Lateralized Frontal Eye Field Activity Precedes Occipital Activity Shortly before Saccades: Evidence for Cortico-cortical Feedback as a Mechanism Underlying Covert Attention Shifts

When an eye movement is prepared, attention is shifted toward the saccade end-goal. This coupling of eye movements and spatial attention is thought to be mediated by cortical connections between the FEFs and the visual cortex. Here, we present evidence for the existence of these connections. A visual discrimination task was performed while recording the EEG. Discrimination performance was significantly improved when the discrimination target and the saccade target matched. EEG results show that frontal activity precedes occipital activity contralateral to saccade direction when the saccade is prepared but not yet executed; these effects were absent in fixation conditions. This is consistent with the idea that the FEF exerts a direct modulatory influence on the visual cortex and enhances perception at the saccade end-goal.

[1]  T. Paus,et al.  Transcranial Magnetic Stimulation of the Human Frontal Eye Field: Effects on Visual Perception and Attention , 2002, Journal of Cognitive Neuroscience.

[2]  Karl J. Friston,et al.  MEG source localization under multiple constraints: An extended Bayesian framework , 2006, NeuroImage.

[3]  G. R Mangun,et al.  Shifting visual attention in space: an electrophysiological analysis using high spatial resolution mapping , 2000, Clinical Neurophysiology.

[4]  G. Mangun,et al.  Dissociating top-down attentional control from selective perception and action , 2001, Neuropsychologia.

[5]  Katherine M. Armstrong,et al.  Visuomotor Origins of Covert Spatial Attention , 2003, Neuron.

[6]  M. Corbetta,et al.  Neural Systems for Visual Orienting and Their Relationships to Spatial Working Memory , 2002, Journal of Cognitive Neuroscience.

[7]  R. Deichmann,et al.  Distinct causal influences of parietal versus frontal areas on human visual cortex: evidence from concurrent TMS-fMRI. , 2008, Cerebral cortex.

[8]  Karl J. Friston,et al.  Bayesian model selection for group studies , 2009, NeuroImage.

[9]  A. Dale,et al.  Improved Localizadon of Cortical Activity by Combining EEG and MEG with MRI Cortical Surface Reconstruction: A Linear Approach , 1993, Journal of Cognitive Neuroscience.

[10]  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.

[11]  Martin Eimer,et al.  Early posterior ERP components do not reflect the control of attentional shifts toward expected peripheral events. , 2003, Psychophysiology.

[12]  M. Corbetta,et al.  Frontoparietal Cortex Controls Spatial Attention through Modulation of Anticipatory Alpha Rhythms , 2009, The Journal of Neuroscience.

[13]  A. Kingstone,et al.  Topic: Cognition , 2003 .

[14]  M. Corbetta,et al.  Top-Down Control of Human Visual Cortex by Frontal and Parietal Cortex in Anticipatory Visual Spatial Attention , 2008, The Journal of Neuroscience.

[15]  Jon Driver,et al.  Attentional Preparation for a Lateralized Visual Distractor: Behavioral and fMRI Evidence , 2006, Journal of Cognitive Neuroscience.

[16]  R. Deichmann,et al.  Concurrent TMS-fMRI and Psychophysics Reveal Frontal Influences on Human Retinotopic Visual Cortex , 2006, Current Biology.

[17]  N. P. Bichot,et al.  Dissociation of visual discrimination from saccade programming in macaque frontal eye field. , 1997, Journal of neurophysiology.

[18]  Björn N. S. Vlaskamp,et al.  TMS pulses on the frontal eye fields break coupling between visuospatial attention and eye movements. , 2007, Journal of neurophysiology.

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

[20]  D H Brainard,et al.  The Psychophysics Toolbox. , 1997, Spatial vision.

[21]  Jan Theeuwes,et al.  An ERP study of preparatory and inhibitory mechanisms in a cued saccade task , 2006, Brain Research.

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

[23]  B Giesbrecht,et al.  Neural mechanisms of top-down control during spatial and feature attention , 2003, NeuroImage.

[24]  Steven L. Miller,et al.  Neural Processes Involved in Directing Attention , 1989, Journal of Cognitive Neuroscience.

[25]  T. Moore,et al.  Microstimulation of the frontal eye field and its effects on covert spatial attention. , 2004, Journal of neurophysiology.

[26]  Karl J. Friston,et al.  Multiple sparse priors for the M/EEG inverse problem , 2008, NeuroImage.

[27]  J. Moake,et al.  This article has been cited by other articles , 2003 .

[28]  Tomás Paus,et al.  Transcranial Magnetic Stimulation of the Human Frontal Eye ®eld Facilitates Visual Awareness , 2022 .

[29]  M. Corbetta,et al.  A Common Network of Functional Areas for Attention and Eye Movements , 1998, Neuron.

[30]  B. Dosher,et al.  The role of attention in the programming of saccades , 1995, Vision Research.

[31]  Jon Driver,et al.  Shifts of attention in light and in darkness: an ERP study of supramodal attentional control and crossmodal links in spatial attention. , 2003, Brain research. Cognitive brain research.

[32]  Eric Castet,et al.  Dynamics of attentional deployment during saccadic programming. , 2006, Journal of vision.

[33]  F. Smulders,et al.  Lateralized ERP components related to spatial orienting: discriminating the direction of attention from processing sensory aspects of the cue. , 2007, Psychophysiology.

[34]  T Moore,et al.  Control of eye movements and spatial attention. , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[35]  D G Pelli,et al.  The VideoToolbox software for visual psychophysics: transforming numbers into movies. , 1997, Spatial vision.

[36]  J D Schall,et al.  Dynamic dissociation of visual selection from saccade programming in frontal eye field. , 2001, Journal of neurophysiology.

[37]  Anna C Nobre,et al.  FEF TMS affects visual cortical activity. , 2006, Cerebral cortex.

[38]  G. Mangun,et al.  The neural mechanisms of top-down attentional control , 2000, Nature Neuroscience.

[39]  Melissa R. Beck,et al.  Attention shifts or volatile representations: What causes binding deficits in visual working memory? , 2012 .

[40]  H. Deubel,et al.  Saccade target selection and object recognition: Evidence for a common attentional mechanism , 1996, Vision Research.

[41]  Neil G. Muggleton,et al.  Timing of Target Discrimination in Human Frontal Eye Fields , 2004, Journal of Cognitive Neuroscience.

[42]  J. Hoffman,et al.  The role of visual attention in saccadic eye movements , 1995, Perception & psychophysics.

[43]  Arnaud Delorme,et al.  EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis , 2004, Journal of Neuroscience Methods.

[44]  G. Rizzolatti,et al.  Reorienting attention across the horizontal and vertical meridians: Evidence in favor of a premotor theory of attention , 1987, Neuropsychologia.

[45]  R. Verleger,et al.  Spatiotemporal overlap between brain activation related to saccade preparation and attentional orienting , 2006, Brain Research.

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

[47]  H. Spekreijse,et al.  Correspondence of presaccadic activity in the monkey primary visual cortex with saccadic eye movements. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[48]  O. Tzeng,et al.  Segregation of visual selection and saccades in human frontal eye fields. , 2008, Cerebral cortex.

[49]  Pierre Pouget,et al.  Attentional selection during preparation of eye movements , 2004, Psychological research.

[50]  D. Robinson,et al.  Shared neural control of attentional shifts and eye movements , 1996, Nature.

[51]  Chi-Hung Juan,et al.  Human frontal eye fields and visual search. , 2003, Journal of neurophysiology.

[52]  Juha Silvanto,et al.  Stimulation of the human frontal eye fields modulates sensitivity of extrastriate visual cortex. , 2006, Journal of neurophysiology.

[53]  A. Nobre,et al.  The dynamics of shifting visuospatial attention revealed by event-related potentials , 2000, Neuropsychologia.

[54]  T. Moore,et al.  The neurobiology of visual attention: finding sources , 2006, Current Opinion in Neurobiology.