neuropil reactivity, distribution and morphology of NADPH diaphorase type I neurons in the barrel cortex of the adult mouse. J. Chem. Neuroanat. 30 (2005) 71-81
31. Freire M.A.M., Oliveira R.B., Picanço-Diniz C.W., and Pereira Jr. A. Differential effects of methylmercury intoxication in the rat's barrel field as evidenced by NADPH diaphorase histochemistry. Neurotoxicology 28 (2007) 175-181
32. Freire M.A.M., Tourinho S.C., Guimarães J.S., Oliveira J.L.F., Picanço-Diniz C.W., Gomes-Leal W., and Pereira Jr. A. Histochemical characterization, distribution and morphometric analysis of NADPH diaphorase neurons in the spinal cord of the agouti. Front. Neuroanat. 2 (2008) 2 10.3389/neuro.05.002.2008
33. Freire M.A.M., Guimarães J.S., Gomes-Leal W., and Pereira Jr. A. Pain modulation by nitric oxide in the spinal cord. Front. Neurosci. 3 (2009) 175-181
34. Gabbott P.L., Jays P.R., and Bacon S.J. Calretinin neurons in human medial prefrontal cortex (areas 24a,b,c, 32′, and 25). J. Comp. Neurol. 381 (1997) 389-410
35. Gomes F.L., Yamada E.S., and Silveira L.C.L. Morphology, size, and distribution of the alpha retinal ganglion cells of the agouti, Dasyprocta aguti. Invest. Ophthalmol. Vis. Sci. 39 (1998) S563
36. Gonchar Y., and Burkhalter A. Three distinct families of GABAergic neurons in rat visual cortex. Cereb. Cortex 7 (1997) 347-358
37. Gonzalez-Albo M.C., Elston G.N., and DeFelipe J. The human temporal cortex: characterization of neurons expressing nitric oxide synthase, neuropeptides and calcium binding proteins, and their glutamate receptor subunit profiles. Cereb. Cortex 11 (2001) 1170-1181
38. Guimarães J.S., Freire M.A.M., Lima R.R., Souza-Rodrigues R.D., Costa A.M., dos Santos C.D., Picanço-Diniz C.W., and Gomes-Leal W. Mechanisms of secondary degeneration in the central nervous system during acute neural disorders and white matter damage. Rev. Neurol. 48 (2009) 304-310
39. Hope B.T., Michael G.J., Knigge K.M., and Vincent S.R. Neuronal NADPH diaphorase is a nitric oxide synthase. Proc. Natl. Acad. Sci. U. S. A. 88 (1991) 2811-2814
40. Horton J.C., and Adams D.L. The cortical column: a structure without a function. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 360 (2005) 837-862
41. Jacobs B., and Scheibel A.B. Regional dendritic variation in primate cortical pyramidal cells. In: Schüz A., and Miller R. (Eds). Cortical Areas: Unity and Diversity (2002), Taylor and Francis, London 111-131
42. Jelinek H., Elston G.N., and Zietsch B. Fractal analysis: pitfalls and revelations in neuroscience. In: Losa G.A., et al. (Ed). Fractals in Biology and Medicine (2005), Birkhauser Verlag AG, Switzerland 85-94
43. Kaas J.H. From mice to men: the evolution of the large, complex human brain. J. Biosci. 30 (2005) 155-165
44. Krubitzer L. In search of a unifying theory of complex brain evolution. Ann. N.Y. Acad. Sci. 1156 (2009) 44-67
45. Larkman A.U. Dendritic morphology of pyramidal neurones in the visual cortex of the rat: I. Branching patterns. J. Comp. Neurol. 306 (1991) 307-319
46. Larkman A.U. Dendritic morphology of pyramidal neurones in the visual cortex of the rat: III. Spine distributions. J. Comp. Neurol. 306 (1991) 332-343
47. Lund J.S., Yoshioka T., and Levitt J.B. Comparison of intrinsic connectivity in different areas of macaque monkey cerebral cortex. Cereb. Cortex 3 (1993) 148-162
48. Luth H.J., Hedlich A., Hilbig H., Winkelmann E., and Mayer B. Morphological analyses of NADPH-diaphorase/nitric oxide synthase positive structures in human visual cortex. J. Neurocytol. 23 (1994) 770-782
49. Mainen Z.F., and Sejnowski T.J. Influence of dendritic structure on firing pattern in model neocortical neurons. Nature 382 (1996) 363-366
50. Malach R. Cortical columns as devices for maximizing neuronal diversity. Trends. Neurosci. 17 (1994) 101-104
51. Matsubara J.A., Chase R., and Thejomayen M. Comparative morphology of three types of projection-identified pyramidal neurons in the superficial layers of cat visual cortex. J. Comp. Neurol. 366 (1996) 93-108
52. Mel B. Why have dendrites? A computational perspective. In: Stuart G., Spruston N., and Häusser M. (Eds). Dendrites (1999), Oxford Univ. Press, New York 271-289
53. Mountcastle V.B. The columnar organization of the neocortex. Brain 120 Pt 4 (1997) 701-722
54. Nelson S. Cortical microcircuits: diverse or canonical?. Neuron 36 (2002) 19-27
55. Norris P.J., Faull R.L., and Emson P.C. Neuronal nitric oxide synthase (nNOS) mRNA expression and NADPH-diaphorase staining in the frontal cortex, visual cortex and hippocampus of control and Alzheimer's disease brains. Mol. Brain Res. 41 (1996) 36-49
56. Oswaldo-Cruz E., Picanço-Diniz C.W., and Silveira L.C.L. Physiological optics of some Amazon rodents with contrasting life style. J. Physiol. 367 (1985) 18P
57. Pereira A., Freire M.A.M., Bahia C.P., Franca J.G., and Picanço-Diniz C.W. The barrel field of the adult mouse SmI cortex as revealed by NADPH-diaphorase histochemistry. NeuroReport 11 (2000) 1889-1892
58. Picanço-Diniz C.W., Oliveira H.L., Silveira L.C.L., and Oswaldo-Cruz E. The visual cortex of the agouti (Dasyprocta aguti): architectonic subdivisions. Braz. J. Med. Biol. Res. 22 (1989) 121-138
59. Picanço-Diniz C.W., Silveira L.C.L., de Carvalho M.S., and Oswaldo-Cruz E. Contralateral visual field representation in area 17 of the cerebral cortex of the agouti: a comparison between the cortical magnification factor and retinal ganglion cell distribution. Neuroscience 44 (1991) 325-333
60. Picanço-Diniz C.W., Silveira L.C.L., and Oswaldo-Cruz E. A comparative survey of magnification factor in V1 and retinal ganglion cell topography of lateral-eyed mammals. In: Lent R. (Ed). The visual system from genesis to maturity (1992), Birkhauser, Boston, Massachusetts, USA 188-197
61. Poirazi P., and Mel B.W. Impact of active dendrites and structural plasticity on the memory capacity of neural tissue. Neuron 29 (2001) 779-796
62. Preuss T.M. What's human about the human brain. In: Gazzaniga M.S. (Ed). The New Cognitive Neurosciences (2000), MIT Press, Cambridge, MA 1219-1234
63. Rall W. Branching dendritic trees and motoneuron membrane resistivity. Exp. Neurol. 1 (1959) 491-527
64. Rall W. Cable theory for dendritic neurons. In: Koch C., and Segev I. (Eds). Methods in neuronal modeling: from synapses to networks (1989), MIT, Cambridge, MA 9-62
65. Rall W., Burke R.E., Holmes W.R., Jack J.J., Redman S.J., and Segev I. Matching dendritic neuron models to experimental data. Physiol. Rev. 72 (1992) S159-186
66. Rocha E.G., Santiago L.F., Freire M.A.M., Gomes-Leal W., Lent R., Houzel J.C., Franca J.G., Pereira Jr. A., and Picanço-Diniz C.W. Callosal axon arbors in the limb representations of the somatosensory cortex (SI) in the agouti (Dasyprocta primnolopha). J. Comp. Neurol. 500 (2007) 255-266
67. Rocha F.A., Ahnelt P.K., Peichl L., Saito C.A., Silveira L.C.L., and De Lima S.M. The topography of cone photoreceptors in the retina of a diurnal rodent, the agouti (Dasyprocta aguti). Vis. Neurosci. 26 (2009) 167-175
68. Rothnie P., Kabaso D., Hof P.R., Henry B.I., and Wearne S.L. Functionally relevant measures of spatial complexity in neuronal dendritic arbors. J. Theor. Biol. 238 (2006) 505-526
69. Sandell J.H. NADPH diaphorase histochemistry in the macaque striate cortex. J. Comp. Neurol. 251 (1986) 388-397
70. Santiago L.F., Rocha E.G., Freire M.A.M., Lent R., Houzel J.C., Picanço-Diniz C.W., Pereira Jr. A., and Franca J.G. The organizational variability of the rodent somatosensory cortex. Rev. Neurosci. 18 (2007) 283-294
71. Scherer-Singler U., Vincent S.R., Kimura H., and McGeer E.G. Demonstration of a unique population of neurons with NADPH-diaphorase histochemistry. J. Neurosci. Meth. 9 (1983) 229-234
72. Schweitzer L., and Renehan W.E. The use of cluster analysis for cell typing. Brain Res. Protoc. 1 (1997) 100-108
73. Segev I. Sound grounds for computing dendrites. Nature 393 (1998) 207-208
74. Silveira L.C.L., Picanço-Diniz C.W., and Oswaldo-Cruz E. Distribution and size of ganglion cells in the retinae of large Amazon rodents. Vis. Neurosci. 2 (1989) 221-235
75. Spruston N. Pyramidal neurons: dendritic structure and synaptic integration. Nat. Rev. Neurosci. 9 (2008) 206-221
76. Spruston N., Stuart G., and Häusser M. Dendritic integration. In: Stuart G., Spruston N., and Häusser M. (Eds). Dendrites (1999), Oxford Univ. Press, New York 231-270
77. Stepanyants A., Hof P.R., and Chklovskii D.B. Geometry and structural plasticity of synaptic connectivity. Neuron 34 (2002) 275-288
78. Stuart G., Spruston N., Sakmann B., and Hausser M. Action potential initiation and backpropagation in neurons of the mammalian CNS. Trends Neurosci. 20 (1997) 125-131
79. Szentagothai J. The "module-concept" in cerebral cortex architecture. Brain Res. 95 (1975) 475-496
80. Tao Z., Van Gool D., Lammens M., and Dom R. NADPH-diaphorase-containing neurons in cortex, subcortical white matter and neostriatum are selectively spared in Alzheimer's disease. Dement. Geriatr. Cogn. Disord. 10 (1999) 460-468
81. Thomas E., and Pearse A.G. The solitary active cells. Histochemical demonstration of damage-resistant nerve cells with a TPN-diaphorase reaction. Acta Neuropathol. (Berl) 27 (1964) 238-249
82. Vetter P., Roth A., and Hausser M. Propagation of action potentials in dendrites depends on dendritic morphology. J. Neurophysiol. 85 (2001) 926-937
83. Vincent S.R., and Kimura H. Histochemical mapping of nitric oxide synthase in the rat brain. Neuroscience 46 (1992) 755-784
84. Wong-Riley M., Anderson B., Liebl W., and Huang Z. Neurochemical organization of the macaque striate cortex: correlation of cytochrome oxidase with Na+K+ATPase, NADPH-diaphorase, nitric oxide synthase, and N-methyl-d-aspartate receptor subunit 1. Neuroscience. 83 (1998) 1025-1045
85. Yan X.X., and Garey L.J. Morphological diversity of nitric oxide synthesising neurons in mammalian cerebral cortex. J. Brain Res. 38 (1997) 165-172