Nitric oxide as a regulatory molecule in the processing of the visual stimulus

Nitric Oxide - Biology and Chemistry

Volumn 36, Issue , 2014, Pages 44-50

  Lima, Monica Gomes ^a   Maximino, Caio ^a,b   Matos Oliveira, Karen Renata ^a   Brasil, Alódia ^a   Crespo Lopez, Maria Elena ^a   Batista, Evander De Jesus Oliveira ^a   Rocha, Fernando Allan De Farias ^a   Picanço Diniz, Domingos Luiz Wanderley ^c   Herculano, Anderson Manoel ^a,b  

^a FEDERAL UNIVERSITY OF PARÁ   (Brazil)

^b The International Zebrafish Neuroscience Research Consortium (ZNRC)   (United States)

^c UNIVERSIDADE FEDERAL DO OESTE DO PARÁ   (Brazil)

Author keywords

Lateral geniculate nucleus; Nitric oxide; Primary visual cortex; Retina; Visual processing; Visual system

Indexed keywords

CYCLIC GMP; NITRIC OXIDE;

BRAIN STEM; HUMAN; LATERAL GENICULATE BODY; NONHUMAN; PRIORITY JOURNAL; RETINA; REVIEW; SIGNAL DETECTION; SIGNAL TRANSDUCTION; STRIATE CORTEX; THALAMUS; VISUAL CORTEX; VISUAL STIMULATION; VISUAL SYSTEM;

LATERAL GENICULATE NUCLEUS; NITRIC OXIDE; PRIMARY VISUAL CORTEX; RETINA; VISUAL PROCESSING; VISUAL SYSTEM;

ALPHA-AMINO-3-HYDROXY-5-METHYL-4-ISOXAZOLEPROPIONIC ACID; ANIMALS; CYCLIC GMP; GENE EXPRESSION REGULATION; GENICULATE BODIES; GLUTAMINE; HUMANS; N-METHYLASPARTATE; NEURONS; NITRIC OXIDE; RETINA; RETINAL GANGLION CELLS; SIGNAL TRANSDUCTION; VISION, OCULAR; VISUAL CORTEX;

EID: 84890817061     PISSN: 10898603     EISSN: 10898611     Source Type: Journal    
DOI: 10.1016/j.niox.2013.10.011     Document Type: Review

References (103)

1. S. Coren Sensation and perception D.K. Freedhein, L.B. Weiner, Handbook of Psychology and Perception 2003 John Wiley & Sons New Jersey 85 108
2. M.E. Levine Fundamentals of Sensation and Perception 2000 Oxford University Press Oxford
3. H. Wässle Parallel processing in the mammalian retina Nat. Rev. Neurosci. 5 2004 747 757 (Pubitemid 39336212)
4. S.G. Solomon, and P. Lennie The machinery of color vision Nat. Neurosci. 8 2007 276 286
5. L.M. Chalupa, and J.S. Werner The Visual Neurosciences 2004 Massachusetts Institute of Technology Massachusetts
6. M.J. Tovée An Introduction to the Visual System 2008 Cambridge University Press New York 240
7. A. Contestabile Roles of NMDA receptor activity and nitric oxide production in brain development Brain Res. Rev. 32 2000 476 509 (Pubitemid 30171317)
8. W.D. Eldred, and A.B. Blute Imaging of nitric in the retina Vision. Res. 45 2005 3469 3486
9. P. Kara, and M.J. Friendlander Arginine analogs modify signal detection by neurons in the visual cortex J. Neurosci. 19 1999 5528 5548 (Pubitemid 29300217)
10. J. Cudeiro, and C. Rivadulla Sight and insight - on the physiological role of nitric oxide in the visual system Trends Neurosci. 22 1999 109 116 (Pubitemid 29151803)
11. J. Cudeiro, C. Rivadulla, R. Rodriguez, K.L. Grieve, S. Martinez-Conde, and C. Acuña Actions of compounds manipulating the nitric oxide system in the cat primary visual cortex J. Physiol. 504 1997 467 478 (Pubitemid 27478420)
12. T. Akira, D. Henry, R.A. Baldwin, and C.G. Wasterlain Nitric oxide participates in excitotoxic mechanisms induced by chemical hypoxia Brain Res. 645 1994 285 290 (Pubitemid 24140135)
13. G.-Y. Wang, L.C. Liets, and L.M. Chalupa Nitric oxide differentially modulates ON and OFF responses of retinal ganglion cells J. Neurophysiol. 90 2003 1304 1313 (Pubitemid 37092607)
14. B.W. Allen, I.T. Demchenko, and C.A. Piantadosi Two faces of nitric oxide: implications for cellular mechanisms of oxygen toxicity J. Appl. Physiol. 106 2009 662 667
15. Z.-H. Pan, M.M. Segal, and S.A. Lipton Nitric oxide-related species inhibit evoked neurotransmission but enhance spontaneous miniature synaptic currents in central neuronal cultures Proc. Natl. Acad. Sci. USA 93 1996 15423 15428 (Pubitemid 27010329)
16. S.Z. Lei, Z.-H. Pan, S.K. Aggarwal, H.-S.V. Chen, J. Hartman, N.J. Sucher, and S.A. Lipton Effect of nitric oxide production on the redox modulatory site of the NMDA receptor-channel complex Neuron 8 1992 1087 1099
17. S.A. Lipton, Y.-B. Choi, Z.-H. Pan, S.Z. Lei, H.-S.V. Chen, N.J. Sucher, J. Loscalzo, D.J. Singel, and J.S. Stamler A redox-based mechanism for the neuroprotective and neurodestructive effects of nitric oxide and related nitroso-compounds Nature 364 1993 626 632 (Pubitemid 23274719)
18. D.S. Bredt, P.M. Hwang, and S.H. Snyder Localization of nitric oxide synthase indicating a neural role for nitric oxide Nature 347 1990 768 770
19. O. Goureau, M. Lepoivre, F. Becquet, and Y. Courtois Differential regulation of inducible nitric oxide synthase by fibroblast growth factors and transforming growth factor beta in bovine retinal pigmented epithelial cells: inverse correlation with cellular proliferation Proc. Natl. Acad. Sci. USA 90 1993 4276 4280 (Pubitemid 23134209)
20. R. Yamamoto, D.S. Bredt, and S.H. Synder The localization of nitric oxide synthase in the rat eye and related cranial ganglia Neuroscience 54 1993 189 200 (Pubitemid 23147098)
21. T.M. Dawson, D.S. Bredt, M. Fotuhi, P.M. Hwang, and S.H. Synder Nitric oxide synthase and neuronal NADPH diaphorase are identical in brain and peripheral tissues Proc. Natl. Acad. USA 88 1991 7797 7801 (Pubitemid 21915241)
22. E.W. Cheon, C.H. Park, S.S. Kang, G.J. Cho, J.M. Yoo, J.K. Song, and W.S. Choi Nitric oxide synthase expression in the transient ischemic rat retina: neuroprotection of betaxolol Neurosci. Lett. 330 2002 265 269 (Pubitemid 35254050)
23. A.H. Neufeld, S. Shareef, and J. Pena Cellular localization of neuronal nitric oxide synthase (NOS-1) in the human and rat retina J. Comp. Neurol. 416 2000 269 275
24. I. Ahmad, and C.J. Barnstable Differential laminar expression of particulate and soluble guanylate cyclase genes in rat retina Exp. Eye Res. 56 1993 51 62 (Pubitemid 23042775)
25. A. Savchenko, S. Barnes, and R.H. Kramer Cyclic-nucleotide-gated channels mediate synaptic feedback by nitric oxide Nature 390 1997 694 698 (Pubitemid 28016358)
26. B.A. Liepe, C. Stone, J. Koistinaho, and D.R. Copenhagen Nitric oxide synthase in muller cells and neurons of salamander and fish retina J. Neurosci. 14 1994 7641 7654
27. F. Rieke, and E.A. Schwartz A cGMP-gated current can control exocytosis at cone synapses Neuron 13 1994 863 873 (Pubitemid 24347299)
28. M. Sato, and T. Ohtsuka Opposite effects of nitric oxide on rod and cone photoreceptors of rat retina in situ Neurosci. Lett. 473 2010 62 66
29. M. Sato, T. Ohtsuka, and W.K. Stell Endogenous nitric oxide enhances the light-response of cones during light-adaptation in the rat retina Vision. Res. 51 2011 131 137
30. T.J. Giove, M.M. Deshpande, and W.D. Eldred Identification of alternate transcripts of neuronal nitric oxide synthase in the mouse retina J. Neurosci. Res. 87 2009 3134 3142
31. M.H. Chun, S.J. Oh, I.B. Kim, and K.Y. Kim Light and electron microscopical analysis of nitric oxide synthase-like immunoreactive neurons in the rat retina Vis. Neurosci. 16 1999 379 389
32. I.B. Kim, E.J. Lee, K.Y. Kim, W.K. Ju, S.J. Oh, C. Joo, and M.H. Chun Immunocytochemical localization of nitric oxide synthase in the mammalian retina Neurosci. Lett. 267 1999 193 196 (Pubitemid 29254094)
33. 2+/calmodulin-dependent nitric oxide synthase and a soluble guanylyl cyclase in vertebrate photoreceptor cells EMBO J. 13 1994 3312 3320
34. C.M. Venturini, R.G. Knowles, R.M. Palmer, and S. Moncada Synthesis of nitric oxide in the bovine retina Biochem. Biophys. Res. Commun. 180 1991 920 925
35. D.H. Shin, H.Y. Lee, H. Kim, E. Lee, K.H. Lee, W.J. Lee, S.S. Cho, and S.H. Baik In situ localization of neuronal nitric oxide synthase (nNOS) mRNA in the rat retina Neurosci. Lett. 270 1999 53 55 (Pubitemid 29322996)
36. M. Zoche, and K.W. Koch Purified retinal nitric oxide synthase enhances ADP-ribosylation of rod outer segment proteins FEBS Lett. 357 1995 178 182
37. T.A. Blute, B. Mayer, and W.D. Eldred Immunocytochemical and histochemical localization of nitric oxide synthase in the turtle retina Vis. Neurosci. 14 1997 717 729 (Pubitemid 27416002)
38. S.H. Haverkamp, and W.D. Eldred Localization of nNOS in photoreceptor, bipolar and horizontal cells in turtle and rat retinas Neuroreport 9 1998 2231 2235 (Pubitemid 28338211)
39. T.A. Blute, M.R. Lee, and W.D. Eldred Direct imaging of NMDA-stimulated nitric oxide production in the retina Vis. Neurosci. 17 2000 557 566
40. S.H. DeVries, and E.A. Schwartz Modulation of an electrical synapse between solitary pairs of catfish horizontal cells by dopamine and second messengers J. Physiol. 414 1989 351 375 (Pubitemid 19177307)
41. E.I. Miyachi, M. Murakami, and T. Nakaki Arginine blocks gap junctions between retinal horizontal cells Neuroreport 1 1990 107 110
42. D. Xin, and S.A. Bloomfield Effects of nitric oxide on horizontal cells in the rabbit retina Vis. Neurosci. 17 2000 799 811 (Pubitemid 32046114)
43. D.G. McMahon, and L.V. Ponomareva Nitric oxide and cGMP modulate retinal glutamate receptors J. Neurophysiol. 76 1996 2307 2315 (Pubitemid 26346407)
44. D. Yu, and W.D. Eldred GABAA and GABAC receptor antagonists increase retinal cyclic GMP levels through nitric oxide synthase J. Comp. Neurol. 483 2003 278 291
45. D. Yu, and W.D. Eldred Nitric oxide stimulates GABA release and inhibits glycine release in retina J. Comp. Neurol. 483 2005 278 291 (Pubitemid 40194422)
46. H. Levy, G. Twig, and I. Perlman Nitric oxide modulates the transfer function between cones and horizontal cells during changing conditions of ambient illumination Eur. J. Neurosci. 20 2004 2963 2974 (Pubitemid 40007290)
47. W.H. Baldridge, and A.J. Fischer Nitric oxide donor stimulated increase of cyclic GMP in the goldfish retina Vis. Neurosci. 18 2001 849 856 (Pubitemid 34507039)
48. B.L. Andrade da Costa, F.G. deMello, and J.N. Hokoc Comparative study of glutamate mediated gamma-aminobutyric acid release from nitric oxide synthase and tyrosine hydroxylase immunoreactive cells of the Cebus apella retina Neurosci. Lett. 302 2001 21 24 (Pubitemid 32244187)
49. R. Yamamoto, D.S. Bredt, T.M. Dawson, S.H. Snyder, and R.A. Stone Enhanced expression of nitric oxide synthase by rat retina following pterygopalatine parasympathetic denervation Brain Res. 631 1993 83 88 (Pubitemid 23351490)
50. J.D. Ding, and R.J. Weinberg Distribution of soluble guanylyl cyclase in rat retina J. Comp. Neurol. 502 2007 734 745 (Pubitemid 46067786)
51. S. Nawy, and C.E. Jahr Suppression by glutamate of cGMP-activated conductance in retinal bipolar cells Nature 346 1990
52. S. Nawy, and C.E. Jahr CGMP-gated conductance in retinal bipolar cells is suppressed by the photoreceptor transmitter Neuron 7 1991 677 683
53. J. Snellman, and S. Nawy CGMP-dependent kinase regulates response sensitivity of the mouse on bipolar cell J. Neurosci. 24 2004 6621 6628 (Pubitemid 38971710)
54. S.L. Mills, and S.C. Massey Differential properties of two gap junctional pathways made by AII amacrine cells Nature 377 1995 734 737
55. R. Shiells, and G. Falk Induction of nitric oxide synthase in glial cells J. Neurochem. 59 1992 897 905
56. G. Donati, C.J. Pournaras, J.L. Munoz, S. Poitry, C.L. Poitry-Yamate, and M. Tsacopoulos Nitric oxide controls arteriolar tone in the retina of the miniature pig Invest. Ophthalmol. Vis. Sci. 36 1995 2228 2237
57. M. Neal, J. Cunningham, and K. Matthews Selective release of nitric oxide from retinal amacrine and bipolar cells Invest. Ophthalmol. Vis. Sci. 39 1998 850 853 (Pubitemid 28207484)
58. P. Ostwald, S.S. Park, A.Y. Toledano, and S. Roth Adenosine receptor blockade and nitric oxide synthase inhibition in the retina: impact upon post-ischemic hyperemia and the electroretinogram Vision. Res. 37 1997 3453 3461 (Pubitemid 27491626)
59. E.J. Lee, K.Y. Kim, T.H. Gu, J.I. Moon, I.B. Kim, M.Y. Lee, S.J. Oh, and M.H. Chun Neuronal nitric oxide synthase is expressed in the axotomized ganglion cells of the rat retina Brain Res. 986 2003 174 180
60. L. Vidal, F. Diaz, A. Villena, M. Moreno, J.G. Campos, and I.P. de Vargas Nitric oxide synthase in retina and optic nerve head of rat with increased intraocular pressure and effect of timolol Brain Res. Bull. 70 2006 406 413 (Pubitemid 44486566)
61. I.B. Kim, S.J. Oh, and M.H. Chun Neuronal nitric oxide synthase immunoreactive neurons in the mammalian retina Micros. Res. Techniq. 50 2000 112 123
62. M.T. Perez, B. Larsson, P. Alm, K.E. Andersson, and B. Ehinger Localisation of neuronal nitric oxide synthase-immunoreactivity in rat and rabbit retinas Exp. Brain Res. 104 1995 207 217
63. L. Cao, and W.D. Eldred Subcellular localization of neuronal nitric oxide synthase in turtle retina: electron immunocytochemistry Vis. Neurosci. 18 2001 949 960 (Pubitemid 34507050)
64. S.J. Oh, H.I. Kim, I.B. Kim, K.Y. Kim, W. Huh, J.W. Chung, and M.H. Chun Morphology and synaptic connectivity of nitric oxide synthase-immunoreactive neurons in the guinea pig retina Cell Tissue Res. 297 1999 397 408 (Pubitemid 29410529)
65. J. Koistinaho, R.A. Swanson, J. de Vente, and S.M. Sagar NADPH-diaphorase (nitric oxide synthase)-reactive amacrine cells of rabbit retina: putative target cells and stimulation by light Neuroscience 57 1993 587 597 (Pubitemid 23350549)
66. E.M. Wexler, P.K. Stanton, and S. Nawy Nitric oxide depresses GABAA receptor function via coactivation of cGMP-dependent kinase and phosphodiesterase J. Neurosci. 18 1998 2342 2349
67. B. Hoffpauir, and E. Gleason Modulation of synaptic function in retinal amacrine cells Integr. Comp. Biol. 45 2005 658 664 (Pubitemid 41441978)
68. B. Hoffpauir, E. McMains, and E. Gleason Nitric oxide transiently converts synaptic inhibition to excitation in retinal amacrine cells J. Neurophysiol. 95 2006 2866 2877
69. S.A. Bloomfield, D. Xin, and T. Osborne Light-induced modulation of coupling between AII amacrine cells in the rabbit retina Vis. Neurosci. 14 1997
70. X.B. Xia, and S.L. Mills Gap junctional regulatory mechanisms in the AII amacrine cell of the rabbit retina Vis. Neurosci. 21 2004
71. D. Xin, and S.A. Bloomfield Comparison of the responses of AII amacrine cells in the dark- and light-adapted rabbit retina Vis. Neurosci. 16 1999 653 665 (Pubitemid 29347758)
72. R.S. Maggesissi, P.F. Gardino, E.M. Guimaraes-Souza, R. Paes-de-Carvalho, R.B. Silva, and K.C. Calaza Modulation of GABA release by nitric oxide in the chick retina: different effects of nitric oxide depending on the cell population Vision Res. 49 2009 2494 2502
73. A. Vielma, L. Delgado, C. Elgueta, R. Osorio, A.G. Palacios, and O. Schmachtenberg Nitric oxide amplifies the rat electroretinogram Exp. Eye Res. 91 2010 700 709
74. I. Ahmad, T. Leinders-Zufall, J.D. Kocsis, G.M. Shepherd, F. Zufall, and C.J. Barnstable Retinal ganglion cells express a cGMP gated cation condutance activatable by NO donors Neuron 12 1994 155 165 (Pubitemid 24044395)
75. F. Kawa, and P. Sterling CGMP modulates spike responses of retinal ganglion cells via a cGMP-gated current Vis. Neurosci. 19 2002 373 380 (Pubitemid 36221916)
76. G.-Y. Wang Unique functional properties of the APB sensitive and insensitive rod pathways signaling light decrements in mouse retinal ganglion cells Vis. Neurosci. 23 2006 127 135 (Pubitemid 43376260)
77. J.P. Nemargut, and G.-Y. Wang Inhibition of nitric oxide synthase desensitizes retinal ganglion cells to light by diminishing their excitatory synaptic currents under light adaptation Vision Res. 49 2009 2936 2947
78. G.-Y. Wang, D.A. Van der List, J.P. Nemargut, J.L. Coombs, and L.M. Chalupa The sensitivity of light-evoked responses of retinal ganglion cells is decreased in nitric oxide synthase gene knockout mice J. Vision 7 2007 1 13
79. J. Cudeiro, C. Rivadulla, R. Rodriguez, S. Martinez-Conde, L. Martinez, K.L. Grieve, and C. Acuña Further observations on the role of nitric oxide in the feline lateral geniculate nucleus Eur. J. Neurosci. 8 1996 144 152 (Pubitemid 26029334)
80. J. Cudeiro, C. Rivadulla, R. Rodriguez, S. Martinez-Conde, C. Acuña, and J.M. Alonso Modulatory influence of putative inhibitors of nitric oxide synthesis on visual processing in the cat lateral geniculate nucleus J. Neurophysiol. 71 1994 146 149 (Pubitemid 24058847)
81. A.K. McCauley, S.T. Frank, and D.W. Godwin Brainstem nitrergic innervation of the mouse visual thalamus Brain Res. 1278 2009 34 49
82. K.S. Cramer, C.A. Leamey, and M. Sur Nitric oxide as a signaling molecule in visual system development R.R. Mize, T.M. Dawson, V.L. Dawson, M.J. Friedlander, Nitric Oxide in Brain Development, Plasticity, and Disease 1998 Elsevier Science B.V. Progress in Brain Research 101 104
83. J. Cudeiro, K.L. Grieve, C. Rivadulla, R. Rodriguez, S. Martinez-Conde, and C. Acuña The role of nitric oxide in the transformation of visual information within the dorsal lateral geniculate nucleus of the cat Neuropharmacology 33 1994 1413 1418 (Pubitemid 24353735)
84. J. Mitrofanis Calbindin immunoreactivity in a subset of cat thalamic reticular neurones J. Neurocytol. 21 1992 495 505
85. Y.I. Egberongbe, S.M. Gentleman, P. Falkai, B. Borgets, J.M. Polak, and G.W. Roberts The distribution of nitric oxide synthase immunoreactivity in the human brain Neuroscience 59 1994 561 578 (Pubitemid 24131512)
86. K. Mizukawa, S.T. Vicent, P.L. McGeer, and E.G. McGeer Distribution of reduced-nicotinamide-adenine-dinucleotide-phosphate diaphorase-positive cells and fibers in the cat central nervous system J. Comp. Neurol. 279 1989 281 311
87. M.E. Bickford, A.E. Günlük, W. Guido, and S.M. Sherman 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 1993 410 430 (Pubitemid 23222162)
88. M.E. Bickford, E. Ramcharan, D.W. Godwin, and N.J. Patel Two types of interneurons in the cat visual thalamus are distinguished by morphology, synaptic connections, and nitric oxide synthase content J. Comp. Neurol. 424 1999 701 717
89. S.A. Lipton Prospects for clinically tolerated NMDA antagonists: open-channel blockers and alternative redox states of nitric oxide Trends Neurosci. 16 1993 527 532 (Pubitemid 23341962)
90. K.R. Hoyt, L.-T. Tang, E. Aizenman, and I.J. Reynolds Nitric oxide modulates NMDA-induced increases in intracellular Ca2+ in cultured rat forebrain neurons Brain Res. 592 1992 310 316
91. C. De Labra, C. Rivadulla, N. Espinosa, M. Dasilva, R. Cao, and J. Cudeiro Different sources of nitric oxide mediate neurovascular coupling in the lateral geniculate nucleus of the cat Front. Syst. Neurosci. 3 2009 1 9
92. A.E. Wiencken, and V.A. Casagrande Endothelial nitric oxide synthetase (eNOS) in astrocytes: another source of nitric oxide in neocortex Glia 26 1999 280 290 (Pubitemid 29257190)
93. K.S. Cramer, A. Angelucci, J.-O. Hahm, M.B. Bogdanov, and M. Sur A role for nitric oxide in the development of the ferret retinogeniculate projection J. Neurosci. 15 1996 7995 8004 (Pubitemid 26405061)
94. S.R. Vicent, and H. Kimura Histochemical mapping of nitric oxide synthase in the rat brain Neuroscience 46 1992 755 784
95. J.H. Sandell NADPH diaphorase histochemistry in the macaque striate cortex J. Comp. Neurol. 251 1986 388 397 (Pubitemid 16032955)
96. S. Kuchiiwa, T. Kuchiiwa, S. Mori, and S. Nakagawa NADPH diaphorase neurones are evenly distributed throughout cat neocortex irrespective of functional specialization of each region Neuroreport 5 1994 1662 1664 (Pubitemid 24265266)
97. P.J. Norris, R.L.M. Faull, and P.C. Emson 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 (Pubitemid 26288142)
98. H.-J. Lüth, A. Hedlich, H. Hilbig, E. Winkelmann, and B. Mayer Morphological analyses of NADPH-diaphorase/nitric oxide synthase positive structures in human visual cortex J. Neurocytol. 23 1994 770 782
99. Y.H. Chung, K.M. Joo, Y.J. Lee, D.H. Shin, and C.I. Cha Postnatal development and age-related changes in the distribution of nitric oxide synthase-immunoreactive neurons in the visual system of rats Neurosci. Lett. 360 2004 1 4 (Pubitemid 38471973)
100. C. Aoki, S. Fenstemaker, M. Lubin, and C.-G. Go Nitric oxide synthase in the visual cortex of monocular monkeys as revealed by light and electron microscopic immunocytochemistry Brain Res. 620 1993 97 113 (Pubitemid 23225849)
101. C. Aoki, J. Rhee, M. Lubin, and T.M. Dawson NMDA-R1 subunit of the cerebral cortex co-localizes with neuronal nitric oxide synthase at preand postsynaptic sites and in spines Brain Res. 750 1997 25 40 (Pubitemid 27116245)
102. B. Clancy, M. Da Silva, F. Hester, and M.J. Friedlander Structure, function, and connectivity of white matter neurons in mammalian visual cortex Soc. Neurosci. Abstr. 23 1997 1268
103. M.J. Friedlander, F.W. Hester, C.D. Gancayco, B.D. Waterhouse, and R.C.S. Lin The role of the ascending serotonergic system in cortical nitric oxide production Soc. Neurosci. Abstr. 21 1995 1753