Neural mechanisms for stimulus selection in cortical areas of the macaque subserving object vision

The present article reviews some recent work on the neuronal mechanisms underlying space-based and feature-based stimulus selection in the primate occipito-temporal pathway of cortical visual processing. Clear evidence demonstrates that activity in areas V4 and IT is high for a stimulus which is selected either for its position in space or for its features, while it is considerably suppressed for other, irrelevant stimuli. Data are discussed within a conceptual framework whereby objects in the visual field always compete for focal resources. According to task demands, any kind of input (objects of a certain category, objects with a certain form, color or motion, objects at a certain location) can be behaviorally relevant. A short-term description (working memory) of the currently relevant object properties controls competitive bias in the visual system, such that inputs matching that description are favored to the disadvantage of task-irrelevant inputs. This framework emphasizes a tight, causal link between memory signals and mechanisms for stimulus selection in visual cortex. In all cases gating of neural activity was constrained by spatial factors. In area V4, responses to an ignored stimulus in the receptive field of the recorded neuron were maximally suppressed when the monkey attended to a second stimulus located within the boundary of the same receptive field, while suppression was virtually absent when attention was directed to a second stimulus well outside the receptive field border. In IT cortex, suppressed responses depended on both the selected and ignored stimuli being within the hemifield contralateral to the recorded hemisphere, while suppression was much reduced when the stimuli were presented across the vertical midline. These spatial constraints on the occurrence of modulation of visual responses may reflect limitations imposed by the local pattern of reciprocal inhibitory connections, which are supposed to underlie competitive interactions among objects in the field, that is among object representations in cortex.

[1]  R. Doty,et al.  Lateralization in the nervous system , 1977 .

[2]  A Treisman,et al.  Feature analysis in early vision: evidence from search asymmetries. , 1988, Psychological review.

[3]  C G Gross,et al.  Responses of inferior temporal cortex and hippocampal neurons during delayed matching to sample in monkeys (Macaca fascicularis). , 1994, Behavioral neuroscience.

[4]  S. Wise,et al.  Visuospatial versus visuomotor activity in the premotor and prefrontal cortex of a primate , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[5]  P. Goldman-Rakic Cellular and circuit basis of working memory in prefrontal cortex of nonhuman primates. , 1990, Progress in brain research.

[6]  P. Goldman-Rakic,et al.  Preface: Cerebral Cortex Has Come of Age , 1991 .

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

[8]  D. Pandya,et al.  Prefrontal cortex in relation to other cortical areas in rhesus monkey: architecture and connections. , 1990, Progress in brain research.

[9]  John K. Tsotsos Analyzing vision at the complexity level , 1990, Behavioral and Brain Sciences.

[10]  P. Goldman-Rakic,et al.  Mnemonic coding of visual space in the monkey's dorsolateral prefrontal cortex. , 1989, Journal of neurophysiology.

[11]  D. Meyer,et al.  Attention and Performance XIV , 1973 .

[12]  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.

[13]  Masataka Watanabe,et al.  Prefrontal unit activity and delayed response: Relation to cue location versus direction of response , 1976, Brain Research.

[14]  Earl K. Miller,et al.  Dual mechanisms of short-term memory Ventral prefrontal cortex , 1993 .

[15]  Joel L. Davis,et al.  Large-Scale Neuronal Theories of the Brain , 1994 .

[16]  S. Grossberg,et al.  Neural networks for vision and image processing , 1992 .

[17]  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.

[18]  P. Goldman-Rakic,et al.  Visuospatial coding in primate prefrontal neurons revealed by oculomotor paradigms. , 1990, Journal of neurophysiology.

[19]  J. Fuster,et al.  Cellular discharge in the dorsolateral prefrontal cortex of the monkey in cognitive tasks , 1982, Experimental Neurology.

[20]  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.

[21]  R. Desimone,et al.  Neural mechanisms of selective visual attention. , 1995, Annual review of neuroscience.

[22]  P. Goldman-Rakic,et al.  Prefrontal neuronal activity in rhesus monkeys performing a delayed anti-saccade task , 1993, Nature.

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

[24]  O. Neumann Beyond capacity: A functional view of attention , 1987 .

[25]  T. Sato,et al.  Effects of attention and stimulus interaction on visual responses of inferior temporal neurons in macaque. , 1988, Journal of neurophysiology.

[26]  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.

[27]  S. Palmer Hierarchical structure in perceptual representation , 1977, Cognitive Psychology.

[28]  Anne Treisman,et al.  Features and objects in visual processing , 1986 .

[29]  P. Goldman-Rakic,et al.  Posterior parietal cortex in rhesus monkey: II. Evidence for segregated corticocortical networks linking sensory and limbic areas with the frontal lobe , 1989, The Journal of comparative neurology.

[30]  Alan D. Baddeley,et al.  Attention: Selection, Awareness, and Control , 1993 .

[31]  Ben Kröse Local structure analyzers as determinants of preattentive pattern discrimination , 1987 .

[32]  R. Desimone,et al.  Activity of neurons in anterior inferior temporal cortex during a short- term memory task , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[34]  J. Allman,et al.  Stimulus specific responses from beyond the classical receptive field: neurophysiological mechanisms for local-global comparisons in visual neurons. , 1985, Annual review of neuroscience.

[35]  H. Barbas Anatomic organization of basoventral and mediodorsal visual recipient prefrontal regions in the rhesus monkey , 1988, The Journal of comparative neurology.

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

[37]  F. Plum Handbook of Physiology. , 1960 .

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

[39]  A. Allport Attention and control: have we been asking the wrong questions? A critical review of twenty-five years , 1993 .

[40]  D. V. van Essen,et al.  Neuronal responses to static texture patterns in area V1 of the alert macaque monkey. , 1992, Journal of neurophysiology.

[41]  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.

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

[43]  J. Fuster,et al.  Inferotemporal neurons distinguish and retain behaviorally relevant features of visual stimuli. , 1981, Science.

[44]  Azriel Rosenfeld,et al.  Human and Machine Vision , 1983 .

[45]  Leslie G. Ungerleider,et al.  Contour, color and shape analysis beyond the striate cortex , 1985, Vision Research.

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

[47]  S Grossberg,et al.  Cortical dynamics of three-dimensional form, color, and brightness perception: II. Binocular theory , 1988, Perception & psychophysics.

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

[49]  David L. Sparks,et al.  Movement selection in advance of action in the superior colliculus , 1992, Nature.

[50]  J. A. Horel,et al.  The performance of visual tasks while segments of the inferotemporal cortex are suppressed by cold , 1987, Behavioural Brain Research.

[51]  C. Gross 7 – The Neural Basis of Stimulus Equivalence Across Retinal Translation , 1977 .

[52]  J. Fuster,et al.  Mnemonic and predictive functions of cortical neurons in a memory task , 1992, Neuroreport.

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

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

[55]  C. Bundesen A theory of visual attention. , 1990, Psychological review.

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

[57]  Earl K. Miller,et al.  The interaction of neural systems for attention and memory , 1994 .

[58]  R. Desimone,et al.  Inferior temporal mechanisms for invariant object recognition. , 1994, Cerebral cortex.

[59]  J. Duncan,et al.  Visual search and stimulus similarity. , 1989, Psychological review.

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

[61]  D. Amaral,et al.  Lesions of the perirhinal and parahippocampal cortices in the monkey produce long-lasting memory impairment in the visual and tactual modalities , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[62]  W. D. Ross,et al.  A Neural Theory of Attentive Visual Search : Interactions of Boundary , Surface , Spatial , and Object Representations By : Stephen Grossberg , 2004 .

[63]  N. Sutherland Outlines of a theory of visual pattern recognition in animals and man , 1968, Proceedings of the Royal Society of London. Series B. Biological Sciences.

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

[65]  R. Desimone,et al.  Multiple memory systems in the visual cortex. , 1995 .

[66]  Jeffrey D. Schall,et al.  Neural basis of saccade target selection in frontal eye field during visual search , 1993, Nature.

[67]  M. Mishkin,et al.  Effects on visual recognition of combined and separate ablations of the entorhinal and perirhinal cortex in rhesus monkeys , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[68]  B. Julesz Textons, the elements of texture perception, and their interactions , 1981, Nature.

[69]  E. Bizzi,et al.  The Cognitive Neurosciences , 1996 .

[70]  R. Desimone,et al.  Spectral properties of V4 neurons in the macaque , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[72]  Allen Allport,et al.  Visual attention , 1989 .

[73]  I. Rock,et al.  The legacy of Gestalt psychology. , 1990, Scientific American.

[74]  J. Fuster,et al.  Functional interactions between inferotemporal and prefrontal cortex in a cognitive task , 1985, Brain Research.

[75]  R. Mansfield,et al.  Analysis of visual behavior , 1982 .

[76]  A. Rosenfeld,et al.  A Theory of Textural Segmentation , 1983 .

[77]  M. Posner Foundations of cognitive science , 1989 .

[78]  Jordan Grafman,et al.  Handbook of Neuropsychology , 1991 .

[79]  H. Heuer,et al.  Perspectives on Perception and Action , 1989 .

[80]  B. C. Motter,et al.  Neural correlates of feature selective memory and pop-out in extrastriate area V4 , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[81]  J. Fuster Unit activity in prefrontal cortex during delayed-response performance: neuronal correlates of transient memory. , 1973, Journal of neurophysiology.

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

[83]  A. Treisman,et al.  A feature-integration theory of attention , 1980, Cognitive Psychology.

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