Priming in Macaque Frontal Cortex during Popout Visual Search: Feature-Based Facilitation and Location-Based Inhibition of Return

In popout search, humans and monkeys are affected by trial-to-trial changes in stimulus features and target location. The neuronal mechanisms underlying such sequential effects have not been examined. Single neurons were recorded in the frontal eye field (FEF) of monkeys performing a popout search during which stimulus features and target position changed unpredictably across trials. Like previous studies, repetition of stimulus features improved performance. This feature-based facilitation of return was manifested in the target discrimination process in FEF: neurons discriminated the target from distractors earlier and better with repetition of stimulus features, corresponding to improvements in saccade latency and accuracy, respectively. The neuronal target selection was mediated by both target enhancement and distractor suppression. In contrast to the repetition of features, repetition of target position increased saccade latency. This location-based inhibition of return was reflected in the neuronal discrimination process but not in the baseline activity in FEF. These results show adjustments of the target selection process in FEF corresponding to and therefore possibly contributing to changes in performance across trials caused by sequential regularities in display properties.

[1]  D. M. Green,et al.  Signal detection theory and psychophysics , 1966 .

[2]  A. L. I︠A︡rbus Eye Movements and Vision , 1967 .

[3]  A. L. Yarbus,et al.  Eye Movements and Vision , 1967, Springer US.

[4]  R. Wurtz,et al.  Visual receptive fields of frontal eye field neurons. , 1973, Brain research.

[5]  Roger Ratcliff,et al.  A revised table of d’ for M-alternative forced choice , 1979 .

[6]  M. Posner,et al.  Attention and the detection of signals. , 1980, Journal of experimental psychology.

[7]  E. Batschelet Circular statistics in biology , 1981 .

[8]  J E Smith,et al.  Simple algorithms for M-alternative forced-choice calculations , 1982, Perception & psychophysics.

[9]  J. Movshon,et al.  The statistical reliability of signals in single neurons in cat and monkey visual cortex , 1983, Vision Research.

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

[11]  L A Krubitzer,et al.  Frontal eye field as defined by intracortical microstimulation in squirrel monkeys, owl monkeys, and macaque monkeys II. cortical connections , 1986, The Journal of comparative neurology.

[12]  I. Ohzawa,et al.  Visual orientation and spatial frequency discrimination: a comparison of single neurons and behavior. , 1987, Journal of neurophysiology.

[13]  I. Ohzawa,et al.  The effects of contrast on visual orientation and spatial frequency discrimination: a comparison of single cells and behavior. , 1987, Journal of neurophysiology.

[14]  L. Optican,et al.  Temporal encoding of two-dimensional patterns by single units in primate inferior temporal cortex. III. Information theoretic analysis. , 1987, Journal of neurophysiology.

[15]  L A Krubitzer,et al.  Frontal eye field as defined by intracortical microstimulation in squirrel monkeys, owl monkeys, and macaque monkeys II. cortical connections , 1986, The Journal of comparative neurology.

[16]  S. Tipper,et al.  Selection of moving and static objects for the control of spatially directed action. , 1990, Journal of experimental psychology. Human perception and performance.

[17]  P. Viviani Eye movements in visual search: cognitive, perceptual and motor control aspects. , 1990, Reviews of oculomotor research.

[18]  Neil A. Macmillan,et al.  Detection Theory: A User's Guide , 1991 .

[19]  S. Wise,et al.  Learning-dependent neuronal activity in the premotor cortex: activity during the acquisition of conditional motor associations , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[20]  M. Bravo,et al.  The role of attention in different visual-search tasks , 1992, Perception & psychophysics.

[21]  J. Movshon,et al.  The analysis of visual motion: a comparison of neuronal and psychophysical performance , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[22]  Keating Cf,et al.  Monkeys and mug shots: cues used by rhesus monkeys (Macaca mulatta) to recognize a human face , 1993 .

[23]  C. Bruce,et al.  Topography of projections to the frontal lobe from the macaque frontal eye fields , 1993, The Journal of comparative neurology.

[24]  C. Keating,et al.  Monkeys and mug shots: cues used by rhesus monkeys (Macaca mulatta) to recognize a human face. , 1993, Journal of comparative psychology.

[25]  M. Segraves,et al.  Primate frontal eye field activity during natural scanning eye movements. , 1994, Journal of neurophysiology.

[26]  K. Nakayama,et al.  Priming of pop-out: I. Role of features , 1994, Memory & cognition.

[27]  J. Schall,et al.  Saccade target selection in frontal eye field of macaque. I. Visual and premovement activation , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[29]  J. Bullier,et al.  Topography of visual cortex connections with frontal eye field in macaque: convergence and segregation of processing streams , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[30]  S. Wise,et al.  Supplementary eye field contrasted with the frontal eye field during acquisition of conditional oculomotor associations. , 1995, Journal of neurophysiology.

[31]  J H Maunsell,et al.  The Brain's Visual World: Representation of Visual Targets in Cerebral Cortex , 1995, Science.

[32]  K. Nakayama,et al.  Priming of pop-out: II. The role of position , 1996, Perception & psychophysics.

[33]  K. Nakayama,et al.  Priming of popout: II. Role of position , 1996 .

[34]  R. Desimone,et al.  Neural mechanisms for visual memory and their role in attention. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[35]  N. P. Bichot,et al.  Visual feature selectivity in frontal eye fields induced by experience in mature macaques , 1996, Nature.

[36]  S. Shimojo,et al.  Location vs Feature: Reaction Time Reveals Dissociation Between Two Visual Functions , 1996, Vision Research.

[37]  Keiji Tanaka,et al.  Inferotemporal cortex and object vision. , 1996, Annual review of neuroscience.

[38]  J. Movshon,et al.  A computational analysis of the relationship between neuronal and behavioral responses to visual motion , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[39]  N. P. Bichot,et al.  Perceptual and motor processing stages identified in the activity of macaque frontal eye field neurons during visual search. , 1996, Journal of neurophysiology.

[40]  R. Desimone,et al.  Neural mechanisms of spatial selective attention in areas V1, V2, and V4 of macaque visual cortex. , 1997, Journal of neurophysiology.

[41]  Richard S. J. Frackowiak,et al.  Functional localization of the system for visuospatial attention using positron emission tomography. , 1997, Brain : a journal of neurology.

[42]  B Jouve,et al.  A mathematical approach to the connectivity between the cortical visual areas of the macaque monkey. , 1998, Cerebral cortex.

[43]  M. A. Basso,et al.  Modulation of Neuronal Activity in Superior Colliculus by Changes in Target Probability , 1998, The Journal of Neuroscience.

[44]  M Corbetta,et al.  Frontoparietal cortical networks for directing attention and the eye to visual locations: identical, independent, or overlapping neural systems? , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[45]  N. P. Bichot,et al.  Spatial selection via feature-driven inhibition of distractor locations , 1998, Perception & psychophysics.

[46]  Kae Nakamura,et al.  Neuronal activity in medial frontal cortex during learning of sequential procedures. , 1998, Journal of neurophysiology.

[47]  D P Munoz,et al.  Influence of previous visual stimulus or saccade on saccadic reaction times in monkey. , 1999, Journal of neurophysiology.

[48]  Robert M. McPeek,et al.  Saccades require focal attention and are facilitated by a short-term memory system , 1999, Vision Research.

[49]  M. Shadlen,et al.  Neural correlates of a decision in the dorsolateral prefrontal cortex of the macaque , 1999, Nature Neuroscience.

[50]  N. P. Bichot,et al.  Effects of similarity and history on neural mechanisms of visual selection , 1999, Nature Neuroscience.

[51]  N. P. Bichot,et al.  Saccade target selection in macaque during feature and conjunction visual search , 1999, Visual Neuroscience.

[52]  N. P. Bichot,et al.  Visuospatial attention: Beyond a spotlight model , 1999, Psychonomic bulletin & review.

[53]  M. Mesulam Spatial attention and neglect: parietal, frontal and cingulate contributions to the mental representation and attentional targeting of salient extrapersonal events. , 1999, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[54]  D. Munoz,et al.  t Immediate Neural Plasticity Shapes Motor Performance , 2000, The Journal of Neuroscience.

[55]  A. Cowey,et al.  Normal discrimination performance accompanied by priming deficits in monkeys with V4 or TEO lesions. , 2000, Neuroreport.

[56]  Repetition priming reveals sustained facilitation and transient inhibition in reaction time. , 2000, Journal of experimental psychology. Human perception and performance.

[57]  G. E. Berrios,et al.  . New York: Cambridge , 2000 .

[58]  A. Villringer,et al.  Involvement of the human frontal eye field and multiple parietal areas in covert visual selection during conjunction search , 2000, The European journal of neuroscience.

[59]  S. Liversedge,et al.  Saccadic eye movements and cognition , 2000, Trends in Cognitive Sciences.

[60]  Joel L. Davis,et al.  Neuronal ensembles : strategies for recording and decoding , 2000 .

[61]  Joaquín M. Fuster,et al.  Executive frontal functions , 2000, Experimental Brain Research.

[62]  N. P. Bichot,et al.  Reliability of Macaque Frontal Eye Field Neurons Signaling Saccade Targets during Visual Search , 2001, The Journal of Neuroscience.

[63]  Joel L. Davis,et al.  Visual attention and cortical circuits , 2001 .

[64]  F. A. Miles,et al.  Single-unit activity in cortical area MST associated with disparity-vergence eye movements: evidence for population coding. , 2001, Journal of neurophysiology.

[65]  E. Miller,et al.  An integrative theory of prefrontal cortex function. , 2001, Annual review of neuroscience.

[66]  J. Duncan An adaptive coding model of neural function in prefrontal cortex , 2001 .

[67]  Satoru Suzuki,et al.  Understanding priming of color-singleton search: Roles of attention at encoding and “retrieval” , 2001, Perception & psychophysics.

[68]  David L. Sheinberg,et al.  Noticing Familiar Objects in Real World Scenes: The Role of Temporal Cortical Neurons in Natural Vision , 2001, The Journal of Neuroscience.

[69]  K. Thompson,et al.  Neural mechanisms of bottom-up selection during visual search , 2001, 2001 Conference Proceedings of the 23rd Annual International Conference of the IEEE Engineering in Medicine and Biology Society.

[70]  W. Newsome,et al.  Neural basis of a perceptual decision in the parietal cortex (area LIP) of the rhesus monkey. , 2001, Journal of neurophysiology.

[71]  D M Levi,et al.  Surround modulation of perceived contrast and the role of brightness induction. , 2001, Journal of vision.

[72]  N. P. Bichot Neural mechanisms of top-down selection during visual search , 2001, 2001 Conference Proceedings of the 23rd Annual International Conference of the IEEE Engineering in Medicine and Biology Society.

[73]  M. Mishkin,et al.  Learning increases stimulus salience in anterior inferior temporal cortex of the macaque. , 2001, Journal of neurophysiology.

[74]  R. Klein,et al.  Negative priming for spatial location? , 2001, Canadian journal of experimental psychology = Revue canadienne de psychologie experimentale.

[75]  N. P. Bichot,et al.  Attention, Eye Movements, and Neurons: Linking Physiology and Behavior , 2001 .

[76]  E. Keller,et al.  Short-term priming, concurrent processing, and saccade curvature during a target selection task in the monkey , 2001, Vision Research.