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Contrast adaptation in striate cortical neurons of the nocturnal primate bush baby (Galago crassicaudatus)

Published online by Cambridge University Press:  02 June 2009

John D. Allison ,
Vivien A. Casagrande ,
Edward J. Debruyn  and
A. B. Bonds
John D. Allison
Affiliation:
Department of Cell Biology, Vanderbilt University, Nashville
Vivien A. Casagrande
Affiliation:
Department of Cell Biology, Vanderbilt University, Nashville Department of Psychology, Vanderbilt University, Nashville
Edward J. Debruyn
Affiliation:
Department of Electrical Engineering, Vanderbilt University, Nashville
A. B. Bonds
Affiliation:
Department of Electrical Engineering, Vanderbilt University, Nashville
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Abstract

It has been argued that in order for the visual system to detect edges accurately under a range of conditions, the visual system needs to adapt to the local contrast level to preserve sensitivity (Blakemore & Campbell, 1969). Cells in the primary visual cortex of cats adapt to stimuli with low to moderate contrast. Curiously, macaque monkey neurons in primary visual cortex (V1) do not show evidence for similar adaptation. To address the question of whether this differential sensitivity in contrast adaptation might be due to phylogenetic variation between cats and primates or to specializations for visual niche (e.g. nocturnal vs. diurnal), contrast adaptation to temporally and spatially optimized gratings was examined in 30 V1 cells of three nocturnal primate bush babies (Galago crassicaudatus). A second objective was to examine the relationship between the degree of contrast adaptation and cell classification or cell location relative to cortical layers or compartments [i.e. cytochrome-oxidase (CO) blobs and interblobs]. All cells were classified (simple vs. complex) and anatomically localized relative to cortical layers and cytochrome-oxidase (CO) blob and interblob compartments. Two independent measures of contrast adaptation were used. In the first test, contrast was sequentially increased from 3–56% and then decreased. The contrast required to maintain a half-maximum response amplitude in the 30 cells tested increased an average of 0.24 (±0.12) log units during the sequential decrements in contrast. For the second test, four sets of five interleaved contrasts within ±1 octave of a central adapting contrast (10%, 14%, 20%, and 28%, respectively) were presented. The cells produced a mean adaptation index of 0.57 (±0.47) which is very similar to that exhibited by cat cortical neurons (0.54 ± 0.41). Interestingly, cells in interblobs showed a trend toward greater adaptation than did blob cells. Moreover, cells in the supragranular layers exhibited greater adaptation than cells in the infragranular layers. No significant differences in adaptation were found to correlate with other cell classification indices. Taken together, our results suggest that contrast adaptation may be more important for maintaining sensitivity in nocturnal species (primates or cats) than in diurnal species (macaque monkeys), and that in the nocturnal bush baby, cells in cortical layers and compartments may be differentially specialized for contrast adaptation.

Keywords

Primary visual cortexContrast gain controlDynamic hysteresisAdaptation indexCytochrome-oxidase blobs
Type
Research Articles
Information
Visual Neuroscience , Volume 10 , Issue 6 , November 1993 , pp. 1129 - 1139
Copyright
Copyright © Cambridge University Press 1993

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References

Albrecht, D.G. & Hamilton, D.B. (1982). Striate cortex of monkey and cat: Contrast-response function. Journal of Neurophysiology 48, 217–237.CrossRefGoogle ScholarPubMed
Albrecht, D.G., Farrar, S.B. & Hamilton, D.B. (1984). Spatial contrast adaptation characteristics of neurones recorded in the cat's visual cortex. Journal of Physiology 347, 713–739.CrossRefGoogle ScholarPubMed
Barlow, H.B., Macleod, D.I.A. & Van Meeteren, A. (1976). Adaptation to gratings: No compensatory advantages found. Vision Research 16, 1043–1045.CrossRefGoogle Scholar
Blakemore, C. & Campbell, F.W. (1969). On the existence of neurones in the human visual system selectively sensitive to the orientation and size of retinal images. Journal of Physiology 203, 237–260.CrossRefGoogle Scholar
Blasdel, G.G. & Lund, J.S. (1983). Termination of afferent axons in macaque striate cortex. Journal of Neuroscience 3, 1389–1413.CrossRefGoogle ScholarPubMed
Bobak, P., Bodis-Wollner, I. & Marx, M.S. (1988). Cortical contrastgain control in human spatial vision. Journal of Physiology 405, 421–437.CrossRefGoogle Scholar
Bonds, A.B. (1991). Temporal dynamics of contrast gain in single cells of the cat striate cortex. Visual Neuroscience 6, 239–255.CrossRefGoogle ScholarPubMed
Bonds, A.B., Casagrande, V.A., Norton, T.T. & DeBruyn, E.J. (1987). Visual resolution and sensitivity in a nocturnal primate (Galago) measured with visual evoked potentials. Vision Research 27, 845–857.CrossRefGoogle Scholar
Born, R.T. & Tootell, R.B. (1991). Spatial-frequency tuning of single units in macaque supragranular striate cortex. Proceeding of the National Academy of Sciences of the U.S.A. 88, 7066–7070.CrossRefGoogle ScholarPubMed
Casagrande, V.A. & DeBruyn, E.J. (1982). The galago visual system: Aspects of normal organization and developmental plasticity. In The Lesser Bushbaby as an Animal Model: Selected Topics, ed. Haines, D.E., pp. 137–167. Boca Raton, Florida: CRC Press.Google Scholar
Condo, G.J. & Casagrande, V.A. (1990). Organization of cytochrome-oxidase staining in the visual cortex of nocturnal primates (Galago crassicaudatus and Galago senegalensis): I. Adult patterns. Journal of Comparative Neurology 293, 632–645.CrossRefGoogle ScholarPubMed
Connolly, M. & Van Essen, D. (1984). The representation of the visual field in parvocellular and magnocellular layers of the lateral genic-ulate nucleus in the macaque monkey. Journal of Comparative Neurology 226, 544–564.CrossRefGoogle Scholar
DeBruyn, E.J. & Bonds, A.B. (1986). Contrast adaptation in the cat is not mediated by GABA. Brain Research 383, 339–342.CrossRefGoogle Scholar
DeBruyn, E.J., Casagrande, V.A., Beck, P.D. & Bonds, A.B. (1993). Visual resolution and sensitivity of single cells in the primary visual cortex (VI) of a nocturnal primate (Bush Baby): Correlation with cortical layers and cytochrome-oxidase patterns. Journal of Neurophysiology 69, 3–18.CrossRefGoogle ScholarPubMed
Florence, S.L. & Casagrande, V.A. (1987). Organization of individual afferent axons in layer IV of striate cortex in a primate. Journal of Neuroscience 7, 3850–3868.CrossRefGoogle ScholarPubMed
Georgeson, M.A. (1985). The effect of spatial adaptation on perceived contrast. Spatial Vision 1, 103–112.CrossRefGoogle ScholarPubMed
Greenlee, M.W. & Heitger, F. (1988). The functional role of contrast adaptation. Vision Research 28, 791–797.CrossRefGoogle ScholarPubMed
Hawken, M.J. & Parker, A.J. (1984). Contrast sensitivity and orientation selectivity in lamina IV of the striate cortex of Old World monkeys. Experimental Brain Research 54, 367–372.CrossRefGoogle ScholarPubMed
Hubel, D.H. & Wiesel, T.N. (1962). Receptive fields, binocular interactions and functional architecture in the cat's visual cortex. Journal of Physiology (London) 160, 106–154.CrossRefGoogle ScholarPubMed
Hubel, D.H. & Livingstone, M.S. (1990). Color and contrast sensitivity in the lateral geniculate body and primary visual cortex of the macaque monkey. Journal of Neuroscience 10, 2223–2237.CrossRefGoogle ScholarPubMed
Irvin, G.E., Casagrande, V.A. & Norton, T.T. (1993). Center/surround relationships of magnocellular, parvocellular, and koniocellular relay cells in primate lateral geniculate nucleus. Visual Neuroscience 10, 363–373.CrossRefGoogle ScholarPubMed
Lachica, E.A., Beck, P.D. & Casagrande, V.A. (1992). Parallel pathways in macaque monkey striate cortex. Anatomically defined columns in layer III. Proceedings of the National Academy of Sciences of the U.S.A. 89, 3566–3570.CrossRefGoogle ScholarPubMed
Lachica, E.A. & Casagrande, V.A. (1992). Direct W-like geniculate projections to the cytochrome-oxidase (CO) blobs in primate visual cortex: Axon morphology. Journal of Comparative Neurology 319, 141–159.CrossRefGoogle Scholar
Lachica, E.A., Beck, P.D. & Casagrande, V.A. (1993). Intrinsic connections of layer III of striate cortex in squirrel monkey and bush baby: Correlation with patterns of cytochrome oxidase. Journal of Comparative Neurology 329, 163–187.CrossRefGoogle ScholarPubMed
Langston, A., Casagrande, V.A. & Fox, R. (1986). Spatial resolution of the galago. Vision Research 26, 791–796.CrossRefGoogle ScholarPubMed
Legge, G.E. (1981). A power law for contrast discrimination. Vision Research 21, 457–467.CrossRefGoogle Scholar
Levick, W.R. (1972). Another tungsten microelectrode. Medical and Biological Engineering 10, 510–515.CrossRefGoogle ScholarPubMed
Maattanen, L.M. & Koenderink, J.J. (1991). Contrast adaptation and contrast-gain control. Experimental Brain Research 87, 205–212.CrossRefGoogle ScholarPubMed
Norton, T.T., Casagrande, V.A., Irvin, G.E., Sesma, M.A. & Petry, H.M. (1988). Contrast-sensitivity functions of W-, X-, and Y-like relay cells in the lateral geniculate nucleus of Bush Baby, Galago crassicaudatus. Journal of Neurophysiology 59, 1639–1656.CrossRefGoogle Scholar
Ohzawa, I., Sclar, G. & Freeman, R.D. (1982). Contrast-gain control in the cat visual cortex. Nature 298, 266–268.CrossRefGoogle ScholarPubMed
Ohzawa, L., Sclar, G. & Freeman, R.D. (1985). Contrast-gain control in the cat's visual system. Journal of Neurophysiology 54, 651–667.CrossRefGoogle ScholarPubMed
Sclar, G., Lennie, P. & DePriest, D. (1989). Contrast adaptation in striate cortex of macaque. Vision Research 29, 747–756.CrossRefGoogle ScholarPubMed
Sclar, G., Maunsell, J.H.R. & Lennle, P. (1990). Coding of image contrast in central visual pathways of the Macaque monkey. Vision Research 30, 1–10.CrossRefGoogle ScholarPubMed
Silverman, M.S., Grosof, D.H., DeValois, R.L. & Elfar, S.D. (1989). Spatial-frequency organization in primate striate cortex. Proceeding of the National Academy of Sciences of the U.S.A. 86, 711–715.CrossRefGoogle ScholarPubMed
Skotton, B., DeValois, R.L., Grosof, D.H., Movshon, J.A., Albrecht, D.G. & Bonds, A.B. (1991). Classifying simple and complex cells on the basis of response modulation. Vision Research 31, 1079–1086.Google Scholar
Tootell, R.B.H., Silverman, M.S., Hamilton, S.L., DeValois, R.L. & Switkes, E. (1988). Function anatomy of macaque striate cortex. III. Color. Journal of Neuroscience 8, 1559–1593.Google ScholarPubMed
Weller, R.E. & Kaas, J.H. (1982). The organization of the visual system in Galago: Comparisons with monkeys. In The Lesser Bush-baby (Galago) as an Animal Model: Selected Topics, ed. Haines, D.E., pp. 107–135. Boca Raton, Florida: CRC Press.Google Scholar
Wong-Riley, M. (1979). Changes in the visual system of monocularly sutured or enucleated cats demonstrable with cytochrome-oxidase histochemistry. Brain Research 171, 11–28.CrossRefGoogle ScholarPubMed