A model for the neuronal implementation of selective visual attention based on temporal correlation among neurons

We propose a model for the neuronal implementation of selective visual attention based on temporal correlation among groups of neurons. Neurons in primary visual cortex respond to visual stimuli with a Poisson distributed spike train with an appropriate, stimulus-dependent mean firing rate. The spike trains of neurons whose receptive fields donot overlap with the “focus of attention” are distributed according to homogeneous (time-independent) Poisson process with no correlation between action potentials of different neurons. In contrast, spike trains of neurons with receptive fields within the focus of attention are distributed according to non-homogeneous (time-dependent) Poisson processes. Since the short-term average spike rates of all neurons with receptive fields in the focus of attention covary, correlations between these spike trains are introduced which are detected by inhibitory interneurons in V4. These cells, modeled as modified integrate-and-fire neurons, function as coincidence detectors and suppress the response of V4 cells associated with non-attended visual stimuli. The model reproduces quantitatively experimental data obtained in cortical area V4 of monkey by Moran and Desimone (1985).

[1]  Ch. von der Malsburg,et al.  A neural cocktail-party processor , 1986, Biological Cybernetics.

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

[3]  B J Richmond,et al.  Concurrent processing and complexity of temporally encoded neuronal messages in visual perception. , 1991, Science.

[4]  D. Sagi,et al.  Vision outside the focus of attention , 1990, Perception & psychophysics.

[5]  W. Singer,et al.  Stimulus‐Dependent Neuronal Oscillations in Cat Visual Cortex: Receptive Field Properties and Feature Dependence , 1990, The European journal of neuroscience.

[6]  R. Eckhorn,et al.  Coherent oscillations: A mechanism of feature linking in the visual cortex? , 1988, Biological Cybernetics.

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

[8]  Jon Driver,et al.  The neurobiology of selective attention , 1992, Current Opinion in Neurobiology.

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

[10]  W. Singer,et al.  Stimulus-specific neuronal oscillations in orientation columns of cat visual cortex. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[11]  B. Julesz Early vision and focal attention , 1991 .

[12]  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.

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

[14]  Leslie G. Ungerleider,et al.  The modular organization of projections from areas V1 and V2 to areas V4 and TEO in macaques , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[15]  Pierre Baldi,et al.  Computing with Arrays of Coupled Oscillators: An Application to Preattentive Texture Discrimination , 1990, Neural Computation.

[16]  W. Singer,et al.  Interhemispheric synchronization of oscillatory neuronal responses in cat visual cortex , 1991, Science.

[17]  William Bialek,et al.  Reading a Neural Code , 1991, NIPS.

[18]  William R. Softky,et al.  The highly irregular firing of cortical cells is inconsistent with temporal integration of random EPSPs , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[19]  M. Tovée,et al.  Oscillatory activity is not evident in the primate temporal visual cortex with static stimuli , 1992, Neuroreport.

[20]  W. Singer Synchronization of cortical activity and its putative role in information processing and learning. , 1993, Annual review of physiology.

[21]  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.

[22]  Tom Heskes,et al.  A Neural Model of Visual Attention , 1995, SNN Symposium on Neural Networks.

[23]  E. Azmitia Microcultures of Dissociated Primary Central Nervous System Neurons , 1990 .

[24]  K. H. Britten,et al.  Power spectrum analysis of bursting cells in area MT in the behaving monkey , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[25]  N. Kanwisher,et al.  Objects, Attributes, and Visual Attention: Which, What, and Where , 1992 .

[26]  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.

[27]  C. Colby,et al.  The Neuroanatomy and Neurophysiology of Attention , 1991 .

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

[29]  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.

[30]  W. Singer,et al.  Oscillatory Neuronal Responses in the Visual Cortex of the Awake Macaque Monkey , 1992, The European journal of neuroscience.

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

[32]  M. Usher,et al.  Segmentation, Binding, and Illusory Conjunctions , 1991, Neural Computation.

[33]  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.

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

[35]  P König,et al.  Synchronization of oscillatory neuronal responses between striate and extrastriate visual cortical areas of the cat. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

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

[37]  R. Llinás,et al.  In vitro neurons in mammalian cortical layer 4 exhibit intrinsic oscillatory activity in the 10- to 50-Hz frequency range. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[38]  Christoph von der Malsburg,et al.  The Correlation Theory of Brain Function , 1994 .

[39]  S W Keele,et al.  Tests of a temporal theory of attentional binding. , 1988, Journal of experimental psychology. Human perception and performance.

[40]  W. Singer,et al.  Temporal coding in the visual cortex: new vistas on integration in the nervous system , 1992, Trends in Neurosciences.

[41]  C. Koch,et al.  Some reflections on visual awareness. , 1990, Cold Spring Harbor symposia on quantitative biology.

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

[43]  M. Young,et al.  On oscillating neuronal responses in the visual cortex of the monkey. , 1992, Journal of neurophysiology.

[44]  W. Singer,et al.  Synchronization of oscillatory neuronal responses in cat striate cortex: Temporal properties , 1992, Visual Neuroscience.

[45]  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.