Selection and Maintenance of Spatial Information by Frontal Eye Field Neurons

Voluntary attention is often allocated according to internally maintained goals. Recent evidence indicates that the frontal eye field (FEF) participates in the deployment of spatial attention, even in the absence of saccadic eye movements. In addition, many FEF neurons maintain persistent representations of impending saccades. However, the role of persistent activity in the general maintenance of spatial information, and its relationship to spatial attention, has not been explored. We recorded the responses of single FEF neurons in monkeys trained to remember cued locations in order to detect changes in targets embedded among distracters in a task that did not involve saccades. We found that FEF neurons persistently encoded the cued location throughout the trial during the delay period, when no visual stimuli were present, and during visual discrimination. Furthermore, FEF activity reliably predicted whether monkeys would detect the target change. Population analyses revealed that FEF neurons with persistent activity were more effective at selecting the target from among distracters than neurons lacking persistent activity. These results demonstrate that FEF neurons maintain spatial information in the absence of saccade preparation and suggest that this maintenance contributes to the selection of relevant visual stimuli.

[1]  Masafumi Yohda,et al.  Contribution of the C-terminal region to the thermostability of the archaeal group II chaperonin from Thermococcus sp. strain KS-1 , 2006, Extremophiles.

[2]  F. Tong,et al.  Decoding reveals the contents of visual working memory in early visual areas , 2009, Nature.

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

[4]  P. Goldman-Rakic,et al.  Mnemonic coding of visual space in the monkey's dorsolateral prefrontal cortex. , 1989, Journal of neurophysiology.

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

[6]  G. Humphreys,et al.  Automatic guidance of attention from working memory , 2008, Trends in Cognitive Sciences.

[7]  Marisa Carrasco,et al.  Attention speeds processing across eccentricity: Feature and conjunction searches , 2006, Vision Research.

[8]  R. Wurtz,et al.  Composition and topographic organization of signals sent from the frontal eye field to the superior colliculus. , 2000, Journal of neurophysiology.

[9]  M. Goldberg,et al.  Behavioral enhancement of visual responses in monkey cerebral cortex. II. Modulation in frontal eye fields specifically related to saccades. , 1981, Journal of neurophysiology.

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

[11]  S. Wise The primate premotor cortex: past, present, and preparatory. , 1985, Annual review of neuroscience.

[12]  Ehud Zohary,et al.  Correlated neuronal discharge rate and its implications for psychophysical performance , 1994, Nature.

[13]  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.

[14]  S. Yantis,et al.  Abrupt visual onsets and selective attention: evidence from visual search. , 1984, Journal of experimental psychology. Human perception and performance.

[15]  D. Rosenbaum Human movement initiation: specification of arm, direction, and extent. , 1980, Journal of experimental psychology. General.

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

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

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

[19]  Ronald A. Rensink,et al.  TO SEE OR NOT TO SEE: The Need for Attention to Perceive Changes in Scenes , 1997 .

[20]  J. L. Conway,et al.  Effects of frontal eye field and superior colliculus ablations on eye movements. , 1979, Science.

[21]  Peter Dayan,et al.  The Effect of Correlated Variability on the Accuracy of a Population Code , 1999, Neural Computation.

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

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

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

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

[26]  Jerald D. Kralik,et al.  Representation of Attended Versus Remembered Locations in Prefrontal Cortex , 2004, PLoS biology.

[27]  F. Tong,et al.  Decoding the visual and subjective contents of the human brain , 2005, Nature Neuroscience.

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

[29]  P. Goldman-Rakic,et al.  Prefrontal neuronal activity in rhesus monkeys performing a delayed anti-saccade task , 1993, Nature.

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

[31]  R. Romo,et al.  Correlated Neuronal Discharges that Increase Coding Efficiency during Perceptual Discrimination , 2003, Neuron.

[32]  Peter H. Schiller,et al.  Paired stimulation of the frontal eye fields and the superior colliculus of the rhesus monkey , 1979, Brain Research.

[33]  R. Wurtz,et al.  Frontal eye field sends delay activity related to movement, memory, and vision to the superior colliculus. , 2001, Journal of neurophysiology.

[34]  Leslie G. Ungerleider,et al.  Increased Activity in Human Visual Cortex during Directed Attention in the Absence of Visual Stimulation , 1999, Neuron.

[35]  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.

[36]  D. Simons Attentional capture and inattentional blindness , 2000, Trends in Cognitive Sciences.

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

[38]  A. Jha,et al.  Tracking the time-course of attentional involvement in spatial working memory: an event-related potential investigation. , 2002, Brain research. Cognitive brain research.

[39]  R. Wurtz,et al.  Enhancement of visual responses in monkey striate cortex and frontal eye fields. , 1976, Journal of neurophysiology.

[40]  C. Gross,et al.  Visuospatial properties of ventral premotor cortex. , 1997, Journal of neurophysiology.

[41]  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.

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

[43]  Edward Awh,et al.  The Role of Spatial Selective Attention in Working Memory for Locations: Evidence from Event-Related Potentials , 2000, Journal of Cognitive Neuroscience.

[44]  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.

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

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

[47]  Byron M. Yu,et al.  Neural Variability in Premotor Cortex Provides a Signature of Motor Preparation , 2006, The Journal of Neuroscience.

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