A Model of the Ventral Visual System Based on Temporal Stability and Local Memory

The cerebral cortex is a remarkably homogeneous structure suggesting a rather generic computational machinery. Indeed, under a variety of conditions, functions attributed to specialized areas can be supported by other regions. However, a host of studies have laid out an ever more detailed map of functional cortical areas. This leaves us with the puzzle of whether different cortical areas are intrinsically specialized, or whether they differ mostly by their position in the processing hierarchy and their inputs but apply the same computational principles. Here we show that the computational principle of optimal stability of sensory representations combined with local memory gives rise to a hierarchy of processing stages resembling the ventral visual pathway when it is exposed to continuous natural stimuli. Early processing stages show receptive fields similar to those observed in the primary visual cortex. Subsequent stages are selective for increasingly complex configurations of local features, as observed in higher visual areas. The last stage of the model displays place fields as observed in entorhinal cortex and hippocampus. The results suggest that functionally heterogeneous cortical areas can be generated by only a few computational principles and highlight the importance of the variability of the input signals in forming functional specialization.

[1]  D. Hubel,et al.  Receptive fields, binocular interaction and functional architecture in the cat's visual cortex , 1962, The Journal of physiology.

[2]  W. Precht The synaptic organization of the brain G.M. Shepherd, Oxford University Press (1975). 364 pp., £3.80 (paperback) , 1976, Neuroscience.

[3]  R. Passingham The hippocampus as a cognitive map J. O'Keefe & L. Nadel, Oxford University Press, Oxford (1978). 570 pp., £25.00 , 1979, Neuroscience.

[4]  E H Adelson,et al.  Spatiotemporal energy models for the perception of motion. , 1985, Journal of the Optical Society of America. A, Optics and image science.

[5]  R. Muller,et al.  The effects of changes in the environment on the spatial firing of hippocampal complex-spike cells , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[6]  M. Sur,et al.  Experimentally induced visual projections into auditory thalamus and cortex. , 1988, Science.

[7]  E. Bostock,et al.  Experience‐dependent modifications of hippocampal place cell firing , 1991, Hippocampus.

[8]  Peter Földiák,et al.  Learning Invariance from Transformation Sequences , 1991, Neural Comput..

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

[10]  Minami Ito,et al.  Size and position invariance of neuronal responses in monkey inferotemporal cortex. , 1995, Journal of neurophysiology.

[11]  Guy M. Wallis,et al.  Using Spatio-temporal Correlations to Learn Invariant Object Recognition , 1996, Neural Networks.

[12]  J. O’Keefe,et al.  Geometric determinants of the place fields of hippocampal neurons , 1996, Nature.

[13]  David J. Field,et al.  Emergence of simple-cell receptive field properties by learning a sparse code for natural images , 1996, Nature.

[14]  Keiji Tanaka,et al.  Representation of Visual Features of Objects in the Inferotemporal Cortex , 1996, Neural Networks.

[15]  E. Rolls,et al.  INVARIANT FACE AND OBJECT RECOGNITION IN THE VISUAL SYSTEM , 1997, Progress in Neurobiology.

[16]  Nancy Kanwisher,et al.  A cortical representation of the local visual environment , 1998, Nature.

[17]  B L McNaughton,et al.  Interpreting neuronal population activity by reconstruction: unified framework with application to hippocampal place cells. , 1998, Journal of neurophysiology.

[18]  The Neuropsychological Theories of Lashley and Hebb: Contemporary Perspectives Fifty Years After Hebb's the Organization of Behavior : Vanuxem Lectures and Selected Theoretical Papers of Lashley , 1998 .

[19]  Suzanna Becker,et al.  Implicit Learning in 3D Object Recognition: The Importance of Temporal Context , 1999, Neural Computation.

[20]  T. Poggio,et al.  Hierarchical models of object recognition in cortex , 1999, Nature Neuroscience.

[21]  R. Vogels Categorization of complex visual images by rhesus monkeys. Part 2: single‐cell study , 1999, The European journal of neuroscience.

[22]  C. Connor,et al.  Responses to contour features in macaque area V4. , 1999, Journal of neurophysiology.

[23]  J. Hegdé,et al.  Selectivity for Complex Shapes in Primate Visual Area V2 , 2000, The Journal of Neuroscience.

[24]  C. Koch,et al.  Category-specific visual responses of single neurons in the human medial temporal lobe , 2000, Nature Neuroscience.

[25]  M. Sur,et al.  Development and plasticity of cortical areas and networks , 2001, Nature Reviews Neuroscience.

[26]  Michael S. Lewicki,et al.  Efficient coding of natural sounds , 2002, Nature Neuroscience.

[27]  Terrence J. Sejnowski,et al.  Slow Feature Analysis: Unsupervised Learning of Invariances , 2002, Neural Computation.

[28]  Nikos K. Logothetis,et al.  The Effect of Image Scrambling on Visual Cortical BOLD Activity in the Anesthetized Monkey , 2002, NeuroImage.

[29]  Brian Lau,et al.  Computational subunits of visual cortical neurons revealed by artificial neural networks , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[30]  Jennifer Mundale Concepts of Localization: Balkanization in the Brain , 2002 .

[31]  Konrad P. Körding,et al.  Learning the Nonlinearity of Neurons from Natural Visual Stimuli , 2003, Neural Computation.

[32]  R. Malach,et al.  Early ‘visual’ cortex activation correlates with superior verbal memory performance in the blind , 2003, Nature Neuroscience.

[33]  Heiko Wersing,et al.  Learning Optimized Features for Hierarchical Models of Invariant Object Recognition , 2003, Neural Computation.

[34]  R. Douglas,et al.  Neuronal circuits of the neocortex. , 2004, Annual review of neuroscience.

[35]  Konrad Paul Kording,et al.  How are complex cell properties adapted to the statistics of natural stimuli? , 2004, Journal of neurophysiology.

[36]  D. Gadian,et al.  Language reorganization in children with early-onset lesions of the left hemisphere: an fMRI study. , 2004, Brain : a journal of neurology.

[37]  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.

[38]  Daniel L. Schacter,et al.  Spatial Representation in the Entorhinal Cortex , 2004 .

[39]  Florentin Woergoetter Faculty Opinions recommendation of A model of the ventral visual system based on temporal stability and local memory. , 2006 .

[40]  Yoonsuck Choe,et al.  Motion-Based Autonomous Grounding: Inferring External World Properties from Encoded Internal Sensory States Alone , 2006, AAAI.