Paired neuron recordings in the prefrontal and inferotemporal cortices reveal that spatial selection precedes object identification during visual search

We addressed the question of how we locate and identify objects in complex natural environments by simultaneously recording single neurons from two brain regions that play different roles in this familiar activity—the frontal eye field (FEF), an area in the prefrontal cortex that is involved in visual spatial selection, and the inferotemporal cortex (IT), which is involved in object recognition—in monkeys performing a covert visual search task. Although the monkeys reported object identity, not location, neural activity specifying target location was evident in FEF before neural activity specifying target identity in IT. These two distinct processes were temporally correlated implying a functional linkage between the end stages of ”where” and “what” visual processing and indicating that spatial selection is necessary for the formation of complex object representations associated with visual perception.

[1]  Thomas D. Albright,et al.  Neural Correlates of Knowledge: Stable Representation of Stimulus Associations across Variations in Behavioral Performance , 2005, Neuron.

[2]  E. Miller,et al.  Response to Comment on "Top-Down Versus Bottom-Up Control of Attention in the Prefrontal and Posterior Parietal Cortices" , 2007, Science.

[3]  F. Hamker The reentry hypothesis: the putative interaction of the frontal eye field, ventrolateral prefrontal cortex, and areas V4, IT for attention and eye movement. , 2005, Cerebral cortex.

[4]  M. Corbetta,et al.  Control of goal-directed and stimulus-driven attention in the brain , 2002, Nature Reviews Neuroscience.

[5]  M. Farah,et al.  Does visual attention select objects or locations? , 1994, Journal of experimental psychology. General.

[6]  J. Deutsch,et al.  Militarized youths in western Côte d’Ivoire: local processes of mobilization, demobilization, and related humanitarian interventions (2002-2007) , 2011 .

[7]  Jacqueline Gottlieb,et al.  Neuronal Correlates of the Set-Size Effect in Monkey Lateral Intraparietal Area , 2008, PLoS biology.

[8]  J. Todd,et al.  The effects of viewing angle, camera angle, and sign of surface curvature on the perception of three-dimensional shape from texture. , 2007, Journal of vision.

[9]  A Treisman,et al.  Feature binding, attention and object perception. , 1998, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[10]  A. Treisman,et al.  Perception of objects in natural scenes: is it really attention free? , 2005, Journal of experimental psychology. Human perception and performance.

[11]  M. Paré,et al.  Neuronal activity in superior colliculus signals both stimulus identity and saccade goals during visual conjunction search. , 2007, Journal of vision.

[12]  Susan L. Franzel,et al.  Guided search: an alternative to the feature integration model for visual search. , 1989, Journal of experimental psychology. Human perception and performance.

[13]  R. Desimone,et al.  Responses of Neurons in Inferior Temporal Cortex during Memory- Guided Visual Search , 1998 .

[14]  Ilya E. Monosov,et al.  Frontal eye field activity enhances object identification during covert visual search. , 2009, Journal of neurophysiology.

[15]  David L. Sheinberg,et al.  The role of temporal cortical areas in perceptual organization. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[16]  J. C. Johnston,et al.  On the locus of visual selection: evidence from focused attention tasks. , 1990, Journal of experimental psychology. Human perception and performance.

[17]  Keiji Tanaka,et al.  The role of the medial prefrontal cortex in achieving goals , 2004, Current Opinion in Neurobiology.

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

[19]  D. Broadbent Task combination and selective intake of information. , 1982, Acta psychologica.

[20]  Edmund T Rolls,et al.  The Receptive Fields of Inferior Temporal Cortex Neurons in Natural Scenes , 2003, The Journal of Neuroscience.

[21]  James J DiCarlo,et al.  Using neuronal latency to determine sensory-motor processing pathways in reaction time tasks. , 2005, Journal of neurophysiology.

[22]  J. Schall,et al.  Neural selection and control of visually guided eye movements. , 1999, Annual review of neuroscience.

[23]  A. Treisman Strategies and models of selective attention. , 1969, Psychological review.

[24]  David L. Sheinberg,et al.  Context Familiarity Enhances Target Processing by Inferior Temporal Cortex Neurons , 2007, The Journal of Neuroscience.

[25]  Tomaso Poggio,et al.  Fast Readout of Object Identity from Macaque Inferior Temporal Cortex , 2005, Science.

[26]  C. Bruce,et al.  Primate frontal eye fields. I. Single neurons discharging before saccades. , 1985, Journal of neurophysiology.

[27]  S. Rose Selective attention , 1992, Nature.

[28]  J. Duncan The locus of interference in the perception of simultaneous stimuli. , 1980, Psychological review.

[29]  David L. Sheinberg,et al.  Activity of Inferior Temporal Cortical Neurons Predicts Recognition Choice Behavior and Recognition Time during Visual Search , 2007, The Journal of Neuroscience.

[30]  Hisao Nishijo,et al.  Neuronal correlates of face identification in the monkey anterior temporal cortical areas. , 2004, Journal of neurophysiology.

[31]  Takashi R Sato,et al.  Neuronal Basis of Covert Spatial Attention in the Frontal Eye Field , 2005, The Journal of Neuroscience.

[32]  J. Duhamel,et al.  Spatial and Temporal Dynamics of Attentional Guidance during Inefficient Visual Search , 2008, PloS one.

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

[34]  M. Tarr,et al.  Visual Object Recognition , 1996, ISTCS.

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

[36]  T. Poggio,et al.  Neural mechanisms of object recognition , 2002, Current Opinion in Neurobiology.

[37]  Robert Sekuler,et al.  Learning to imitate novel motion sequences. , 2007, Journal of vision.

[38]  R. Vogels,et al.  Spatial sensitivity of macaque inferior temporal neurons , 2000, The Journal of comparative neurology.

[39]  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.

[40]  Takashi R Sato,et al.  Search Efficiency but Not Response Interference Affects Visual Selection in Frontal Eye Field , 2001, Neuron.

[41]  C. Koch,et al.  Computational modelling of visual attention , 2001, Nature Reviews Neuroscience.

[42]  J. Deutsch,et al.  Attention: Some theoretical considerations. , 1963 .