The Effects of Prefrontal Cortex Inactivation on Object Responses of Single Neurons in the Inferotemporal Cortex during Visual Search

Inferotemporal cortex (IT) is believed to be directly involved in object processing and necessary for accurate and efficient object recognition. The frontal eye field (FEF) is an area in the primate prefrontal cortex that is involved in visual spatial selection and is thought to guide spatial attention and eye movements. We show that object-selective responses of IT neurons and behavioral performance are affected by changes in frontal eye field activity. This was found in monkeys performing a search classification task by temporarily inactivating subregions of FEF while simultaneously recording the activity from single neurons in IT. The effect on object selectivity and performance was specific, occurring in a predictable spatially dependent manner and was strongest when the IT neuron's preferred target was presented in the presence of distractors. FEF inactivation did not affect IT responses on trials in which the nonpreferred target was presented in the search array.

[1]  Nicholas A. Steinmetz,et al.  Top-down control of visual attention , 2010, Current Opinion in Neurobiology.

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

[3]  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.

[4]  E. Miller,et al.  Top-Down Versus Bottom-Up Control of Attention in the Prefrontal and Posterior Parietal Cortices , 2007, Science.

[5]  Leslie G. Ungerleider,et al.  Object vision and spatial vision: two cortical pathways , 1983, Trends in Neurosciences.

[6]  P. H. Schiller,et al.  The effects of frontal eye field and dorsomedial frontal cortex lesions on visually guided eye movements , 1998, Nature Neuroscience.

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

[8]  Kirk G. Thompson,et al.  Cognitively directed spatial selection in the frontal eye field in anticipation of visual stimuli to be discriminated , 2009, Vision Research.

[9]  Tirin Moore,et al.  Rapid enhancement of visual cortical response discriminability by microstimulation of the frontal eye field , 2007, Proceedings of the National Academy of Sciences.

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

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

[12]  Chi-Hung Juan,et al.  Dissociation of spatial attention and saccade preparation. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[13]  Robert Desimone,et al.  Feature-Based Attention in the Frontal Eye Field and Area V4 during Visual Search , 2011, Neuron.

[14]  Jeffrey D. Schall,et al.  The detection of visual signals by macaque frontal eye field during masking , 1999, Nature Neuroscience.

[15]  David L. Sheinberg,et al.  Paired neuron recordings in the prefrontal and inferotemporal cortices reveal that spatial selection precedes object identification during visual search , 2010, Proceedings of the National Academy of Sciences.

[16]  M. Goldberg,et al.  Attention, intention, and priority in the parietal lobe. , 2010, Annual review of neuroscience.

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

[18]  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.

[19]  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.

[20]  Ilya E. Monosov,et al.  Measurements of Simultaneously Recorded Spiking Activity and Local Field Potentials Suggest that Spatial Selection Emerges in the Frontal Eye Field , 2008, Neuron.

[21]  Lance M. Optican,et al.  Unix-based multiple-process system, for real-time data acquisition and control , 1982 .

[22]  Leslie G. Ungerleider,et al.  Visual responses to targets and distracters by inferior temporal neurons after lesions of extrastriate areas V4 and TEO , 2004, Neuroreport.

[23]  R. Desimone,et al.  High-Frequency, Long-Range Coupling Between Prefrontal and Visual Cortex During Attention , 2009, Science.

[24]  O. Hikosaka,et al.  Visual and Anticipatory Bias in Three Cortical Eye Fields of the Monkey during an Adaptive Decision-Making Task , 2002, The Journal of Neuroscience.

[25]  J. Schall,et al.  Visual and Motor Connectivity and the Distribution of Calcium-Binding Proteins in Macaque Frontal Eye Field: Implications for Saccade Target Selection , 2009, Front. Neuroanat..

[26]  M. Segraves,et al.  Muscimol-induced inactivation of monkey frontal eye field: effects on visually and memory-guided saccades. , 1999, Journal of neurophysiology.

[27]  Thomas Serre,et al.  Object decoding with attention in inferior temporal cortex , 2011, Proceedings of the National Academy of Sciences.

[28]  T. Moore,et al.  CONTROL OF VISUAL CORTICAL SIGNALS BY PREFRONTAL DOPAMINE , 2011, Nature.

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

[30]  Peter W Dicke,et al.  Neuron-specific contribution of the superior colliculus to overt and covert shifts of attention , 2004, Nature Neuroscience.

[31]  Richard J Krauzlis,et al.  Inactivation of primate superior colliculus impairs covert selection of signals for perceptual judgments , 2010, Nature Neuroscience.

[32]  Katherine M. Armstrong,et al.  Selective gating of visual signals by microstimulation of frontal cortex , 2003, Nature.

[33]  Katherine M. Armstrong,et al.  Visual and oculomotor selection: links, causes and implications for spatial attention , 2006, Trends in Cognitive Sciences.

[34]  Tirin Moore,et al.  Selective Attention from Voluntary Control of Neurons in Prefrontal Cortex , 2011, Science.

[35]  G. Orban,et al.  Searching for a salient target involves frontal regions. , 2010, Cerebral cortex.

[36]  Puiu F. Balan,et al.  Task specific computations in attentional maps , 2009, Vision Research.

[37]  Tirin Moore,et al.  Changes in Visual Receptive Fields with Microstimulation of Frontal Cortex , 2006, Neuron.

[38]  Robert H. Wurtz,et al.  Subcortical Modulation of Attention Counters Change Blindness , 2004, The Journal of Neuroscience.

[39]  R. Desimone,et al.  Competitive Mechanisms Subserve Attention in Macaque Areas V2 and V4 , 1999, The Journal of Neuroscience.

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

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