Normalization Models Applied to Orientation Masking in the Human Infant

Human infants can discriminate the orientation of lines within the first week after birth (Atkinson et al., 1988; Slater et al., 1988) but have immature orientation-selective pattern masking until after 6 months of age (Morrone and Burr, 1986). Here the development of orientation processing is further examined using a visual-evoked potential paradigm and normalization models of pattern masking. Contrast response functions were measured for 1 cycle per degree (cpd) gratings, counterphase-reversed in contrast at either 3.3 or 5.5 Hz. A second 1 cpd, 20% contrast, 8.3 Hz grating of either the same or orthogonal orientation was added as a mask. Evoked responses associated with the test grating, the mask, and intermodulation between the two were individually extracted using spectral analysis of the scalp-recorded EEG. Adults exhibited orientation selectivity in the masking of their test component responses and in nonlinear intermodulation between the test and mask stimuli. Infants <5 months old, however, demonstrated nonselective masking or a reversed selectivity in their responses to the test component, with adult-like orientation selectivity in their intermodulation responses. Within the context of a normalization model of pattern masking, the results are consistent with the existence of oriented filters early in life the responses of which are normalized immaturely until ∼5 months of age.

[1]  D. Burr,et al.  Functional implications of cross-orientation inhibition of cortical visual cells. I. Neurophysiological evidence , 1982, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[2]  D. G. Albrecht,et al.  Visual cortex neurons in monkeys and cats: Detection, discrimination, and identification , 1997, Visual Neuroscience.

[3]  C. Blakemore,et al.  Innate and environmental factors in the development of the kitten's visual cortex. , 1975, The Journal of physiology.

[4]  Hugh R. Wilson,et al.  Development of spatiotemporal mechanisms in infant vision , 1988, Vision Research.

[5]  J. Movshon,et al.  Spatial summation in the receptive fields of simple cells in the cat's striate cortex. , 1978, The Journal of physiology.

[6]  A. B. Bonds.  Development of Orientation Tuning in the Visual Cortex of Kittens , 1979 .

[7]  K. Obermayer,et al.  Organization of ocular dominance and orientation columns in the striate cortex of neonatal macaque monkeys , 1995, Visual Neuroscience.

[8]  D. Hubel,et al.  Ordered arrangement of orientation columns in monkeys lacking visual experience , 1974, The Journal of comparative neurology.

[9]  D. Regan,et al.  Objective evidence for phase-independent spatial frequency analysis in the human visual pathway , 1988, Vision Research.

[10]  A. Norcia,et al.  An adaptive filter for steady-state evoked responses. , 1995, Electroencephalography and clinical neurophysiology.

[11]  J. M. Foley,et al.  Human luminance pattern-vision mechanisms: masking experiments require a new model. , 1994, Journal of the Optical Society of America. A, Optics, image science, and vision.

[12]  D. Regan,et al.  Nonlinearity in human visual responses to two-dimensional patterns, and a limitation of fourier methods , 1987, Vision Research.

[13]  A. B. Bonds.  Role of Inhibition in the Specification of Orientation Selectivity of Cells in the Cat Striate Cortex , 1989, Visual Neuroscience.

[14]  D. Heeger,et al.  Comparison of contrast-normalization and threshold models of the responses of simple cells in cat striate cortex , 1997, Visual Neuroscience.

[15]  H. Wilson,et al.  Orientation bandwidths of spatial mechanisms measured by masking. , 1984, Journal of the Optical Society of America. A, Optics and image science.

[16]  D. Heeger.  Half-squaring in responses of cat striate cells , 1992, Visual Neuroscience.

[17]  D. G. Albrecht,et al.  Motion selectivity and the contrast-response function of simple cells in the visual cortex , 1991, Visual Neuroscience.

[18]  John M. Foley,et al.  Analysis of the effect of pattern adaptation on pattern pedestal effects: A two-process model , 1997, Vision Research.

[19]  R. Shapley,et al.  Directional selectivity and spatiotemporal structure of receptive fields of simple cells in cat striate cortex. , 1991, Journal of neurophysiology.

[20]  J. Movshon,et al.  Linearity and Normalization in Simple Cells of the Macaque Primary Visual Cortex , 1997, The Journal of Neuroscience.

[21]  F. Campbell,et al.  Electrophysiological evidence for the existence of orientation and size detectors in the human visual system , 1970, The Journal of physiology.

[22]  R. L. Valois,et al.  The orientation and direction selectivity of cells in macaque visual cortex , 1982, Vision Research.

[23]  K. Albus,et al.  Early post‐natal development of neuronal function in the kitten's visual cortex: a laminar analysis. , 1984, The Journal of physiology.

[24]  R. Shapley,et al.  Linear mechanisms of directional selectivity in simple cells of cat striate cortex. , 1987, Proceedings of the National Academy of Sciences of the United States of America.

[25]  I. Bodis-Wollner,et al.  VEPs in humans reveal high and low spatial contrast mechanisms. , 1984, Investigative ophthalmology & visual science.

[26]  J. Nelson,et al.  The assessment of evoked potential contrast thresholds using real-time retrieval. , 1984, Investigative ophthalmology & visual science.

[27]  A. Slater,et al.  Orientation Discrimination and Cortical Function in the Human Newborn , 1988, Perception.

[28]  A. Norcia,et al.  Spatial frequency sweep VEP: Visual acuity during the first year of life , 1985, Vision Research.

[29]  Anthony M. Norcia,et al.  Development of contrast sensitivity in the human infant , 1990, Vision Research.

[30]  D. Ferster,et al.  Direction selectivity of synaptic potentials in simple cells of the cat visual cortex. , 1997, Journal of neurophysiology.

[31]  D. Burr,et al.  Development of visual inhibitory interactions in kittens , 1991, Visual Neuroscience.

[32]  G. J. Burton,et al.  Evidence for non-linear response processes in the human visual system from measurements on the thresholds of spatial beat frequencies. , 1973, Vision research.

[33]  D. Hubel,et al.  The development of ocular dominance columns in normal and visually deprived monkeys , 1980, The Journal of comparative neurology.

[34]  H C Howland,et al.  Infant astigmatism measured by photorefraction. , 1978, Science.

[35]  Denis G. Pelli,et al.  Accurate control of contrast on microcomputer displays , 1991, Vision Research.

[36]  F. Campbell,et al.  Orientational selectivity of the human visual system , 1966, The Journal of physiology.

[37]  J. M. Foley,et al.  Temporal sensitivity of human luminance pattern mechanisms determined by masking with temporally modulated stimuli , 1999, Vision Research.

[38]  M C Morrone,et al.  Inhibitory interactions in the human vision system revealed in pattern‐evoked potentials. , 1987, The Journal of physiology.

[39]  P. Heggelund,et al.  Development of spatial receptive-field organization and orientation selectivity in kitten striate cortex. , 1985, Journal of neurophysiology.

[40]  M. Stryker,et al.  Quantitative study of cortical orientation selectivity in visually inexperienced kitten. , 1976, Journal of neurophysiology.

[41]  Daphne Maurer,et al.  The discrimination of orientation by young infants , 1980, Vision Research.

[42]  O. Braddick,et al.  Orientation- and motion-selective mechanisms in infants , 1993 .

[43]  P. Schiller,et al.  Quantitative studies of single-cell properties in monkey striate cortex. II. Orientation specificity and ocular dominance. , 1976, Journal of neurophysiology.

[44]  Y. Chino,et al.  Postnatal Development of Binocular Disparity Sensitivity in Neurons of the Primate Visual Cortex , 1997, The Journal of Neuroscience.

[45]  J. Victor,et al.  A new statistic for steady-state evoked potentials. , 1991, Electroencephalography and clinical neurophysiology.

[46]  J. Kulikowski,et al.  VEPs and contrast , 1983, Vision Research.

[47]  R Held,et al.  Astigmatism in infants. , 1978, Science.

[48]  Michael S. Landy,et al.  Nonlinear Model of Neural Responses in Cat Visual Cortex , 1991 .

[49]  R. Manny.  Orientation selectivity of 3-month-old infants , 1992, Vision Research.

[50]  K. Nakayama,et al.  Steady state visual evoked potentials in the alert primate , 1982, Vision Research.

[51]  J. P. Thomas,et al.  Neural recoding in human pattern vision: model and mechanisms , 1999, Vision Research.

[52]  Anthony M. Norcia,et al.  Measurement of spatial contrast sensitivity with the swept contrast VEP , 1989, Vision Research.

[53]  J. M. Foley,et al.  Contrast masking in human vision. , 1980, Journal of the Optical Society of America.

[54]  K. Miller,et al.  Correlation-Based Development of Ocularly Matched Orientation and Ocular Dominance Maps: Determination of Required Input Activities , 1998, The Journal of Neuroscience.

[55]  J. Atkinson,et al.  Development of Orientation Discrimination in Infancy , 1988, Perception.

[56]  R D Freeman,et al.  Development of inhibitory mechanisms in the kitten's visual cortex , 1996, Visual Neuroscience.

[57]  David C. Burr,et al.  Evidence for the existence and development of visual inhibition in humans , 1986, Nature.