Neuronal tuning and associative mechanisms in form representation.

We examine the hypothesis that the form representation in the anterior inferotemporal (AIT) cortex is acquired through learning. According to this hypothesis, perceptual aspects of the temporal association area are closely related to its visual representation, in that the response selectivity of AIT neurons can be influenced by visual experience. On the basis of the neurophysiological evidence, we summarize two neuronal mechanisms that subserve the acquisition of form selectivity in AIT neurons. The first mechanism is neuronal tuning to particular stimuli that were learned in a cognitive task. The second mechanism is association, with which relevant information can be retrieved from other stored memories. On the grounds that long-term memory of objects is acquired and organized by at least these two neuronal mechanisms in the temporal association area, we further present a model of the cognitive memory system that unifies perception and imagery.

[1]  Y. Miyashita Neuronal correlate of visual associative long-term memory in the primate temporal cortex , 1988, Nature.

[2]  R. Desimone,et al.  Stimulus-selective properties of inferior temporal neurons in the macaque , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[3]  D. N. Spinelli,et al.  Visual Experience Modifies Distribution of Horizontally and Vertically Oriented Receptive Fields in Cats , 1970, Science.

[4]  D. B. Bender,et al.  Visual properties of neurons in inferotemporal cortex of the Macaque. , 1972, Journal of neurophysiology.

[5]  M J Farah,et al.  Mechanisms of imagery-perception interaction. , 1989, Journal of experimental psychology. Human perception and performance.

[6]  D C Van Essen,et al.  Information processing in the primate visual system: an integrated systems perspective. , 1992, Science.

[7]  R. L. Gregory,et al.  Perceptual filling in of artificially induced scotomas in human vision , 1991, Nature.

[8]  M. Posner,et al.  Deficits in human visual spatial attention following thalamic lesions. , 1987, Proceedings of the National Academy of Sciences of the United States of America.

[9]  M. Pettet,et al.  Dynamic changes in receptive-field size in cat primary visual cortex. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[10]  I. Riches,et al.  The effects of visual stimulation and memory on neurons of the hippocampal formation and the neighboring parahippocampal gyrus and inferior temporal cortex of the primate , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[11]  Laura H. Goldstein,et al.  Verbal and Abstract Designs Paired Associate Learning After Unilateral Temporal Lobectomy , 1988, Cortex.

[12]  D. Hubel,et al.  Receptive fields of single neurones in the cat's striate cortex , 1959, The Journal of physiology.

[13]  T. Bliss,et al.  A synaptic model of memory: long-term potentiation in the hippocampus , 1993, Nature.

[14]  R. Malenka,et al.  Long-term depression: not so depressing after all. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[15]  D. LaBerge,et al.  Positron emission tomographic measurements of pulvinar activity during an attention task , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[16]  R. Desimone,et al.  The representation of stimulus familiarity in anterior inferior temporal cortex. , 1993, Journal of neurophysiology.

[17]  L. Weiskrantz,et al.  Perception of Redundant Cues by Monkeys with Inferotemporal Lesions , 1967, Nature.

[18]  Amiram Grinvald,et al.  Iso-orientation domains in cat visual cortex are arranged in pinwheel-like patterns , 1991, Nature.

[19]  J. Leo van Hemmen,et al.  Temporal association , 1991 .

[20]  A. Karni,et al.  The time course of learning a visual skill , 1993, Nature.

[21]  R. Desimone,et al.  Parallel neuronal mechanisms for short-term memory. , 1994, Science.

[22]  N. Logothetis,et al.  View-dependent object recognition by monkeys , 1994, Current Biology.

[23]  E. Adelson Perceptual organization and the judgment of brightness. , 1993, Science.

[24]  Ronen Basri,et al.  Recognition by Linear Combinations of Models , 1991, IEEE Trans. Pattern Anal. Mach. Intell..

[25]  H. Hirsch,et al.  Physiological consequences for the cat's visual cortex of effectively restricting early visual experience with oriented contours. , 1978, Journal of neurophysiology.

[26]  C. Gross Visual Functions of Inferotemporal Cortex , 1973 .

[27]  G. F. Cooper,et al.  Development of the Brain depends on the Visual Environment , 1970, Nature.

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

[29]  G Westheimer,et al.  A quantitative measure for short-term cortical plasticity in human vision , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[30]  T. Wiesel,et al.  Receptive field dynamics in adult primary visual cortex , 1992, Nature.

[31]  B. Milner,et al.  Disorders of learning and memory after temporal lobe lesions in man. , 1972, Clinical neurosurgery.

[32]  D. V. van Essen,et al.  A neurobiological model of visual attention and invariant pattern recognition based on dynamic routing of information , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[33]  C. Gross,et al.  Representation of visual stimuli in inferior temporal cortex. , 1992, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[34]  Y. Miyashita,et al.  Neuronal tuning to learned complex forms in vision. , 1994, Neuroreport.

[35]  J. Maunsell,et al.  How parallel are the primate visual pathways? , 1993, Annual review of neuroscience.

[36]  D. Marr,et al.  Representation and recognition of the spatial organization of three-dimensional shapes , 1978, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[37]  Keiji Tanaka,et al.  Coding visual images of objects in the inferotemporal cortex of the macaque monkey. , 1991, Journal of neurophysiology.

[38]  J M Fuster,et al.  Neuronal firing in the inferotemporal cortex of the monkey in a visual memory task , 1982, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[39]  H. Christopher Longuet-Higgins,et al.  Recognizing three dimensions , 1990, Nature.

[40]  P. Goldman-Rakic,et al.  Dissociation of object and spatial processing domains in primate prefrontal cortex. , 1993, Science.

[41]  Minami Ito,et al.  Columns for visual features of objects in monkey inferotemporal cortex , 1992, Nature.

[42]  Martha Wilson,et al.  Inferotemporal cortex and categorical perception of visual stimuli by monkeys , 1981, Neuropsychologia.

[43]  H. Sakai,et al.  Enhancement of inferior temporal neurons during visual discrimination. , 1987, Journal of neurophysiology.

[44]  K Tanaka,et al.  Neuronal mechanisms of object recognition. , 1993, Science.

[45]  R. Desimone,et al.  Shape recognition and inferior temporal neurons. , 1983, Proceedings of the National Academy of Sciences of the United States of America.

[46]  John Duncan,et al.  A neural basis for visual search in inferior temporal cortex , 1993, Nature.

[47]  H. Spitzer,et al.  Temporal encoding of two-dimensional patterns by single units in primate inferior temporal cortex. I. Response characteristics. , 1987, Journal of neurophysiology.

[48]  Ralph Roskies,et al.  Fourier Descriptors for Plane Closed Curves , 1972, IEEE Transactions on Computers.

[49]  A. J. Mistlin,et al.  Neurones responsive to faces in the temporal cortex: studies of functional organization, sensitivity to identity and relation to perception. , 1984, Human neurobiology.

[50]  C. B. Cave,et al.  The Role of Parts and Spatial Relations in Object Identification , 1993, Perception.

[51]  H H Bülthoff,et al.  Psychophysical support for a two-dimensional view interpolation theory of object recognition. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[52]  Y. Miyashita,et al.  Memory and imagery in the temporal lobe , 1993, Current Opinion in Neurobiology.

[53]  Leslie G. Ungerleider,et al.  ‘What’ and ‘where’ in the human brain , 1994, Current Opinion in Neurobiology.

[54]  Alex Pentland,et al.  Perceptual Organization and the Representation of Natural Form , 1986, Artif. Intell..

[55]  P. Dean Effects of inferotemporal lesions on the behavior of monkeys. , 1976, Psychological bulletin.

[56]  J. Kaas Plasticity of sensory and motor maps in adult mammals. , 1991, Annual review of neuroscience.

[57]  B. Motter Neural correlates of attentive selection for color or luminance in extrastriate area V4 , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[58]  W. Singer,et al.  The Involvement of N‐Methyl‐D‐Aspartate Receptors in Induction and Maintenance of Long‐Term Potentiation in Rat Visual Cortex , 1990, The European journal of neuroscience.

[59]  H. Spitzer,et al.  Increased attention enhances both behavioral and neuronal performance. , 1988, Science.

[60]  G. Orban,et al.  Cue-invariant shape selectivity of macaque inferior temporal neurons. , 1993, Science.

[61]  C. Gilbert,et al.  Axonal sprouting accompanies functional reorganization in adult cat striate cortex , 1994, Nature.

[62]  W R RUSSELL,et al.  The Physiology of Memory , 1958, Proceedings of the Royal Society of Medicine.

[63]  E. Miller,et al.  Habituation-like decrease in the responses of neurons in inferior temporal cortex of the macaque , 1991, Visual Neuroscience.

[64]  J. Kaas,et al.  Reorganization of retinotopic cortical maps in adult mammals after lesions of the retina. , 1990, Science.

[65]  G. Blasdel,et al.  Orientation selectivity, preference, and continuity in monkey striate cortex , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[66]  S. Petersen,et al.  The pulvinar and visual salience , 1992, Trends in Neurosciences.

[67]  V. Ramachandran,et al.  Behavioral and magnetoencephalographic correlates of plasticity in the adult human brain. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[68]  M. Petrides Deficits on conditional associative-learning tasks after frontal- and temporal-lobe lesions in man , 1985, Neuropsychologia.

[69]  Y. Miyashita,et al.  Neural organization for the long-term memory of paired associates , 1991, Nature.

[70]  L. Squire,et al.  The medial temporal lobe memory system , 1991, Science.

[71]  R. Desimone,et al.  A neural mechanism for working and recognition memory in inferior temporal cortex. , 1991, Science.

[72]  A. Damasio Category-related recognition defects as a clue to the neural substrates of knowledge , 1990, Trends in Neurosciences.

[73]  L. Squire Memory and the hippocampus: a synthesis from findings with rats, monkeys, and humans. , 1992, Psychological review.

[74]  D. V. van Essen,et al.  Selectivity for polar, hyperbolic, and Cartesian gratings in macaque visual cortex. , 1993, Science.

[75]  E Tulving,et al.  Priming and human memory systems. , 1990, Science.

[76]  K Nakayama,et al.  Experiencing and perceiving visual surfaces. , 1992, Science.

[77]  Y. Frégnac,et al.  A cellular analogue of visual cortical plasticity , 1988, Nature.

[78]  A. J. Mistlin,et al.  Visual neurones responsive to faces , 1987, Trends in Neurosciences.

[79]  R. Desimone,et al.  Selective attention gates visual processing in the extrastriate cortex. , 1985, Science.

[80]  M. Mishkin A memory system in the monkey. , 1982, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[81]  B. C. Motter Focal attention produces spatially selective processing in visual cortical areas V1, V2, and V4 in the presence of competing stimuli. , 1993, Journal of neurophysiology.

[82]  T. Poggio,et al.  A network that learns to recognize three-dimensional objects , 1990, Nature.

[83]  D. Gaffan,et al.  Hippocampus: memory, habit and voluntary movement. , 1985, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[84]  B. McNaughton,et al.  Hippocampal synaptic enhancement and information storage within a distributed memory system , 1987, Trends in Neurosciences.

[85]  J. Fuster Inferotemporal units in selective visual attention and short-term memory. , 1990, Journal of neurophysiology.

[86]  R Desimone,et al.  The physiology of memory: recordings of things past. , 1992, Science.

[87]  S. Kosslyn Aspects of a cognitive neuroscience of mental imagery. , 1988, Science.

[88]  M Mishkin,et al.  Neural substrates of visual stimulus-stimulus association in rhesus monkeys , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[89]  Donald J. Foss,et al.  Human Associative Memory: A Brief Edition. , 1981 .

[90]  M. K. Jones,et al.  Imagery as a mnemonic aid after left temporal lobectomy: contrast between material-specific and generalized memory disorders. , 1974, Neuropsychologia.

[91]  Aubrey J. Yates,et al.  INTELLECTUAL CHANGES FOLLOWING TEMPORAL LOBECTOMY FOR PSYCHOMOTOR EPILEPSY , 1955, Journal of neurology, neurosurgery, and psychiatry.

[92]  D H Hubel,et al.  Effects of monocular exposure to oriented lines on monkey striate cortex. , 1986, Brain research.

[93]  I. Biederman Recognition-by-components: a theory of human image understanding. , 1987, Psychological review.

[94]  Y. Miyashita,et al.  Neuronal correlate of pictorial short-term memory in the primate temporal cortexYasushi Miyashita , 1988, Nature.