Human Frontal Eye Fields and Spatial Priming of Pop-out

Priming of pop-out is a form of implicit memory that facilitates detection of a recently inspected search target. Repeated presentation of a target's features or its spatial position improves detection speed (feature/spatial priming). This study investigated a role for the human frontal eye fields (FEFs) in the priming of color pop-out. To test the hypothesis that the FEFs play a role in short-term memory storage, transcranial magnetic stimulation (TMS) was applied during the intertrial interval. There was no effect of TMS on either spatial or feature priming. To test whether the FEFs are important when a saccade is being programmed to a repeated target color or location, TMS was applied during the search array. TMS over the left but not the right FEFs abolished spatial priming, but had no effect on feature priming. These findings demonstrate functional specialization of the left FEFs for spatial priming, and distinguish this role from target discrimination and saccade-related processes. The results suggest that the left FEFs integrate a spatial memory signal with an evolving saccade program, which facilitates saccades to a recently inspected location.

[1]  Tracy R. Henderson,et al.  Simple metric for scaling motor threshold based on scalp-cortex distance: application to studies using transcranial magnetic stimulation. , 2005, Journal of neurophysiology.

[2]  Jon Driver,et al.  Visual Selection and Posterior Parietal Cortex: Effects of Repetitive Transcranial Magnetic Stimulation on Partial Report Analyzed by Bundesen's Theory of Visual Attention , 2005, The Journal of Neuroscience.

[3]  Vincent P. Ferrera,et al.  Effects of Gaze Shifts on Maintenance of Spatial Memory in Macaque Frontal Eye Field , 2003, The Journal of Neuroscience.

[4]  K. Nakayama,et al.  Priming of popout: III. A short-term implicit memory system beneficial for rapid target selection , 2000 .

[5]  D. Munoz,et al.  t Immediate Neural Plasticity Shapes Motor Performance , 2000, The Journal of Neuroscience.

[6]  D M Levi,et al.  Surround modulation of perceived contrast and the role of brightness induction. , 2001, Journal of vision.

[7]  Vincent P. Ferrera,et al.  Effects of electrical microstimulation in monkey frontal eye field on saccades to remembered targets , 2005, Vision Research.

[8]  Alex Martin,et al.  Properties and mechanisms of perceptual priming , 1998, Current Opinion in Neurobiology.

[9]  P. Goldman-Rakic,et al.  Matching patterns of activity in primate prefrontal area 8a and parietal area 7ip neurons during a spatial working memory task. , 1998, Journal of neurophysiology.

[10]  R. Henson,et al.  Neural response suppression, haemodynamic repetition effects, and behavioural priming , 2003, Neuropsychologia.

[11]  Robert M. McPeek,et al.  Saccades require focal attention and are facilitated by a short-term memory system , 1999, Vision Research.

[12]  K. Nakayama,et al.  Priming of pop-out: I. Role of features , 1994, Memory & cognition.

[13]  Alan Cowey,et al.  Temporal aspects of visual search studied by transcranial magnetic stimulation , 1997, Neuropsychologia.

[14]  Puiu F. Balan,et al.  Effects of Spontaneous Eye Movements on Spatial Memory in Macaque Periarcuate Cortex , 2003, The Journal of Neuroscience.

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

[16]  Ravi S. Menon,et al.  Human fMRI evidence for the neural correlates of preparatory set , 2002, Nature Neuroscience.

[17]  M. Goldberg,et al.  Spatial processing in the monkey frontal eye field. I. Predictive visual responses. , 1997, Journal of neurophysiology.

[18]  A. Villringer,et al.  Involvement of the human frontal eye field and multiple parietal areas in covert visual selection during conjunction search , 2000, The European journal of neuroscience.

[19]  N. P. Bichot,et al.  Effects of similarity and history on neural mechanisms of visual selection , 1999, Nature Neuroscience.

[20]  A. Cowey,et al.  Normal discrimination performance accompanied by priming deficits in monkeys with V4 or TEO lesions. , 2000, Neuroreport.

[21]  R. Rafal,et al.  Transcranial Magnetic Stimulation of the Prefrontal Cortex Delays Contralateral Endogenous Saccades , 1997, Journal of Cognitive Neuroscience.

[22]  Ulrich Büttner,et al.  TMS evidence for smooth pursuit gain control by the frontal eye fields. , 2009, Cerebral cortex.

[23]  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.

[24]  T. Paus,et al.  Cortical regions involved in eye movements, shifts of attention, and gaze perception , 2005, Human brain mapping.

[25]  R. Passingham,et al.  The Attentional Role of the Left Parietal Cortex: The Distinct Lateralization and Localization of Motor Attention in the Human Brain , 2001, Journal of Cognitive Neuroscience.

[26]  D P Munoz,et al.  Time course of a repetition effect on saccadic reaction time in non-human primates. , 2002, Archives italiennes de biologie.

[27]  Jöran Lepsien,et al.  The Timing of Neural Activity during Shifts of Spatial Attention , 2009, Journal of Cognitive Neuroscience.

[28]  J R Duhamel,et al.  The updating of the representation of visual space in parietal cortex by intended eye movements. , 1992, Science.

[29]  C. Kennard,et al.  Impaired spatial working memory across saccades contributes to abnormal search in parietal neglect. , 2001, Brain : a journal of neurology.

[30]  Tony Ro,et al.  Inhibition of return and the human frontal eye fields , 2003, Experimental Brain Research.

[31]  E. Keller,et al.  Short-term priming, concurrent processing, and saccade curvature during a target selection task in the monkey , 2001, Vision Research.

[32]  Chris Rorden,et al.  Transcranial magnetic stimulation of the left human frontal eye fields eliminates the cost of invalid endogenous cues , 2005, Neuropsychologia.

[33]  Árni Kristjánsson,et al.  Priming of Color and Position during Visual Search in Unilateral Spatial Neglect , 2005, Journal of Cognitive Neuroscience.

[34]  Michael Petrides,et al.  Local Morphology Predicts Functional Organization of the Dorsal Premotor Region in the Human Brain , 2006, The Journal of Neuroscience.

[35]  D. Gitelman,et al.  Neuroanatomic Overlap of Working Memory and Spatial Attention Networks: A Functional MRI Comparison within Subjects , 1999, NeuroImage.

[36]  R. Wurtz,et al.  Visual receptive fields of frontal eye field neurons. , 1973, Brain research.

[37]  Jillian H. Fecteau,et al.  Exploring the consequences of the previous trial , 2003, Nature Reviews Neuroscience.

[38]  R. Desimone,et al.  Neural mechanisms for visual memory and their role in attention. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[39]  N. Kanwisher,et al.  Cortical Regions Involved in Perceiving Object Shape , 2000, The Journal of Neuroscience.

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

[41]  Carlo Marzi,et al.  The role of frontal eye-fields and superior colliculi in visual search and non-visual search in rhesus monkeys , 1982, Behavioural Brain Research.

[42]  J. Mattingley,et al.  Impaired Working Memory for Location but not for Colour or Shape in Visual Neglect: a Comparison of Parietal and Non-Parietal Lesions , 2004, Cortex.

[43]  J. Rothwell,et al.  Motor and phosphene thresholds: a transcranial magnetic stimulation correlation study , 2001, Neuropsychologia.

[44]  J. Schall Neural correlates of decision processes: neural and mental chronometry , 2003, Current Opinion in Neurobiology.

[45]  Robert M McPeek,et al.  Competition between saccade goals in the superior colliculus produces saccade curvature. , 2003, Journal of neurophysiology.

[46]  R. Klein,et al.  Inhibition of return , 2000, Trends in Cognitive Sciences.

[47]  P. Goldman-Rakic,et al.  Inactivation of parietal and prefrontal cortex reveals interdependence of neural activity during memory-guided saccades. , 2000, Journal of neurophysiology.

[48]  Gianluca Campana,et al.  Priming of motion direction and area V5/MT: a test of perceptual memory. , 2002, Cerebral cortex.

[49]  Jon Driver,et al.  Revisiting Previously Searched Locations in Visual Neglect: Role of Right Parietal and Frontal Lesions in Misjudging Old Locations as New , 2005, Journal of Cognitive Neuroscience.

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

[51]  Clayton E. Curtis,et al.  Maintenance of Spatial and Motor Codes during Oculomotor Delayed Response Tasks , 2004, The Journal of Neuroscience.

[52]  D P Munoz,et al.  Neuronal Correlates for Preparatory Set Associated with Pro-Saccades and Anti-Saccades in the Primate Frontal Eye Field , 2000, The Journal of Neuroscience.

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

[54]  Clayton E Curtis,et al.  Selection and maintenance of saccade goals in the human frontal eye fields. , 2006, Journal of neurophysiology.

[55]  M. Bravo,et al.  The role of attention in different visual-search tasks , 1992, Perception & psychophysics.

[56]  R. P. Maguire,et al.  Event-related fMRI responses in the human frontal eye fields in a randomized pro- and antisaccade task , 2001, NeuroImage.

[57]  J. Jonides,et al.  Overlapping mechanisms of attention and spatial working memory , 2001, Trends in Cognitive Sciences.

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

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

[60]  E Tulving,et al.  Priming and human memory systems. , 1990, Science.

[61]  K. Nakayama,et al.  Priming of pop-out: II. The role of position , 1996, Perception & psychophysics.

[62]  Jeffrey D Schall,et al.  The neural selection and control of saccades by the frontal eye field. , 2002, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[63]  B. Gaymard,et al.  The frontal eye field is involved in spatial short-term memory but not in reflexive saccade inhibition , 1999, Experimental Brain Research.

[64]  Neil G. Muggleton,et al.  On the roles of the human frontal eye fields and parietal cortex in visual search , 2006 .

[65]  Robert M. McPeek,et al.  Superior colliculus activity related to concurrent processing of saccade goals in a visual search task. , 2002, Journal of neurophysiology.

[66]  R. Klein,et al.  Contribution of the Primate Superior Colliculus to Inhibition of Return , 2002, Journal of Cognitive Neuroscience.

[67]  E. Macaluso,et al.  Neural basis for priming of pop-out during visual search revealed with fMRI. , 2007, Cerebral cortex.