Anterior Intraparietal Sulcus is Sensitive to Bottom–Up Attention Driven by Stimulus Salience

Frontal eye fields (FEF) and anterior intraparietal sulcus (aIPS) are involved in the control of voluntary attention in humans, but their functional differences remain poorly understood. We examined the activity in these brain regions as a function of task-irrelevant changes in target and nontarget perceptual salience during a sustained spatial attention task. Both aIPS and FEF were engaged during selective attention. FEF, but not aIPS, was sensitive to the direction of spatial attention. Conversely, aIPS, but not FEF, was modulated by the relative perceptual salience of the target and nontarget stimuli. These results demonstrate separable roles for FEF and aIPS in attentional control with FEF more involved in goal-directed spatial attention and aIPS relatively more sensitive to bottom–up attentional influences driven by stimulus salience.

[1]  R. Andersen,et al.  Visual receptive field organization and cortico‐cortical connections of the lateral intraparietal area (area LIP) in the macaque , 1990, The Journal of comparative neurology.

[2]  M. Sereno,et al.  Retinotopy and Attention in Human Occipital, Temporal, Parietal, and Frontal Cortex , 2008 .

[3]  Leslie G. Ungerleider,et al.  Mechanisms of visual attention in the human cortex. , 2000, Annual review of neuroscience.

[4]  Jason B. Mattingley,et al.  Enhancement of visual selection during transient disruption of parietal cortex , 2006, Brain Research.

[5]  J. Theeuwes,et al.  Electrophysiological Evidence of the Capture of Visual Attention , 2006, Journal of Cognitive Neuroscience.

[6]  M. Behrmann,et al.  Parietal cortex and attention , 2004, Current Opinion in Neurobiology.

[7]  D. Heeger,et al.  Sustained Activity in Topographic Areas of Human Posterior Parietal Cortex during Memory-Guided Saccades , 2006, The Journal of Neuroscience.

[8]  Jan Theeuwes,et al.  Endogenous and exogenous attention shifts are mediated by the same large-scale neural network , 2004, NeuroImage.

[9]  Maurizio Corbetta,et al.  Asymmetry of Anticipatory Activity in Visual Cortex Predicts the Locus of Attention and Perception , 2007, The Journal of Neuroscience.

[10]  N. Kanwisher,et al.  The Generality of Parietal Involvement in Visual Attention , 1999, Neuron.

[11]  Karl J. Friston,et al.  Statistical parametric maps in functional imaging: A general linear approach , 1994 .

[12]  C. Koch,et al.  A saliency-based search mechanism for overt and covert shifts of visual attention , 2000, Vision Research.

[13]  Troy A W Visser,et al.  A re-examination of the impact of object processing on shifts of spatial attention , 2011, Attention, perception & psychophysics.

[14]  Clayton E Curtis,et al.  Cortical activity time locked to the shift and maintenance of spatial attention. , 2008, Cerebral cortex.

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

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

[17]  Howard E Egeth,et al.  Biased competition and visual search: the role of luminance and size contrast , 2007, Psychological research.

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

[19]  R. Wurtz,et al.  Comparison of cortico-cortical and cortico-collicular signals for the generation of saccadic eye movements. , 2002, Journal of neurophysiology.

[20]  S. Luck,et al.  The neural site of attention matches the spatial scale of perception , 2010 .

[21]  E. Reed The Ecological Approach to Visual Perception , 1989 .

[22]  D. Gitelman,et al.  Covert Visual Spatial Orienting and Saccades: Overlapping Neural Systems , 2000, NeuroImage.

[23]  Lotfi B Merabet,et al.  Visual Topography of Human Intraparietal Sulcus , 2007, The Journal of Neuroscience.

[24]  E. Macaluso,et al.  Dissociation of stimulus relevance and saliency factors during shifts of visuospatial attention. , 2007, Cerebral cortex.

[25]  S. Luck,et al.  Neural sources of focused attention in visual search. , 2000, Cerebral cortex.

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

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

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

[29]  E. DeYoe,et al.  A physiological correlate of the 'spotlight' of visual attention , 1999, Nature Neuroscience.

[30]  G. Mangun,et al.  Author ' s personal copy Research Report fMRI evidence for both generalized and specialized components of attentional control , 2007 .

[31]  J. D. Connolly,et al.  Saccade preparation signals in the human frontal and parietal cortices. , 2008, Journal of neurophysiology.

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

[33]  Bruce D. McCandliss,et al.  The Relation of Brain Oscillations to Attentional Networks , 2007, The Journal of Neuroscience.

[34]  D. Heeger,et al.  Topographic maps of visual spatial attention in human parietal cortex. , 2005, Journal of neurophysiology.

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

[36]  C. Kennard,et al.  The anatomy of visual neglect , 2003 .

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

[38]  D. Somers,et al.  Multiple Spotlights of Attentional Selection in Human Visual Cortex , 2004, Neuron.

[39]  Kristina M. Visscher,et al.  The neural bases of momentary lapses in attention , 2006, Nature Neuroscience.

[40]  Karl J. Friston,et al.  Interhemispheric Integration of Visual Processing during Task-Driven Lateralization , 2007, The Journal of Neuroscience.

[41]  Richard S. J. Frackowiak,et al.  Neurobiological measures of human selective attention , 2001, Neuropsychologia.

[42]  Biyu J. He,et al.  Breakdown of Functional Connectivity in Frontoparietal Networks Underlies Behavioral Deficits in Spatial Neglect , 2007, Neuron.

[43]  Marisa Carrasco,et al.  Feature-based attention modulates orientation-selective responses in human visual cortex , 2010 .

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

[45]  G. Mangun,et al.  Dissociating top-down attentional control from selective perception and action , 2001, Neuropsychologia.

[46]  Michael L. Platt,et al.  Neural correlates of decision variables in parietal cortex , 1999, Nature.

[47]  H. Egeth,et al.  Target-nontarget similarity modulates stimulus-driven control in visual search , 2006, Psychonomic bulletin & review.

[48]  E. Miller,et al.  Response to Comment on "Top-Down Versus Bottom-Up Control of Attention in the Prefrontal and Posterior Parietal Cortices" , 2007, Science.

[49]  George R. Mangun,et al.  Right temporoparietal junction activation by a salient contextual cue facilitates target discrimination , 2011, NeuroImage.

[50]  Pia Rotshtein,et al.  On-line attentional selection from competing stimuli in opposite visual fields: effects on human visual cortex and control processes. , 2006, Journal of neurophysiology.

[51]  K. Nakayama,et al.  Sustained and transient components of focal visual attention , 1989, Vision Research.

[52]  Karin Mogg,et al.  Neural activity associated with attention orienting triggered by gaze cues: A study of lateralized ERPs , 2010, Social neuroscience.

[53]  N. Lavie Perceptual load as a necessary condition for selective attention. , 1995, Journal of experimental psychology. Human perception and performance.

[54]  R. Rafal,et al.  Competition between endogenous and exogenous orienting of visual attention. , 2005, Journal of experimental psychology. General.

[55]  Gereon R. Fink,et al.  Cue validity modulates the neural correlates of covert endogenous orienting of attention in parietal and frontal cortex , 2006, NeuroImage.

[56]  M I Sereno,et al.  Analysis of retinotopic maps in extrastriate cortex. , 1994, Cerebral cortex.

[57]  M. Greicius,et al.  Resting-state functional connectivity reflects structural connectivity in the default mode network. , 2009, Cerebral cortex.

[58]  C. Bundesen A theory of visual attention. , 1990, Psychological review.

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

[60]  D. Spalding The Principles of Psychology , 1873, Nature.

[61]  H. J. Muller,et al.  Reflexive and voluntary orienting of visual attention: time course of activation and resistance to interruption. , 1989, Journal of experimental psychology. Human perception and performance.

[62]  Andrew R. Mayer,et al.  An Event-related fMRI Study of Exogenous Orienting: Supporting Evidence for the Cortical Basis of Inhibition of Return? , 2004, Journal of Cognitive Neuroscience.

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

[64]  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.

[65]  A. Nobre,et al.  The Large-Scale Neural Network for Spatial Attention Displays Multifunctional Overlap But Differential Asymmetry , 1999, NeuroImage.

[66]  C. Eriksen,et al.  Allocation of attention in the visual field. , 1985, Journal of experimental psychology. Human perception and performance.

[67]  M. Corbetta,et al.  The Reorienting System of the Human Brain: From Environment to Theory of Mind , 2008, Neuron.

[68]  R. Desimone,et al.  Interacting Roles of Attention and Visual Salience in V4 , 2003, Neuron.

[69]  S. Yantis,et al.  On the distinction between visual salience and stimulus-driven attentional capture. , 1999, Journal of experimental psychology. Human perception and performance.

[70]  S. Yantis,et al.  Transient neural activity in human parietal cortex during spatial attention shifts , 2002, Nature Neuroscience.

[71]  DeLiang Wang,et al.  The role of priming in conjunctive visual search , 2002, Cognition.

[72]  J. Gottlieb From Thought to Action: The Parietal Cortex as a Bridge between Perception, Action, and Cognition , 2007, Neuron.

[73]  Stephen M. Rao,et al.  Neural Basis of Endogenous and Exogenous Spatial Orienting: A Functional MRI Study , 1999, Journal of Cognitive Neuroscience.

[74]  G. Boynton,et al.  Feature-Based Attentional Modulations in the Absence of Direct Visual Stimulation , 2007, Neuron.

[75]  David E. Irwin,et al.  Capturing attention , 1981, Cognition.

[76]  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.

[77]  James W Bisley,et al.  Neural correlates of attention and distractibility in the lateral intraparietal area. , 2006, Journal of neurophysiology.

[78]  S. Yantis,et al.  Uniqueness of abrupt visual onset in capturing attention , 1988, Perception & psychophysics.

[79]  G L Shulman,et al.  INAUGURAL ARTICLE by a Recently Elected Academy Member:A default mode of brain function , 2001 .

[80]  R. Ratcliff,et al.  Retrieval Processes in Recognition Memory , 1976 .

[81]  Ralph Weidner,et al.  What is “Odd” in Posner's Location-cueing Paradigm? Neural Responses to Unexpected Location and Feature Changes Compared , 2009, Journal of Cognitive Neuroscience.

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

[83]  Jacqueline Gottlieb,et al.  The lateral intraparietal area as a salience map: the representation of abrupt onset, stimulus motion, and task relevance , 2000, Vision Research.

[84]  Andrew R. Mayer,et al.  Neural networks underlying endogenous and exogenous visual–spatial orienting , 2004, NeuroImage.

[85]  Pierre Jolicoeur,et al.  Tracking the Location of Visuospatial Attention in a Contingent Capture Paradigm , 2008, Journal of Cognitive Neuroscience.

[86]  Maurizio Corbetta,et al.  Visuospatial reorienting signals in the human temporo‐parietal junction are independent of response selection , 2006, The European journal of neuroscience.

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

[88]  M. Raichle,et al.  Searching for a baseline: Functional imaging and the resting human brain , 2001, Nature Reviews Neuroscience.

[89]  S. Yantis,et al.  Spatially selective representations of voluntary and stimulus-driven attentional priority in human occipital, parietal, and frontal cortex. , 2007, Cerebral cortex.

[90]  Neil G. Muggleton,et al.  TMS over right posterior parietal cortex induces neglect in a scene-based frame of reference , 2006, Neuropsychologia.

[91]  Sabine Kastner,et al.  Topographic maps in human frontal cortex revealed in memory-guided saccade and spatial working-memory tasks. , 2007, Journal of neurophysiology.

[92]  T. Paus Location and function of the human frontal eye-field: A selective review , 1996, Neuropsychologia.

[93]  F. J. Friedrich,et al.  Effects of parietal injury on covert orienting of attention , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[94]  Marlene Behrmann,et al.  Cortical systems mediating visual attention to both objects and spatial locations. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[95]  Thomas Goschke,et al.  A neural system for evaluating the behavioural relevance of salient events outside the current focus of attention , 2010, Brain Research.

[96]  Vinod Menon,et al.  Functional connectivity in the resting brain: A network analysis of the default mode hypothesis , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[97]  G. Shulman,et al.  Medial prefrontal cortex and self-referential mental activity: Relation to a default mode of brain function , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[98]  W. Hockley Analysis of response time distributions in the study of cognitive processes. , 1984 .

[99]  M. Behrmann,et al.  Spatial probability as an attentional cue in visual search , 2005, Perception & psychophysics.

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

[101]  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.

[102]  Colin Blakemore,et al.  Spatial Attention Changes Excitability of Human Visual Cortex to Direct Stimulation , 2007, Current Biology.

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

[104]  David J Heeger,et al.  Neural correlates of sustained spatial attention in human early visual cortex. , 2007, Journal of neurophysiology.

[105]  Maurizio Corbetta,et al.  Oculomotor activity and visual spatial attention , 1995, Behavioural Brain Research.

[106]  Arno Villringer,et al.  Visual Feature and Conjunction Searches of Equal Difficulty Engage Only Partially Overlapping Frontoparietal Networks , 2002, NeuroImage.

[107]  Bijan Pesaran,et al.  Free choice activates a decision circuit between frontal and parietal cortex , 2008, Nature.

[108]  Jacqueline Gottlieb,et al.  LIP responses to a popout stimulus are reduced if it is overtly ignored , 2006, Nature Neuroscience.

[109]  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.

[110]  R. Dolan,et al.  Attentional load and sensory competition in human vision: modulation of fMRI responses by load at fixation during task-irrelevant stimulation in the peripheral visual field. , 2005, Cerebral cortex.

[111]  F. J. Friedrich,et al.  Spatial attention deficits in humans: a comparison of superior parietal and temporal-parietal junction lesions. , 1998, Neuropsychology.

[112]  Andrew B. Leber,et al.  Coordination of Voluntary and Stimulus-Driven Attentional Control in Human Cortex , 2005, Psychological science.

[113]  T. A. Kelley,et al.  Cortical mechanisms for shifting and holding visuospatial attention. , 2008, Cerebral cortex.

[114]  Yaoda Xu The Role of the Superior Intraparietal Sulcus in Supporting Visual Short-Term Memory for Multifeature Objects , 2007, The Journal of Neuroscience.

[115]  J. Downar,et al.  A multimodal cortical network for the detection of changes in the sensory environment , 2000, Nature Neuroscience.

[116]  Karl J. Friston,et al.  Modelling Geometric Deformations in Epi Time Series , 2022 .

[117]  M. Posner,et al.  Neural systems control of spatial orienting. , 1982, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

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

[119]  D. Heeger,et al.  Spatial attention affects brain activity in human primary visual cortex. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

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

[121]  Gereon R Fink,et al.  Cerebral correlates of alerting, orienting and reorienting of visuospatial attention: an event-related fMRI study , 2004, NeuroImage.

[122]  Arno Villringer,et al.  Parietal activation during visual search in the absence of multiple distractors , 2003, Neuroreport.

[123]  J. Theeuwes Abrupt luminance change pops out; abrupt color change does not , 1995, Perception & psychophysics.

[124]  N. J. Herrod,et al.  Maintaining and shifting attention within left or right hemifield. , 2000, Cerebral cortex.

[125]  N. P. Bichot,et al.  Dissociation of visual discrimination from saccade programming in macaque frontal eye field. , 1997, Journal of neurophysiology.

[126]  M. Carrasco Covert attention increases contrast sensitivity: Psychophysical, neurophysiological and neuroimaging studies. , 2006, Progress in brain research.

[127]  M. Posner,et al.  Attention and the detection of signals. , 1980, Journal of experimental psychology.

[128]  P D MCCORMACK,et al.  THE POSITIVE SKEW OBSERVED IN REACTION TIME DISTRIBUTIONS. , 1964, Canadian journal of psychology.

[129]  W. James,et al.  The Principles of Psychology. , 1983 .

[130]  M. Goldberg,et al.  Saccades, salience and attention: the role of the lateral intraparietal area in visual behavior. , 2006, Progress in brain research.