Velocity sensitivity and direction selectivity of neurons in areas V1 and V2 of the monkey: influence of eccentricity.

One hundred and forty two neurons in V1 and V2 were quantitatively tested using a multihistogram technique in paralyzed and anesthetized macaque monkeys. V1 neurons with receptive fields within 2 degrees from the fixation point (central V1 sample) and V1 neurons with eccentric receptive fields (15-25 degrees eccentricity, peripheral V1 sample) were compared to assess changes in velocity sensitivity and direction selectivity with eccentricity. The central V1 sample was compared with V2 neurons with receptive fields in the same part of the visual field (central V2 sample) to compare the involvement of both areas in the analysis of motion. Velocity sensitivity of V1 neurons shifts to faster velocities with increasing eccentricity. V1 and V2 neurons subserving central vision have similar preference for slow movements. All neurons could be classified into three categories according to their velocity-response curves: velocity low pass, velocity broad band, and velocity tuned. Most cells in parts of V1 and V2 subserving central vision are velocity low pass. As eccentricity increases in V1, velocity low-pass cells give way to velocity broad-band cells. There is a significant correlation between velocity upper cutoff and receptive field width among V1 neurons. The change in upper cutoff velocity with eccentricity depends both on temporal and spatial factors. Direction selectivity depends on stimulus velocity in most V1 cells. Neurons in the central V1 sample retain their direction selectivity at lower speeds than do neurons in the peripheral V1 sample. The proportion of direction-selective cells is low in both V1 and V2. In V1, direction selectivity decreases with eccentricity. In V1, both velocity upper cutoff and direction selectivity correlate more with laminar position than with receptive field type. The similarity between V1 of the monkey and area 17 of the cat, and the dissimilarity between V2 of the monkey and area 18 of the cat, are discussed.

[1]  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.

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

[3]  R. Wurtz.  Visual receptive fields of striate cortex neurons in awake monkeys. , 1969, Journal of neurophysiology.

[4]  D. Hubel,et al.  Stereoscopic Vision in Macaque Monkey: Cells sensitive to Binocular Depth in Area 18 of the Macaque Monkey Cortex , 1970, Nature.

[5]  S. Zeki.  Functional organization of a visual area in the posterior bank of the superior temporal sulcus of the rhesus monkey , 1974, The Journal of physiology.

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

[7]  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.

[8]  G. Poggio,et al.  Spatial and chromatic properties of neurons subserving foveal and parafoveal vision in rhesus monkey , 1975, Brain Research.

[9]  J. Movshon.  The velocity tuning of single units in cat striate cortex. , 1975, The Journal of physiology.

[10]  David A. Robinson,et al.  Miniature eye movements of fixation in rhesus monkey , 1975, Vision Research.

[11]  S. McKee,et al.  Visual acuity in the presence of retinal-image motion. , 1975, Journal of the Optical Society of America.

[12]  J. Lund,et al.  The origin of efferent pathways from the primary visual cortex, area 17, of the macaque monkey as shown by retrograde transport of horseradish peroxidase , 1975, The Journal of comparative neurology.

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

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

[15]  D. C. Essen,et al.  Visual areas of the mammalian cerebral cortex. , 1979 .

[16]  G. Orban,et al.  Response to movement of neurons in areas 17 and 18 of the cat: velocity sensitivity. , 1981, Journal of neurophysiology.

[17]  G. Orban,et al.  Is stimulus movement of particular importance in the functioning of cat visual cortex? , 1981, Brain Research.

[18]  G. Poggio,et al.  Mechanisms of static and dynamic stereopsis in foveal cortex of the rhesus monkey , 1981, The Journal of physiology.

[19]  K. Yoshida,et al.  The projection from the dorsal lateral geniculate nucleus of the thalamus to extrastriate visual association cortex in the macaque monkey , 1981, Neuroscience Letters.

[20]  D. C. Essen,et al.  The middle temporal visual area in the macaque: Myeloarchitecture, connections, functional properties and topographic organization , 1981, The Journal of comparative neurology.

[21]  G. Orban,et al.  The influence of eccentricity on receptive field types and orientation selectivity in areas 17 and 18 of the cat , 1981, Brain Research.

[22]  G. Orban,et al.  Response to movement of neurons in areas 17 and 18 of the cat: direction selectivity. , 1981, Journal of neurophysiology.

[23]  M. Yukie,et al.  Direct projection from the dorsal lateral geniculate nucleus to the prestriate cortex in macaque monkeys , 1981, The Journal of comparative neurology.

[24]  J. Duysens,et al.  Functional properties of area 19 as compared to area 17 of the cat , 1982, Brain Research.

[25]  D C Van Essen,et al.  Functional properties of neurons in middle temporal visual area of the macaque monkey. I. Selectivity for stimulus direction, speed, and orientation. , 1983, Journal of neurophysiology.

[26]  B. Cleland,et al.  Response to the velocity of moving visual stimuli of the brisk classes of ganglion cells in the cat retina. , 1983, The Journal of physiology.

[27]  J J Koenderink,et al.  Detection of coherent movement in peripherally viewed random-dot patterns. , 1983, Journal of the Optical Society of America.

[28]  E. Goldstein,et al.  Velocity tuning of cells in dorsal lateral geniculate nucleus and retina of the cat. , 1983, Journal of neurophysiology.

[29]  J. Maunsell,et al.  The connections of the middle temporal visual area (MT) and their relationship to a cortical hierarchy in the macaque monkey , 1983, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[30]  Professor Dr. Guy A. Orban.  Neuronal Operations in the Visual Cortex , 1983, Studies of Brain Function.

[31]  D. C. Essen,et al.  The visual field representation in striate cortex of the macaque monkey: Asymmetries, anisotropies, and individual variability , 1984, Vision Research.

[32]  G. Orban.  Velocity Tuned Cortical Cells and Human Velocity Discrimination , 1985 .

[33]  G A Orban,et al.  Velocity discrimination in central and peripheral visual field. , 1985, Journal of the Optical Society of America. A, Optics and image science.

[34]  G. A. Orban,et al.  Receptive field properties of neurones in visual area 1 and visual area 2 in the baboon , 1985, Neuroscience.

[35]  G. Orban,et al.  Velocity selectivity in the cat visual system. III. Contribution of temporal factors. , 1985, Journal of neurophysiology.

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

[37]  G. Orban,et al.  Velocity selectivity in the cat visual system. II. Independence from interactions between different loci. , 1985, Journal of neurophysiology.