Spatial and temporal frequency tuning in striate cortex: functional uniformity and specializations related to receptive field eccentricity

In light of anatomical evidence suggesting differential connection patterns in central vs. peripheral representations of cortical areas, we investigated the extent to which the response properties of cells in the primary visual area (V1) of the marmoset change as a function of eccentricity. Responses to combinations of the spatial and temporal frequencies of visual stimuli were quantified for neurons with receptive fields ranging from 3° to 70° eccentricity. Optimal spatial frequencies and stimulus speeds reflected the expectation that the responses of cells throughout V1 are essentially uniform, once scaled according to the cortical magnification factor. In addition, temporal frequency tuning was similar throughout V1. However, spatial frequency tuning curves depended both on the cell’s optimal spatial frequency and on the receptive field eccentricity: cells with peripheral receptive fields showed narrower bandwidths than cells with central receptive fields that were sensitive to the same optimal spatial frequency. Although most V1 cells had separable spatial and temporal frequency tuning, the proportion of neurons displaying significant spatiotemporal interactions increased in the representation of far peripheral vision (> 50°). In addition, of the fewer than 5% of V1 cells that showed robust (spatial frequency independent) selectivity to stimulus speed, most were concentrated in the representation of the far periphery. Spatiotemporal interactions in the responses of many cells in the peripheral representation of V1 reduced the ambiguity of responses to high‐speed (> 30°/s) signals. These results support the notion of a relative specialization for motion processing in the far peripheral representations of cortical areas, including V1.

[1]  D. Tolhurst,et al.  On the variety of spatial frequency selectivities shown by neurons in area 17 of the cat , 1981, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[2]  Jerome Baron,et al.  Spatiotemporal frequency and speed tuning in the owl visual wulst , 2009, The European journal of neuroscience.

[3]  K. Fujii,et al.  Visualization for the analysis of fluid motion , 2005, J. Vis..

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

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

[6]  R. Hess,et al.  Temporal frequency filters in the human peripheral visual field , 1992, Vision Research.

[7]  A. Mizuno,et al.  A change of the leading player in flow Visualization technique , 2006, J. Vis..

[8]  S. Sherman,et al.  Receptive-field characteristics of neurons in cat striate cortex: Changes with visual field eccentricity. , 1976, Journal of neurophysiology.

[9]  M G Rosa,et al.  Visuotopic organisation of striate cortex in the marmoset monkey (Callithrix jacchus) , 1996, The Journal of comparative neurology.

[10]  Eero P. Simoncelli,et al.  Representing retinal image speed in visual cortex , 2001, Nature Neuroscience.

[11]  Marcello G P Rosa,et al.  Preparation for the in vivo recording of neuronal responses in the visual cortex of anaesthetised marmosets (Callithrix jacchus). , 2003, Brain research. Brain research protocols.

[12]  Xiangmin Xu,et al.  How do functional maps in primary visual cortex vary with eccentricity? , 2007, The Journal of comparative neurology.

[13]  G. Elston,et al.  The second visual area in the marmoset monkey: Visuotopic organisation, magnification factors, architectonical boundaries, and modularity , 1997, The Journal of comparative neurology.

[14]  Paul Azzopardi,et al.  Uneven mapping of magnocellular and parvocellular projections from the lateral geniculate nucleus to the striate cortex in the macaque monkey , 1999, Vision Research.

[15]  Pascal Barone,et al.  Contrast Adaptation Contributes to Contrast-Invariance of Orientation Tuning of Primate V1 Cells , 2009, PloS one.

[16]  A. Straw,et al.  Contrast sensitivity of insect motion detectors to natural images. , 2008, Journal of vision.

[17]  P Fattori,et al.  Functional properties of neurons in area V1 of awake macaque monkeys: peripheral versus central visual field representation. , 1993, Archives italiennes de biologie.

[18]  Paul R. Martin,et al.  Spatial coding and response redundancy in parallel visual pathways of the marmoset Callithrix jacchus , 2005, Visual Neuroscience.

[19]  E. Schwartz,et al.  Cerebral Cortex doi:10.1093/cercor/bhn016 The Intrinsic Shape of Human and Macaque Primary Visual Cortex , 2008 .

[20]  Alexander Thiele,et al.  Speed skills: measuring the visual speed analyzing properties of primate MT neurons , 2001, Nature Neuroscience.

[21]  G. Elston,et al.  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 , 1998, The Journal of comparative neurology.

[22]  J. Perrone A Single Mechanism Can Explain the Speed Tuning Properties of MT and V1 Complex Neurons , 2006, The Journal of Neuroscience.

[23]  Leslie G. Ungerleider,et al.  Organization of visual inputs to the inferior temporal and posterior parietal cortex in macaques , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[24]  M. J. Wright,et al.  Visual motion and cortical velocity , 1983, Nature.

[25]  BsnNr C. Srorn,et al.  CLASSIFYING SIMPLE AND COMPLEX CELLS ON THE BASIS OF RESPONSE MODULATION , 2002 .

[26]  J. Movshon,et al.  Spatial and temporal contrast sensitivity of neurones in areas 17 and 18 of the cat's visual cortex. , 1978, The Journal of physiology.

[27]  D. G. Albrecht,et al.  Visual cortical receptive fields in monkey and cat: Spatial and temporal phase transfer function , 1989, Vision Research.

[28]  J. Movshon,et al.  Spatial and temporal contrast sensitivity of striate cortical neurones , 1975, Nature.

[29]  D. Purves,et al.  Correlated Size Variations in Human Visual Cortex, Lateral Geniculate Nucleus, and Optic Tract , 1997, The Journal of Neuroscience.

[30]  Jeffrey B. Nyquist,et al.  Spatial and temporal limits of motion perception across variations in speed, eccentricity, and low vision. , 2009, Journal of vision.

[31]  D. Tolhurst,et al.  Spatial‐frequency tuning and geniculocortical projections in the visual cortex (areas 17 and 18) of the pigmented ferret , 1998, The European journal of neuroscience.

[32]  John A. Perrone,et al.  A visual motion sensor based on the properties of V1 and MT neurons , 2004, Vision Research.

[33]  M. Rosa,et al.  A distinct anatomical network of cortical areas for analysis of motion in far peripheral vision , 2006, The European journal of neuroscience.

[34]  C. Baker,et al.  Spatio-temporal frequency separability in area 18 neurons of the cat , 1993, Vision Research.

[35]  M. Wong-Riley Changes in the visual system of monocularly sutured or enucleated cats demonstrable with cytochrome oxidase histochemistry , 1979, Brain Research.

[36]  Alexander Thiele,et al.  A model of speed tuning in MT neurons , 2002, Vision Research.

[37]  S. McKee,et al.  The detection of motion in the peripheral visual field , 1984, Vision Research.

[38]  S J Anderson,et al.  Peripheral spatial vision: limits imposed by optics, photoreceptors, and receptor pooling. , 1991, Journal of the Optical Society of America. A, Optics and image science.

[39]  R. Holub,et al.  Response of Visual Cortical Neurons of the cat to moving sinusoidal gratings: response-contrast functions and spatiotemporal interactions. , 1981, Journal of neurophysiology.

[40]  D. H. Kelly Retinal inhomogeneity. I. Spatiotemporal contrast sensitivity. , 1984, Journal of the Optical Society of America. A, Optics and image science.

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

[42]  A. Berthoz,et al.  Perception of linear horizontal self-motion induced by peripheral vision (linearvection) basic characteristics and visual-vestibular interactions , 1975, Experimental Brain Research.

[43]  J. Dichgans,et al.  Differential effects of central versus peripheral vision on egocentric and exocentric motion perception , 1973, Experimental Brain Research.

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

[45]  Nicholas J. Priebe,et al.  Tuning for Spatiotemporal Frequency and Speed in Directionally Selective Neurons of Macaque Striate Cortex , 2006, The Journal of Neuroscience.

[46]  J. Rovamo,et al.  Visual resolution, contrast sensitivity, and the cortical magnification factor , 2004, Experimental Brain Research.

[47]  Leo L. Lui,et al.  Spatial and temporal frequency selectivity of neurons in the middle temporal visual area of new world monkeys (Callithrix jacchus) , 2007, The European journal of neuroscience.

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

[49]  A. Berthoz,et al.  Visual contribution to rapid motor responses during postural control , 1978, Brain Research.

[50]  Leo L. Lui,et al.  Functional response properties of neurons in the dorsomedial visual area of New World monkeys (Callithrix jacchus). , 2006, Cerebral cortex.

[51]  J. Rovamo,et al.  Temporal contrast sensitivity and cortical magnification , 1982, Vision Research.

[52]  W. H. Dobelle,et al.  The topography and variability of the primary visual cortex in man. , 1974, Journal of neurosurgery.

[53]  E. Switkes,et al.  Functional anatomy of macaque striate cortex. V. Spatial frequency , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[54]  M P Eckert,et al.  Efficient coding of natural time varying images in the early visual system. , 1993, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[55]  E. Switkes,et al.  Functional anatomy of macaque striate cortex. III. Color , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[56]  D. Ruppert The Elements of Statistical Learning: Data Mining, Inference, and Prediction , 2004 .

[57]  Robert O. Duncan,et al.  Cortical Magnification within Human Primary Visual Cortex Correlates with Acuity Thresholds , 2003, Neuron.

[58]  B. B. Lee,et al.  Topography of ganglion cells and photoreceptors in the retina of a New World monkey: The marmoset Callithrix jacchus , 1996, Visual Neuroscience.

[59]  P. Bessou,et al.  Specificity of the monocular crescents of the visual field in postural control. , 1999, Comptes rendus de l'Academie des sciences. Serie III, Sciences de la vie.

[60]  Nicholas J. Priebe,et al.  The Neural Representation of Speed in Macaque Area MT/V5 , 2003, The Journal of Neuroscience.

[61]  A. Yuille,et al.  A model for the estimate of local image velocity by cells in the visual cortex , 1990, Proceedings of the Royal Society of London. B. Biological Sciences.

[62]  A. Hyvärinen,et al.  Spatial frequency tuning in human retinotopic visual areas. , 2008, Journal of vision.

[63]  RussLL L. Ds Vnlos,et al.  SPATIAL FREQUENCY SELECTIVITY OF CELLS IN MACAQUE VISUAL CORTEX , 2022 .

[64]  G. Elston,et al.  Visual Responses of Neurons in the Middle Temporal Area of New World Monkeys after Lesions of Striate Cortex , 2000, The Journal of Neuroscience.

[65]  C Blakemore,et al.  Functional architecture of area 17 in normal and monocularly deprived marmosets (Callithrix jacchus) , 1996, Visual Neuroscience.

[66]  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.

[67]  John H. R. Maunsell,et al.  The visual field representation in striate cortex of the macaque monkey: Asymmetries, anisotropies, and individual variability , 1984, Vision Research.

[68]  S. Grossberg,et al.  Neural dynamics of motion perception: Direction fields, apertures, and resonant grouping , 1993, Perception & psychophysics.

[69]  G. Orban,et al.  Velocity sensitivity and direction selectivity of neurons in areas V1 and V2 of the monkey: influence of eccentricity. , 1986, Journal of neurophysiology.

[70]  R Gattass,et al.  Topographic organization of cortical input to striate cortex in the Cebus monkey: A fluorescent tracer study , 1991, The Journal of comparative neurology.

[71]  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.

[72]  G. DeAngelis,et al.  A Logarithmic, Scale-Invariant Representation of Speed in Macaque Middle Temporal Area Accounts for Speed Discrimination Performance , 2005, The Journal of Neuroscience.

[73]  G. Johansson Studies on Visual Perception of Locomotion , 1977, Perception.