Hostname: page-component-8448b6f56d-cfpbc Total loading time: 0 Render date: 2024-04-17T10:57:12.600Z Has data issue: false hasContentIssue false
  • English
  • Français

Uniformity and diversity of response properties of neurons in the primary visual cortex: Selectivity for orientation, direction of motion, and stimulus size from center to far periphery

Published online by Cambridge University Press:  25 October 2013

HSIN-HAO YU  and
MARCELLO G.P. ROSA
HSIN-HAO YU*
Affiliation:
Department of Physiology, Monash University, Clayton, Victoria, Australia
MARCELLO G.P. ROSA
Affiliation:
Department of Physiology, Monash University, Clayton, Victoria, Australia Monash Vision Group, Monash University, Clayton, Victoria, Australia
*
*Address correspondence to: Hsin-Hao Yu, Department of Physiology, Monash University, Clayton, VIC 3800, Australia. E-mail: hsin-hao.yu@monash.edu
Get access Rights & Permissions [Opens in a new window]

Abstract

Although the primary visual cortex (V1) is one of the most extensively studied areas of the primate brain, very little is known about how the far periphery of visual space is represented in this area. We characterized the physiological response properties of V1 neurons in anaesthetized marmoset monkeys, using high-contrast drifting gratings. Comparisons were made between cells with receptive fields located in three regions of V1, defined by eccentricity: central (3–5°), near peripheral (5–15°), and far peripheral (>50°). We found that orientation selectivity of individual cells was similar from the center to the far periphery. Nonetheless, the proportion of orientation-selective neurons was higher in central visual field representation than in the peripheral representations. In addition, there were similar proportions of cells representing all orientations, with the exception of the representation of the far periphery, where we detected a bias favoring near-horizontal orientations. The proportions of direction-selective cells were similar throughout V1. When the center/surround organization of the receptive fields was tested with gratings with varying diameters, we found that the population of neurons that was suppressed by large gratings was smaller in the far periphery, although the strength of suppression in these cells tended to be stronger. In addition, the ratio between the diameters of the excitatory centers and suppressive surrounds was similar across the entire visual field. These results suggest that, superimposed on the broad uniformity of V1, there are subtle physiological differences, which indicate that spatial information is processed differently in the central versus far peripheral visual fields.

Keywords

V1Orientation selectivityDirection selectivityCenter–surroundCallithrix jacchus
Type
Research Articles
Information
Visual Neuroscience , Volume 31 , Issue 1 , January 2014 , pp. 85 - 98
Copyright
Copyright © Cambridge University Press 2013 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Albright, T.D. (1989). Centrifugal directional bias in the middle temporal visual area (MT) of the macaque. Visual Neuroscience 2, 177–188.CrossRefGoogle ScholarPubMed
Angelucci, A., Levitt, J.B., Walton, E., Hupé, J.-M., Bullier, J. & Lund, J.S. (2002). Circuits for local and global signal integration in primary visual cortex. The Journal of Neuroscience 22, 8633–8646.CrossRefGoogle ScholarPubMed
Appelle, S. (1972). Perception and discrimination as a function of stimulus orientation: The “oblique effect” in man and animals. Psychological Bulletin 78, 266–278.CrossRefGoogle Scholar
Bardy, C., Huang, J.Y., Wang, C., FitzGibbon, T. & Dreher, B. (2006). ‘Simplification’ of responses of complex cells in cat striate cortex: Suppressive surrounds and ‘feedback’ inactivation. The Journal of Physiology 574, 731–750.CrossRefGoogle ScholarPubMed
Battaglini, P.P., Galletti, C. & Fattori, P. (1993). Functional properties of neurons in area V1 of awake macaque monkeys: Peripheral versus central visual field representation. Archives Italiennes de Biologie 131, 303–315.Google ScholarPubMed
Berkley, M.A., Kitterle, F. & Watkins, D.W. (1975). Grating visibility as a function of orientation and retinal eccentricity. Vision Research 15, 239–244.CrossRefGoogle ScholarPubMed
Berthoz, A., Pavard, B. & Young, L.R. (1975). Perception of linear horizontal self-motion induced by peripheral vision (linearvection): Basic characteristics and visual-vestibular interactions. Experimental Brain Research 23, 471–489.CrossRefGoogle ScholarPubMed
Bessou, M., Séverac Cauquil, A., Dupui, P., Montoya, R. & Bessou, P. (1999). Specificity of the monocular crescents of the visual field in postural control. Comptes Rendus de l’Académie des Sciences III 322, 749–757.Google ScholarPubMed
Bourne, J.A. & Rosa, M.G.P. (2003). Preparation for the in vivo recording of neuronal responses in the visual cortex of anaesthetised marmosets (Callithrix jacchus). Brain Research Protocols 11, 168–177.CrossRefGoogle ScholarPubMed
Brandt, T., Dichgans, J. & Koenig, E. (1973). Differential effects of central versus peripheral vision on egocentric and exocentric motion perception. Experimental Brain Research 16, 476–491.CrossRefGoogle Scholar
Cavanaugh, J.R., Bair, W. & Movshon, J.A. (2002 a). Nature and interaction of signals from the receptive field centre and surround in macaque V1 neurons. Journal of Neurophysiology 88, 2530–2546.CrossRefGoogle ScholarPubMed
Cavanaugh, J.R., Bair, W. & Movshon, J.A. (2002 b). Selectivity and spatial distribution of signals from the receptive field surround in macaque V1 neurons. Journal of Neurophysiology 88, 2547–2556.CrossRefGoogle ScholarPubMed
Chaplin, T.A., Yu, H.-H. & Rosa, M.G.P. (2013). Representation of the visual field in the primary visual area of the marmoset monkey: Magnification factors, point-image size and proportionality to retinal ganglion cell density. The Journal of Comparative Neurology 521, 1001–1019.CrossRefGoogle ScholarPubMed
De Valois, R.L., Yund, E.W. & Helper, N. (1982 a). The orientation and direction selectivity of cells in macaque visual cortex. Vision Research 22, 531–544.CrossRefGoogle ScholarPubMed
De Valois, R.L., Albrecht, D.G. & Thorell, L.G. (1982 b). Spatial frequency selectivity of cells in macaque visual cortex. Vision Research 22, 545–559.CrossRefGoogle ScholarPubMed
DeAngelis, G.C., Robson, J.G., Ohzawa, I. & Freeman, R.D. (1992). Organization of suppression in receptive fields in cat visual cortex. Journal of Neurophysiology 68, 144–163.CrossRefGoogle ScholarPubMed
Fisher, N.I. (1993). Statistical Analysis of Circular Data. New York: Cambridge University Press.CrossRefGoogle Scholar
Forte, J., Hashemi-Nezhad, M., Dobbie, W.J., Dreher, B. & Martin, P.R. (2005). Spatial coding and response redundancy in parallel visual pathways of the marmoset Callithrix jacchus. Visual Neuroscience 22, 249–491.CrossRefGoogle ScholarPubMed
Fritsches, K.A. & Rosa, M.G.P. (1996). Visuotopic organization of striate cortex in the marmoset monkey (Callithrix jacchus). The Journal of Comparative Neurology 372, 264–282.3.0.CO;2-1>CrossRefGoogle ScholarPubMed
Furmanski, C.S. & Engel, S.A. (2000). An oblique effect in human primary visual cortex. Nature Neuroscience 3, 535–536.CrossRefGoogle ScholarPubMed
Gallyas, F. (1979). Silver staining of myelin by means of physical development. Neurology Research 1, 203–209.CrossRefGoogle ScholarPubMed
Gattass, R., Sousa, A.P.B., Mishkin, M. & Ungerleider, L.G. (1997). Cortical projections of area V2 in the macaque. Cerebral Cortex 7, 110–129.CrossRefGoogle ScholarPubMed
Gattass, R., Sousa, A.P.B. & Rosa, M.G.P. (1987). Visual topology of V1 in the Cebus monkey. The Journal of Comparative Neurology 259, 529–548.CrossRefGoogle Scholar
Gur, M., Kagan, I. & Snodderly, D.M. (2005). Orientation and direction selectivity of neurons in V1 of alert monkeys: Functional relationship and laminar distribution. Cerebral Cortex 15, 1207–1221.CrossRefGoogle Scholar
Hassler, R. (1966). Comparative anatomy of the central visual system in day- and night-active primates. In Evolution of the Forebrain, ed. Hassler, R. & Stephen, H., pp. 419–434. Stuttgart, Germany: Thieme.CrossRefGoogle Scholar
Henry, C.A., Joshi, S., Xing, D., Shapley, R.M. & Hawken, M.J. (2013). Functional characterization of the extraclassical receptive field in macaque V1: Contrast, orientation, and temporal dynamics. The Journal of Neuroscience 33, 6230–6242.CrossRefGoogle ScholarPubMed
Hess, R.F. & Dakin, S.C. (1997). Absence of contour linking in peripheral vision. Nature 390, 602–604.CrossRefGoogle ScholarPubMed
Hubel, D.H. & Wiesel, T.N. (1974). Uniformity of monkey striate cortex: A parallel relationship between field size, scatter, and magnification factor. The Journal of Comparative Neurology 158, 295–306.CrossRefGoogle ScholarPubMed
Jones, H.E., Grieve, K.L., Wang, W. & Sillito, A.M. (2001). Surround suppression in primate V1. Journal of Neurophysiology 86, 2011–2028.CrossRefGoogle ScholarPubMed
Li, B., Peterson, M.R. & Freeman, R.D. (2003). Oblique effect: A neural basis in the visual cortex. Journal of Neurophysiology 90, 204–217.CrossRefGoogle ScholarPubMed
Li, C.-Y. & Li, W. (1994). Extensive integration field beyond the classical receptive field of cat’s striate cortical neurons – classification and tuning properties. Vision Research 34, 2337–2355.Google ScholarPubMed
Livingstone, M.S. & Hubel, D.H. (1984). Anatomy and physiology of a color system in the primate visual cortex. Journal of Neuroscience 4, 309–356.CrossRefGoogle ScholarPubMed
Lui, L.L, Bourne, J.A. & Rosa, M.G.P. (2006). Functional response properties of neurons in the dorsomedial visual area of new world monkeys (Callithrix jacchus). Cerebral Cortex 16, 162–177.CrossRefGoogle ScholarPubMed
Mäkelä, P., Näsänen, R., Rovamo, J. & Melmoth, D. (2001). Identification of facial images in peripheral vision. Vision Research 41, 599–610.CrossRefGoogle ScholarPubMed
Mansfield, R.J. & Ronner, S.F. (1978). Orientation anisotropy in monkey visual cortex. Brain Research 149, 229–234.CrossRefGoogle Scholar
McKee, S.P. & Nakayama, K. (1984). The detection of motion in the peripheral visual field. Vision Research 24, 25–32.CrossRefGoogle ScholarPubMed
Nowak, L.G. & Barone, P. (2009). Contrast adaptation contributes to contrast-invariance of orientation tuning of primate V1 cells. PLoS One 4, 4781.CrossRefGoogle ScholarPubMed
Orban, G.A. & Kennedy, H. (1981). The influence of eccentricity on receptive field types and orientation selectivity in area 17 and 18 of the cat. Brain Research 208, 203–208.CrossRefGoogle Scholar
Orban, G.A., Kennedy, H. & Bullier, J. (1986). Velocity sensitivity and direction selectivity of neurons in area V1 and V2 of the monkey: influences of eccentricity. Journal of Neurophysiology 56, 462–480.CrossRefGoogle ScholarPubMed
Orban, G.A., Vandenbussche, E. & Vogels, R. (1984). Human orientation discrimination tested with long stimuli. Vision Research 24, 121–128.CrossRefGoogle ScholarPubMed
Palmer, S.M. & Rosa, M.G.P. (2006). A distinct anatomical network of cortical areas for analysis of motion in far peripheral vision. The European Journal of Neuroscience 24, 2389–2405.CrossRefGoogle ScholarPubMed
Paradiso, M.A. & Carney, T. (1988). Orientation discrimination as a function of stimulus eccentricity and size: Nasal/temporal retinal asymmetry. Vision Research 28, 867–874.CrossRefGoogle ScholarPubMed
Payne, B.R. & Berman, N. (1983). Functional organization of neurons in cat striate cortex: Variations in preferred orientation and orientation selectivity with receptive-field type, ocular dominance, and location in visual-field map. Journal of Neurophysiology 49, 1051–1072.CrossRefGoogle ScholarPubMed
Petrov, Y., Carandini, M. & McKee, S. (2005). Two distinct mechanisms of suppression in human vision. The Journal of Neuroscience 25, 8704–8707.CrossRefGoogle ScholarPubMed
Pointer, J.S. (1986). The cortical magnification factor and photopic vision. Biological Reviews 61, 97–119.CrossRefGoogle ScholarPubMed
Ringach, D.L., Shapley, R.M. & Hawken, M.J. (2002). Orientation selectivity in macaque V1: Diversity and laminar dependence. The Journal of Neuroscience 22, 5639–5651.CrossRefGoogle ScholarPubMed
Rosa, M.G.P. & Elston, G.N. (1998). Visuotopic organisation and neuronal response selectivity for direction of motion in visual areas of the caudal temporal lobe of the marmoset monkey (Callithrix jacchus): Middle temporal area, middle temporal crescent, and surrounding cortex. The Journal of Comparative Neurology 393, 505–527.3.0.CO;2-4>CrossRefGoogle ScholarPubMed
Rosa, M.G.P., Fritsches, K.A. & Elston, G.N. (1997). The second visual area in the marmoset monkey: Visuotopic organisation, magnification factors, architectonical boundaries, and modularity. The Journal of Comparative Neurology 387, 547–567.3.0.CO;2-2>CrossRefGoogle ScholarPubMed
Rosa, M.G.P., Gattass, R., Fiorani, M. Jr. & Soares, J.G.M. (1992). Laminar, columnar and topographic aspects of ocular dominance in the primary visual cortex of Cebus monkeys. Experimental Brain Research 88, 249–264.CrossRefGoogle ScholarPubMed
Rosa, M.G.P., Gattass, R. & Soares, J.G.M. (1991). A quantitative analysis of cytochrome oxidase-rich patches in the primary visual cortex of Cebus monkeys: Topographic distribution and effects of late monocular enucleation. Experimental Brain Research 84, 195–209.CrossRefGoogle ScholarPubMed
Rosa, M.G.P., Soares, J.G.M., Fiorani, M. & Gattass, R. (1993). Cortical afferents of visual area MT in the Cebus monkey: Possible homologies between New and Old World monkeys. Visual Neuroscience 10, 827–855.CrossRefGoogle ScholarPubMed
Rovamo, J., Virsu, V. & Näsänen, R. (1978). Cortical magnification factor predicts the photopic contrast sensitivity of peripheral vision. Nature 271, 54–56.CrossRefGoogle ScholarPubMed
Sceniak, M., Ringach, D.L., Hawken, M.J. & Shapley, R. (1999). Contrast’s effect on spatial summation by macaque V1 neurons. Nature Neuroscience 2, 733–739.CrossRefGoogle ScholarPubMed
Sengpiel, F., Troilo, D., Kind, P.C., Graham, B. & Blakemore, C. (1996). Functional architecture of area 17 in normal and monocularly deprived marmosets (Callithrix jacchus). Visual Neuroscience 13, 145–160.CrossRefGoogle ScholarPubMed
Sengpiel, F., Sen, A. & Blackmore, C. (1997). Characteristics of surround inhibition in cat area 17. Experimental Brain Research 116, 216–228.CrossRefGoogle ScholarPubMed
Scobey, R.P. (1982). Human visual orientation discrimination. Journal of Neurophysiology 48, 18–26.CrossRefGoogle ScholarPubMed
Seriès, P., Lorenceau, J. & Frégnac, Y. (2003). The “silent” surround of V1 receptive fields: theory and experiments. Journal of Physiology, Paris 97, 453–474.CrossRefGoogle Scholar
Skottun, B.C., De Valois, R.L., Grosof, D.H., Movshon, J.A., Albrecht, D.G. & Bonds, A.B. (1991). Classifying simple and complex cells on the basis of response modulation. Vision Research 31, 1079–1086.CrossRefGoogle ScholarPubMed
Sousa, A.P.B., Piñon, M.C.G.P., Gattass, R. & Rosa, M.G.P. (1991). Topographic organization of cortical input to striate cortex in the Cebus monkey: A fluorescent tracer study. The Journal of Comparative Neurology 308, 665–682.CrossRefGoogle ScholarPubMed
Spinelli, D., Bazzeo, A. & Vicario, G.B. (1984). Orientation selectivity in the peripheral visual field. Perception 13, 41–47.CrossRefGoogle Scholar
Stephenson, C.M.E., Knapp, A.J. & Braddick, O.J. (1991). Discrimination of spatial phase shows a qualitative difference between foveal and peripheral processing. Vision Research 31, 1315–1326.CrossRefGoogle Scholar
Strasburger, H., Rentschler, I. & Jüttner, M. (2011). Peripheral vision and pattern recognition: A review. Journal of Vision 11, 13.CrossRefGoogle ScholarPubMed
Swindale, N.V. (1998). Orientation tuning curves: Empirical description and estimation of parameters. Biological Cybernetics 78, 45–56.CrossRefGoogle ScholarPubMed
To, M.P.S., Regan, B.C., Wood, D. & Mollon, J.D. (2011). Vision out of the corner of the eye. Vision Research 51, 203–214.CrossRefGoogle ScholarPubMed
van de Grind, W.A., van Doorn, A.J. & Koenderink, J.J. (1983). Detection of coherent movement in peripherally viewed random-dot patterns. Journal of the Optical Society of America. A, Optics, Image Science, and Vision 73, 1674–1683.Google ScholarPubMed
Vandenbussche, E., Vogels, R. & Orban, G.A. (1986). Human orientation discrimination: Changes with eccentricity in normal and amblyopic vision. Investigative Ophthalmology & Visual Science 27, 237–245.Google ScholarPubMed
Virsu, V. & Rovamo, J. (1979). Visual resolution, contrast sensitivity, and cortical magnification factor. Experimental Brain Research 37, 475–494.CrossRefGoogle ScholarPubMed
Walker, G.A., Ohzawa, I. & Freeman, R.D. (2000). Suppression outside the classical cortical receptive field. Visual Neuroscience 17, 369–379.CrossRefGoogle ScholarPubMed
Williams, A.L., Singh, K.D. & Smith, A.T. (2003). Surround modulation measured with functional MRI in the human visual cortex. Journal of Neurophysiology 89, 525–533.CrossRefGoogle ScholarPubMed
Wong-Riley, M. (1979). Changes in the visual system of monocularly sutured or enucleated cats demonstrable with cytochrome oxidase histochemistry. Brain Research 171, 11–28.CrossRefGoogle ScholarPubMed
Xing, J. & Heeger, D.J. (2000). Centre-surround interactions in foveal and peripheral vision. Vision Research 40, 3065–3072.CrossRefGoogle Scholar
Yu, H.-H., Chaplin, T.A., Davies, A.J., Verma, R. & Rosa, M.G.P. (2012). A specialized area in limbic cortex for fast analysis of peripheral vision. Current Biology: CB 22, 1351–1357.CrossRefGoogle ScholarPubMed
Yu, H.-H., Verma, R., Yang, Y., Tibballs, H.A., Lui, L.L., Reser, D.H. & Rosa, M.G.P. (2010). Spatial and temporal frequency tuning in striate cortex: Functional uniformity and specializations related to receptive field eccentricity. The European Journal of Neuroscience 31, 1043–1062.CrossRefGoogle ScholarPubMed