Attention Governs Action in the Primate Frontal Eye Field

While the motor and attentional roles of the frontal eye field (FEF) are well documented, the relationship between them is unknown. We exploited the known influence of visual motion on the apparent positions of targets, and measured how this illusion affects saccadic eye movements during FEF microstimulation. Without microstimulation, saccades to a moving grating are biased in the direction of motion, consistent with the apparent position illusion. Here we show that microstimulation of spatially aligned FEF representations increases the influence of this illusion on saccades. Rather than simply impose a fixed-vector signal, subthreshold stimulation directed saccades away from the FEF movement field, and instead more strongly in the direction of visual motion. These results demonstrate that the attentional effects of FEF stimulation govern visually guided saccades, and suggest that the two roles of the FEF work together to select both the features of a target and the appropriate movement to foveate it.

[1]  Eileen Kowler,et al.  The role of saccades in the perception of texture patterns , 1992, Vision Research.

[2]  S G Lisberger,et al.  Postsaccadic enhancement of initiation of smooth pursuit eye movements in monkeys. , 1998, Journal of neurophysiology.

[3]  O. Blanke,et al.  Location of the human frontal eye field as defined by electrical cortical stimulation: anatomical, functional and electrophysiological characteristics , 2000, Neuroreport.

[4]  John H.R. Maunsell,et al.  Behavioral Detection of Electrical Microstimulation in Different Cortical Visual Areas , 2007, Current Biology.

[5]  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.

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

[7]  V. Ferrera,et al.  Modification of Saccades Evoked by Stimulation of Frontal Eye Field during Invisible Target Tracking , 2004, The Journal of Neuroscience.

[8]  Dylan F. Cooke,et al.  Defensive movements evoked by air puff in monkeys. , 2003, Journal of neurophysiology.

[9]  D. Robinson Eye movements evoked by collicular stimulation in the alert monkey. , 1972, Vision research.

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

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

[12]  B. Richmond,et al.  Implantation of magnetic search coils for measurement of eye position: An improved method , 1980, Vision Research.

[13]  Shin'ya Nishida,et al.  Influence of motion signals on the perceived position of spatial pattern , 1999, Nature.

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

[15]  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.

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

[17]  W. Penfield,et al.  The Cerebral Cortex of Man: A Clinical Study of Localization of Function , 1968 .

[18]  E Bizzi,et al.  Discharge of Frontal Eye Field Neurons during Eye Movements in Unanesthetized Monkeys , 1967, Science.

[19]  J. Gold,et al.  Representation of a perceptual decision in developing oculomotor commands , 2000, Nature.

[20]  E. Miller,et al.  Microstimulation of Frontal Cortex Can Reorder a Remembered Spatial Sequence , 2006, PLoS biology.

[21]  M. Carrasco,et al.  Attention alters appearance , 2004, Nature Neuroscience.

[22]  G. Edelman,et al.  Signal and sense : local and global order in perceptual maps , 1990 .

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

[24]  J. Hanley,et al.  The meaning and use of the area under a receiver operating characteristic (ROC) curve. , 1982, Radiology.

[25]  Etienne Olivier,et al.  Contribution of the Monkey Frontal Eye Field to Covert Visual Attention , 2006, The Journal of Neuroscience.

[26]  M. Turatto,et al.  Attention makes moving objects be perceived to move faster , 2007, Vision Research.

[27]  Vyacheslav P. Tuzlukov,et al.  Signal detection theory , 2001 .

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

[29]  M. Posner,et al.  Orienting of Attention* , 1980, The Quarterly journal of experimental psychology.

[30]  R. Steinman,et al.  The role of small saccades in counting , 1977, Vision Research.

[31]  A. Fuchs,et al.  A method for measuring horizontal and vertical eye movement chronically in the monkey. , 1966, Journal of applied physiology.

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

[33]  A. Fuchs,et al.  Eye movements evoked by stimulation of frontal eye fields. , 1969, Journal of neurophysiology.

[34]  Timothy D. Hanks,et al.  Microstimulation of macaque area LIP affects decision-making in a motion discrimination task , 2006, Nature Neuroscience.

[35]  Carrie J. McAdams,et al.  Effects of Attention on the Reliability of Individual Neurons in Monkey Visual Cortex , 1999, Neuron.

[36]  Robert M. McPeek,et al.  Deficits in saccade target selection after inactivation of superior colliculus , 2004, Nature Neuroscience.

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

[38]  T. Pasternak,et al.  Microstimulation of cortical area MT affects performance on a visual working memory task. , 2001, Journal of neurophysiology.

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

[40]  S G Lisberger,et al.  Effect of changing feedback delay on spontaneous oscillations in smooth pursuit eye movements of monkeys. , 1992, Journal of neurophysiology.

[41]  V. Ramachandran,et al.  Illusory Displacement of Equiluminous Kinetic Edges , 1990, Perception.

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

[43]  D. Sparks,et al.  Spatial localization of saccade targets. I. Compensation for stimulation-induced perturbations in eye position. , 1983, Journal of neurophysiology.

[44]  D L Sparks,et al.  Effects of low-frequency stimulation of the superior colliculus on spontaneous and visually guided saccades. , 1993, Journal of neurophysiology.

[45]  Stephen G. Lisberger,et al.  Serial linkage of target selection for orienting and tracking eye movements , 2002, Nature Neuroscience.

[46]  C. Bruce,et al.  Primate frontal eye fields. II. Physiological and anatomical correlates of electrically evoked eye movements. , 1985, Journal of neurophysiology.

[47]  Justin L. Gardner,et al.  Linked Target Selection for Saccadic and Smooth Pursuit Eye Movements , 2001, The Journal of Neuroscience.

[48]  I. Kaufman The Cerebral Cortex of Man: A Clinical Study of Localization of Function , 1951 .

[49]  P H Schiller,et al.  Look and see: how the brain moves your eyes about. , 2001, Progress in brain research.

[50]  Naoki Abe,et al.  The “lob-pass” problem and an on-line learning model of rational choice , 1993, COLT '93.

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

[52]  R. Dodge Visual perception during eye movement , 1900 .

[53]  Junying Yuan,et al.  Selective gating of visual signals by microstimulation of frontal cortex , 2022 .

[54]  G. B. Stanton,et al.  Cytoarchitectural characteristic of the frontal eye fields in macaque monkeys , 1989, The Journal of comparative neurology.

[55]  J. Mattingley,et al.  Neurodisruption of selective attention: insights and implications , 2005, Trends in Cognitive Sciences.

[56]  Tirin Moore,et al.  Visually guided behavior after V1 lesions in young and adult monkeys and its relation to blindsight in humans. , 2004, Progress in brain research.

[57]  J. O'Regan,et al.  Optimal landing position in reading isolated words and continuous text , 1990, Perception & psychophysics.

[58]  P. Schiller,et al.  Interactions between visually and electrically elicited saccades before and after superior colliculus and frontal eye field ablations in the rhesus monkey , 2004, Experimental Brain Research.

[59]  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.

[60]  V. Ferrera,et al.  Radial motion bias in macaque frontal eye field , 2006, Visual Neuroscience.

[61]  S G Lisberger,et al.  Temporal properties of visual motion signals for the initiation of smooth pursuit eye movements in monkeys. , 1994, Journal of neurophysiology.

[62]  Robert H Wurtz,et al.  Enhanced Performance with Brain Stimulation: Attentional Shift or Visual Cue? , 2006, The Journal of Neuroscience.

[63]  David Whitney,et al.  Motion distorts visual space: shifting the perceived position of remote stationary objects , 2000, Nature Neuroscience.

[64]  James R Müller,et al.  Microstimulation of the superior colliculus focuses attention without moving the eyes. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[65]  David Whitney,et al.  Contribution of bottom-up and top-down motion processes to perceived position. , 2006, Journal of experimental psychology. Human perception and performance.

[66]  K. D. De Valois,et al.  Vernier acuity with stationary moving Gabors. , 1991, Vision research.

[67]  David Whitney,et al.  The influence of visual motion on perceived position , 2002, Trends in Cognitive Sciences.

[68]  Ziv M. Williams,et al.  Selective enhancement of associative learning by microstimulation of the anterior caudate , 2006, Nature Neuroscience.

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

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