Ignoring the Elephant in the Room: A Neural Circuit to Downregulate Salience

How do we ignore stimuli that are salient but irrelevant when our task is to select a lower salient stimulus? Since bottom–up processes favor high saliency, detection of a low-salient target in the presence of highly salient distractors requires top–down attentional guidance. Previous studies have demonstrated that top–down attention can modulate perceptual processing and also that the control of attention is driven by frontoparietal regions. However, to date, there is no direct evidence on the cause and effect relationship between control regions and perceptual processing. Here, we report the first evidence demonstrating a neural circuit for the downregulation of salient distractors when a low-salient target is selected, combining brain imaging using functional magnetic resonance imaging with brain stimulation by transcranial magnetic stimulation. Using these combined techniques, we were able to identify a cause and effect relationship in the suppression of saliency, based on an interaction between the left intraparietal sulcus (IPS) and a region implicated in visual processing in our task (the left occipital pole). In particular, low-salient stimuli were selected by the left IPS suppressing early visual areas that would otherwise respond to a high-saliency distractor in the task. Apart from providing a first documentation of the neural circuit supporting selection by saliency, these data can be critical for understanding the underlying causes of problems in ignoring irrelevant salience that are found in both acquired and neurodevelopmental disorders (e.g., attention deficit/hyperactivity disorder or autism).

[1]  Stephen M. Smith,et al.  General multilevel linear modeling for group analysis in FMRI , 2003, NeuroImage.

[2]  Karl J. Friston,et al.  Psychophysiological and Modulatory Interactions in Neuroimaging , 1997, NeuroImage.

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

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

[5]  J. Bullier Integrated model of visual processing , 2001, Brain Research Reviews.

[6]  Vincent Walsh,et al.  Right parietal cortex plays a critical role in change blindness. , 2006, Cerebral cortex.

[7]  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.

[8]  Alan C. Evans,et al.  A new anatomical landmark for reliable identification of human area V5/MT: a quantitative analysis of sulcal patterning. , 2000, Cerebral cortex.

[9]  C. W. Hess,et al.  Transcranial stimulation of the human frontal eye field by magnetic pulses , 2004, Experimental Brain Research.

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

[11]  G. Orban,et al.  Comparative mapping of higher visual areas in monkeys and humans , 2004, Trends in Cognitive Sciences.

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

[13]  J. Talairach,et al.  Co-Planar Stereotaxic Atlas of the Human Brain: 3-Dimensional Proportional System: An Approach to Cerebral Imaging , 1988 .

[14]  M. Mesulam A cortical network for directed attention and unilateral neglect , 1981, Annals of neurology.

[15]  A. Cowey,et al.  Visual field defects after frontal eye-field lesions in monkeys. , 1971, Brain research.

[16]  C. Frith,et al.  Neural correlates of change detection and change blindness , 2001, Nature Neuroscience.

[17]  Leslie G. Ungerleider,et al.  The neural basis of biased competition in human visual cortex , 2001, Neuropsychologia.

[18]  Richard A. Tyrrell,et al.  A rapid technique to assess the resting states of the eyes and other threshold phenomena: The Modified Binary Search (MOBS) , 1988 .

[19]  M. Goldberg,et al.  A Rapid and Precise On-Response in Posterior Parietal Cortex , 2004, The Journal of Neuroscience.

[20]  Stephen M Smith,et al.  Fast robust automated brain extraction , 2002, Human brain mapping.

[21]  Carlo Miniussi,et al.  The role of the right dorsolateral prefrontal cortex in visual change awareness , 2004, Neuroreport.

[22]  Vincent Walsh,et al.  The perceptual and functional consequences of parietal top-down modulation on the visual cortex. , 2009, Cerebral cortex.

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

[24]  Stephen M. Smith,et al.  Improved Optimization for the Robust and Accurate Linear Registration and Motion Correction of Brain Images , 2002, NeuroImage.

[25]  Jeffrey D. Schall,et al.  The detection of visual signals by macaque frontal eye field during masking , 1999, Nature Neuroscience.

[26]  A. T. Smith,et al.  Attentional suppression of activity in the human visual cortex , 2000, Neuroreport.

[27]  G R Grice,et al.  Forest before trees? It depends where you look , 1983, Perception & psychophysics.

[28]  Stephen M. Smith,et al.  A global optimisation method for robust affine registration of brain images , 2001, Medical Image Anal..

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

[30]  E. Wassermann Risk and safety of repetitive transcranial magnetic stimulation: report and suggested guidelines from the International Workshop on the Safety of Repetitive Transcranial Magnetic Stimulation, June 5-7, 1996. , 1998, Electroencephalography and clinical neurophysiology.

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

[32]  E. G. Keating,et al.  Saccadic disorders caused by cooling the superior colliculus or the frontal eye field, or from combined lesions of both structures , 1988, Brain Research.

[33]  Maurizio Corbetta,et al.  Anticipatory Suppression of Nonattended Locations in Visual Cortex Marks Target Location and Predicts Perception , 2008, The Journal of Neuroscience.

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

[35]  Jens Schwarzbach,et al.  Cerebral Cortex Advance Access published May 27, 2004 Control of Object-based Attention in Human Cortex , 2022 .

[36]  Glyn W. Humphreys,et al.  Reflexive and Preparatory Selection and Suppression of Salient Information in the Right and Left Posterior Parietal Cortex , 2009, Journal of Cognitive Neuroscience.

[37]  Simon B. Eickhoff,et al.  A new SPM toolbox for combining probabilistic cytoarchitectonic maps and functional imaging data , 2005, NeuroImage.

[38]  S. Yantis,et al.  Selective visual attention and perceptual coherence , 2006, Trends in Cognitive Sciences.

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

[40]  Martin Eimer,et al.  Cortico-cortical interactions in spatial attention: A combined ERP/TMS study. , 2006, Journal of neurophysiology.

[41]  Walsh,et al.  Trickle-down theories of vision , 2006 .

[42]  Juha Silvanto,et al.  Baseline cortical excitability determines whether TMS disrupts or facilitates behavior. , 2008, Journal of neurophysiology.

[43]  R. Desimone,et al.  Selective attention gates visual processing in the extrastriate cortex. , 1985, Science.

[44]  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.

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

[46]  Gianluca Campana,et al.  Visual area V5/MT remembers "what" but not "where". , 2004, Cerebral cortex.

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

[48]  Stephen M. Smith,et al.  Temporal Autocorrelation in Univariate Linear Modeling of FMRI Data , 2001, NeuroImage.

[49]  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.

[50]  Jeffrey D. Schall,et al.  Neural basis of saccade target selection in frontal eye field during visual search , 1993, Nature.

[51]  J. Bullier,et al.  Topography of visual cortex connections with frontal eye field in macaque: convergence and segregation of processing streams , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[53]  Karl J. Friston,et al.  Acute Changes in Frontoparietal Activity after Repetitive Transcranial Magnetic Stimulation over the Dorsolateral Prefrontal Cortex in a Cued Reaction Time Task , 2006, The Journal of Neuroscience.

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

[55]  Alan C. Evans,et al.  A Three-Dimensional Statistical Analysis for CBF Activation Studies in Human Brain , 1992, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[56]  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.

[57]  Carmel Mevorach,et al.  Driven to less distraction: rTMS of the right parietal cortex reduces attentional capture in visual search. , 2009, Cerebral cortex.

[58]  Michael Brady,et al.  Improved Optimization for the Robust and Accurate Linear Registration and Motion Correction of Brain Images , 2002, NeuroImage.

[59]  Mark W. Woolrich,et al.  Multilevel linear modelling for FMRI group analysis using Bayesian inference , 2004, NeuroImage.

[60]  M. Mesulam,et al.  Spatial attention and neglect: parietal, frontal and cingulate contributions to the mental representation and attentional targeting of salient extrapersonal events. , 1999, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[61]  Glyn W. Humphreys,et al.  The Left Intraparietal Sulcus Modulates the Selection of Low Salient Stimuli , 2009, Journal of Cognitive Neuroscience.

[62]  Robert T. Knight,et al.  Top-down Enhancement and Suppression of the Magnitude and Speed of Neural Activity , 2005, Journal of Cognitive Neuroscience.

[63]  M. Rushworth,et al.  Functionally Specific Reorganization in Human Premotor Cortex , 2007, Neuron.

[64]  Glyn W. Humphreys,et al.  Effects of saliency, not global dominance, in patients with left parietal damage , 2006, Neuropsychologia.

[65]  C. D. Frith,et al.  Brain Activations during Visual Search: Contributions of Search Efficiency versus Feature Binding , 2003, NeuroImage.

[66]  J C Rothwell,et al.  The planning and guiding of reading saccades: a repetitive transcranial magnetic stimulation study. , 2001, Cerebral cortex.

[67]  S. Kastner,et al.  Stimulus context modulates competition in human extrastriate cortex , 2005, Nature Neuroscience.

[68]  J Duncan,et al.  Responses of neurons in macaque area V4 during memory-guided visual search. , 2001, Cerebral cortex.

[69]  R. Goebel,et al.  Imaging the brain activity changes underlying impaired visuospatial judgments: simultaneous FMRI, TMS, and behavioral studies. , 2007, Cerebral cortex.

[70]  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.

[71]  Richard S. J. Frackowiak,et al.  Area V5 of the human brain: evidence from a combined study using positron emission tomography and magnetic resonance imaging. , 1993, Cerebral cortex.

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

[73]  Carmel Mevorach,et al.  Opposite biases in salience-based selection for the left and right posterior parietal cortex , 2006, Nature Neuroscience.

[74]  A. Cowey,et al.  Motion perception and perceptual learning studied by magnetic stimulation. , 1999, Electroencephalography and clinical neurophysiology. Supplement.

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

[76]  Nancy Kanwisher,et al.  fMRI evidence for objects as the units of attentional selection , 1999, Nature.

[77]  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.

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

[79]  H. Kennedy,et al.  Laminar Distribution of Neurons in Extrastriate Areas Projecting to Visual Areas V1 and V4 Correlates with the Hierarchical Rank and Indicates the Operation of a Distance Rule , 2000, The Journal of Neuroscience.

[80]  Alan Cowey,et al.  Transcranial magnetic stimulation and cognitive neuroscience , 2000, Nature Reviews Neuroscience.

[81]  Joel R. Meyer,et al.  A large-scale distributed network for covert spatial attention: further anatomical delineation based on stringent behavioural and cognitive controls. , 1999, Brain : a journal of neurology.

[82]  Leslie G. Ungerleider,et al.  Mechanisms of directed attention in the human extrastriate cortex as revealed by functional MRI. , 1998, Science.

[83]  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.

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

[85]  Carmel Mevorach,et al.  Attending to local form while ignoring global aspects depends on handedness: evidence from TMS , 2005, Nature Neuroscience.

[86]  R. Desimone,et al.  Responses of Neurons in Inferior Temporal Cortex during Memory- Guided Visual Search , 1998 .