Neural Basis of Vision

The neural basis of vision is examined from the point of view of the anatomical organization of the primate visual system and the responses of single neurons. The recent developments of imaging studies in humans are also examined. The chapter opens with a section on the receptive field of visual neurons, from the historical definition to modern concepts. The following section is devoted to the various representations of receptive fields parameters: retinotopic and nonretinotopic maps in various structures of the visual system. The third section is a description of the anatomical and functional organization of the primate visual system, with a special emphasis on the different cortical areas, their roles, and their interactions. The fourth section is devoted to the analysis of the relationship between visual perception and the responses of single units in nonhuman primates. The last section addresses a number of unanswered or rarely addressed issues in animal studies, such as the neural basis of consciousness and mental representations, the importance of visual exploration of the environment, the neural basis of 3D vision, and the role of feedback connections. Keywords: cortical map; functional architecture; neuroanatomy; neurophysiology; receptive field; visual cortex

[1]  R. Tootell,et al.  Where is 'dorsal V4' in human visual cortex? Retinotopic, topographic and functional evidence. , 2001, Cerebral cortex.

[2]  J. Bullier,et al.  Visual latencies in areas V1 and V2 of the macaque monkey , 1995, Visual Neuroscience.

[3]  W. Newsome,et al.  Microstimulation in visual area MT: effects on direction discrimination performance , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[4]  Jean Bullier,et al.  The Timing of Information Transfer in the Visual System , 1997 .

[5]  M. Stryker,et al.  Relation of cortical cell orientation selectivity to alignment of receptive fields of the geniculocortical afferents that arborize within a single orientation column in ferret visual cortex , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[6]  H. Sakata,et al.  Selectivity for the shape, size, and orientation of objects for grasping in neurons of monkey parietal area AIP. , 2000, Journal of neurophysiology.

[7]  G. Blasdel,et al.  Differential imaging of ocular dominance and orientation selectivity in monkey striate cortex , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[8]  G. Orban,et al.  Three-Dimensional Shape Coding in Inferior Temporal Cortex , 2000, Neuron.

[9]  K. Rockland,et al.  Convergence and branching patterns of round, type 2 corticopulvinar axons , 1998, The Journal of comparative neurology.

[10]  R. Vautin,et al.  Magnification factor and receptive field size in foveal striate cortex of the monkey , 2004, Experimental Brain Research.

[11]  John H. R. Maunsell,et al.  How parallel are the primate visual pathways? , 1993, Annual review of neuroscience.

[12]  Hong Zhou,et al.  Representation of stereoscopic edges in monkey visual cortex , 2000, Vision Research.

[13]  A. Parker,et al.  Sense and the single neuron: probing the physiology of perception. , 1998, Annual review of neuroscience.

[14]  H. K. Hartline,et al.  THE RECEPTIVE FIELDS OF OPTIC NERVE FIBERS , 1940 .

[15]  J. Maunsell,et al.  Neuronal correlates of inferred motion in primate posterior parietal cortex , 1995, Nature.

[16]  David L. Sheinberg,et al.  Noticing Familiar Objects in Real World Scenes: The Role of Temporal Cortical Neurons in Natural Vision , 2001, The Journal of Neuroscience.

[17]  R. Malach,et al.  Object-related activity revealed by functional magnetic resonance imaging in human occipital cortex. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[18]  W. Newsome,et al.  Deciding about motion: linking perception to action , 1997, Journal of Comparative Physiology A.

[19]  J. M. Hupé,et al.  Cortical feedback improves discrimination between figure and background by V1, V2 and V3 neurons , 1998, Nature.

[20]  W. Pohl,et al.  Dissociation of spatial discrimination deficits following frontal and parietal lesions in monkeys. , 1973, Journal of comparative and physiological psychology.

[21]  M. Arbib,et al.  Grasping objects: the cortical mechanisms of visuomotor transformation , 1995, Trends in Neurosciences.

[22]  J. Kaas,et al.  Do superior colliculus projection zones in the inferior pulvinar project to MT in primates? , 1999, The European journal of neuroscience.

[23]  D. Hubel,et al.  Anatomy and physiology of a color system in the primate visual cortex , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[24]  Jean Bullier,et al.  Reversible deactivation of cerebral network components , 1996, Trends in Neurosciences.

[25]  I. Ohzawa,et al.  Asymmetric Suppression Outside the Classical Receptive Field of the Visual Cortex , 1999, The Journal of Neuroscience.

[26]  J. Kaas Theories of Visual Cortex Organization in Primates , 1997 .

[27]  N. Logothetis,et al.  Neurophysiological investigation of the basis of the fMRI signal , 2001, Nature.

[28]  Carl R Olson,et al.  Object-based vision and attention in primates , 2001, Current Opinion in Neurobiology.

[29]  A. Dale,et al.  Functional analysis of primary visual cortex (V1) in humans. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[30]  I. Ohzawa,et al.  Spatiotemporal organization of simple-cell receptive fields in the cat's striate cortex. II. Linearity of temporal and spatial summation. , 1993, Journal of neurophysiology.

[31]  S. Petersen,et al.  Direction-specific adaptation in area MT of the owl monkey , 1985, Brain Research.

[32]  R. von der Heydt,et al.  Mechanisms of contour perception in monkey visual cortex. II. Contours bridging gaps , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[33]  R. W. Rodieck Quantitative analysis of cat retinal ganglion cell response to visual stimuli. , 1965, Vision research.

[34]  T. Albright Direction and orientation selectivity of neurons in visual area MT of the macaque. , 1984, Journal of neurophysiology.

[35]  S. Zeki Functional specialisation in the visual cortex of the rhesus monkey , 1978, Nature.

[36]  R Vogels,et al.  Responses of monkey inferior temporal neurons to luminance-, motion-, and texture-defined gratings. , 1995, Journal of neurophysiology.

[37]  C. Koch,et al.  Are we aware of neural activity in primary visual cortex? , 1995, Nature.

[38]  I. Ohzawa,et al.  Spatiotemporal organization of simple-cell receptive fields in the cat's striate cortex. I. General characteristics and postnatal development. , 1993, Journal of neurophysiology.

[39]  M. Desmurget,et al.  An ‘automatic pilot’ for the hand in human posterior parietal cortex: toward reinterpreting optic ataxia , 2000, Nature Neuroscience.

[40]  H. Sakata,et al.  Parietal neurons represent surface orientation from the gradient of binocular disparity. , 2000, Journal of neurophysiology.

[41]  S. Petersen,et al.  The pulvinar and visual salience , 1992, Trends in Neurosciences.

[42]  P. H. Schiller,et al.  The effects of V4 and middle temporal (MT) area lesions on visual performance in the rhesus monkey , 1993, Visual Neuroscience.

[43]  A. Dale,et al.  New images from human visual cortex , 1996, Trends in Neurosciences.

[44]  B. Boycott,et al.  Functional architecture of the mammalian retina. , 1991, Physiological reviews.

[45]  A. Dale,et al.  Functional Analysis of V3A and Related Areas in Human Visual Cortex , 1997, The Journal of Neuroscience.

[46]  D. Hubel,et al.  Receptive fields, binocular interaction and functional architecture in the cat's visual cortex , 1962, The Journal of physiology.

[47]  G. Glover,et al.  Retinotopic organization in human visual cortex and the spatial precision of functional MRI. , 1997, Cerebral cortex.

[48]  J R Duhamel,et al.  The updating of the representation of visual space in parietal cortex by intended eye movements. , 1992, Science.

[49]  K. Hoffmann,et al.  Synchronization of Neuronal Activity during Stimulus Expectation in a Direction Discrimination Task , 1997, The Journal of Neuroscience.

[50]  J. Bakin,et al.  Visual Responses in Monkey Areas V1 and V2 to Three-Dimensional Surface Configurations , 2000, The Journal of Neuroscience.

[51]  W. Newsome,et al.  A selective impairment of motion perception following lesions of the middle temporal visual area (MT) , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[52]  R. Desimone,et al.  Responses of Neurons in Inferior Temporal Cortex during Memory- Guided Visual Search , 1998 .

[53]  A. Dale,et al.  Visual motion aftereffect in human cortical area MT revealed by functional magnetic resonance imaging , 1995, Nature.

[54]  P. H. Schiller Effect of lesions in visual cortical area V4 on the recognition of transformed objects , 1995, Nature.

[55]  M. Cynader,et al.  Direction-selective adaptation in simple and complex cells in cat striate cortex. , 1988, Journal of neurophysiology.

[56]  S. W. Kuffler Discharge patterns and functional organization of mammalian retina. , 1953, Journal of neurophysiology.

[57]  Jean Bullier,et al.  The Role of Area 17 in the Transfer of Information to Extrastriate Visual Cortex , 1994 .

[58]  N. Logothetis,et al.  Neuronal correlates of subjective visual perception. , 1989, Science.

[59]  J. Bullier,et al.  The role of feedback connections in shaping the responses of visual cortical neurons. , 2001, Progress in brain research.

[60]  R. Desimone,et al.  Modulation of Oscillatory Neuronal Synchronization by Selective Visual Attention , 2001, Science.

[61]  J. Kaas,et al.  The organization of the second visual area (V II) in the owl monkey: a second order transformation of the visual hemifield. , 1974, Brain research.

[62]  R. von der Heydt,et al.  Illusory contours and cortical neuron responses. , 1984, Science.

[63]  P. O. Bishop,et al.  Orientation specificity and response variability of cells in the striate cortex. , 1973, Vision research.

[64]  C. Gilbert,et al.  Axonal sprouting accompanies functional reorganization in adult cat striate cortex , 1994, Nature.

[65]  D. B. Bender,et al.  Visual properties of neurons in inferotemporal cortex of the Macaque. , 1972, Journal of neurophysiology.

[66]  E. Callaway Local circuits in primary visual cortex of the macaque monkey. , 1998, Annual review of neuroscience.

[67]  Y. Frégnac,et al.  Visual input evokes transient and strong shunting inhibition in visual cortical neurons , 1998, Nature.

[68]  R. von der Heydt,et al.  Mechanisms of contour perception in monkey visual cortex. I. Lines of pattern discontinuity , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[69]  S. Engel,et al.  Colour tuning in human visual cortex measured with functional magnetic resonance imaging , 1997, Nature.

[70]  C. Gilbert,et al.  Learning to see: experience and attention in primary visual cortex , 2001, Nature Neuroscience.

[71]  R. Desimone,et al.  Neural Mechanisms of Visual Working Memory in Prefrontal Cortex of the Macaque , 1996, The Journal of Neuroscience.

[72]  Keiji Tanaka,et al.  Inferotemporal cortex and object vision. , 1996, Annual review of neuroscience.

[73]  D. Ts'o,et al.  Visual topography in primate V2: multiple representation across functional stripes , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[74]  V. Lamme,et al.  The distinct modes of vision offered by feedforward and recurrent processing , 2000, Trends in Neurosciences.

[75]  Leslie G. Ungerleider,et al.  Microsaccadic eye movements and firing of single cells in the striate cortex of macaque monkeys , 2000, Nature Neuroscience.

[76]  M Dojat,et al.  Moving illusory contours activate primary visual cortex: an fMRI study. , 2000, Cerebral cortex.

[77]  E. J. Tehovnik,et al.  Eye Movements Modulate Visual Receptive Fields of V4 Neurons , 2001, Neuron.

[78]  J. Bullier Integrated model of visual processing , 2001, Brain Research Reviews.

[79]  G. DeAngelis,et al.  Cortical area MT and the perception of stereoscopic depth , 1998, Nature.

[80]  P. O. Bishop,et al.  Receptive fields of simple cells in the cat striate cortex , 1973, The Journal of physiology.

[81]  M. Segraves,et al.  Primate frontal eye field activity during natural scanning eye movements. , 1994, Journal of neurophysiology.

[82]  Jeffrey D. Schall,et al.  Neural basis of deciding, choosing and acting , 2001, Nature Reviews Neuroscience.

[83]  G. Poggio,et al.  Binocular interaction and depth sensitivity in striate and prestriate cortex of behaving rhesus monkey. , 1977, Journal of neurophysiology.

[84]  John H. R. Maunsell,et al.  Hierarchical organization and functional streams in the visual cortex , 1983, Trends in Neurosciences.

[85]  M. Rosa Visuotopic Organization of Primate Extrastriate Cortex , 1997 .

[86]  A. Sillito The contribution of inhibitory mechanisms to the receptive field properties of neurones in the striate cortex of the cat. , 1975, The Journal of physiology.

[87]  J. Kaas,et al.  Reorganization of retinotopic cortical maps in adult mammals after lesions of the retina. , 1990, Science.

[88]  J. Kaas,et al.  The reorganization of somatosensory cortex following peripheral nerve damage in adult and developing mammals. , 1983, Annual review of neuroscience.

[89]  Y. Miyashita Inferior temporal cortex: where visual perception meets memory. , 1993, Annual review of neuroscience.

[90]  M. Perenin,et al.  Discrimination of motion direction in perimetrically blind fields. , 1991, Neuroreport.

[91]  R. Guillery,et al.  On the actions that one nerve cell can have on another: distinguishing "drivers" from "modulators". , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[92]  N. Logothetis,et al.  Psychophysical and physiological evidence for viewer-centered object representations in the primate. , 1995, Cerebral cortex.

[93]  C. Koch,et al.  Neuronal connections underlying orientation selectivity in cat visual cortex , 1987, Trends in Neurosciences.

[94]  R. Desimone,et al.  Columnar organization of directionally selective cells in visual area MT of the macaque. , 1984, Journal of neurophysiology.

[95]  U. Eysel,et al.  GABA-induced inactivation of functionally characterized sites in cat striate cortex: Effects on orientation tuning and direction selectivity , 1997, Visual Neuroscience.

[96]  D J Felleman,et al.  Modular Organization of Occipito-Temporal Pathways: Cortical Connections between Visual Area 4 and Visual Area 2 and Posterior Inferotemporal Ventral Area in Macaque Monkeys , 1997, The Journal of Neuroscience.

[97]  D. Hubel,et al.  Microsaccadic eye movements and firing of single cells in the striate cortex of macaque monkeys , 2000, Nature Neuroscience.

[98]  Yoichi Sugita,et al.  Grouping of image fragments in primary visual cortex , 1999, Nature.

[99]  R O Duncan,et al.  Occlusion and the Interpretation of Visual Motion: Perceptual and Neuronal Effects of Context , 2000, The Journal of Neuroscience.

[100]  D. J. Felleman,et al.  Distributed hierarchical processing in the primate cerebral cortex. , 1991, Cerebral cortex.

[101]  M. Goldberg,et al.  The representation of visual salience in monkey parietal cortex , 1998, Nature.

[102]  J. Movshon,et al.  The analysis of visual motion: a comparison of neuronal and psychophysical performance , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[103]  S. Thorpe,et al.  Neural processing of stereopsis as a function of viewing distance in primate visual cortical area V1 , 1996 .

[104]  David J. Calkins,et al.  Evidence that Circuits for Spatial and Color Vision Segregate at the First Retinal Synapse , 1999, Neuron.

[105]  Andrew J. Parker,et al.  Local Disparity Not Perceived Depth Is Signaled by Binocular Neurons in Cortical Area V1 of the Macaque , 2000, The Journal of Neuroscience.

[106]  J. Lund,et al.  Anatomical organization of macaque monkey striate visual cortex. , 1988, Annual review of neuroscience.

[107]  DH Hubel,et al.  Segregation of form, color, and stereopsis in primate area 18 , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[108]  S. Sherman Tonic and burst firing: dual modes of thalamocortical relay , 2001, Trends in Neurosciences.

[109]  W. Singer Synchronization of cortical activity and its putative role in information processing and learning. , 1993, Annual review of physiology.

[110]  J. Malpeli,et al.  Cat medial interlaminar nucleus: retinotopy, relation to tapetum and implications for scotopic vision. , 1984, Journal of neurophysiology.

[111]  S. Celebrini,et al.  Gaze direction controls response gain in primary visual-cortex neurons , 1999, Nature.

[112]  David J. Freedman,et al.  Categorical representation of visual stimuli in the primate prefrontal cortex. , 2001, Science.

[113]  David L. Sheinberg,et al.  The role of temporal cortical areas in perceptual organization. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[114]  N. Logothetis,et al.  Shape representation in the inferior temporal cortex of monkeys , 1995, Current Biology.

[115]  G. Orban,et al.  Practising orientation identification improves orientation coding in V1 neurons , 2001, Nature.

[116]  P A Salin,et al.  Corticocortical connections in the visual system: structure and function. , 1995, Physiological reviews.

[117]  A. Goodchild,et al.  Segregation of receptive field properties in the lateral geniculate nucleus of a New-World monkey, the marmoset Callithrix jacchus. , 1998, Journal of neurophysiology.

[118]  D. Fitzpatrick,et al.  A systematic map of direction preference in primary visual cortex , 1996, Nature.

[119]  Catherine Tallon-Baudry,et al.  Induced γ-Band Activity during the Delay of a Visual Short-Term Memory Task in Humans , 1998, The Journal of Neuroscience.