Visual properties of neurons in area V4 of the macaque: sensitivity to stimulus form.

Area V4, a visuotopically organized area in prestriate cortex of the macaque, is the major source of visual input to the inferior temporal cortex, known to be crucial for object recognition. To examine the selectivity of cells in V4 for stimulus form, we quantitatively measured the responses of 322 cells to bars varying in length, width, orientation, and polarity of contrast, and sinusoidal gratings varying in spatial frequency, phase, orientation, and overall size. All of the cells recorded in V4 were located on the lower portion of the prelunate gyrus. Receptive fields were located almost exclusively within the representation of the central 5 degrees of the lower visual field, and receptive field size, in linear dimension, was 4-7 times greater than that in the corresponding representation of striate cortex (V1). Nearly all receptive fields consisted of overlapping dark and light zones, like "classic" complex fields in V1, but the relative strengths of the dark and light zones often differed. A few cells responded exclusively to light or dark stimuli. Many cells in V4 were selective for stimulus orientation, and a few were selective for direction of motion as well. Although the median orientation bandwidth of the orientation-selective cells (52 degrees) was wider than that reported for oriented cells in V1, approximately 8% of the oriented cells had bandwidths of less than 30 degrees, which is nearly as narrow as the most narrowly tuned cells in V1. The proportion of cells selective for direction of motion (13%) was not markedly different from that reported in V1. The large majority of V4 cells were tuned to the length and width of bars, and the "shape" of the optimal bar varied from cell to cell, as has been reported for cells in the dorsolateral visual area (DL) of the owl monkey, a possible homologue of V4 in the macaque. Preferred lengths and widths varied independently from approximately 0.05 to 6 degrees, with the smallest preferred bars about the size of the smallest receptive fields in V1 and the largest preferred bars larger than any fields in V1. The relationship between the size of the optimal bar and the size of the receptive field varied from cell to cell. Some cells, for example, responded best to bars much narrower or shorter than the field, whereas other cells responded best to bars that filled (but did not extend beyond) the excitatory field in the length, width, or both dimensions.(ABSTRACT TRUNCATED AT 400 WORDS)

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

[2]  D H HUBEL,et al.  RECEPTIVE FIELDS AND FUNCTIONAL ARCHITECTURE IN TWO NONSTRIATE VISUAL AREAS (18 AND 19) OF THE CAT. , 1965, Journal of neurophysiology.

[3]  D. Hubel,et al.  Receptive fields and functional architecture of monkey striate cortex , 1968, The Journal of physiology.

[4]  S. Zeki Cortical projections from two prestriate areas in the monkey. , 1971, Brain research.

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

[6]  S. Zeki,et al.  Colour coding in rhesus monkey prestriate cortex. , 1973, Brain research.

[7]  L. Maffei,et al.  The visual cortex as a spatial frequency analyser. , 1973, Vision research.

[8]  B. Dow Functional classes of cells and their laminar distribution in monkey visual cortex. , 1974, Journal of neurophysiology.

[9]  L. Palmer,et al.  Visual receptive fields of single striate corical units projecting to the superior colliculus in the cat. , 1974, Brain research.

[10]  D. Hubel,et al.  Uniformity of monkey striate cortex: A parallel relationship between field size, scatter, and magnification factor , 1974, The Journal of comparative neurology.

[11]  P. Schiller,et al.  Quantitative studies of single-cell properties in monkey striate cortex. III. Spatial frequency. , 1976, Journal of neurophysiology.

[12]  P. Schiller,et al.  Quantitative studies of single-cell properties in monkey striate cortex. I. Spatiotemporal organization of receptive fields. , 1976, Journal of neurophysiology.

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

[14]  C. Gross 7 – The Neural Basis of Stimulus Equivalence Across Retinal Translation , 1977 .

[15]  J. Baizer,et al.  Visual responses of area 18 neurons in awake, behaving monkey. , 1977, Journal of neurophysiology.

[16]  C. Gilbert Laminar differences in receptive field properties of cells in cat primary visual cortex , 1977, The Journal of physiology.

[17]  D. C. Essen,et al.  The topographic organization of rhesus monkey prestriate cortex. , 1978, The Journal of physiology.

[18]  S. Zeki Uniformity and diversity of structure and function in rhesus monkey prestriate visual cortex. , 1978, The Journal of physiology.

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

[20]  J. Movshon,et al.  Receptive field organization of complex cells in the cat's striate cortex. , 1978, The Journal of physiology.

[21]  M. Mishkin,et al.  Role of inferior temporal cortex in interhemispheric transfer , 1979, Brain Research.

[22]  F. Gallyas Silver staining of myelin by means of physical development. , 1979, Neurological research.

[23]  R. Desimone,et al.  Visual areas in the temporal cortex of the macaque , 1979, Brain Research.

[24]  D. G. Albrecht,et al.  Visual cortical neurons: are bars or gratings the optimal stimuli? , 1980, Science.

[25]  R. Desimone,et al.  Prestriate afferents to inferior temporal cortex: an HRP study , 1980, Brain Research.

[26]  P. Gouras,et al.  Spectral selectivity of cells and its dependence on slit length in monkey visual cortex. , 1980, Journal of neurophysiology.

[27]  S. Zeki The representation of colours in the cerebral cortex , 1980, Nature.

[28]  S. Petersen,et al.  Dimensional selectivity of neurons in the dorsolateral visual area of the owl monkey , 1980, Brain Research.

[29]  Leslie G. Ungerleider Two cortical visual systems , 1982 .

[30]  F M de Monasterio,et al.  Spectral bandwidths of color-opponent cells of geniculocortical pathway of macaque monkeys. , 1982, Journal of neurophysiology.

[31]  S. Schein,et al.  Is there a high concentration of color-selective cells in area V4 of monkey visual cortex? , 1982, Journal of neurophysiology.

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

[33]  D. G. Albrecht,et al.  Spatial frequency selectivity of cells in macaque visual cortex , 1982, Vision Research.

[34]  S. Zeki The distribution of wavelength and orientation selective cells in different areas of monkey visual cortex , 1983, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[35]  S. Zeki Colour coding in the cerebral cortex: The reaction of cells in monkey visual cortex to wavelengths and colours , 1983, Neuroscience.

[36]  Daniel A. Pollen,et al.  Visual cortical neurons as localized spatial frequency filters , 1983, IEEE Transactions on Systems, Man, and Cybernetics.

[37]  R. Desimone,et al.  Shape recognition and inferior temporal neurons. , 1983, Proceedings of the National Academy of Sciences of the United States of America.

[38]  S. Zeki Colour coding in the cerebral cortex: The responses of wavelength-selective and colour-coded cells in monkey visual cortex to changes in wavelength composition , 1983, Neuroscience.

[39]  D. Tolhurst,et al.  On the distinctness of simple and complex cells in the visual cortex of the cat. , 1983, The Journal of physiology.

[40]  W. Maguire,et al.  Visuotopic organization of the prelunate gyrus in rhesus monkey , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[41]  R. Desimone,et al.  Stimulus-selective properties of inferior temporal neurons in the macaque , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[43]  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.

[44]  D. Pollen,et al.  Spatial and temporal frequency selectivity of neurones in visual cortical areas V1 and V2 of the macaque monkey. , 1985, The Journal of physiology.

[45]  E. DeYoe,et al.  Segregation of efferent connections and receptive field properties in visual area V2 of the macaque , 1985, Nature.

[46]  P. Lennie,et al.  Spatial frequency analysis in the visual system. , 1985, Annual review of neuroscience.

[47]  J Allman,et al.  Direction- and Velocity-Specific Responses from beyond the Classical Receptive Field in the Middle Temporal Visual Area (MT) , 1985, Perception.

[48]  C. R. Michael Laminar segregation of color cells in the monkey's striate cortex , 1985, Vision Research.

[49]  S. Zeki,et al.  Segregation of pathways leading from area V2 to areas V4 and V5 of macaque monkey visual cortex , 1985, Nature.

[50]  Leslie G. Ungerleider,et al.  Contour, color and shape analysis beyond the striate cortex , 1985, Vision Research.

[51]  D. Hubel,et al.  Complex–unoriented cells in a subregion of primate area 18 , 1985, Nature.

[52]  H. Spitzer,et al.  Simple- and complex-cell response dependences on stimulation parameters. , 1985, Journal of neurophysiology.

[53]  J. Allman,et al.  Stimulus specific responses from beyond the classical receptive field: neurophysiological mechanisms for local-global comparisons in visual neurons. , 1985, Annual review of neuroscience.

[54]  Ellen Covey,et al.  Cortical Visual Areas of the Macaque: Possible Substrates for Pattern Recognition Mechanisms , 1985 .

[55]  Steven W. Zucker,et al.  Early orientation selection: Tangent fields and the dimensionality of their support , 1985, Comput. Vis. Graph. Image Process..

[56]  R. Vautin,et al.  Color cell groups in foveal striate cortex of the behaving macaque. , 1985, Journal of neurophysiology.

[57]  Leslie G. Ungerleider The Corticocortical Pathways for Object Recognition and Spatial Perception , 1985 .

[58]  H. Spitzer,et al.  A complex-cell receptive-field model. , 1985, Journal of neurophysiology.

[59]  R. Desimone,et al.  Selective attention gates visual processing in the extrastriate cortex. , 1985, Science.

[60]  D. B. Bender,et al.  Global visual processing in the monkey superior colliculus , 1986, Brain Research.

[61]  Leslie G. Ungerleider,et al.  Cortical connections of visual area MT in the macaque , 1986, The Journal of comparative neurology.

[62]  D. J. Felleman,et al.  Anatomical and physiological asymmetries related to visual areas V3 and VP in macaque extrastriate cortex , 1986, Vision Research.