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Neural models and physiological reality

Published online by Cambridge University Press:  06 March 2008

BARRY B. LEE
BARRY B. LEE*
Affiliation:
SUNY College of Optometry, New York Max Planck Institute for Biophysical Chemistry, Göttingen, Germany
*
Address correspondence and reprint requests to: B.B. Lee, SUNY Optometry, 33 West 42nd Street, New York, NY 10036. E-mail: [email protected]
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Abstract

Neural models of retinal processing provide an important tool for analyzing retinal signals and their functional significance. However, it is here argued that in biological reality, retinal connectivity is unlikely to be as specific as ideal neural models might suggest. The retina is thought to provide functionally specific signals, but this specificity is unlikely to be anatomically complete. This is illustrated by examples of cone connectivity to macaque ganglion cells. For example, cells of the magnocellular pathway appear to avoid short-wavelength cone input, so that such input is negligible under normal conditions. However, there is anatomical, physiological, and psychophysical evidence that under special conditions, weak input may be revealed. Second, ideal models of how retinal information is centrally utilized have to take into account the biological reality of retinal signals. The stochastic nature of impulse trains modifies signal-to-noise ratio in unexpected ways. Also, non-linearities in cell responses make, for example, multiplexing of luminance and chromatic signals in the parvocellular pathway impracticable. The purpose of this analysis is to show than ideal neural models must confront an often more complex and nuanced physiological reality.

Keywords

Ganglion cellMagnocellularParvocellularMidget parasol
Type
Perspective
Information
Visual Neuroscience , Volume 25 , Issue 3 , May 2008 , pp. 231 - 241
Copyright
Copyright © Cambridge University Press 2008

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References

REFERENCES

Barlow, H.B. (1994). What is the computational goal of the neocortex? In Large Scale Neuronal Theories of the Brain, ed. Koch, C. & Davis, J.L.Cambridge: MIT Press.Google Scholar
Barlow, H.B. & Levick, W.R. (1969). Three factors limiting the reliable detection of light by retinal ganglion cells of the cat. Journal of Physiology 200, 1–24.Google Scholar
Baylor, D.A., Nunn, B.J. & Schnapf, J.L. (1987). Spectral sensitivity of cones of the monkey Macaca fascicularis. Journal of Physiology 390, 145–160.Google Scholar
Brindley, G.S. (1960). Physiology of the Retina and the Visual Pathway. London: Arnold.Google Scholar
Britten, K.H., Shadlen, M.N., Newsome, W.T. & Movshon, J.A. (1992). The analysis of visual motion: A comparison of neural and psychophysical performance. Journal of Neuroscience 12, 4745–4765.CrossRefGoogle Scholar
Buchsbaum, G. & Gottschalk, A. (1983). Trichromacy, opponent colours coding and optimum colour information transmission in the retina. Proceedings of the Royal Society of London B 220, 89–113.Google Scholar
Burns, B.D. (1968). The Uncertain Nervous System. London: Edward Arnold.Google Scholar
Buzas, P., Blessing, E.M., Szmadja, B.A. & Martin, P.R. (2006). Specificity of M and L cone inputs to receptive fields in the parvocellular pathway: Random wiring with functional bias. Journal of Neuroscience 26, 11148–11161.Google Scholar
Calkins, D.J. & Sterling, P. (1996). Absence of spectrally specific lateral inputs to midget ganglion cells in primate retina. Nature 381, 613–615.Google Scholar
Cavonius, C.R. & Robbins, D.O. (1973). Relationship between luminance and visual acuity of the rhesus monkey. Journal of Physiology 232, 501–511.Google Scholar
Chatterjee, S. & Callaway, E.M. (2002). S cone contributions to the magnocellular visual pathway in macaque monkey. Neuron 35, 1135–1146.Google Scholar
Croner, L.J. & Kaplan, E. (1995). Receptive fields of P and M ganglion cells across the primate retina. Vision Research 35, 7–24.Google Scholar
Crook, J.M., Lange-Malecki, B., Lee, B.B. & Valberg, A. (1988). Visual resolution of macaque retinal ganglion cells. Journal of Physiology 396, 205–224.CrossRefGoogle ScholarPubMed
Dacey, D.M. (1999). Primate retina: Cell types, circuits and color opponency. Progress in Retinal and Eye Research 18, 737–763.CrossRefGoogle Scholar
Dacey, D.M. & Lee, B.B. (1994). The ‘blue-on’ opponent pathway in primate retina originates from a distinct bistratified ganglion cell type. Nature 367, 731–735.Google Scholar
Dacey, D.M., Peterson, B.B. & Robinson, F.R. (2002). Identification of an S-cone opponent OFF pathway in the macaque retina: Morphology, physiology and possible circuitry. Investigative Ophthalmology and Visual Science 43, E-Abstract 2983.Google Scholar
de Monasterio, F.M. & Gouras, P. (1975). Functional properties of ganglion cells of the rhesus monkey retina. Journal of Physiology 251, 167–195.CrossRefGoogle Scholar
Derrington, A.M., Krauskopf, J. & Lennie, P. (1984). Chromatic mechanisms in lateral geniculate nucleus of macaque. Journal of Physiology 357, 241–265.Google Scholar
Derrington, A.M. & Lennie, P. (1984). Spatial and temporal contrast sensitivities of neurones in lateral geniculate nucleus of macaque. Journal of Physiology 357, 219–240.Google Scholar
Drasdo, N. (1989). Receptive field densities of the ganglion cells of the human retina. Vision Research 29, 985–988.Google Scholar
Dunn, F.A., Lankheet, M.J. & Rieke, F. (2007). Light adaptation in cone vision involves switching between receptor and post-receptor sites. Nature 449, 603–606.Google Scholar
Grünert, U., Greferath, U., Boycott, B.B. & Wässle, H. (1993). Parasol (Pa) ganglion cells of the primate fovea: Immunocytochemical staining with antibodies against GABAA-receptors. Vision Research 33, 1–14.Google Scholar
Hofer, H., Carroll, J., Neitz, J., Neitz, M. & williams, D.R. (2005). Organization of the human trichromatic cone mosaic. Journal of Neuroscience 25, 9669–9779.CrossRefGoogle Scholar
Ingling, C.R. & Martinez-Uriegas, E. (1983). The spatio-chromatic signal of the r-g channel. In Colour Vision: Physiology and Psychophysics, ed. Mollon, J. & Sharpe, L.T.London: Academic Press.Google Scholar
Johnson, E.N., Hawken, M.J. & Shapley, R. (2004). Cone inputs in macaque primary visual cortex. Journal of Neurophysiology 91, 2501–2514.Google Scholar
Kaiser, P.K., Lee, B.B., Martin, P.R. & Valberg, A. (1990). The physiological basis of the minimally distinct border demonstrated in the ganglion cells of the macaque retina. Journal of Physiology 422, 153–183.Google Scholar
Kingdom, F.A.A. (2003). Color brings relief to human vision. Nature Neuroscience 6, 641–644.CrossRefGoogle ScholarPubMed
Lee, B.B. (1991). On the relation between cellular sensitivity and psychophysical detection. In From Pigments to Perception, ed. Valberg, A. & Lee, B.B., pp. 105–115. London: Plenum Press.Google Scholar
Lee, B.B. (2003). Structure of receptive field centers of midget retinal ganglion cells. In Normal and Defective Color Vision, ed. Mollon, J.D., Knoblauch, K. & Pokorny, J., pp. 63–70. Oxford: Oxford University Press.Google Scholar
Lee, B.B., Kremers, J. & Yeh, T. (1998). Receptive fields of primate ganglion cells studied with a novel technique. Visual Neuroscience 15, 161–175.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. Journal of Physiology 404, 323–347.Google Scholar
Lee, B.B., Rüttiger, L. & Sun, H. (2005). Ganglion cell signals and mechanisms for the localization of moving targets. Perception 34, 975–981.Google Scholar
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 of the Royal Society B 230, 293–314.Google Scholar
Lee, B.B., Wehrhahn, C., Westheimer, G. & Kremers, J. (1993). Macaque ganglion cell responses to stimuli that elicit hyperacuity in man: Detection of small displacements. Journal of Neuroscience 13, 1001–1009.Google Scholar
Lee, B.B., Wehrhahn, C., Westheimer, G. & Kremers, J. (1995). The spatial precision of macaque ganglion cell responses in relation to vernier acuity of human observers. Vision Research 35, 2743–2758.Google Scholar
Lee, S.C. & Grünert, U. (2007). Connections of diffuse bipolar cells in primate retina are biased against S-cones. Journal of Comparative Neurology 502, 126–140.Google Scholar
Lennie, P. & D'Zmura, M.D. (1988). Mechanisms of color vision. CRC Critical Reviews in Neurobiology 3, 333–400.Google Scholar
Lennie, P., Haake, P.W. & Williams, D.R. (1991). The design of chromatically opponent receptive fields. In Computational Models of Visual Processing, ed. Landy, M.S. & Movshon, J.A., pp. 71–82. Cambridge: MIT Press.Google Scholar
Lennie, P., Krauskopf, J. & Sclar, G. (1990). Chromatic mechanisms in striate cortex of macaque. The Journal of Neuroscience 10, 649–669.Google Scholar
MacLeod, D.I.A. & van der Twer, T. (2003). The pleistochrome: Optimal opponent codes for natural colours. In Color Perception: Mind and the Physical World, ed. Mausfeld, R. & Heyer, D.Oxford: Oxford University Press.Google Scholar
Martin, P.R., Lee, B.B., White, A.J., Solomon, S.G. & Rüttiger, L. (2001). Chromatic sensitivity of ganglion cells in peripheral primate retina. Nature 410, 933–936.CrossRefGoogle Scholar
McMahon, M.J., Lankheet, M.J., Lennie, P. & Williams, D.R. (2000). Fine structure of parvocellular receptive fields in the primate fovea revealed by laser interferometry. Journal of Neuroscience 20, 2043–2053.Google Scholar
Merigan, W.H., Katz, L.M. & Maunsell, J.H.R. (1991). The effects of parvocellular lateral geniculate lesions on the acuity and contrast sensitivity of macaque monkeys. Journal of Neuroscience 11, 994–1001.Google Scholar
Mollon, J.D. (1991). Uses and evolutionary origins of primate color vision. In Evolution of the Eye and Visual System, vol. 2, ed. Cronly-Dillon, J.R. & Gregory, R.L., pp. 306–319. London: MacMillan.Google Scholar
Paulus, W. & Kröger-Paulus, A. (1983). A new concept of retinal colour coding. Vision Research 23, 529–540.CrossRefGoogle ScholarPubMed
Peichl, L. & Wassle, H. (1979). Size, scatter and coverage of ganglion cell receptive field centres in the cat retina. Journal of Physiology 291, 117–141.Google Scholar
Polyak, S.L. (1941). The Retina. Chicago: University of Chicago Press.Google Scholar
Reid, R.C. & Shapley, R.M. (1992). Spatial structure of cone inputs to receptive fields in primate lateral geniculate nucleus. Nature 356, 716–718.CrossRefGoogle ScholarPubMed
Reid, R.C. & Shapley, R.M. (2002). Space and time maps of cone photoreceptor signals in macaque lateral geniculate nucleus. Journal of Neuroscience 22, 6158–6175.Google Scholar
Rüttiger, L., Lee, B.B. & Sun, H. (2002). Transient cells can be neurometrically sustained: The positional accuracy of retinal signals to moving targets. Journal of Vision 2, 232–242.Google Scholar
Shapley, R. & Perry, V.H. (1986). Cat and monkey retinal ganglion cells and their visual functional roles. Trends in Neurosciences 9, 229–235.Google Scholar
Sholl, D. (1956). The Organization of the Cerebral Cortex. New York: Wiley.Google Scholar
Smith, V.C. & Pokorny, J. (1972). Spectral sensitivity of color-blind observers and the human cone photopigments. Vision Research 12, 2059.Google Scholar
Smith, V.C. & Pokorny, J. (1975). Spectral sensitivity of the foveal cone photo pigments between 400 and 500 nm. Vision Research 15, 161–171.Google Scholar
Solomon, S.G., Lee, B.B., White, A.J., Ruttiger, L. & Martin, P.R. (2005). Chromatic organization of ganglion cell receptive fields in the peripheral retina. Journal of Neuroscience 25, 4527–4539.Google Scholar
Stockman, A., MacLeod, D.I.A. & LeBrun, S.J. (1993). Faster than the eye can see: Blue cones respond to rapid flicker. Journal of the Optical Society of America A 10, 1396–1402.Google Scholar
Stromeyer, C.F., Lee, J. & Eskew, R.T. Jr. (1992). Peripheral chromatic sensitivity for flashes: A post-receptoral red-green asymmetry. Vision Research 32, 1865–1873.CrossRefGoogle Scholar
Sun, H. & Lee, B.B. (2004). A single mechanism for both luminance and chromatic grating vernier tasks: Evidence from temporal summation. Visual Neuroscience 21, 315–320.CrossRefGoogle ScholarPubMed
Sun, H., Lee, B.B. & Rüttiger, L. (2003). Coding of position of achromatic and chromatic edges by retinal ganglion cells. In Normal and Defective Colour Vision, ed. Mollon, J.D., Pokorny, J. & Knoblauch, K., pp. 79–87. Oxford: Oxford University Press.Google Scholar
Sun, H., Ruttiger, L. & Lee, B.B. (2004). The spatiotemporal precision of ganglion cell signals: A comparison of physiological and psychophysical performance with moving gratings. Vision Research 44, 19–33.Google Scholar
Sun, H., Smithson, H., Zaidi, Q. & Lee, B.B. (2006a). Do magnocellular and parvocellular ganglion cells avoid short-wavelength cone input. Visual Neuroscience 23, 323–330.Google Scholar
Sun, H., Smithson, H., Zaidi, Q. & Lee, B.B. (2006b). Specificity of cone inputs to macaque ganglion cells. Journal of Neurophysiology 95, 837–849.Google Scholar
Szmajda, B.A., Buzas, P., Fitzgibbon, T. & Martin, P.R. (2006). Geniculocortical relay of blue-off signals in the primate visual system. Proceedings of the National Academy of Science U.S.A. 103, 19512–19517.Google Scholar
Teller, D.Y. (1984). Linking propositions. Vision Research 24, 1233–1246.Google Scholar
Valberg, A., Lee, B.B., Kaiser, P.K. & Kremers, J. (1992). Responses of macaque ganglion cells to movement of chromatic borders. Journal of Physiology 458, 579–602.Google Scholar
van der Twer, T. & MacLeod, D.I. (2001). Optimal nonlinear codes for the perception of natural colors. Network 12, 395–407.CrossRefGoogle Scholar
Vorobyev, M. & Osorio, D. (1998). Receptor noise as a determinant of colour thresholds. Proceedings of the Royal Society B 265, 351–358.Google Scholar
Wässle, H. & Boycott, B.B. (1991). Functional architecture of the mammalian retina. Physiological Reviews 71, 447–480.CrossRefGoogle ScholarPubMed
Westheimer, G. & McKee, S.P. (1975). Visual acuity in the presence of retinal-image motion. Journal of the Optical Society of America 65, 847–850.Google Scholar
Yeh, T., Lee, B.B. & Kremers, J. (1995). The temporal response of ganglion cells of the macaque retina to cone-specific modulation. Journal of the Optical Society of America A 12, 456–464.Google Scholar