A neurobiological model of visual attention and invariant pattern recognition based on dynamic routing of information

We present a biologically plausible model of an attentional mechanism for forming position- and scale-invariant representations of objects in the visual world. The model relies on a set of control neurons to dynamically modify the synaptic strengths of intracortical connections so that information from a windowed region of primary visual cortex (V1) is selectively routed to higher cortical areas. Local spatial relationships (i.e., topography) within the attentional window are preserved as information is routed through the cortex. This enables attended objects to be represented in higher cortical areas within an object-centered reference frame that is position and scale invariant. We hypothesize that the pulvinar may provide the control signals for routing information through the cortex. The dynamics of the control neurons are governed by simple differential equations that could be realized by neurobiologically plausible circuits. In preattentive mode, the control neurons receive their input from a low-level “saliency map” representing potentially interesting regions of a scene. During the pattern recognition phase, control neurons are driven by the interaction between top-down (memory) and bottom-up (retinal input) sources. The model respects key neurophysiological, neuroanatomical, and psychophysical data relating to attention, and it makes a variety of experimentally testable predictions.

[1]  W. Pitts,et al.  How we know universals; the perception of auditory and visual forms. , 1947, The Bulletin of mathematical biophysics.

[2]  J. R. Lee,et al.  How Does the Striate Cortex Begin the Reconstruction of the Visual World? , 1971, Science.

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

[4]  R. Wurtz,et al.  Activity of superior colliculus in behaving monkey. I. Visual receptive fields of single neurons. , 1972, Journal of neurophysiology.

[5]  Mortimer Mishkin,et al.  Cortical Visual Areas and Their Interactions , 1972 .

[6]  S M Anstis,et al.  Letter: A chart demonstrating variations in acuity with retinal position. , 1974, Vision research.

[7]  D Marr,et al.  Cooperative computation of stereo disparity. , 1976, Science.

[8]  D B Lindsley,et al.  Effect of pulvinar lesions on visual pattern discrimination in monkeys. , 1976, Journal of neurophysiology.

[9]  A. Hendrickson,et al.  The distribution of pulvinar terminals in visual areas 17 and 18 of the monkey , 1977, Brain Research.

[10]  P Cavanagh,et al.  Size and Position Invariance in the Visual System , 1978, Perception.

[11]  D. Robinson,et al.  Parietal association cortex in the primate: sensory mechanisms and behavioral modulations. , 1978, Journal of neurophysiology.

[12]  A I Basbaum,et al.  Brainstem control of spinal pain-transmission neurons. , 1978, Annual review of physiology.

[13]  L. Benevento,et al.  A comparison of the organization of the projections of the dorsal lateral geniculate nucleus, the inferior pulvinar and adjacent lateral pulvinar to primary visual cortex (area 17) in the macaque monkey , 1979, Brain Research.

[14]  A. Hendrickson,et al.  The structural organization of the inferior and lateral subdivision of the Macaca monkey pulvinar , 1979, The Journal of comparative neurology.

[15]  D. Robinson,et al.  Behavioral enhancement of visual responses in monkey cerebral cortex. I. Modulation in posterior parietal cortex related to selective visual attention. , 1981, Journal of neurophysiology.

[16]  Geoffrey E. Hinton.  A Parallel Computation that Assigns Canonical Object-Based Frames of Reference , 1981, IJCAI.

[17]  B. C. Motter,et al.  The influence of attentive fixation upon the excitability of the light- sensitive neurons of the posterior parietal cortex , 1981, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[18]  I. Ohzawa,et al.  Contrast gain control in the cat visual cortex , 1982, Nature.

[19]  Leslie G. Ungerleider.  Two cortical visual systems , 1982 .

[20]  M. Colonnier,et al.  A laminar analysis of the number of neurons, glia, and synapses in the visual cortex (area 17) of adult macaque monkeys , 1982, The Journal of comparative neurology.

[21]  J J Hopfield,et al.  Neural networks and physical systems with emergent collective computational abilities. , 1982, Proceedings of the National Academy of Sciences of the United States of America.

[22]  Y. Tsal.  Movements of attention across the visual field. , 1983, Journal of experimental psychology. Human perception and performance.

[23]  S. Palmer.  The Psychology of Perceptual Organization: A Transformational Approach , 1983 .

[24]  James R. Bergen,et al.  Parallel versus serial processing in rapid pattern discrimination , 1983, Nature.

[25]  F. J. Friedrich,et al.  Effects of parietal injury on covert orienting of attention , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[26]  J J Hopfield,et al.  Neurons with graded response have collective computational properties like those of two-state neurons. , 1984, Proceedings of the National Academy of Sciences of the United States of America.

[27]  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.

[28]  F. Crick.  Function of the thalamic reticular complex: the searchlight hypothesis. , 1984, Proceedings of the National Academy of Sciences of the United States of America.

[29]  D. Bouwhuis,et al.  Attention and performance X : control of language processes , 1986 .

[30]  M. Posner,et al.  Components of visual orienting , 1984 .

[31]  D. B. Bender,et al.  Effects of kainic acid and radiofrequency lesions of the pulvinar on visual discrimination in the monkey , 1984, Brain Research.

[32]  R. Remington,et al.  Moving attention: Evidence for time-invariant shifts of visual selective attention , 1984, Perception & psychophysics.

[33]  S. Petersen,et al.  Pulvinar nuclei of the behaving rhesus monkey: visual responses and their modulation. , 1985, Journal of neurophysiology.

[34]  S Ullman,et al.  Shifts in selective visual attention: towards the underlying neural circuitry. , 1985, Human neurobiology.

[35]  Patrick Cavanagh,et al.  Local log polar frequency analysis in the striate cortex as a basis for size and orientation invariance , 1985 .

[36]  Geoffrey E. Hinton,et al.  Shape Recognition and Illusory Conjunctions , 1985, IJCAI.

[37]  Ellen Covey,et al.  Cortical Visual Areas of the Macaque: Possible Substrates for Pattern Recognition Mechanisms , 1985 .

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

[39]  John H. R. Maunsell,et al.  The projections from striate cortex (V1) to areas V2 and V3 in the macaque monkey: Asymmetries, areal boundaries, and patchy connections , 1986, The Journal of comparative neurology.

[40]  C. Eriksen,et al.  Visual attention within and around the field of focal attention: A zoom lens model , 1986, Perception & psychophysics.

[41]  D C Van Essen,et al.  Shifter circuits: a computational strategy for dynamic aspects of visual processing. , 1987, Proceedings of the National Academy of Sciences of the United States of America.

[42]  R. Desimone,et al.  Visual properties of neurons in area V4 of the macaque: sensitivity to stimulus form. , 1987, Journal of neurophysiology.

[43]  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.

[44]  C. Eriksen,et al.  Movement of attentional focus across the visual field: A critical look at the evidence , 1987, Perception & psychophysics.

[45]  S. Petersen,et al.  Contributions of the pulvinar to visual spatial attention , 1987, Neuropsychologia.

[46]  K. Fukushima.  Neural network model for selective attention in visual pattern recognition and associative recall. , 1987, Applied optics.

[47]  R. Baron.  The cerebral computer , 1987 .

[48]  J Wilson,et al.  Spatial Frequency and Selective Attention to Local and Global Information , 1987, Perception.

[49]  A. Treisman.  Features and Objects: The Fourteenth Bartlett Memorial Lecture , 1988, The Quarterly journal of experimental psychology. A, Human experimental psychology.

[50]  R. Llinás.  The intrinsic electrophysiological properties of mammalian neurons: insights into central nervous system function. , 1988, Science.

[51]  D. Whitteridge,et al.  Selective responses of visual cortical cells do not depend on shunting inhibition , 1988, Nature.

[52]  Pentti Kanerva,et al.  Sparse Distributed Memory , 1988 .

[53]  K D Miller,et al.  Visual responses in adult cat visual cortex depend on N-methyl-D-aspartate receptors. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[54]  K. Nakayama,et al.  Sustained and transient components of focal visual attention , 1989, Vision Research.

[55]  Lawrence D. Jackel,et al.  Backpropagation Applied to Handwritten Zip Code Recognition , 1989, Neural Computation.

[56]  David LaBerge,et al.  Thalamic and Cortical Mechanisms of Attention Suggested by Recent Positron Emission Tomographic Experiments , 1990, Journal of Cognitive Neuroscience.

[57]  P. A. Sandon.  Simulating Visual Attention , 1990, Journal of Cognitive Neuroscience.

[58]  Joachim M. Buhmann,et al.  Size and distortion invariant object recognition by hierarchical graph matching , 1990, 1990 IJCNN International Joint Conference on Neural Networks.

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

[60]  C. Koch,et al.  Towards a neurobiological theory of consciousness , 1990 .

[61]  R. Desimone,et al.  Attentional control of visual perception: cortical and subcortical mechanisms. , 1990, Cold Spring Harbor symposia on quantitative biology.

[62]  C. Cherniak.  The Bounded Brain: Toward Quantitative Neuroanatomy , 1990, Journal of Cognitive Neuroscience.

[63]  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.

[64]  M. Posner,et al.  The attention system of the human brain. , 1990, Annual review of neuroscience.

[65]  Michael Conley,et al.  Organization of the Visual Sector of the Thalamic Reticular Nucleus in Galago , 1990, The European journal of neuroscience.

[66]  C. Blakemore,et al.  Vision: The iconic bottleneck and the tenuous link between early visual processing and perception , 1990 .

[67]  Kevan A. C. Martin,et al.  Control of Neuronal Output by Inhibition at the Axon Initial Segment , 1990, Neural Computation.

[68]  David C. Van Essen,et al.  Information processing strategies and pathways in the primate retina and visual cortex , 1990 .

[69]  D. C. Essen,et al.  Modular and hierarchical organization of extrastriate visual cortex in the macaque monkey. , 1990, Cold Spring Harbor symposia on quantitative biology.

[70]  I. Biederman,et al.  Evidence for Complete Translational and Reflectional Invariance in Visual Object Priming , 1991, Perception.

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

[72]  B Julesz,et al.  The speed of attentional shifts in the visual field. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[73]  Subutai Ahmad,et al.  VISIT: A Neural Model of Covert Visual Attention , 1991, NIPS.

[74]  Bruno A. Olshausen,et al.  Pattern recognition, attention, and information bottlenecks in the primate visual system , 1991, Defense, Security, and Sensing.

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

[76]  M. Corbetta,et al.  Selective and divided attention during visual discriminations of shape, color, and speed: functional anatomy by positron emission tomography , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[77]  P Cavanagh,et al.  Attention-based motion perception. , 1992, Science.

[78]  T. Poggio,et al.  Multiplying with synapses and neurons , 1992 .

[79]  Bartlett W. Mel.  NMDA-Based Pattern Discrimination in a Modeled Cortical Neuron , 1992, Neural Computation.

[80]  David LaBerge,et al.  A Network Simulation of Thalamic Circuit Operations in Selective Attention , 1992, Neural Computation.

[81]  Mriganka Sur,et al.  NMDA receptors in sensory information processing , 1992, Current Opinion in Neurobiology.

[82]  J R Duhamel,et al.  The updating of the representation of visual space in parietal cortex by intended eye movements. , 1992, Science.

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

[84]  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.

[85]  K. Sillar.  Spinal pattern generation and sensory gating mechanisms , 1992, Current Biology.

[86]  D. Pelli,et al.  The information capacity of visual attention , 1992, Vision Research.

[87]  R. Douglas,et al.  GABA-mediated inhibition in the neural networks of visual cortex. , 1992, Progress in brain research.

[88]  D Mumford,et al.  On the computational architecture of the neocortex. II. The role of cortico-cortical loops. , 1992, Biological cybernetics.

[89]  A. Morel,et al.  Segregated thalamocortical pathways to inferior parietal and inferotemporal cortex in macaque monkey , 1992, Visual Neuroscience.

[90]  C. Koch,et al.  An oscillation-based model for the neuronal basis of attention , 1993, Vision Research.

[91]  Eric O. Postma,et al.  The Gating Lattice: A Neural Substrate for Dynamic Gating , 1993 .

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

[93]  Bruno A. Olshausen,et al.  Dynamic routing strategies in sensory, motor, and cognitive processing , 1994 .