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Effects of wavelength on the timing and laminar distribution of illuminance-evoked activity in macaque V1

Published online by Cambridge University Press:  02 June 2009

S.J. Givre
Affiliation:
Departments of Neuroscience and Neurology, Rose F. Kennedy Center, Albert Einstein College of Medicine, Bronx, NY
J.C. Arezzo
Affiliation:
Departments of Neuroscience and Neurology, Rose F. Kennedy Center, Albert Einstein College of Medicine, Bronx, NY
C.E. Schroeder
Affiliation:
Departments of Neuroscience and Neurology, Rose F. Kennedy Center, Albert Einstein College of Medicine, Bronx, NY

Abstract

Responses to full-field colored flashes (red, blue, and green) were compared with those to illuminancematched white flashes in area V1, optic radiations, and the lateral geniculate nucleus of two alert macaques. Laminar profiles of visual evoked potentials (VEPs), current source density, and multiunit activity were obtained using multicontact electrodes capable of sampling from all layers of cortex or lateral geniculate nucleus, simultaneously. In striate cortex, stimulation with colored flash enhanced transmembrane current flow dramatically in both layer 4c and the supragranular laminae. Stimulation with red evoked the largest enhancement in every electrode penetration. The mean peak amplitudes of current sinks evoked by red were 203% and 537% of those evoked by white light in layer 4c and the supragranular laminae, respectively. Color effects in VI were preceded by an initial epoch of wavelength-insensitive activity. In layer 4c, the red effect reached significance, on average, at 47 ms, or ≈24 ms after the onset of transmembrane current flow. In the supragranular layers, the red effect reached significance, on average, at 55 ms, or ≈14 ms after the onset of current flow. Recordings from optic radiations in the white matter below V1 and from lateral geniculate nucleus showed no significant difference in the responses to color and illuminance-matched white light. Enhancement of supragranular current flow with color stimulation increased the contribution of these laminae to the generation of the surface VHP. Comparison of the surface VHP wave forms evoked by white and color stimuli may, therefore, help to differentiate the responses of the granular and supragranular laminae.

Type
Research Articles
Copyright
Copyright © Cambridge University Press 1995

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References

Allison, T., Begleiter, A., McCarthy, G., Roessler, E., Nobre, A. & Spencer, D.D. (1993). Electrophysiological studies of color processing in human visual cortex. Electroencephalography and Clinical Neurophysiology 88, 343355.CrossRefGoogle ScholarPubMed
Barna, J., Arezzo, J.C. & Vaughan, H.G., JR. (1981). A new multicontact array for the simultaneous recording of field potentials and unit activity. Electroencephalography and Clinical Neurophysiology 52, 494496.CrossRefGoogle Scholar
Blasdel, G.G. & Fitzpatrick, D. (1984). Physiological organization of layer 4 in macaque striate cortex. Journal of Neuroscience 4(3), 880895.CrossRefGoogle ScholarPubMed
Casagrande, V.A. & Lachica, E.A. (1992). What are the cytochrome oxidase (CO) blobs and interblobs really segregating? Investigative Ophthalmology and Visual Science (Suppl.) 33(4), 900.Google Scholar
Cavender, S.A., Hobson, R.R., Chao, G.-M., Weinstein, G.W. & Odom, J.V. (1992). Comparison of preoperative visual evoked potentials to contrast sensitivity and visual acuity after cataract extraction. Documenta Ophthalmologica 81, 181188.CrossRefGoogle ScholarPubMed
DeYoe, E.A. & Van Essen, D.C. (1988). Concurrent processing streams in monkey visual cortex. Trends in Neuroscience 11(5), 219236.CrossRefGoogle ScholarPubMed
Fitzpatrick, D., Itoh, K. & Diamond, I.T. (1973). The laminar organization of the lateral geniculate body and the striate cortex in the squirrel monkey (Saimiri sciureus). Journal of Neuroscience 3, 673702.CrossRefGoogle Scholar
Fitzpatrick, D., Lund, J.S. & Blasdel, G.G. (1985). Intrinsic connections of macaque striate cortex: Afferent and efferent connections of lamina 4c. Journal of Neuroscience 5(12), 33293349.CrossRefGoogle ScholarPubMed
Foxe, J., Mehta, A.D., Ulbert, I., Simpson, G.V., Vaughan, H.G. Jr., Ritter, W., Schroeder, M.M. & Schroeder, C.E. (1994). Integration of human and monkey electrophysiology in the study of sensory processing and attention. Society for Neuroscience Abstracts 20, 576.Google Scholar
Freeman, J.A. & Nicholson, C. (1975). Experimental optimization of current source-density technique for anuran cerebellum. Journal of Neurophysiology 38, 369382.CrossRefGoogle ScholarPubMed
Givre, S.J., Schroeder, C.E. & Arezzo, J.C. (1994). Contribution of extrastriate area V4 to the surface-recorded flash VEP in the awake macaque. Vision Research 34(4), 415438.CrossRefGoogle Scholar
Horton, J.C. & Hubel, D.H. (1980). Cytochrome oxidase stain preferentially labels intersections of ocular dominance and vertical orientation columns in macaque striate cortex. Society for Neuroscience Abstracts 6, 315.Google Scholar
Horton, J.C. & Hubel, D.H. (1981). Regular patchy distribution of cytochrome oxidase staining in primary visual cortex of macaque monkey. Nature 292, 762764.CrossRefGoogle ScholarPubMed
Hubel, D. & Livingstone, M. (1990). Color puzzles. Cold Spring Harbor Symposium on Quantitative Biology 55, 643649.CrossRefGoogle ScholarPubMed
Humphrey, A.L. & Hendrickson, A.E. (1980). Radial zones of high metabolic activity in squirrel monkey striate cortex. Society for Neuroscience Abstracts 6, 315.Google Scholar
Kaplan, E. & Shapley, R.M. (1982). X and Y cells in the lateral geniculate nucleus of macaque monkeys. Journal of Physiology (London) 330, 125143.CrossRefGoogle ScholarPubMed
Komatsu, H., Ideura, Y., Kaji, S. & Yamane, S. (1992). Color selectivity of neurons in the inferior temporal cortex of the awake macaque. Journal of Neuroscience 12(2), 408424.CrossRefGoogle ScholarPubMed
Kraut, M., Arezzo, J.C. & Vaughan, H.G. Jr., (1985). Intracortical generators of the flash VHP in monkeys. Electroencephalography and Clinical Neurophysiology 62, 300312.CrossRefGoogle Scholar
Legatt, A.D., Arezzo, J.C. & Vaughan, H.G. Jr., (1980). Averaged multiple-unit activity as an estimate of phasic changes in local neuronal activity. Journal of Neuroscience Methods 2, 203217.CrossRefGoogle ScholarPubMed
Lennie, P., Krauskopf, J. & Sclar, G. (1990). Chromatic mechanisms in striate cortex of macaque. Journal of Neuroscience 10(2), 649669.CrossRefGoogle ScholarPubMed
Livingstone, M.S., Hubel, D.H. (1982). Thalamic inputs to cytochrome oxidase-rich regions in the monkey visual cortex. Proceedings of the National Academy of Sciences of the U.S.A. 79, 60986101.CrossRefGoogle ScholarPubMed
Livingstone, M.S. & Hubel, D.H. (1984). Anatomy and physiology of a color system in the primate visual cortex. Journal of Neuroscience 4(1), 309356.CrossRefGoogle ScholarPubMed
Livingstone, M.S. & Hubel, D.H. (1987). Psychophysical evidence for separate channels for the perception of form, color, movement and depth. Journal of Neuroscience 7(11), 34163468.CrossRefGoogle ScholarPubMed
Lund, J.S., Lund, R.D., Hendrickson, A.E., Bunt, A.H. & Fuchs, A.F. (1975). The origin of efferent pathways from the primary visual cortex, area 17, of the macaque monkey as shown by retrograde transport of horseradish peroxidase. Journal of Comparative Neurology 164(3), 287303.CrossRefGoogle ScholarPubMed
Lund, J.S. (1987). Local circuit neurons of macaque monkey striate cortex: I. Neurons of laminae 4C and 5A. Journal of Comparative Neurology 257, 6092.CrossRefGoogle ScholarPubMed
Lund, J.S. (1988). Anatomical organization of macaque monkey striate visual cortex. Annual Review of Neuroscience 11, 253288.CrossRefGoogle ScholarPubMed
Maunsell, J.H.R. & Newsome, W.T. (1987). Visual processing in monkey extrastriate cortex. Annual Review of Neuroscience 10, 363401.CrossRefGoogle ScholarPubMed
Odom, J.V., Hobson, R., Coldren, J.T., Chao, G.-M. & Weinstein, G.W. (1987). 10-Hz flash visual evoked potentials predict post-cataract extraction visual acuity. Documenta Ophthalmologica 66, 292299.CrossRefGoogle ScholarPubMed
Odom, J.V., Chao, G.-M., Hobson, R. & Weinstein, G.W. (1988). Prediction of post cataract visual acuity: 10-Hz visually evoked potentials. Ophthalmic Surgery 19, 212218.Google Scholar
Schein, S.J. & Desimone, R. (1990). Spectral properties of V4 neurons in the macaque. Journal of Neuroscience 10(10), 33693389.CrossRefGoogle ScholarPubMed
Schroeder, C.E. & Givre, S.J. (1991). Temporal organization of the visual system in the awake macaque. Society for Neuroscience Abstracts 17(2), 1568.Google Scholar
Schroeder, C.E. & Givre, S.J. (1992). Functional fast and slow processing lines in the macaque form and color pathway. Investigative Ophthalmology and Visual Science (Suppl.) 33(4), 1131.Google Scholar
Schroeder, C.E., Mehta, A., Givre, S.J. & Steinschneider, M. (1993). Functional dissociation of parallel visual streams in the macaque temporal lobe. Investigative Ophthalmology and Visual Science (Suppl.) 34(4), 813.Google Scholar
Schroeder, C.E., Tenke, C.E., Arezzo, J.C. & Vaughan, H.G. Jr., (1989). Timing and distribution of flash-evoked activity in the lateral geniculate nucleus of the alert monkey. Brain Research 477, 183195.CrossRefGoogle ScholarPubMed
Schroeder, C.E., Tenke, C.E., Arezzo, J.C. & Vaughan, H.G. Jr., (1990 a). Binocularity in the lateral geniculate nucleus of the alert monkey. Brain Research 521, 303310.CrossRefGoogle Scholar
Schroeder, C.E., Tenke, C.E., Givre, S.J., Arezzo, J.C. & Vaughan, H.G. Jr., (1990 b). Laminar analysis of bicuculline-induced epilep-tiform activity in area 17 of the awake macaque. Brain Research 515, 326330.CrossRefGoogle ScholarPubMed
Schroeder, C.E., Tenke, C.E. & Givre, S.J. (1992). Subcortical contributions to the surface recorded flash-VEP in the awake macaque. Electroencephalography and Clinical Neurophysiology 84, 219231.CrossRefGoogle Scholar
Schroeder, C.E., Tenke, C.E., Givre, S.J., Arezzo, J.C. & Vaughan, H.G. Jr., (1991). Striate cortical contribution to the surface-recorded pattern-reversal VEP in the alert monkey. Vision Research 31, 11431157.CrossRefGoogle Scholar
Shapley, R., Kaplan, E. & Soodak, R. (1981). Spatial summation and contrast sensitivity of X and Y cells in the lateral geniculate nucleus of the macaque. Nature 292, 543545.CrossRefGoogle ScholarPubMed
Tootell, R.B.H., Sllverman, M.S., Hamilton, S.L., De Valois, R.L. & Switkes, E. (1988). Functional anatomy of macaque striate cortex. III. Color. Journal of Neuroscience 8(5), 15691593.CrossRefGoogle ScholarPubMed
Ts'o, D.Y. & Gilbert, C.D. (1988). The organization of chromatic and spatial interactions in the primate striate cortex. Journal of Neuroscience 8(5), 17121727.CrossRefGoogle ScholarPubMed
Ungerleider, L.G. & Mishkin, M. (1982). Two cortical visual systems. In Analysis of Visual behavior, ed. Ingle, D.J., Goodale, M.A. & Mansfield, R.J.W., pp. 549585. Cambridge, Massachusetts: MIT Press.Google Scholar
Vadrevu, V.L., Cavender, S. & Odom, J.V. (1992). Use of 10-Hz Hash visual evoked potentials in prediction of final visual acuity in diabetic eyes with vitreous hemorrhage. Documenta Ophthalmologica 79, 371382.CrossRefGoogle Scholar
Van Essen, D.C. & Maunsell, J.H.R. (1983). Hierarchical organization and functional streams in the visual cortex. Trends in Neuroscience 6, 370375.CrossRefGoogle Scholar
White, C.T., White, C.L. & Hintze, R.W. (1986). Temporal interactions among the color and pattern-specific components of the visual evoked potentials. HFSOL Technical Letter 71–86–04, Navy Personnel Research and Development Center, San Diego, California.Google Scholar