Shape perception reduces activity in human primary visual cortex

Visual perception involves the grouping of individual elements into coherent patterns that reduce the descriptive complexity of a visual scene. The physiological basis of this perceptual simplification remains poorly understood. We used functional MRI to measure activity in a higher object processing area, the lateral occipital complex, and in primary visual cortex in response to visual elements that were either grouped into objects or randomly arranged. We observed significant activity increases in the lateral occipital complex and concurrent reductions of activity in primary visual cortex when elements formed coherent shapes, suggesting that activity in early visual areas is reduced as a result of grouping processes performed in higher areas. These findings are consistent with predictive coding models of vision that postulate that inferences of high-level areas are subtracted from incoming sensory information in lower areas through cortical feedback.

[1]  S. Edelman,et al.  Cue-Invariant Activation in Object-Related Areas of the Human Occipital Lobe , 1998, Neuron.

[2]  C. Gilbert,et al.  Topography of contextual modulations mediated by short-range interactions in primary visual cortex , 1999, Nature.

[3]  Judea Pearl,et al.  Probabilistic reasoning in intelligent systems - networks of plausible inference , 1991, Morgan Kaufmann series in representation and reasoning.

[4]  A. Dale,et al.  Cortical Surface-Based Analysis II: Inflation, Flattening, and a Surface-Based Coordinate System , 1999, NeuroImage.

[5]  Josh H. McDermott,et al.  Functional imaging of human visual recognition. , 1996, Brain research. Cognitive brain research.

[6]  D. Wilkin,et al.  Neuron , 2001, Brain Research.

[7]  Bartlett W. Mel SEEMORE: Combining Color, Shape, and Texture Histogramming in a Neurally Inspired Approach to Visual Object Recognition , 1997, Neural Computation.

[8]  D. M. Green,et al.  Signal detection theory and psychophysics , 1966 .

[9]  N. Kanwisher,et al.  Cortical Regions Involved in Perceiving Object Shape , 2000, The Journal of Neuroscience.

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

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

[12]  Á. Pascual-Leone,et al.  Fast Backprojections from the Motion to the Primary Visual Area Necessary for Visual Awareness , 2001, Science.

[13]  Anders M. Dale,et al.  Cortical Surface-Based Analysis I. Segmentation and Surface Reconstruction , 1999, NeuroImage.

[14]  M Corbetta,et al.  Attentional modulation of neural processing of shape, color, and velocity in humans. , 1990, Science.

[15]  G. Recanzone,et al.  Expansion of the cortical representation of a specific skin field in primary somatosensory cortex by intracortical microstimulation. , 1992, Cerebral cortex.

[16]  M. Gazzaniga,et al.  The new cognitive neurosciences , 2000 .

[17]  Victor A. F. Lamme The neurophysiology of figure-ground segregation in primary visual cortex , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[18]  J. M. Hupé,et al.  Cortical feedback improves discrimination between figure and background by V1, V2 and V3 neurons , 1998, Nature.

[19]  H. Cunningham,et al.  Percepts of rigid motion within and across apertures. , 1991, Journal of experimental psychology. Human perception and performance.

[20]  Edward H. Adelson,et al.  Motion illusions as optimal percepts , 2002, Nature Neuroscience.

[21]  M. Lévesque Perception , 1986, The Yale Journal of Biology and Medicine.

[22]  Jared Rutter,et al.  Regulation of Clock and NPAS2 DNA Binding by the Redox State of NAD Cofactors , 2001, Science.

[23]  Kunihiko Fukushima,et al.  Neocognitron: A self-organizing neural network model for a mechanism of pattern recognition unaffected by shift in position , 1980, Biological Cybernetics.

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

[25]  Vision Research , 1961, Nature.

[26]  Karl J. Friston,et al.  Analysis of functional MRI time‐series , 1994, Human Brain Mapping.

[27]  E H Adelson,et al.  Beyond Junctions: Nonlocal form Constraints on Motion Interpretation , 2001, Perception.

[28]  A. Hasman,et al.  Probabilistic reasoning in intelligent systems: Networks of plausible inference , 1991 .

[29]  Maggie Shiffrar,et al.  The influence of terminators on motion integration across space , 1992, Vision Research.

[30]  S. Lisberger,et al.  Analysis of a naturally occurring asymmetry in vertical smooth pursuit eye movements in a monkey. , 1992, Journal of neurophysiology.

[31]  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.

[32]  Rajesh P. N. Rao,et al.  Predictive coding in the visual cortex: a functional interpretation of some extra-classical receptive-field effects. , 1999 .

[33]  T. Hendler,et al.  A hierarchical axis of object processing stages in the human visual cortex. , 2001, Cerebral cortex.

[34]  A Berthoz,et al.  Visual perception of motion and 3-D structure from motion: an fMRI study. , 2000, Cerebral cortex.

[35]  Stephen A. Engel,et al.  Neural Response to Perception of Volume in the Lateral Occipital Complex , 2001, Neuron.

[36]  D. Mumford On the computational architecture of the neocortex , 2004, Biological Cybernetics.