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Objective assessment of chromatic and achromatic pattern adaptation reveals the temporal response properties of different visual pathways

Published online by Cambridge University Press:  04 December 2012

ANTHONY G. ROBSON  and
JANUS J. KULIKOWSKI
ANTHONY G. ROBSON*
Affiliation:
Department of Electrophysiology, Moorfields Eye Hospital, London, UK Institute of Ophthalmology, University College London, London, UK
JANUS J. KULIKOWSKI
Affiliation:
Faculty of Life Sciences, Manchester, University of Manchester, UK
*
*Address correspondence and reprint requests to: Dr. Anthony G. Robson, Department of Electrophysiology, Moorfields Eye Hospital, 162 City Road, London, EC1V 2PD, UK. E-mail: [email protected]
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Abstract

The aim was to investigate the temporal response properties of magnocellular, parvocellular, and koniocellular visual pathways using increment/decrement changes in contrast to elicit visual evoked potentials (VEPs). Static achromatic and isoluminant chromatic gratings were generated on a monitor. Chromatic gratings were modulated along red/green (R/G) or subject-specific tritanopic confusion axes, established using a minimum distinct border criterion. Isoluminance was determined using minimum flicker photometry. Achromatic and chromatic VEPs were recorded to contrast increments and decrements of 0.1 or 0.2 superimposed on the static gratings (masking contrast 0–0.6). Achromatic increment/decrement changes in contrast evoked a percept of apparent motion when the spatial frequency was low; VEPs to such stimuli were positive in polarity and largely unaffected by high levels of static contrast, consistent with transient response mechanisms. VEPs to finer achromatic gratings showed marked attenuation as static contrast was increased. Chromatic VEPs to R/G or tritan chromatic contrast increments were of negative polarity and showed progressive attenuation as static contrast was increased, in keeping with increasing desensitization of the sustained responses of the color-opponent visual pathways. Chromatic contrast decrement VEPs were of positive polarity and less sensitive to pattern adaptation. The relative contribution of sustained/transient mechanisms to achromatic processing is spatial frequency dependent. Chromatic contrast increment VEPs reflect the sustained temporal response properties of parvocellular and koniocellular pathways. Cortical VEPs can provide an objective measure of pattern adaptation and can be used to probe the temporal response characteristics of different visual pathways.

Keywords

Visual evoked potentialColor visionKoniocellularParvocellularMagnocellular
Type
Review Articles
Information
Visual Neuroscience , Volume 29 , Issue 6 , November 2012 , pp. 301 - 313
Copyright
Copyright © Cambridge University Press 2012

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References

Arden, G.B., Gunduz, K. & Perry, S. (1988). Colour vision testing with a computer graphics system. Clinical Vision Sciences 2, 303–320.Google Scholar
Barbur, J.L., Konstantakopoulou, E., Rodriguez-Carmona, M., Harlow, J.A., Robson, A.G. & Moreland, J.D. (2010). The Macular Assessment Profile test - a new VDU-based technique for measuring the spatial distribution of the macular pigment, lens density and rapid flicker sensitivity. Ophthalmic and Physiological Optics 30, 470–483.CrossRefGoogle Scholar
Bedford, R.E. & Wyszecki, G. (1957). Axial chromatic aberration of the human eye. Journal of the Optical Society of America 47, 564–565.CrossRefGoogle ScholarPubMed
Berninger, T.A. & Arden, G.B. (1991). Visual evoked cortical potential with chromatic stimuli. In Principles and Practice of Clinical Electrophysiology of Vision, ed. Heckinlively, J.R. & Arden, G.B., pp. 147–150. St Louis, MO: Mosby Year Book.Google Scholar
Berninger, T.A., Arden, G.B., Hogg, C.R. & Frumkes, T. (1989). Separable evoked retinal and cortical potentials from each major visual pathway: Preliminary results. The British Journal of Ophthalmology 73, 502–511.CrossRefGoogle ScholarPubMed
Binnie, C.D., Rowan, A.J. & Gutter, T.H. (1982). A Manual of Electro-encephalographic Technology. Cambridge, UK: Cambridge University Press.Google Scholar
Blakemore, C. & Campbell, F.W. (1969). On the existence of neurons in the visual system selectively sensitive to the orientation and size of retinal images. The Journal of Physiology 203, 237–260.CrossRefGoogle Scholar
Bodis-Wollner, I., Hendley, C.D. & Kulikowski, J.J. (1972). Electrophysiological and psychophysical responses to modulation of contrast of a grating pattern. Perception 1, 341–349.CrossRefGoogle ScholarPubMed
Boynton, R.N. (1978). Ten years of research with the minimally distinct border. In Visual Psychophysics and Physiology, ed. Armington, J.C., Krauskopf, J. & Wooten, B.R., pp. 193–208. London: Academic Press.CrossRefGoogle Scholar
Bradley, A., Switkes, E. & DeValois, K.K. (1988). Orientation and spatial frequency selectivity of adaptation to colour and luminance gratings. Vision Research 28, 841–856.CrossRefGoogle ScholarPubMed
Campbell, F.W. & Kulikowski, J.J. (1966). Orientational selectivity of the human visual system. The Journal of Physiology 187, 437–445.CrossRefGoogle ScholarPubMed
Campbell, F.W. & Kulikowski, J.J. (1971). An electrophysiological measure of the psychophysical threshold. The Journal of Physiology 217, 54P–55P.Google Scholar
Campbell, F.W. & Maffei, L. (1970). Electrophysiological evidence of the existence of orientation and size detectors in the human visual system. The Journal of Physiology 207, 635–652.CrossRefGoogle ScholarPubMed
Campbell, F.W. & Robson, J.G. (1968). Application of Fourier Analysis to the visibility of gratings. The Journal of Physiology 207, 635–652.CrossRefGoogle Scholar
Carden, D., Kulikowski, J.J., Murray, I.J. & Parry, N.R.A. (1985). Human occipital potentials evoked by the onset of equiluminant chromatic gratings. The Journal of Physiology 369, P44.Google Scholar
Cavanagh, P. & Anstis, S. (1991). The contribution of colour motion in normal and colour deficient observers. Vision Research 31, 2109–2148.CrossRefGoogle Scholar
Charman, W.N. (1991). Limits on the visual performance set by eye’s optics and the retinal cone mosaic. In Limits of Vision, ed. Kulikowski, J.J., Walsh, V. & Murray, I.J., pp. 81–96. Basingstoke, UK: Macmillan.Google Scholar
Crognale, M.A., Rabin, E., Switkes, E. & Adams, A.J. (1993). Selective loss of S-pathway sensitivity in central serous choroidopathy revealed by spatio-chromatic visual evoked cortical potentials. In Colour Vision Deficiencies, ed. Drum, B.Dordrecht, The Netherlands: Kluwer.Google Scholar
Degli-Esposti, S., Egan, C., Bunce, C., Moreland, J.D., Bird, A.C. & Robson, A.G. (2012). Macular pigment parameters in patients with macular telangiectasia (MacTel) and normal subjects: Implications of a novel analysis. Investigative Ophthalmology and Visual Science 53, 6568–6575.CrossRefGoogle ScholarPubMed
Dreher, B., Fukada, Y. & Rodieck, R.W. (1976). Identification, classification and anatomical segregation of cells with X-like and Y-like properties in the LGN of old world primates. The Journal of Physiology 258, 433–453.CrossRefGoogle Scholar
D’Souza, D.V., Auer, T., Strasburger, H., Frahm, J. & Lee, B.B. (2011). Temporal frequency and chromatic processing in humans: An fMRI study of the cortical visual areas. Journal of Vision 11, 1–17.Google ScholarPubMed
Eisner, A. & Macleod, D.I.A. (1980). Blue sensitive cones do not contribute to luminance. Journal of the Optical Society of America 70, 121–123.CrossRefGoogle Scholar
Enroth-Cugell, C. & Robson, J.G. (1966). The contrast sensitivity of retinal ganglion cells of the cat. The Journal of Physiology 187, 517–522.CrossRefGoogle ScholarPubMed
Flitcroft, D.I. (1989). The interactions between chromatic aberration, defocus and stimulus chromaticity: Implications for visual physiology and colorimetry. Vision Research 29, 349–360.CrossRefGoogle ScholarPubMed
Gomes, B.D., Souza, G.S., Rodrigues, A.R., Saito, C.A., Silveira, L.C. & da Silva Filho, M. (2006). Normal and dichromatic color discrimination measured with transient visual evoked potential. Visual Neuroscience 23, 617–627.CrossRefGoogle ScholarPubMed
Gomes, B.D., Souza, G.S., Saito, C.A., da Silva Filho, M., Rodrigues, A.R., Ventura, D.F. & Silveira, L.C. (2010). Cone contrast influence on components of the pattern onset/offset VECP. Ophthalmic and Physiological Optics 30, 518–524.CrossRefGoogle ScholarPubMed
Gouras, P. (1968). Identification of cone mechanisms in monkey ganglion cells. The Journal of Physiology 199, 533–537.CrossRefGoogle ScholarPubMed
Grigsby, S.S., Vingrys, A.J., Benes, S.C. & King-Smith, P.E. (1991). Correlation of chromatic, spatial, and temporal sensitivity in optic nerve disease. Investigative Ophthalmology and Visual Science 32, 3252–3262.Google ScholarPubMed
Hicks, T.P., Lee, B.B. & Vidyasagar, T.R. (1983). The responses of cells in the macaque lateral geniculate nucleus to sinusoidal gratings. The Journal of Physiology 337, 183–200.CrossRefGoogle ScholarPubMed
Hubel, D.H. & Wiesel, T.N. (1962). Receptive fields, binocular interaction and functional architecture in the cat’s visual cortex. The Journal of Physiology 160, 106–154.CrossRefGoogle ScholarPubMed
Jasper, H.H. (1958). Report of the committee on methods of clinical examination in electroencephalography. Electroencephalography and Clinical Neurophysiology 10, 370–375.Google Scholar
Johnson, E.N., Hawken, M.J. & Shapley, R. (2001). The spatial transformation of color in the primary visual cortex of the macaque monkey. Nature Neuroscience 4, 409–416.CrossRefGoogle ScholarPubMed
Kaplan, E. & Shapley, R.M. (1982). X and Y cells in the lateral geniculate nucleus of macaque monkeys. The Journal of Physiology 330, 125–143.CrossRefGoogle ScholarPubMed
Kulikowski, J.J. (1969). Limiting conditions of visual perception. Prace Instytutu Automatyki 77. Warsaw, Poland. English translation 1973.Google Scholar
Kulikowski, J.J. (1971). Effect of eye movements on the contrast sensitivity of spatio-temporal patterns. Vision Research 11, 261–273.CrossRefGoogle ScholarPubMed
Kulikowski, J.J. (1974). Human averaged occipital potentials evoked by pattern and movement. The Journal of Physiology 242, 70P–71P.Google ScholarPubMed
Kulikowski, J.J. (1978). Pattern and movement detection in man and rabbit: Separation and comparison of occipital potentials. Vision Research 18, 183–189.CrossRefGoogle ScholarPubMed
Kulikowski, J.J. (1991). On the nature of visual evoked potentials, unit responses and psychophysics. In From Pigments to Perception: Advances in Understanding Visual Processes, ed. Valberg, A. & Lee, B.B., pp. 197–209. New York: Plenum Press.CrossRefGoogle Scholar
Kulikowski, J.J. & Carden, D. (1989). Scalp VEPs to chromatic and achromatic gratings in macaques with ablated visual area 4. In Seeing Contour and Colour, ed. Kulikowski, J.J., Dickinson, C.M. & Murray, I.J., pp. 586–590. Oxford, UK: Pergamon Press.Google Scholar
Kulikowski, J.J. & Gorea, A. (1978). Complete adaptation to pattern stimuli; a necessary and sufficient condition for Weber’s law for contrast. Vision Research 18, 1223–1227.CrossRefGoogle ScholarPubMed
Kulikowski, J.J. & Kozak, W.H.H. (1967). ERG visual evoked response and pattern detection in man. In Advances in Electrophysiology and Pathology of the Visual System, ed. Schmoger, E.ISCERG Symposium VI, pp. 186–192. Leipzig, Germany: Thieme.Google Scholar
Kulikowski, J.J. & Kranda, K. (1977). Detection of coarse patterns with minimum contribution from rods. Vision Research 17, 653–656.CrossRefGoogle ScholarPubMed
Kulikowski, J.J., McKeefry, D.J. & Robson, A.G. (1997). Selective stimulation of colour mechanisms: An empirical perspective. Spatial Vision 10, 379–402.Google ScholarPubMed
Kulikowski, J.J., Murray, I.J. & Parry, N.R.A. (1989). Electrophysiological correlates of chromatic opponent and achromatic stimulation in man. In Colour Vision Deficiencies IX, ed. Drum, B. & Verriest, G., pp. 145–153. Dordrecht, The Netherlands: Kluwer Academic Publishers.CrossRefGoogle Scholar
Kulikowski, J.J. & Parry, N.R.A. (1987). Human occipital potentials evoked by achromatic or chromatic checkerboards and gratings. The Journal of Physiology 388, 45P.Google Scholar
Kulikowski, J.J., Robson, A.G. & McKeefry, D.J. (1996). Specificity and selectivity of chromatic visual evoked potentials. Vision Research 36, 3397–3401.CrossRefGoogle ScholarPubMed
Kulikowski, J.J., Robson, A.G. & Murray, I.J. (2002). Scalp VEPs and intra-cortical responses to chromatic and achromatic stimuli in primates. Documenta Ophthalmologica 105, 243–279.CrossRefGoogle ScholarPubMed
Kulikowski, J.J. & Tolhurst, D.J. (1973). Psychophysical evidence for sustained and transient detectors in human vision. The Journal of Physiology 232, 149–162.CrossRefGoogle ScholarPubMed
Kulikowski, J.J. & Walsh, V. (1993). Colour vision: Isolating mechanisms in overlapping streams. Progress in Brain Research 95, 417–426.CrossRefGoogle ScholarPubMed
Lee, B.B., Martin, P.R. & Valberg, A. (1989). Nonlinear summation of M- and L-cone inputs to phasic retinal ganglion cells of the macaque. The Journal of Neuroscience 9, 1433–1442.CrossRefGoogle ScholarPubMed
Legge, G.E. & Foley, J.M. (1980). Contrast masking in human vision. Journal of the Optical Society of America 70, 1458–1471.CrossRefGoogle ScholarPubMed
Lund, J.S., Wu, Q., Hardingham, P.T. & Levitt, J.B. (1995). Cells and circuits contributing to functional properties in area V1 of macaque monkey cerebral cortex. Journal of Anatomy 187, 563–581.Google ScholarPubMed
McKeefry, D.J., Russell, M.H.A., Murray, I.J. & Kulikowski, J.J. (1996). Amplitude and phase variations of harmonic components in human achromatic and chromatic VEPs. Visual Neuroscience 13, 639–653.CrossRefGoogle Scholar
Mihaylova, M., Stomonyakov, V. & Vassilev, A. (1999). Peripheral and central delay in processing high spatial frequencies: Reaction time and VEP latency studies. Vision Research 39, 699–706.CrossRefGoogle ScholarPubMed
Mollon, J.D. & Polden, P.G. (1977). Saturation of a retinal cone mechanism. Nature 265, 243–246.CrossRefGoogle ScholarPubMed
Moreland, J.D. & Bhatt, P. (1984). Retinal distribution of retinal pigment. Documenta Ophthalmologica. Proceedings Series 39, 127–132.CrossRefGoogle Scholar
Moreland, J.D., Robson, A.G., Soto-Leon, N. & Kulikowski, J.J. (1998). Macular pigment and the colour-specificity of visual evoked potentials. Vision Research 38, 3241–3245.CrossRefGoogle ScholarPubMed
Murray, I.J., Daugirdiene, A., Vaitkevicius, H., Kulikowski, J.J. & Stanikunas, R. (2006). Almost complete colour constancy achieved with full-field adaptation. Vision Research 46, 3067–3078.CrossRefGoogle ScholarPubMed
Murray, I.J., Parry, N.R.A., Carden, D. & Kulikowski, J.J. (1987). Human visual evoked potentials to chromatic and achromatic gratings. Clinical Vision Sciences 1, 231–244.Google Scholar
Parry, N.R.A., Kulikowski, J.J., Murray, J.J., Kranda, K. & Ott, H. (1988). Visual evoked potentials and reaction times to chromatic and achromatic stimulation. In Psychopharmacology and Reaction Time, ed. Hindmarch, I., Aufdembrinke, B. & Ott, H., pp. 155–176. New York: Wiley.Google Scholar
Parry, N.R.A. & Murray, I.J. (1997). In John Dalton’s Colour Vision Legacy, ed. Dickinson, C.M., Murray, I.J. & Carden, D., pp. 115–123. London: Taylor and Francis.Google Scholar
Parry, N.R.A., Murray, I.J. & Kulikowski, J.J. (1987). VEPs to chromatic stimulation: Comparison of normal and colour defectives. Electroencephalography and Clinical Neurophysiology 67, 75P.Google Scholar
Parry, N.R.A. & Robson, A.G. (2012). Optimisation of large field tritan stimuli using concentric isoluminant annuli. Journal of Vision 12 (12):11, 1–13, http://www.journalofvision.org/content/12/12/11, doi:10.1167/12.12.11.CrossRefGoogle Scholar
Plant, G.T., Zimmern, R.L. & Durden, K. (1983). Transient visually evoked potentials and onset of sinusoidal gratings. Electroencephalography and Clinical Neurophysiology 56, 47–58.CrossRefGoogle ScholarPubMed
Porciatti, V. & Sartucci, F. (1999). Normative data for onset VEPs to red-green and blue-yellow chromatic contrast. Clinical Neurophysiology 110, 772–781.CrossRefGoogle ScholarPubMed
Previc, F.H. (1986). Visual evoked potentials to luminance and chromatic contrast in rhesus monkeys. Vision Research 26, 1897–1907.CrossRefGoogle ScholarPubMed
Rabin, J., Switkes, E., Crognale, M., Schneck, M.E. & Adams, A.J. (1994). Visual evoked potentials in three-dimensional colour space: Correlates of spatio-chromatic processing. Vision Research 34, 2657–2671.CrossRefGoogle ScholarPubMed
Regan, D. (1968). A high frequency mechanism which underlies visual evoked potentials. Electroencephalography and Clinical Neurophysiology 25, 231–237.CrossRefGoogle ScholarPubMed
Robson, A.G., Holder, G.E., Moreland, J.D. & Kulikowski, J.J. (2006). Chromatic VEP assessment of human macular pigment: Comparison with minimum motion and minimum flicker profiles. Visual Neuroscience 23, 275–283.CrossRefGoogle ScholarPubMed
Robson, A.G. & Kulikowski, J.J. (1995). Verification of VEPs elicited by gratings containing tritanopic pairs of hues. The Journal of Physiology 475, 22P.Google Scholar
Robson, A.G. & Kulikowski, J.J. (1998). Objective specification of tritanopic confusion lines using visual evoked potentials. Vision Research 38, 3499–3503.CrossRefGoogle ScholarPubMed
Robson, A.G. & Kulikowski, J.J. (2001). The effects of chromatic and achromatic pattern adaption on VEPs. Colour Research and Application Supplement volume 26, 133–135.Google Scholar
Robson, A.G., Kulikowski, J.J., Korostenskaja, M., Neveu, M., Hogg, C.R. & Holder, G.E. (2003 a). Integration times reveal mechanisms responding to isoluminant chromatic gratings: A two-centre Visual Evoked Potential study. In Normal and Defective Colour Vision, ed. Mollon, J.D., Pokorny, J. & Knoblauch, K., pp. 130–137. Oxford, UK: Oxford University Press.CrossRefGoogle Scholar
Robson, A.G., McKeefry, D.J. & Kulikowski, J.J. (1997). Visual evoked potentials: Special requirements for blue. In John Dalton’s Colour Vision Legacy, ed. Dickinson, C.M., Murray, I.J. & Carden, D., pp. 115–123. London: Taylor and Francis.Google Scholar
Robson, A.G., Moreland, J.D., Pauleikhoff, D., Morrissey, T., Holder, G.E., Fitzke, F.W., Bird, A.C. & van Kuijk, F.J. (2003 b). Macular pigment density and distribution: Comparison of fundus autofluorescence with minimum motion photometry. Vision Research 43, 1765–1775.CrossRefGoogle ScholarPubMed
Robson, A.G. & Parry, N.R. (2008). Measurement of macular pigment optical density and distribution using the steady-state visual evoked potential. Visual Neuroscience 25, 575–583.CrossRefGoogle ScholarPubMed
Russell, M.H.A., Kulikowski, J.J. & Murray, I.J. (1987). Spatial frequency dependence of the human evoked potential. In Evoked Potentials III, ed. Barber, C. & Blum, T., pp. 231–239. London: Butterworths PublicationsGoogle Scholar
Schiller, P.H. & Colby, C.L. (1983). The responses of single cells in the LGN of the rhesus monkey to colour and luminance contrast. Vision Research 23, 1631–1641.CrossRefGoogle ScholarPubMed
Spekreijse, H., van Der Tweel, L.H. & Zuidema, T.H. (1973). Contrast evoked responses in man. Vision Research 13, 1577–1601.CrossRefGoogle ScholarPubMed
Suttle, C.M. & Harding, G.F.A. (1999). Morphology of transient VEPs to luminance and chromatic pattern onset and offset. Vision Research 39, 1577–1584.CrossRefGoogle ScholarPubMed
Switkes, E., Crognale, M., Rabin, J., Schneck, M.E. & Adams, A.J. (1996). Reply to “Specificity and selectivity of chromatic visual evoked potentials”. Vision Research 36, 3403–3405.Google Scholar
Switkes, E., Bradley, A. & DeValois, K.K. (1988). Contrast dependence and mechanisms of masking interactions among chromatic and luminance gratings. Journal of the Optical Society of America A, Optics and Image Science 5, 1149–1162.CrossRefGoogle ScholarPubMed
Tansley, B.W. & Boynton, R.M. (1978). Chromatic border perception: The role of red- and green-sensitive cones. Vision Research 18, 683–697.CrossRefGoogle ScholarPubMed
Tekavčič Pompe, M., Stirn Kranjc, B. & Brecelj, J. (2010). Chromatic VEP in children with congenital colour vision deficiency. Ophthalmic and Physiological Optics 30, 693–698.CrossRefGoogle ScholarPubMed
Tolhurst, D.J. (1972). Adaptation to square-wave gratings: Inhibition between spatial frequency channels in the human visual system. The Journal of Physiology 226, 231–248.CrossRefGoogle ScholarPubMed
van der Tweel, L.H. (1964). Relation between psychophysics and electrophysiology of flicker. Documenta Ophthalmologica. Advances in Ophthalmology 18, 287–304.CrossRefGoogle ScholarPubMed
Vidyasagar, T.R., Kulikowski, J.J., Lipnicki, D.M. & Dreher, B. (2002). Convergence of parvocellular and magnocellular information channels in the primary visual cortex of the macaque. The European Journal of Neuroscience 16, 945–956.CrossRefGoogle ScholarPubMed
Vidyasagar, T.R., Kulikowski, J.J., Robson, A.G. & Dreher, B. (1998). Responses of V1 cells in primate reveal excitatory convergence of P and M channels. The European Journal of Neuroscience 10, S239.Google Scholar
Weigelt, S., Muckli, L. & Kohler, A. (2008). Functional magnetic resonance imaging in visual neuroscience. Reviews in the Neurosciences 19, 363–380.CrossRefGoogle ScholarPubMed
White, A.J.R., Wilder, H.D., Goodchild, A.K., Sefton, J. & Martin, P.R. (1998). Segregation of receptive field properties in the lateral geniculate nucleus of a new-world monkey, the marmoset Callithrix jacchus. Journal of Neurophysiology 80, 2063–2076.CrossRefGoogle ScholarPubMed
Zeki, S.M. (1974). Functional organization of a visual area in the posterior bank of the superior temporal sulcus of the rhesus monkey. The Journal of Physiology 236, 549–573.CrossRefGoogle ScholarPubMed
Zeki, S., Watson, J.D., Lueck, C.J., Friston, K.J., Kennard, C. & Frackowiak, R.S. (1991). A direct demonstration of functional specialization in human visual cortex. The Journal of Neuroscience 11, 641–649.CrossRefGoogle ScholarPubMed