A perceptual representation in the frontal eye field during covert visual search that is more reliable than the behavioral report

Neuronal activity in the frontal eye field (FEF) identifies locations of behaviorally important objects for guiding attention and eye movements. We recorded neural activity in the FEF of monkeys trained to manually turn a lever towards the location of a pop‐out target of a visual search array without shifting gaze. We examined whether the reliability of the neural representation of the salient target location predicted the monkeys’ accuracy of reporting target location. We found that FEF neurons reliably encoded the location of the target stimulus not only on correct trials but also on error trials. The representation of target location in FEF persisted until the manual behavioral report but did not increase in magnitude. This result suggests that, in the absence of an eye movement report, FEF encodes the perceptual information necessary to perform the task but does not accumulate this sensory evidence towards a perceptual decision threshold. These results provide physiological evidence that, under certain circumstances, accurate perceptual representations do not always lead to accurate behavioral reports and that variability in processes outside of perception must be considered to account for the variability in perceptual choice behavior.

[1]  Em Mead,et al.  Society for Neuroscience Annual Meeting , 2009 .

[2]  Saul Sternberg,et al.  The discovery of processing stages: Extensions of Donders' method , 1969 .

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

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

[5]  G. D. Logan,et al.  Dynamics of saccade target selection: Race model analysis of double step and search step saccade production in human and macaque , 2007, Vision Research.

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

[7]  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.

[8]  N. P. Bichot,et al.  Frontal eye field activity before visual search errors reveals the integration of bottom-up and top-down salience. , 2005, Journal of neurophysiology.

[9]  A. Neuringer Operant variability: Evidence, functions, and theory , 2002, Psychonomic bulletin & review.

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

[11]  R. Romo,et al.  Neuronal Correlates of a Perceptual Decision in Ventral Premotor Cortex , 2004, Neuron.

[12]  C. Bruce,et al.  Topography of projections to the frontal lobe from the macaque frontal eye fields , 1993, The Journal of comparative neurology.

[13]  David E. Irwin,et al.  Modern mental chronometry , 1988, Biological Psychology.

[14]  M. Goldberg,et al.  Neuronal Activity in the Lateral Intraparietal Area and Spatial Attention , 2003, Science.

[15]  J. Schall,et al.  Role of frontal eye fields in countermanding saccades: visual, movement, and fixation activity. , 1998, Journal of neurophysiology.

[16]  A. Allport,et al.  Selection for action: Some behavioral and neurophysiological considerations of attention and action , 1987 .

[17]  A. Chauvin,et al.  Control of sensorimotor variability by consequences. , 2007, Journal of neurophysiology.

[18]  J. Kalaska,et al.  Neural Correlates of Reaching Decisions in Dorsal Premotor Cortex: Specification of Multiple Direction Choices and Final Selection of Action , 2005, Neuron.

[19]  Takashi R Sato,et al.  Effects of Stimulus-Response Compatibility on Neural Selection in Frontal Eye Field , 2003, Neuron.

[20]  M. Corbetta,et al.  An Event-Related Functional Magnetic Resonance Imaging Study of Voluntary and Stimulus-Driven Orienting of Attention , 2005, The Journal of Neuroscience.

[21]  Byounghoon Kim,et al.  Saccade Target Selection in the Superior Colliculus: A Signal Detection Theory Approach , 2008, The Journal of Neuroscience.

[22]  J. Gold,et al.  The neural basis of decision making. , 2007, Annual review of neuroscience.

[23]  J. Schall,et al.  Neural Control of Voluntary Movement Initiation , 1996, Science.

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

[25]  J. Gold,et al.  The Influence of Behavioral Context on the Representation of a Perceptual Decision in Developing Oculomotor Commands , 2003, The Journal of Neuroscience.

[26]  N. P. Bichot,et al.  Priming in Macaque Frontal Cortex during Popout Visual Search: Feature-Based Facilitation and Location-Based Inhibition of Return , 2002, The Journal of Neuroscience.

[27]  D. Norman Categorization of action slips. , 1981 .

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

[29]  H Pashler,et al.  Shifting visual attention and selecting motor responses: distinct attentional mechanisms. , 1991, Journal of experimental psychology. Human perception and performance.

[30]  Puiu F. Balan,et al.  Integration of Visuospatial and Effector Information during Symbolically Cued Limb Movements in Monkey Lateral Intraparietal Area , 2006, The Journal of Neuroscience.

[31]  Jacqueline Gottlieb,et al.  Integration of Exogenous Input into a Dynamic Salience Map Revealed by Perturbing Attention , 2006, The Journal of Neuroscience.

[32]  Clay B. Holroyd,et al.  A mechanism for error detection in speeded response time tasks. , 2005, Journal of experimental psychology. General.

[33]  H. Nothdurft Attention shifts to salient targets , 2002, Vision Research.

[34]  H. Heuer,et al.  Perspectives on Perception and Action , 1989 .

[35]  M. Paré,et al.  Guidance of eye movements during visual conjunction search: local and global contextual effects on target discriminability. , 2006, Journal of neurophysiology.

[36]  J. Brožek Attention and Performance II. , 1971 .

[37]  M. Shadlen,et al.  Response of Neurons in the Lateral Intraparietal Area during a Combined Visual Discrimination Reaction Time Task , 2002, The Journal of Neuroscience.

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

[39]  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.

[40]  K. Pribram,et al.  Cortical involvement in visual scan in the monkey , 1993, Perception & psychophysics.

[41]  R. Ratcliff,et al.  A comparison of macaque behavior and superior colliculus neuronal activity to predictions from models of two-choice decisions. , 2003, Journal of neurophysiology.

[42]  Philip L. Smith,et al.  Dual diffusion model for single-cell recording data from the superior colliculus in a brightness-discrimination task. , 2007, Journal of neurophysiology.

[43]  N. P. Bichot,et al.  A visual salience map in the primate frontal eye field. , 2005, Progress in brain research.

[44]  Aditya Murthy,et al.  Frontal eye field contributions to rapid corrective saccades. , 2007, Journal of neurophysiology.

[45]  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.

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

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

[48]  Jeffrey N. Rouder,et al.  Modeling Response Times for Two-Choice Decisions , 1998 .