Population receptive field estimates in human visual cortex

We introduce functional MRI methods for estimating the neuronal population receptive field (pRF). These methods build on conventional visual field mapping that measures responses to ring and wedge patterns shown at a series of visual field locations and estimates the single position in the visual field that produces the largest response. The new method computes a model of the population receptive field from responses to a wide range of stimuli and estimates the visual field map as well as other neuronal population properties, such as receptive field size and laterality. The visual field maps obtained with the pRF method are more accurate than those obtained using conventional visual field mapping, and we trace with high precision the visual field maps to the center of the foveal representation. We report quantitative estimates of pRF size in medial, lateral and ventral occipital regions of human visual cortex. Also, we quantify the amount of input from ipsi- and contralateral visual fields. The human pRF size estimates in V1-V3 agree well with electrophysiological receptive field measurements at a range of eccentricities in corresponding locations within monkey and human visual field maps. The pRF method is non-invasive and can be applied to a wide range of conditions when it is useful to link fMRI signals in the visual pathways to neuronal receptive fields.

[1]  C. Gilbert,et al.  Long-range horizontal connections and their role in cortical reorganization revealed by optical recording of cat primary visual cortex , 1995, Nature.

[2]  N. Kanwisher,et al.  The lateral occipital complex and its role in object recognition , 2001, Vision Research.

[3]  Alex R. Wade,et al.  Two-dimensional mapping of the central and parafoveal visual field to human visual cortex. , 2007, Journal of neurophysiology.

[4]  R. W. Rodieck.  The First Steps in Seeing , 1998 .

[5]  M. Carrasco,et al.  Transient Attention Enhances Perceptual Performance and fMRI Response in Human Visual Cortex , 2005, Neuron.

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

[7]  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.

[8]  Behzad Mansouri,et al.  The fidelity of the cortical retinotopic map in human amblyopia , 2007, The European journal of neuroscience.

[9]  Guy Marchal,et al.  Multimodality image registration by maximization of mutual information , 1997, IEEE Transactions on Medical Imaging.

[10]  Brian A Wandell,et al.  Visual field map clusters in human cortex , 2005, Philosophical Transactions of the Royal Society B: Biological Sciences.

[11]  P. Bandettini,et al.  Spatial Heterogeneity of the Nonlinear Dynamics in the FMRI BOLD Response , 2001, NeuroImage.

[12]  Roger Fletcher,et al.  A Rapidly Convergent Descent Method for Minimization , 1963, Comput. J..

[13]  R. Malach,et al.  Object-related activity revealed by functional magnetic resonance imaging in human occipital cortex. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[14]  T. Ebner,et al.  Local and propagated vascular responses evoked by focal synaptic activity in cerebellar cortex. , 1997, Journal of neurophysiology.

[15]  Talma Hendler,et al.  Center–periphery organization of human object areas , 2001, Nature Neuroscience.

[16]  N. Logothetis,et al.  Neurophysiological investigation of the basis of the fMRI signal , 2001, Nature.

[17]  Matthias Niemeier,et al.  A contralateral preference in the lateral occipital area: sensory and attentional mechanisms. , 2004, Cerebral cortex.

[18]  M. D’Esposito,et al.  The Variability of Human, BOLD Hemodynamic Responses , 1998, NeuroImage.

[19]  D. Heeger,et al.  Two Retinotopic Visual Areas in Human Lateral Occipital Cortex , 2006, The Journal of Neuroscience.

[20]  Karl J. Friston,et al.  Human Brain Function , 1997 .

[21]  Andrew T. Smith,et al.  Surround modulation measured with functional MRI in the human visual cortex. , 2003, Journal of neurophysiology.

[22]  Nikos K Logothetis,et al.  Interpreting the BOLD signal. , 2004, Annual review of physiology.

[23]  David J Heeger,et al.  Neural correlates of sustained spatial attention in human early visual cortex. , 2007, Journal of neurophysiology.

[24]  B. Fischer,et al.  Visual field representations and locations of visual areas V1/2/3 in human visual cortex. , 2003, Journal of vision.

[25]  R. Hess,et al.  Modulation of V1 activity by shape: image-statistics or shape-based perception? , 2006, Journal of neurophysiology.

[26]  Gabriele Lohmann,et al.  Within-subject variability of BOLD response dynamics , 2003, NeuroImage.

[27]  D H Brainard,et al.  The Psychophysics Toolbox. , 1997, Spatial vision.

[28]  G. Glover,et al.  Retinotopic organization in human visual cortex and the spatial precision of functional MRI. , 1997, Cerebral cortex.

[29]  R Gattass,et al.  Representation of the visual field in the second visual area in the Cebus monkey , 1988, The Journal of comparative neurology.

[30]  Mark D'Esposito,et al.  Variation of BOLD hemodynamic responses across subjects and brain regions and their effects on statistical analyses , 2004, NeuroImage.

[31]  D G Pelli,et al.  The VideoToolbox software for visual psychophysics: transforming numbers into movies. , 1997, Spatial vision.

[32]  E. DeYoe,et al.  Mapping striate and extrastriate visual areas in human cerebral cortex. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[33]  C. Gross,et al.  Visual topography of V2 in the macaque , 1981, The Journal of comparative neurology.

[34]  Alan C. Evans,et al.  Automatic volumetric segmentation of human visual retinotopic cortex , 2003, NeuroImage.

[35]  A. Dale,et al.  New images from human visual cortex , 1996, Trends in Neurosciences.

[36]  Ricardo Gattass,et al.  Third tier ventral extrastriate cortex in the New World monkey, Cebus apella , 2000, Experimental Brain Research.

[37]  D Le Bihan,et al.  Detection of fMRI activation using Cortical Surface Mapping , 2001, Human brain mapping.

[38]  G. Glover.  Deconvolution of Impulse Response in Event-Related BOLD fMRI1 , 1999, NeuroImage.

[39]  Alan C. Evans,et al.  A general statistical analysis for fMRI data , 2000, NeuroImage.

[40]  R. Tootell,et al.  Where is 'dorsal V4' in human visual cortex? Retinotopic, topographic and functional evidence. , 2001, Cerebral cortex.

[41]  Karl J. Friston,et al.  Analysis of fMRI Time-Series Revisited , 1995, NeuroImage.

[42]  Jeff H. Duyn,et al.  Temporal dynamics of the BOLD fMRI impulse response , 2005, NeuroImage.

[43]  N. Logothetis.  The Underpinnings of the BOLD Functional Magnetic Resonance Imaging Signal , 2003, The Journal of Neuroscience.

[44]  D. V. van Essen,et al.  Processing of color, form and disparity information in visual areas VP and V2 of ventral extrastriate cortex in the macaque monkey , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[45]  Stephen V. David,et al.  Parametric reverse correlation reveals spatial linearity of retinotopic human V1 BOLD response , 2004, NeuroImage.

[46]  A. Dale,et al.  Functional Analysis of V3A and Related Areas in Human Visual Cortex , 1997, The Journal of Neuroscience.

[47]  B. Wandell,et al.  Visualization and Measurement of the Cortical Surface , 2000, Journal of Cognitive Neuroscience.

[48]  Guillermo Sapiro,et al.  Creating connected representations of cortical gray matter for functional MRI visualization , 1997, IEEE Transactions on Medical Imaging.

[49]  Karl J. Friston,et al.  Analysis of fMRI Time-Series Revisited—Again , 1995, NeuroImage.

[50]  D J Heeger,et al.  Robust multiresolution alignment of MRI brain volumes , 2000, Magnetic resonance in medicine.

[51]  J. Victor,et al.  Population encoding of spatial frequency, orientation, and color in macaque V1. , 1994, Journal of neurophysiology.

[52]  Essa Yacoub,et al.  Spatio-temporal point-spread function of fMRI signal in human gray matter at 7 Tesla , 2007, NeuroImage.

[53]  Karl J. Friston,et al.  Rigid Body Registration , 2003 .

[54]  A. Dale,et al.  The representation of the ipsilateral visual field in human cerebral cortex. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[55]  A. T. Smith,et al.  Estimating receptive field size from fMRI data in human striate and extrastriate visual cortex. , 2001, Cerebral cortex.

[56]  Scott L. Zeger,et al.  Non‐linear Fourier Time Series Analysis for Human Brain Mapping by Functional Magnetic Resonance Imaging , 1997 .

[57]  Rainer Goebel,et al.  Receptive field size-dependent attention effects in simultaneously presented stimulus displays , 2006, NeuroImage.

[58]  A. Grinvald,et al.  Interactions Between Electrical Activity and Cortical Microcirculation Revealed by Imaging Spectroscopy: Implications for Functional Brain Mapping , 1996, Science.

[59]  D. J. Felleman,et al.  Receptive field properties of neurons in area V3 of macaque monkey extrastriate cortex. , 1987, Journal of neurophysiology.

[60]  D. Somers,et al.  Functional MRI reveals spatially specific attentional modulation in human primary visual cortex. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[61]  Alex R. Wade,et al.  Visual field maps and stimulus selectivity in human ventral occipital cortex , 2005, Nature Neuroscience.

[62]  E C Wong,et al.  Processing strategies for time‐course data sets in functional mri of the human brain , 1993, Magnetic resonance in medicine.

[63]  R. Turner,et al.  Event-Related fMRI: Characterizing Differential Responses , 1998, NeuroImage.

[64]  Adrian T. Lee,et al.  fMRI of human visual cortex , 1994, Nature.

[65]  R Gattass,et al.  Visual topography of V1 in the Cebus monkey , 1987, The Journal of comparative neurology.

[66]  Wim Vanduffel,et al.  The Radial Bias: A Different Slant on Visual Orientation Sensitivity in Human and Nonhuman Primates , 2006, Neuron.

[67]  David J Heeger,et al.  Response Suppression in V1 Agrees with Psychophysics of Surround Masking , 2003, The Journal of Neuroscience.

[68]  S. Petersen,et al.  Characterizing the Hemodynamic Response: Effects of Presentation Rate, Sampling Procedure, and the Possibility of Ordering Brain Activity Based on Relative Timing , 2000, NeuroImage.

[69]  Daniel Yoshor,et al.  Receptive fields in human visual cortex mapped with surface electrodes. , 2007, Cerebral cortex.

[70]  J W Belliveau,et al.  Borders of multiple visual areas in humans revealed by functional magnetic resonance imaging. , 1995, Science.

[71]  Brian A. Wandell,et al.  Distinguishing visual field map clusters: A new paradigm , 2010 .

[72]  G. Glover,et al.  Self‐navigated spiral fMRI: Interleaved versus single‐shot , 1998, Magnetic resonance in medicine.

[73]  N. Kanwisher,et al.  A Preference for Contralateral Stimuli in Human Object- and Face-Selective Cortex , 2007, PloS one.

[74]  D. Heeger,et al.  Linear Systems Analysis of Functional Magnetic Resonance Imaging in Human V1 , 1996, The Journal of Neuroscience.

[75]  Jean-Baptiste Poline,et al.  Inverse retinotopy: Inferring the visual content of images from brain activation patterns , 2006, NeuroImage.

[76]  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.

[77]  W T Newsome,et al.  Ventral posterior visual area of the macaque: Visual topography and areal boundaries , 1986, The Journal of comparative neurology.

[78]  G H Glover,et al.  Simple analytic spiral K‐space algorithm , 1999, Magnetic resonance in medicine.

[79]  Leslie G. Ungerleider,et al.  Modulation of sensory suppression: implications for receptive field sizes in the human visual cortex. , 2001, Journal of neurophysiology.