Comparison of Spatial Summation Properties of Neurons in Macaque V1 and V2

In visual cortex, responses to stimulation of the receptive field (RF) are modulated by simultaneous stimulation of the RF surround. The mechanisms for surround modulation remain unidentified. We previously proposed that in the primary visual cortex (V1), near surround modulation is mediated by geniculocortical and horizontal connections and far surround modulation by interareal feedback connections. To understand spatial integration in the secondary visual cortex (V2) and its underlying circuitry, we have characterized spatial summation in different V2 layers and stripe compartments and compared it to that in V1. We used grating stimuli in circular and annular apertures of different sizes to estimate the extent and sensitivity of RF and surround components in V1 and V2. V2 RFs and surrounds were twice as large as those in V1. As in V1, V2 RFs doubled in size when measured at low contrast. In both V1 and V2, surrounds were about fivefold the size of the RF and the far surround could exceed 12.5° in radius, averaging 5.5° in V1 and 9.2° in V2. The strength of surround suppression was similar in both areas. Thus although differing in spatial scale, the interactions among RF components are similar in V1 and V2, suggesting similar underlying mechanisms. As in V1, the extent of V2 horizontal connections matches that of the RF center, but is much smaller than the largest far surrounds, which likely derive from interareal feedback. In V2, we found no laminar or stripe differences in size and magnitude of surround suppression, suggesting conservation across stripes of the basic circuit for surround modulation.

[1]  H. Tamura,et al.  Less Segregated Processing of Visual Information in V2 than in V1 of the Monkey Visual Cortex , 1996, The European journal of neuroscience.

[2]  K. Rockland,et al.  Intrinsic collaterals of layer 6 meynert cells and functional columns in primate v1 , 2003, Neuroscience.

[3]  I. Ohzawa,et al.  Suppression outside the classical cortical receptive field , 2000, Visual Neuroscience.

[4]  J. B. Levitt,et al.  Receptive fields and functional architecture of macaque V2. , 1994, Journal of neurophysiology.

[5]  Gyula Sáry,et al.  Functional Organization of Visual Cortex in the Owl Monkey , 2004, The Journal of Neuroscience.

[6]  Robert Desimone,et al.  Cortical Connections of Area V4 in the Macaque , 2008 .

[7]  J. Movshon,et al.  Time Course and Time-Distance Relationships for Surround Suppression in Macaque V1 Neurons , 2003, The Journal of Neuroscience.

[8]  K. Obermayer,et al.  The Role of Feedback in Shaping the Extra-Classical Receptive Field of Cortical Neurons: A Recurrent Network Model , 2006, The Journal of Neuroscience.

[9]  D. Ts'o,et al.  Functional organization of primate visual cortex revealed by high resolution optical imaging. , 1990, Science.

[10]  David C. Van Essen,et al.  Multiple processing streams in occipitotemporal visual cortex , 1994, Nature.

[11]  J. Lund,et al.  Intrinsic laminar lattice connections in primate visual cortex , 1983, The Journal of comparative neurology.

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

[13]  Leslie G. Ungerleider,et al.  The modular organization of projections from areas V1 and V2 to areas V4 and TEO in macaques , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[14]  R. Tootell,et al.  Functional anatomy of the second visual area (V2) in the macaque , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[15]  K. Rockland,et al.  Laminar origins and terminations of cortical connections of the occipital lobe in the rhesus monkey , 1979, Brain Research.

[16]  C. Blakemore,et al.  The neural mechanism of binocular depth discrimination , 1967, The Journal of physiology.

[17]  P. Lennie,et al.  The Impact of Suppressive Surrounds on Chromatic Properties of Cortical Neurons , 2004, The Journal of Neuroscience.

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

[19]  Anna W. Roe,et al.  A Map for Horizontal Disparity in Monkey V2 , 2008, Neuron.

[20]  I. Ohzawa,et al.  Length and width tuning of neurons in the cat's primary visual cortex. , 1994, Journal of neurophysiology.

[21]  S. Zeki,et al.  The functional organization of area V2, I: Specialization across stripes and layers , 2002, Visual Neuroscience.

[22]  Robert Desimone,et al.  Cortical connections of area V4 in the macaque. , 2000, Cerebral cortex.

[23]  G. Orban,et al.  Search for color 'center(s)' in macaque visual cortex. , 2004, Cerebral cortex.

[24]  J. M. Hupé,et al.  Conduction Velocities V 1 and V 2 of the Monkey Have Similar Rapid Feedforward and Feedback Connections Between Areas , .

[25]  L. Schwabe,et al.  Response facilitation from the "suppressive" receptive field surround of macaque V1 neurons. , 2007, Journal of neurophysiology.

[26]  T. Wiesel,et al.  Functional organization of the visual cortex. , 1983, Progress in brain research.

[27]  K R Gegenfurtner,et al.  Processing of color, form, and motion in macaque area V2 , 1996, Visual Neuroscience.

[28]  Lawrence C. Sincich,et al.  Divided by Cytochrome Oxidase: A Map of the Projections from V1 to V2 in Macaques , 2002, Science.

[29]  H. Kennedy,et al.  Topography of the afferent connectivity of area 17 in the macaque monkey: A double‐labelling study , 1986, The Journal of comparative neurology.

[30]  J. Bullier,et al.  Feedforward and feedback connections between areas V1 and V2 of the monkey have similar rapid conduction velocities. , 2001, Journal of neurophysiology.

[31]  Paul Antoine Salin,et al.  Visuotopic organization of corticocortical connections in the visual system of the cat , 1992, The Journal of comparative neurology.

[32]  W. Martin Usrey,et al.  Origin and Dynamics of Extraclassical Suppression in the Lateral Geniculate Nucleus of the Macaque Monkey , 2008, Neuron.

[33]  Leslie G. Ungerleider,et al.  Cortical projections of area V2 in the macaque. , 1997, Cerebral cortex.

[34]  S. Zeki,et al.  The functional organization of area V2, II: The impact of stripes on visual topography , 2002, Visual Neuroscience.

[35]  Bin Zhang,et al.  Delayed maturation of receptive field center/surround mechanisms in V2. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[36]  C. Blakemore,et al.  Characteristics of surround inhibition in cat area 17 , 1997, Experimental Brain Research.

[37]  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.

[38]  C. Blakemore,et al.  Lateral inhibition between orientation detectors in the cat's visual cortex , 2004, Experimental Brain Research.

[39]  H. Kennedy,et al.  A double-labeling investigation of the afferent connectivity to cortical areas V1 and V2 of the macaque monkey , 1985, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[40]  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.

[41]  Edward M Callaway,et al.  Visual spatial summation in macaque geniculocortical afferents. , 2006, Journal of neurophysiology.

[42]  R. L. Thorndike.  Who belongs in the family? , 1953 .

[43]  G Westheimer,et al.  Dynamics of spatial summation in primary visual cortex of alert monkeys. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[44]  J. B. Levitt,et al.  The spatial extent over which neurons in macaque striate cortex pool visual signals , 2002, Visual Neuroscience.

[45]  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.

[46]  Iwona Stepniewska,et al.  Reappraisal of DL/V4 boundaries based on connectivity patterns of dorsolateral visual cortex in macaques. , 2005, Cerebral cortex.

[47]  J. Movshon,et al.  Nature and interaction of signals from the receptive field center and surround in macaque V1 neurons. , 2002, Journal of neurophysiology.

[48]  R. Shapley,et al.  Visual spatial characterization of macaque V1 neurons. , 2001, Journal of neurophysiology.

[49]  J. Lund,et al.  Anatomical substrates for functional columns in macaque monkey primary visual cortex. , 2003, Cerebral cortex.

[50]  J. B. Levitt,et al.  Intrinsic cortical connections in macaque visual area V2: Evidence for interaction between different functional streams , 1994, The Journal of comparative neurology.

[51]  E. Peterhans,et al.  Functional Organization of Area V2 in the Alert Macaque , 1993, The European journal of neuroscience.

[52]  Youping Xiao,et al.  Projections from primary visual cortex to cytochrome oxidase thin stripes and interstripes of macaque visual area 2. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

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

[54]  G. Orban,et al.  The organization of orientation selectivity throughout macaque visual cortex. , 2002, Cerebral cortex.

[55]  Lawrence C. Sincich,et al.  The circuitry of V1 and V2: integration of color, form, and motion. , 2005, Annual review of neuroscience.

[56]  A. Roe,et al.  Cerebral Cortex Advance Access published June 18, 2007 Functional Organization of Color Domains in V1 and V2 of Macaque Monkey Revealed by Optical Imaging , 2022 .

[57]  J. Nelson,et al.  Orientation-selective inhibition from beyond the classic visual receptive field , 1978, Brain Research.

[58]  Alessandra Angelucci,et al.  Contribution of feedforward thalamic afferents and corticogeniculate feedback to the spatial summation area of macaque V1 and LGN , 2006, The Journal of comparative neurology.

[59]  P. O. Bishop.  NEURAL MECHANISMS FOR BINOCULAR DEPTH DISCRIMINATION , 1981 .

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

[61]  A. Angelucci,et al.  Contribution of feedforward, lateral and feedback connections to the classical receptive field center and extra-classical receptive field surround of primate V1 neurons. , 2006, Progress in brain research.

[62]  D. J. Felleman,et al.  A spatially organized representation of colour in macaque cortical area V2 , 2003, Nature.

[63]  Farran Briggs,et al.  Laminar patterns of local excitatory input to layer 5 neurons in macaque primary visual cortex. , 2005, Cerebral cortex.

[64]  J. B. Levitt,et al.  Circuits for Local and Global Signal Integration in Primary Visual Cortex , 2002, The Journal of Neuroscience.

[65]  J. Rossier,et al.  Classification of fusiform neocortical interneurons based on unsupervised clustering. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[66]  P A Salin,et al.  Visuotopic organization of corticocortical connections in the visual system. , 1993, Progress in brain research.

[67]  T. Wiesel,et al.  The influence of contextual stimuli on the orientation selectivity of cells in primary visual cortex of the cat , 1990, Vision Research.

[68]  Anna W. Roe,et al.  Functional organization of color domains in V1 and V2 of Macaque monkey revealed by optical imaging , 2010 .

[69]  J. Kaas,et al.  Topographic patterns of V2 cortical connections in macaque monkeys , 1996, The Journal of comparative neurology.

[70]  Semir Zeki,et al.  Feature binding in the feedback layers of area V2. , 2009, Cerebral cortex.

[71]  R. Shapley,et al.  Contrast's effect on spatial summation by macaque V1 neurons , 1999, Nature Neuroscience.

[72]  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.