Effective connectivity during feature-based attentional capture: evidence against the attentional reorienting hypothesis of TPJ.

The most prevalent neurobiological theory of attentional control posits 2 distinct brain networks: The dorsal and ventral attention networks. The role of the dorsal attentional network in top-down attentional control is well established, but there is less evidence for the putative role of the ventral attentional network in initiating stimulus-driven reorienting. Here, we used functional magnetic resonance imaging and dynamic causal modeling (DCM) to test the role of the ventral and dorsal networks in attentional reorienting during instances of attentional capture by a target-colored distracter. In the region of interest analyses, we found that frontal eye field (FEF) was selectively activated by conditions where attention was reoriented (i.e. to spatial cues and target-colored distracters). In contrast, temporoparietal junction (TPJ) responded positively to all stimulus conditions. The DCM results indicated that FEF received sensory inputs earlier than TPJ, and that only the connection from FEF to TPJ was modulated by the appearance of the target-colored distracter. The results provide novel empirical evidence against the idea that TPJ generates stimulus-driven reorientations of attention. We conclude that our results are incompatible with existing theories of TPJ involvement in the stimulus-driven reorientation of attention and discuss alternative explanations such as contextual updating.

[1]  Marina Schmid,et al.  An Introduction To The Event Related Potential Technique , 2016 .

[2]  D. Basso,et al.  TMS on right frontal eye fields induces an inflexible focus of attention. , 2014, Cerebral cortex.

[3]  O. Tzeng,et al.  Right temporoparietal junction and attentional reorienting , 2013, Human brain mapping.

[4]  Stefan Pollmann,et al.  Dorsal and ventral working memory-related brain areas support distinct processes in contextual cueing , 2013, NeuroImage.

[5]  Patrick Dupont,et al.  Cytoarchitectonic mapping of attentional selection and reorienting in parietal cortex , 2013, NeuroImage.

[6]  Marta I. Garrido,et al.  Dynamic Causal Modelling of epileptic seizure propagation pathways: A combined EEG–fMRI study , 2012, NeuroImage.

[7]  Karl J. Friston,et al.  Deconstructing the Architecture of Dorsal and Ventral Attention Systems with Dynamic Causal Modeling , 2012, The Journal of Neuroscience.

[8]  S. Luck,et al.  A Common Neural Mechanism for Preventing and Terminating the Allocation of Attention , 2012, The Journal of Neuroscience.

[9]  J. Duhamel,et al.  Differential effects of parietal and frontal inactivations on reaction times distributions in a visual search task , 2012, Front. Integr. Neurosci..

[10]  Morris Moscovitch,et al.  Cognitive contributions of the ventral parietal cortex: an integrative theoretical account , 2012, Trends in Cognitive Sciences.

[11]  Sarah Shomstein,et al.  Cognitive functions of the posterior parietal cortex: top-down and bottom-up attentional control , 2012, Front. Integr. Neurosci..

[12]  Joy J. Geng,et al.  Contextual Knowledge Configures Attentional Control Networks , 2011, The Journal of Neuroscience.

[13]  Jon Driver,et al.  Visual Selection and the Human Frontal Eye Fields: Effects of Frontal Transcranial Magnetic Stimulation on Partial Report Analyzed by Bundesen's Theory of Visual Attention , 2011, The Journal of Neuroscience.

[14]  Rainer Goebel,et al.  The identification of interacting networks in the brain using fMRI: Model selection, causality and deconvolution , 2011, NeuroImage.

[15]  Olivier David,et al.  fMRI connectivity, meaning and empiricism Comments on: Roebroeck et al. The identification of interacting networks in the brain using fMRI: Model selection, causality and deconvolution , 2011, NeuroImage.

[16]  Klaas E. Stephan,et al.  Dynamic causal modelling: A critical review of the biophysical and statistical foundations , 2011, NeuroImage.

[17]  Barry Giesbrecht,et al.  Electrophysiological Evidence for Spatiotemporal Flexibility in the Ventrolateral Attention Network , 2011, PloS one.

[18]  Karl J. Friston,et al.  Effective connectivity: Influence, causality and biophysical modeling , 2011, NeuroImage.

[19]  Robert Desimone,et al.  Feature-Based Attention in the Frontal Eye Field and Area V4 during Visual Search , 2011, Neuron.

[20]  M. Catani,et al.  A lateralized brain network for visuospatial attention , 2011, Nature Neuroscience.

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

[22]  Kaustubh Supekar,et al.  Dissociable connectivity within human angular gyrus and intraparietal sulcus: evidence from functional and structural connectivity. , 2010, Cerebral cortex.

[23]  Karl J. Friston,et al.  Dynamic causal modeling , 2010, Scholarpedia.

[24]  E. Macaluso,et al.  Neural correlates of the spatial and expectancy components of endogenous and stimulus-driven orienting of attention in the Posner task. , 2010, Cerebral cortex.

[25]  E. Macaluso,et al.  Right temporal-parietal junction engagement during spatial reorienting does not depend on strategic attention control , 2010, Neuropsychologia.

[26]  Karl J. Friston,et al.  Comparing Families of Dynamic Causal Models , 2010, PLoS Comput. Biol..

[27]  Karl J. Friston,et al.  Ten simple rules for dynamic causal modeling , 2010, NeuroImage.

[28]  Deanna M. Barch,et al.  When less is more: TPJ and default network deactivation during encoding predicts working memory performance , 2010, NeuroImage.

[29]  E. Miller,et al.  Serial, Covert Shifts of Attention during Visual Search Are Reflected by the Frontal Eye Fields and Correlated with Population Oscillations , 2009, Neuron.

[30]  George R. Mangun,et al.  Anterior Intraparietal Sulcus is Sensitive to Bottom–Up Attention Driven by Stimulus Salience , 2009, Journal of Cognitive Neuroscience.

[31]  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.

[32]  R. Desimone,et al.  High-Frequency, Long-Range Coupling Between Prefrontal and Visual Cortex During Attention , 2009, Science.

[33]  M. Corbetta,et al.  Interaction of Stimulus-Driven Reorienting and Expectation in Ventral and Dorsal Frontoparietal and Basal Ganglia-Cortical Networks , 2009, The Journal of Neuroscience.

[34]  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.

[35]  C. Segebarth,et al.  Identifying Neural Drivers with Functional MRI: An Electrophysiological Validation , 2008, PLoS biology.

[36]  Manos Tsakiris,et al.  The role of the right temporo-parietal junction in maintaining a coherent sense of one's body , 2008, Neuropsychologia.

[37]  A. Milner,et al.  Contralateral visual search deficits following TMS. , 2008, Journal of neuropsychology.

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

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

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

[41]  Karl J. Friston,et al.  The effect of prior visual information on recognition of speech and sounds. , 2008, Cerebral cortex.

[42]  Jason P. Mitchell Activity in right temporo-parietal junction is not selective for theory-of-mind. , 2008, Cerebral cortex.

[43]  M. Corbetta,et al.  Right TPJ deactivation during visual search: functional significance and support for a filter hypothesis. , 2007, Cerebral cortex.

[44]  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.

[45]  J. Decety,et al.  The Role of the Right Temporoparietal Junction in Social Interaction: How Low-Level Computational Processes Contribute to Meta-Cognition , 2007, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[46]  J. Polich Updating P300: An integrative theory of P3a and P3b , 2007, Clinical Neurophysiology.

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

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

[49]  Parashkev Nachev,et al.  Space and the parietal cortex , 2007, Trends in Cognitive Sciences.

[50]  Guy A. Orban,et al.  Mapping the parietal cortex of human and non-human primates , 2006, Neuropsychologia.

[51]  Katrin Amunts,et al.  The human inferior parietal cortex: Cytoarchitectonic parcellation and interindividual variability , 2006, NeuroImage.

[52]  Risa Sawaki,et al.  Stimulus context determines whether non-target stimuli are processed as task-relevant or distractor information , 2006, Clinical Neurophysiology.

[53]  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.

[54]  Timothy Edward John Behrens,et al.  Connection patterns distinguish 3 regions of human parietal cortex. , 2006, Cerebral cortex.

[55]  R. Sparing,et al.  Hemiextinction induced by transcranial magnetic stimulation over the right temporo-parietal junction , 2006, Neuroscience.

[56]  Karl J. Friston,et al.  Synaptic Plasticity and Dysconnection in Schizophrenia , 2006, Biological Psychiatry.

[57]  N. Squires,et al.  Electrophysiological correlates of categorization: P300 amplitude as index of target similarity , 2006, Biological Psychology.

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

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

[60]  S. Luck An Introduction to the Event-Related Potential Technique , 2005 .

[61]  N. Lavie,et al.  The role of working memory in attentional capture , 2005, Psychonomic bulletin & review.

[62]  Allen Azizian,et al.  Event-related potentials as an index of similarity between words and pictures. , 2005, Psychophysiology.

[63]  G. Fink,et al.  REVIEW: The functional organization of the intraparietal sulcus in humans and monkeys , 2005, Journal of anatomy.

[64]  Jonathan D. Cohen,et al.  Decision making, the P3, and the locus coeruleus-norepinephrine system. , 2005, Psychological bulletin.

[65]  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.

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

[67]  Igor Schindler,et al.  An exploration of the role of the superior temporal gyrus in visual search and spatial perception using TMS , 2014 .

[68]  Karl J. Friston,et al.  Biophysical models of fMRI responses , 2004, Current Opinion in Neurobiology.

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

[70]  Karl J. Friston,et al.  Comparing dynamic causal models , 2004, NeuroImage.

[71]  Rainer Goebel,et al.  Attentional systems in target and distractor processing: a combined ERP and fMRI study , 2004, NeuroImage.

[72]  Karl J. Friston,et al.  Where bottom-up meets top-down: neuronal interactions during perception and imagery. , 2004, Cerebral cortex.

[73]  J. Mattingley,et al.  Fast and slow parietal pathways mediate spatial attention , 2004, Nature Neuroscience.

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

[75]  M. Corbetta,et al.  Quantitative analysis of attention and detection signals during visual search. , 2003, Journal of neurophysiology.

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

[77]  Karl J. Friston,et al.  Dynamic causal modelling , 2003, NeuroImage.

[78]  Andrew B. Leber,et al.  Made you blink! Contingent attentional capture produces a spatial blink , 2002, Perception & psychophysics.

[79]  E. Macaluso,et al.  Supramodal Effects of Covert Spatial Orienting Triggered by Visual or Tactile Events , 2002, Journal of Cognitive Neuroscience.

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

[81]  J. Downar,et al.  A cortical network sensitive to stimulus salience in a neutral behavioral context across multiple sensory modalities. , 2002, Journal of neurophysiology.

[82]  M. A. Steinmetz,et al.  Neuronal responses in area 7a to multiple-stimulus displays: I. neurons encode the location of the salient stimulus. , 2001, Cerebral cortex.

[83]  M. A. Steinmetz,et al.  Neuronal responses in area 7a to multiple stimulus displays: II. responses are suppressed at the cued location. , 2001, Cerebral cortex.

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

[85]  M. Bertini,et al.  Voluntary oculomotor performance upon awakening after total sleep deprivation. , 2000, Sleep.

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

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

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

[89]  R T Knight,et al.  Anatomic bases of event-related potentials and their relationship to novelty detection in humans. , 1998, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[90]  J. Ford,et al.  Combined event‐related fMRI and EEG evidence for temporal—parietal cortex activation during target detection , 1997, Neuroreport.

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

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

[93]  Karl J. Friston,et al.  Spatial registration and normalization of images , 1995 .

[94]  J. C. Johnston,et al.  Involuntary covert orienting is contingent on attentional control settings. , 1992, Journal of experimental psychology. Human perception and performance.

[95]  S. Yamaguchi,et al.  Anterior and posterior association cortex contributions to the somatosensory P300 , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[96]  S. Yantis,et al.  Abrupt visual onsets and selective attention: voluntary versus automatic allocation. , 1990, Journal of experimental psychology. Human perception and performance.

[97]  R. Knight,et al.  Contributions of temporal-parietal junction to the human auditory P3 , 1989, Brain Research.

[98]  E. Donchin Presidential address, 1980. Surprise!...Surprise? , 1981, Psychophysiology.

[99]  William L. Wilkie,et al.  Presidential Address: 1980 , 1981 .

[100]  P. Cooke Presidential address 1980. , 1980, The Hospital and health services review.

[101]  R. C. Oldfield The assessment and analysis of handedness: the Edinburgh inventory. , 1971, Neuropsychologia.

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