Cytochrome oxidase and NADPH-diaphorase on the afferent relay branch of the optokinetic reflex in the opossum

Journal of Comparative Neurology

Volumn 398, Issue 2, 1998, Pages 206-224

  Vargas, C D ^a   Sousa, A O ^a   Bittencourt, F L R ^a   Santos, C M ^a   Pereira Jr , A ^a   Bernardes, R F ^a   Rocha Miranda, C E ^a   Volchan, E ^a  

^a FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

Author keywords

Accessory optic system; Inferior olive; Metabolic activity; Nucleus of the optic tract; Pretectum

Indexed keywords

CYTOCHROME C OXIDASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN REGION; ENZYME LOCALIZATION; INFERIOR OLIVE; NERVE PROJECTION; NONHUMAN; OPOSSUM; OPTIC TRACT; OPTOKINETIC STIMULATION; PRIORITY JOURNAL; RETINA; SENSORY NERVE;

ANIMALS; ELECTRON TRANSPORT COMPLEX IV; NADPH DEHYDROGENASE; NEURONS, AFFERENT; NYSTAGMUS, OPTOKINETIC; OLIVARY NUCLEUS; OPOSSUMS; REFLEX; RETINA; SUPERIOR COLLICULUS;

EID: 0032563740     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1096-9861(19980824)398:2<206::AID-CNE4>3.0.CO;2-4     Document Type: Article

References (114)

1. Allman, J. and S. Zucker (1990) Cytochrome oxidase and functional coding in primate striate cortex: A hypothesis. In Cold Spring Harbor Symposium in Quantitative Biology, Vol LV, Cold Spring Harbor, NY: Cold Spring Harbor Lab. Press, pp. 979-982.
2. Avendaño, C. and M.A. Juretschke (1980) The pretectal region of the cat: A structural and topographic study with stereotaxic coordinates. J. Comp. Neurol. 193:69-88.
3. Ballas, I. and K.P. Hoffmann (1985) A correlation between receptive field properties and morphological structures in the pretectum of the cat. J. Comp. Neurol. 238:417-438.
4. Baleydier, C., M. Magnin, and H.M. Cooper (1990) Macaque accessory optic system: Connections with the pretectum. J. Comp. Neurol. 302:405-416.
5. Benassi, C., G.P. Biral, F. Lui, C.A. Porro, and R. Corazza (1989) The interstitial nucleus of the superior fasciculus, posterior bundle (INSFp) in the guinea pig: Another nucleus of the accessory optic system processing the vertical retinal slip signal. Vis. Neurosci. 2:377-382.
6. Berman, N. (1977) Connections of the pretectum in the cat. J. Comp. Neurol. 174:227-254.
7. Blümke, I., P.R. Hof, J.H. Morrisson, and M.R. Celio (1990) Distribution of parvalbumin immunoreactivity in the visual cortex of old world monkeys and humans. J. Comp. Neurol. 301:417-432.
8. Buttner-Ennever, J.A., B. Cohen, A.K.E. Horn, and H. Reisine (1996) Efferent pathways of the nucleus of the optic tract in monkey and their role in eye movements. J. Comp. Neurol. 373:90-107.
9. Born, R.T. and R.B.H. Tootell (1992) Segregation of global and local motion processing in primate middle temporal visual area. Nature 357:497-499.
10. Caballero-Bleda, M., B. Fernandez, and L. Puelles (1992) The pretectal complex of the rabbit: Distribution of acetylcholinesterase and reduced nicotinamide adenine dinucleotide diaphorase activities. Acta Anat. 144:7-16.
11. Cavalcante, L.A., C.E. Rocha-Miranda, and R. Lent (1975) Hypothalamic, tectal and accessory optic projections in the opossum. Brain Res. 84:302-307.
12. Cazin, L., W. Precht, and J. Lannou (1980) Optokinetic responses of vestibular nucleus neurons in the cat. Pflugers Arch. 384:31-38.
13. Carroll, E.W. and M.T.T. Wong-Riley (1984) Quantitative light and electron microscopic analysis of cytochrome oxidase rich zones in the striate cortex of the squirrel monkey. J. Comp. Neurol. 222:1-17.
14. Chandrasekaran, K., J. Stoll, S.I. Rapoport, and D. Brady (1993) Localization of cytochrome oxidase activity and COX mRNA in the perirhinal and superior temporal sulci of the monkey brain. Brain Res. 606:213-219.
15. Clarke, R.J., R.A. Giolli, R.H.I. Blanks, Y. Torigoe, and J.H. Fallon (1989) Neurons of the medial terminal accessory optic nucleus of the rat are poorly collateralized. Vis. Neurosci. 2:269-273.
16. Cohen, B., D. Schiff, and J. Buttner (1990) Contribution of the nucleus of the optic tract to optokinetic afternystagmus in the monkey: Clinical implications. In B. Cohen and I. Bodis-Wollner (eds): Vision and the Brain. New York: Raven Press, pp. 233-255.
17. Coleman, L.A. and L.D. Beazley (1988) The accessory optic system of the wallaby, Setonix brachyurus: Anatomy of normal animals and after early unilateral eye removal. J. Comp. Neurol. 273:359-376.
18. Collewijn, H. (1975) Direction selective units in the rabbit's nucleus of the optic tract. Brain Res. 100:489-508.
19. Condo, G.J. and V.A. Casagrande (1990) Organization of cytochrome oxidase staining in the visual cortex of nocturnal primates (Galago crassicaudatus and Galago senegalensis): I. Adult patterns. J. Comp. Neurol. 293:632-645.
20. Cooper, H.M. and M. Magnin (1986) A common mammalian plan of accessory optic system organization revealed in all primates. Nature 324:457-459.
21. Cooper, H.M., C. Baleydier, and M. Magnin (1990) Macaque accessory optic system: I. Definition of the medial terminal nucleus. J. Comp. Neurol. 302:394-404.
22. DeYoe, E.A., T.C. Trusk, and M.T.T. Wong-Riley (1995) Activity correlates of cytochrome oxidase defined compartments in granular and supragranular layers of primary visual cortex of macaque monkey. Vis. Neurosci. 12:629-639.
23. Distler, C. and K.P. Hoffmann (1993) Visual receptive fields properties in kitten pretectal nucleus of the optic tract and dorsal terminal nucleus of the accessory optic tract. J. Neurophysiol. 70:814-827.
24. Edwards, D.P., K.P. Purpura, and E. Kaplan (1995) Contrast sensitivity and spatial frequency response of primate cortical neurons in and around the cytochrome oxidase blobs. Vision Res. 11:1501-1523.
25. Farias, M.F., R. Gattass, M.C. Piñón, and L.G. Ungerleider (1997) Tangential distribution of cytochrome oxidase-rich blobs in the primary visual cortex of macaque monkeys. J. Comp. Neurol. 386:217-228.
26. Franca, J.G., J.L.M. Nascimento, C.W. Picanço-Diniz, J.A.S. Quaresma, and A.L.C. Silva (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.
27. Giolli, R.A. and M.D. Guthrie (1969) The primary optic projections in the rabbit. An experimental degeneration study. J. Comp. Neurol. 136:99-126.
28. Giolli, R.A., R.H.I. Blanks, and Y. Torigoe (1984) Pretectal and brainstem projections of the medial terminal nucleus of the accessory optic system of the rabbit and rat as studied by anterograde and retrograde neuronal tracing methods. J. Comp. Neurol. 227:228-251.
29. Giolli, R.A., G.M. Peterson, C.E. Ribak, H.M. McDonald, R.H.I. Blanks, and J.H. Fallon (1985) GABAergic neurons comprise a major cell type in rodent visual relay nuclei: An immunocytochemical study of pretectal and accessory optic nuclei. Exp. Brain Res. 61:194-203.
30. Giolli, R.A., Y. Torigoe, R.H.I. Blanks, and M.H. Mc Donald (1988) Projections of the dorsal and lateral terminal accessory optic nuclei and of the interstitial nucleus of the superior fascicles (posterior fibers) in the rabbit and rat. J. Comp. Neurol. 277:608-620.
31. Giolli, R.A., R.J. Clarke, Y. Torigoe, R.H.I. Blanks, and J.H. Fallon (1992) GABAergic and non-GABAergic projections of optic nuclei including the visual tegmental relay zone to the nucleus of the optic tract and dorsal terminal accessory optic nucleus in rat. J. Comp. Neurol. 319:349-358.
32. Grasse, K.L. and M.S. Cynader (1982) Electrophysiology of the medial terminal nucleus of the accessory optic system in the cat. J. Neurophysiol. 48:490-504.
33. Grasse, K.L. and M.S. Cynader (1984) Electrophysiology of lateral and dorsal terminal nuclei of the cat accessory optic system. J. Neurophysiol. 51:276-293.
34. Hamasaki, D. and E. Marg (1962) Microelectrode study of accessory optic tract in the rabbit. Am. J. Physiol. 202:480-486.
35. Hayhow, W.G. (1959) An experimental study of the accessory optic fiber system in the cat. J. Comp. Neurol. 113:281-313.
36. Hayhow, W.G. (1966) The accessory optic system in the marsupial phalanger, Trichosurus vupecula. J. Comp. Neurol. 126:653-672.
37. Hendrickson, A.E., S.P. Hunt, and J.Y. Wu (1981) Immunocytochemical localization of glutamic acid decarboxylase in monkey striate cortex. Nature 292:605-607.
38. Hevner, R.F, S. Liu, and M.T.T. Wong-Riley (1995) A metabolic map of cytochrome oxidase in the rat brain: Histochemical, densitometric and biochemical studies. Neuroscience 65:313-342.
39. Hoffmann, K.P. and C. Distler (1989) Quantitative analysis of visual receptive fields of neurons in nucleus of the optic tract and dorsal terminal nucleus of the accessory optic tract in macaque monkey. J. Neurophysiol 62:416-428.
40. Hoffmann, K.P. and A. Schoppmann (1975) Retinal input to direction-selective cells in the nucleus tractus opticus in the cat. Brain Res. 99:359-366.
41. Hoffmann, K.P. and A. Schoppmann (1981) A quantitative analysis of the direction-specific response of neurons in the cat's nucleus of the optic tract. Exp. Brain Res. 42:146-157.
42. Hoffmann, K.P., K. Berend, and A. Schoppmann (1976) a direct afferent visual pathway from the nucleus of the optic tract to the inferior olive in the cat. Brain Res. 115:150-153.
43. Hoffmann, K.P., C. Distler, R. Erickson, and W. Mader (1988) Physiological and anatomical identification of the nucleus of the optic tract and dorsal terminal nucleus of the accessory optic tract in monkeys. Exp. Brain. Res. 69:635-644.
44. Holstege, G. and H. Collewijn (1982) The efferent connections of the nucleus of the optic tract and superior colliculus in the rabbit. J. Comp. Neurol. 209:139-175.
45. Horn, A.E. and K.P. Hoffmann (1987) Combined GABA-immunocytochemistry and TMB-HRP histochemistry of pretectal nuclei projecting to the inferior olive in rats, cats and monkeys. Brain Res. 409:133-138.
46. Horton, J.C. (1984) Cytochrome oxidase patches: A new cytoarchitectonic feature of monkey visual cortex. Philos. Trans. R. Soc. Lond. 304:199-253.
47. Horton, J.C. and D.H. Hubel (1981) Regular patchy distribution of cytochrome oxidase staining on primary visual cortex of macaque monkey. Nature 292:762-764
48. Hutchins, B. and J.T. Weber (1985a) The pretectal olivary nucleus of the cat: Evidence for a two-tailed structure. Brain Res. 331:150-154.
49. Hutchins, B. and J.T. Weber (1985b) The pretectal complex of the monkey: A reinvestigation of the morphology and retinal terminations. J. Comp. Neurol. 232:425-442.
50. Ibbotson, M.R. and R.F. Mark (1994) Wide-field nondirectional visual units in the pretectum: Do they suppress ocular following of saccade-induced visual stimulation. J. Neurophysiol. 72:1448-1450.
51. Ibbotson, M.R., R.F. Mark, and T.L. Maddess (1994) Spatiotemporal response properties of direction-selective neurons in the nucleus of the optic tract and dorsal terminal nucleus of the Wallaby, Macropus eugenii. J. Neurophysiol. 72:2927-2943.
52. Johnson, J.K. and V.A. Casagrande (1995) Distribution of calcium-binding proteins within the parallel visual pathways of a primate (Galago crassicaudatus) J. Comp. Neurol. 356:238-260.
53. Kageyama, G.H. and R.L. Meyer (1988) Histochemical localization of cytochrome oxidase in the retina and optic tectum of normal goldfish: A combined cytochrome oxidase-horseradish peroxidase study. J. Comp. Neurol. 270:354-371.
54. Kageyama, G.H. and M. Wong-Riley (1982) Histochemical localization of cytochrome oxidase in the hippocampus: Correlation with specific neuronal types and afferent pathways. Neuroscience 7:2337-2361.
55. Kageyama, G.H. and M. Wong-Riley (1984) The histochemical localization of cytochrome oxidase in the retina and lateral geniculate nucleus of the ferret, cat and monkey, with particular reference to retinal mosaics and ON/OFF center visual channels. J. Neurosci. 4:2445-2459.
56. Kageyama, G.H. and M. Wong-Riley (1985) An analysis of the cellular localization of cytochrome oxidase in the lateral geniculate nucleus of the adult cat. J. Comp. Neurol. 242:338-357.
57. Kanaseki, T. and J.M. Sprague (1974) Anatomical organization of pretectal nuclei and tectal laminae in the cat. J. Comp. Neurol. 158:319-338.
58. Klauer, S., F. Sengpiel, and K.P. Hoffmann (1990) Visual response properties and afferents of nucleus of the optic tract in the ferret. Exp. Brain Res. 83:178-189.
59. Klooster, J., J.J.L. van der Want, and G. Vrensen (1983) Retinopretectal projections in albino and pigmented rabbits: An autoradiographic study. Brain Res. 288:1-12.
60. Koontz, M.A., R.W. Rodieck, and S.G. Farmer (1985) The retinal projection to the cat pretectum. J. Comp. Neurol. 236:42-59.
61. Korp, B.G., R.H.I. Blanks, and Y. Torigoe (1989) Projections of the nucleus of the optic tract to the nucleus reticularis tegmenti pontis and prepositus hypoglossi nucleus in the pigmented rat as demonstrated by anterograde and retrograde transport methods. Vis. Neurosci. 2:275-286.
62. Kubota, T., M. Morimoto, T. Kanaseki, and H. Inomata (1987) Projection from the pretectal nuclei to the dorsal lateral geniculate nucleus in the cat: A wheat germ agglutinin-horseradish peroxidase study. Brain Res. 421:30-40.
63. Land, P. (1987) Dependence of cytochrome oxidase activity in the rat lateral geniculate nucleus on retinal innervation. J. Comp. Neurol. 262:78-89.
64. Lent, R., L.A. Cavalcante, and C.E. Rocha-Miranda (1976) Retinofugal projections in the opossum. An anterograde degeneration and radioautographic study. Brain Res. 107:9-26.
65. Linden, R. and C.E. Rocha-Miranda (1981) The pretectal complex in the opossum: Projections from the striate cortex and correlation with retinal terminal fields. Brain Res. 207:267-277.
66. Livingstone, M. and D. Hubel (1984) Anatomy and physiology of a color system in primate visual cortex. J. Neurosci. 4:309-356.
67. Maekawa, K., T. Takeda, and M. Kimura (1984) Responses of the nucleus of the optic tract neurons projecting to the nucleus reticularis tegmenti pontis upon optokinetic stimulation in the rabbit. Neurosci. Res. 2:1-25.
68. Magnin, M., H. Kennedy, and K.P. Hoffmann (1989) A double labeling investigation of the pretectal visuo-vestibular pathways. Vis. Neurosci. 3:53-58.
69. Mesulam, M.M. (1978) Tetramethyl benzidine for horseradish peroxidase neurohistochemistry: A non-carcinogenic blue reaction-product with superior sensitivity for visualizing neural afferents and efferents. J. Histochem. Cytochem. 26:106-117.
70. Mustari, M.J. and A.F. Fuchs (1989) Response properties of single units in the lateral terminal nucleus of the accessory optic system in the behaving primate. J. Neurophysiol. 61:1207-1219.
71. Mustari, M.J., A.F. Fuchs, C.R.S. Kaneko, and F.R. Robinson (1994) Anatomical connections of the primate nucleus of the optic tract. J. Comp. Neurol. 349:111-128.
72. Narbors, L.B. and R.R. Mize (1991) A unique neuronal organization in the cat pretectum revealed by antibodies to the calcium binding protein Calbindin D-28K. J. Neurosci. 11:2460-2476.
73. Nasi, J.P. (1993) O reflexo optocinético horizontal. Estudo anatômico e eletrofisiologico no gambá (Didelphis marsupialis aurita) normal e com enucleação monocular precoce. PHD thesis at the Biophysics Institute Carlos Chagas Filho, UFRJ, Brazil.
74. Nasi, J.P., Volchan, E., M.T. Tecles, R.F. Bernardes, and C.E. Rocha-Miranda (1997) The horizontal optokinetic reflex of the opossum (Didelphis marsupialis aurita): Physiological and anatomical studies in normal and early mononucleated specimens. Vis. Res. 37:1207-1216.
75. Nunes Cardozo, B. and J. Van der Want (1990) Ultrastructural organization of the retino-pretecto-olivary pathway in the rabbit. J. Comp. Neurol. 291:313-327.
76. Oswaldo-Cruz, E. and C.E. Rocha-Miranda (1968) The brain of the opossum (Didelphis marsupialis). A cytoarchitectonic atlas in stereotaxic coordinates. Biophysics Institute Carlos Chagas Filho, UFRJ, Brazil.
77. Pereira, Jr., A., E. Volchan, R.F. Bernardes, and C.E. Rocha-Miranda (1994) Binocularity in the nucleus of the optic tract of the opossum. Exp. Brain Res. 102:327-338.
78. Robertson, R.T. (1983) Efferents of the pretectal complex: Separate populations of neurons project to lateral thalamus and to inferior olive. Brain Res. 258:91-95.
79. Rocha-Miranda, C.E. and R. Lent (1978) Opossum Neurobiology (Neurobiologia do Gambá). Academia Brasileira de Ciências, Rio de Janeiro, Brazil.
80. Rosa, M.G.P., R. Gattass, and J.G.M. Soares (1991) A quantitative analysis of cytochrome oxidase-rich patches in the primary visual cortex of Cebus monkeys: Topographic distribution and effects of late monocular enucleation. Exp. Brain Res. 84:195-209.
81. Rose, J.E. (1942) The thalamus of the sheep: Cellular and fibrous structure and comparison with pig, rabbit and cat. J. Comp. Neurol. 77:469-523.
82. Royce, G.G., J.P. Ward, and J.K. Harting (1976) Retinofugal pathways in two marsupials. J. Comp. Neurol. 170:391-414.
83. Saint-Cyr, J.A. and J. Courville (1981) Sources of descending afferents to the inferior olive from the upper brainstem in the cat as revealed by the retrograde transport of horseradish peroxidase. J. Comp. Neurol. 198:567-581.
84. Sandell, J.H. (1986) NADPH diaphorase histochemistry in the macaque striate cortex. J. Comp. Neurol. 251:388-397.
85. Scalia, F. (1972) The termination of retinal axons in the pretectal region of mammals. J. Comp. Neurol. 145:223-258.
86. Scalia, F. and V. Arango (1979) Topographic organization of the projections of the retina to the pretectal region in the rat. J. Comp. Neurol. 186:271-292.
87. 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.
88. Schmidt, M. (1996) Neurons in the cat pretectum that project to the dorsal lateral geniculate are activated during saccades. J. Neurophysiol. 76:2907-2918.
89. Schmidt, M., D. Schiff, and M. Bentivoglio (1995) Independent efferent populations in the nucleus of the optic tract: An anatomical and physiological study in rat and cat. J. Comp. Neurol. 360:271-285.
90. Schmidt, M., G. Lehnert, R.G. Baker, and K.P. Hoffmann (1996) Dendritic morphology of projection neurons in the cat pretectum. J. Comp. Neurol. 369:520-532.
91. Seligman, A.M., M.J. Karnowsky, H.L. Wasserkrug, and J.S. Hanker (1968) Nondroplet ultrastructural demonstration of cytochrome oxidase activity with a polymerizing osmiophilic agent, diaminobenzidine (DAB). J. Cell Biol. 38:1-14.
92. Silverman, M.S., D.H. Grosof, R.L. De Valois, and S.D. Elfar (1989) Spatial-frequency organization in primate striate cortex. Proc. Natl. Acad. Sci. USA 86:711-715.
93. Simpson, J.I. (1984) The accessory optic system. Annu. Rev. Neurosci. 7:13-41.
94. Simpson, J.I., R.E. Soodak, and R. Hese (1979) the accessory optic system and its relation to vestibulocerebellum. In R. Granit and O. Pompeiano (eds): Reflex Control of Posture and Movement. Prog. Brain Res. Vol. 50. Amsterdam: Elsevier/North Holland Biomedical Press, pp. 715-724.
95. Simpson, J.I., R.A. Giolli, and R.H.I. Blanks (1988) The pretectal nuclear complex and the accessory optic system. In J.A. Buttner-Ennever (ed): Neuroanatomy of the Oculomotor System. Amsterdam: Elsevier, pp. 335-364.
96. Sudkamp, S. and M. Schmidt (1995) Physiological characterization of pretectal neurons projecting to the lateral posterior-pulvinar complex in the cat. Eur. J. Neurosci. 7:881-888.
97. Terasawa, K., K. Otani, and J. Yamada (1979) Descending pathways of the nucleus of the optic tract in the rat. Brain Res. 173:405-417.
98. Tootell, R.B., S.L. Hamilton, and M.S. Silverman (1985) Topography of cytochrome oxidase activity in the owl monkey cortex. J. Neurosci. 5:2766-2800.
99. Van der Togt, C. and J. Van der Want (1992) Variation in form and axonal termination in the nucleus of the optic tract of the rat: The medial terminal nucleus input on the neurons projecting to the inferior olive. J. Comp. Neurol. 325:446-461.
100. Van der Togt, C., J. Van der Want, and M. Schmidt (1993) Segregation of direction selective neurons and synaptic organization of inhibitory intranuclear connections in the medial terminal nucleus of the rat: An electrophysiological and immunoelectron microscopical study. J. Comp. Neurol. 338:175-192.
101. Vargas, C.D, E. Volchan, J.P. Nasi, R.F. Bernardes, and C.E. Rocha-Miranda (1996) The nucleus of the optic tract (NOT) and the dorsal terminal nucleus of opossums (Didelphis marsupialis aurita). Brain Behav. Evol. 48:1-15.
102. Vargas, C.D., E. Volchan, J.N. Hokoç, A. Pereira, Jr., R.F. Bernardes, and C.E. Rocha-Miranda (1997) On the functional anatomy of the nucleus of the optic tract-dorsal terminal nucleus commissural connection in the opossum (Dideplhis marsupialis aurita). Neuroscience 76:313-321.
103. Volchan, E., C.E. Rocha-Miranda, C.W. Picanço-Diniz, B. Zinsmeisser, R.F. Bernardes, and J.G. Franca (1989) Visual response properties of the pretectal nucleus of the optic tract in the opossum. Exp. Brain Res. 78:380-386.
104. Volchan, E., A. Pereira, Jr., C.D. Vargas, and C.E. Rocha-Miranda (1996) The nucleus of the optic tract of the opossum. Rev. Bras. Biol. 56:373-380.
105. Walberg, F., T. Nordby, K.P. Hoffmann, and H. Hollander (1981) Olivary afferents from the pretectal nuclei in the cat. Anat. Embryol. 161:291-304.
106. Watanabe, S., I. Kato, S. Sato, T. Okada, and M. Norita (1991) Descending pathways from the nucleus of the optic tract in the Fuscata monkey. Soc. Neurosci. Abst. 17:113.
107. Weber, J.T. (1985) Pretectal complex and accessory optic system of primates. Brain Behav. Evol. 26:117-140.
108. Weber, J.T. and J.K. Harting (1980) The efferent projections of the pretectal complex: An autoradiographic and horseradish peroxidase analysis. Brain Res. 194:1-28.
109. Wong-Riley, M.T.T. (1976) Endogenous peroxidatic activity in brainstem neurons as demonstrated by staining with diaminobenzidine in normal squirrel monkeys. Brain Res. 108:257-277.
110. Wong-Riley, M.T.T. (1979) changes in the visual system of monocularly sutured or enucleated cats demonstrable with cytochrome oxidase histochemistry. Brain Res. 171:11-28.
111. Wong-Riley, M.T.T. (1989) Cytochrome oxidase: An endogenous metabolic marker of neuronal activity. Trends Neurosci. 12:94-102.
112. Wong-Riley, M.T.T. and T.T. Norton (1988) Histochemical localization of cytochrome oxidase activity in the visual system of the tree shrew: Normal patterns and the effect of retinal impulse blockade. J. Comp. Neurol. 272:562-578.
113. Wong-Riley, M.T.T., M.M. Merzenich, and P.A. Leake (1978) Changes in endogenous enzymatic reactivity to DAB induced by neuronal inactivity. Brain Res. 141:185-192.
114. Zhang, H.Y. and K.P. Hoffmann (1993) retinal projections to the pretectum, accessory optic system and superior colliculus in pigmented and albino ferrets. Eur. J. Neurosci. 5:486-500.