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Spatial sensitivity, responsivity, and surround suppression of LGN cell responses in the macaque

Published online by Cambridge University Press:  18 September 2013

THORSTEIN SEIM  and
ARNE VALBERG
THORSTEIN SEIM*
Affiliation:
MikroSens, Slependen, Norway
ARNE VALBERG*
Affiliation:
Norwegian University of Science and Technology, Institute of Physics, Trondheim, Norway
*
*Address correspondence to: Arne Valberg, Institute of Physics, Norwegian University of Science and Technology, N-7491 Trondheim, Norway. E-mail: thorstein.seim@gmail.com
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Abstract

Responses of cells in the lateral geniculate nucleus (LGN) of the macaque monkey have been measured for different sizes of chromatic and achromatic stimuli, with relative luminance spanning a range of 3–6 log units. Homogeneous illuminated test fields, centered on the receptive field, were used. Responses to these stimuli deviated from what is expected for the grating stimuli used to study the contrast-sensitive mechanisms in the visual pathway. For test fields smaller than the center of the receptive field, both the excitatory and the inhibitory cone-opponent components were present in the response, and the sensitivity to both components increased with the same factor when the test field increased in size (area summation). For test field areas extending into the suppressive surround of the extraclassical receptive field, the excitatory and the inhibitory cone opponents were both suppressed, again by the same factor. This suppression of the cell’s responsiveness, as a function of test spot area, was described by a logarithmic function, and the spatial sensitivity of attenuation could therefore be described by a power function of radius. The logarithmic suppression was clear for parvocellular and koniocellular cells but was more prominent for magnocellular cells. The surround field suppression was also found for the prepotential inputs to LGN cells, indicating a retinal origin. The difference of Gaussian (DOG) model has been used successfully to describe the cells’ contrast behavior for grating stimuli. However, this model fails to describe the constant excitatory/inhibitory response balance needed to obtain color (hue) stability for light stimuli of different sizes but with the same Commission Internationale de l’Eclairage (CIE) chromaticity and luminance factor. Neither the constant responsiveness found in the center of the receptive field nor the suppressive response in the surround can be described by the DOG model.

Keywords

LGN opponent cellsReceptive fieldsDOGSurround suppressionColor stability
Type
Research Article
Information
Visual Neuroscience , Volume 30 , Issue 4 , July 2013 , pp. 153 - 167
Copyright
Copyright © Cambridge University Press 2013 

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References

Alitto, H.J. & Usrey, W.M. (2008). Origin and dynamics of extraclassical suppression in the lateral geniculate nucleus of the macaque monkey. Neuron 57, 135–146.CrossRefGoogle ScholarPubMed
Allman, J., Miezin, F. & Mcguinnes, E. (1985). Stimulus specific responses from beyond the classical receptive field: Neurophysiological mechanisms for local-global comparisons in visual neurons. Annual Review of Neuroscience 8, 407–430.CrossRefGoogle ScholarPubMed
Babadi, B., Casti, A., Xiao, Y., Kaplan, E. & Paninski, L. (2010). A generalized linear model of the impact of direct and indirect inputs to the lateral geniculate nucleus. Journal of Vision 22, 1–14.Google Scholar
Barlow, H.B., Fitzhugh, R. & Kuffler, S.W. (1957). Change of organization in the receptive fields of the cat’s retina during dark adaptation. The Journal of Physiology 139, 338–354.CrossRefGoogle Scholar
Benardete, E.A. & Kaplan, E. (1999). The dynamics of primate M retinal ganglion cells. Visual Neuroscience 16, 355–368.CrossRefGoogle ScholarPubMed
Bonin, V., Mante, V. & Carandini, M. (2005). The suppressive field of neurons in lateral geniculate nucleus. The Journal of Neuroscience 23, 10844–10856.CrossRefGoogle Scholar
Camp, A.J., Tailby, C. & Solomon, S.G. (2009). Adaptable mechanisms that regulate the contrast response of neurons in the primate lateral geniculate nucleus. The Journal of Neuroscience 29, 5009–5021.CrossRefGoogle ScholarPubMed
Cavanaugh, J.R., Bair, W., & Movshon, J.A. (2002). Nature and interaction of signals from the receptive field center and surround in macaque V1 neurons. Journal of Neurophysiology 88, 2530–2546.CrossRefGoogle ScholarPubMed
Crook, J.D., Manookin, M.B., Packer, O.S. & Dacey, M.D. (2011). Horizontal cell feedback without cone type-selective inhibition mediates “red-green” colour opponency in midget ganglion cells of the primate retina. The Journal of Neuroscience 3, 1762–1772.CrossRefGoogle Scholar
Crook, J.M., Lange-Malecki, B., Lee, B.B. & Valberg, A. (1988). Visual resolution of macaque retinal ganglion cells. The Journal of Physiology 396, 205–224.CrossRefGoogle ScholarPubMed
Dacey, D., Packer, O.S., Diller, L., Brainard, D., Peterson, B. & Lee, B. (2000). Center surround receptive field structure of cone bipolar cells in primate retina. Vision Research 40, 1801–1811.CrossRefGoogle ScholarPubMed
De Monasterio, F.M. & Gouras, P. (1975). Functional properties of ganglion cells of the rhesus monkey retina. The Journal of Physiology 251, 167.CrossRefGoogle ScholarPubMed
Einevoll, G.T., Jurkus, P. & Heggelund, P. (2011). Coarse-to-fine changes of receptive fields in lateral geniculate nucleus have a transient and a sustained component that depend on distinct mechanisms. Plos One, 6, 1–19. www.plosone.org.CrossRefGoogle Scholar
Enroth-Cugell, C. & Robson, J. (1966). The contrast sensitivity of retinal ganglion cells of the cat. The Journal of Physiology 187, 517–552.CrossRefGoogle ScholarPubMed
Ghosh, K., Sarkar, S. & Bhaumik, H. (2005). A possible mechanism of zero-crossing detection using the concept of the extended classical receptive field of retinal ganglion cells. Biological Cybernetics 93, 1–5.CrossRefGoogle ScholarPubMed
Hartline, H.K. (1938). The response of single optic nerve fibers of the vertebrate eye to illumination of the retina. American Journal of Physiology 121, 400–415.CrossRefGoogle Scholar
Hawken, M.J. & Parker, A.J. (1990). Detection and discrimination mechanisms in the striate cortex of the Old-world Monkey. In Vision: Coding and Efficiency, ed. Blakemore, C., pp 103–116. Cambridge, UK: Cambridge UP.Google Scholar
Hubel, D.H. & Wiesel, T.N. (1961). Integrative action in the cat’s lateral geniculate body. The Journal of Physiology 155, 385–398.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
Krüger, J. & Fischer, B. (1973). Strong periphery effect in cat retinal ganglion cells. Excitatory responses in ON- and OFF-center neurons to single grid displacements. Experimental Brain Research 18, 316–318.CrossRefGoogle Scholar
Kuffler, S.W. (1953). Discharge patterns and functional organization of mammalian retina. Journal of Neurophysiology 16, 37–68.CrossRefGoogle ScholarPubMed
Lee, B.B., Martin, P.R. & Valberg, A. (1988). The physiological basis of heterochromatic flicker photometry demonstrated in the ganglion cells of the macaque retina. The Journal of Physiology 404, 323–347.CrossRefGoogle ScholarPubMed
Lee, B.B., Valberg, A., Tigwell, D.A. & Tryti, J. (1987). An account of responses of spectrally opponent neurons in macaque lateral geniculate nucleus to successive contrast. Proceedings. Biological sciences/The Royal Society 230, 293–314.Google ScholarPubMed
Lee, B.B., Virsu, V. & Creutzfeldt, O.D. (1983). Linear signal transmission from prepotentials to cells in the macaque lateral geniculate nucleus. Experimental Brain Research 52, 50–56.CrossRefGoogle ScholarPubMed
Levick, W.R., Cleland, B.G. & Dubin, M.W. (1972). Lateral geniculate neurons of cat: Retinal inputs and physiology. Investigative Ophthalmology 11, 302–311.Google ScholarPubMed
Linsenmeier, R.A., Frishman, L.J., Jakiela, H.G. & Enroth-Cugell, C. (1982). Receptive field properties of x and y cells in the cat retina derived from contrast sensitivity measurements. Vision Research 22, 1173–1183.CrossRefGoogle ScholarPubMed
McMahon, M.J., Packer, O.S. & Dacey, D.M. (2004). The classical receptive field surround of primate parasol ganglion cells is mediated primarily by a non-GABAergic pathway. The Journal of Neuroscience 24, 3736–3745.CrossRefGoogle ScholarPubMed
Packer, O.S. & Dacey, D.M. (2002). Receptive field structure of H1 horizontal cells in macaque monkey retina. Journal of Vision 2, 272–292.CrossRefGoogle ScholarPubMed
Peichl, L. & Wässle, H. (1979). Size, scatter and coverage of ganglion cell receptive field centres in the cat retina. The Journal of Physiology 291, 117–141.CrossRefGoogle ScholarPubMed
Rodieck, R.W.E. (1965). Quantitative analysis of cat retinal ganglion cell response to visual stimuli. Vision Research 5, 583–601.CrossRefGoogle ScholarPubMed
Ruksenas, O., Fjeld, I.T. & Heggelund, P. (2000). Spatial summation and center- surround antagonism in the receptive field of single units in the dorsal lateral geniculate nucleus of cat: Comparison with retinal input. Visual Neuroscience 17, 855–870.CrossRefGoogle ScholarPubMed
Seim, T., Valberg, A. & Lee, B.B. (2012). Visual signal processing in the macaque lateral geniculate nucleus. Visual Neuroscience 29, 105–117.CrossRefGoogle ScholarPubMed
Singer, W. & Creutzfeldt, O.D. (1970). Reciprocal lateral inhibition of On- and Off-center neurones in the lateral geniculate body of the cat. Experimental Brain Research 10, 311–330.CrossRefGoogle Scholar
Solomon, S.G, Lee, B.B. & Sun, H. (2006). Suppressive surrounds and contrast gain in magnocellular-pathway retinal ganglion cells of macaque. The Journal of Neuroscience 26, 8715–8726.CrossRefGoogle ScholarPubMed
Solomon, S.G., Peirce, J.W. & Lennie, P. (2004). The impact of suppressive surrounds on chromatic properties of cortical neurons. The Journal of Neuroscience 24, 148–160.CrossRefGoogle ScholarPubMed
Solomon, S.G., White, A.J.R. & Martin, P. (2002). Extraclassical receptive field properties of parvocellular, magnocellular, and koniocellular cells in the primate lateral geniculate nucleus. The Journal of Neuroscience 22, 338–349.CrossRefGoogle ScholarPubMed
Stockmann, A. & Sharpe, L. (2000). The spectral sensitivity of the middle- and long-wavelength sensitive cones derived from measurements in observers with known genotype. Vision Research 40, 1711–1737.CrossRefGoogle Scholar
Valberg, A., Lee, B.B., Creutzfeldt, O.D. & Tigwell, D.A. (1983). Luminance ratio and the spectral responsiveness of cells in the macaque lateral geniculate nucleus. In Colour Vision, ed. Mollon, J.D. & Sharpe, L.T., pp. 235–243. London, Academic Press.Google Scholar
Valberg, A., Lee, B.B., Tigwell, D.A. & Creutzfeldt, O.D. (1985). A simultaneous contrast effect of steady remote surrounds on responses of cells in macaque lateral geniculate nucleus. Experimental Brain Research 58, 604–608.CrossRefGoogle ScholarPubMed
Valberg, A., Lee, B.B. & Tryti, J. (1987). Simulation of responses of spectrally-opponent neurones in the macaque lateral geniculate nucleus to chromatic and achromatic light stimuli. Vision Research 27, 867–882.CrossRefGoogle ScholarPubMed
Valberg, A. & Seim, T. (2008). Neural mechanisms of chromatic and achromatic vision. Color Research & Application 33, 433–443.CrossRefGoogle Scholar
Valberg, A., Seim, T., Lee, B.B. & Tryti, J. (1986). Reconstruction of equidistant color space from responses of visual neurones of macaques. Journal of the Optical Society of America. A, Optics, Image Science, and Vision 3, 1726–1734.CrossRefGoogle ScholarPubMed
Valeton, J.M. & Van Norren, D. (1983). Light adaptation of primate cones: An analysis based on extracellular data. Vision Research 23, 1539–1547.CrossRefGoogle ScholarPubMed
Veruki, M.L. & Hartveit, E. (2002). AII (Rod) amacrine cells form a network of electrically coupled interneurons in the mammalian retina. Neuron 33, 935–946.CrossRefGoogle Scholar
Walker, G.A., Ohzawa, I. & Freeman, R.D. (2000). Suppression outside the classical cortical receptive field. Visual Neuroscience 17, 369–379.CrossRefGoogle ScholarPubMed
Watanabe, M. & Rodieck, R.W. (1989). Parasol and midget ganglion cells of the primate retina. The Journal of Comparative Neurology 289, 434–454.CrossRefGoogle ScholarPubMed
Webb, B.S., Tinsley, C.J., Vincent, J. & Derrington, A.M. (2005). Spatial distribution of suppressive signals outside the classical receptive field in lateral geniculate nucleus. Journal of Neurophysiology 94, 1789–1797.CrossRefGoogle ScholarPubMed
Wiesel, T.N. & Hubel, D.H. (1966). Spatial and chromatic interactions in the lateral geniculate body of the rhesus monkey. Journal of Neurophysiology 29, 1115–1156.CrossRefGoogle ScholarPubMed