A critical role of temporoparietal junction in the integration of top‐down and bottom‐up attentional control

Information processing can be biased toward behaviorally relevant and salient stimuli by top‐down (goal‐directed) and bottom‐up (stimulus‐driven) attentional control processes respectively. However, the neural basis underlying the integration of these processes is not well understood. We employed functional magnetic resonance imaging (fMRI) and transcranial direct‐current stimulation (tDCS) in humans to examine the brain mechanisms underlying the interaction between these two processes. We manipulated the cognitive load involved in top‐down processing and stimulus surprise involved in bottom‐up processing in a factorial design by combining a majority function task and an oddball paradigm. We found that high cognitive load and high surprise level were associated with prolonged reaction time compared to low cognitive load and low surprise level, with a synergistic interaction effect, which was accompanied by a greater deactivation of bilateral temporoparietal junction (TPJ). In addition, the TPJ displayed negative functional connectivity with right middle occipital gyrus, which is involved in bottom‐up processing (modulated by the interaction effect), and the right frontal eye field (FEF), which is involved in top‐down control. The enhanced negative functional connectivity between the TPJ and right FEF was accompanied by a larger behavioral interaction effect across subjects. Application of cathodal tDCS over the right TPJ eliminated the interaction effect. These results suggest that the TPJ plays a critical role in processing bottom‐up information for top‐down control of attention. Hum Brain Mapp 36:4317–4333, 2015. © 2015 Wiley Periodicals, Inc.

[1]  C. Frith,et al.  The Role of Working Memory in Visual Selective Attention , 2001, Science.

[2]  Karl J. Friston,et al.  Dynamic causal models of neural system dynamics: current state and future extensions , 2007, Journal of Biosciences.

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

[4]  Takashi R Sato,et al.  Effects of search efficiency on surround suppression during visual selection in frontal eye field. , 2004, Journal of neurophysiology.

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

[6]  Jin Fan,et al.  The activation of attentional networks , 2005, NeuroImage.

[7]  Jin Fan,et al.  Searching for the Majority: Algorithms of Voluntary Control , 2008, PloS one.

[8]  M. Raichle,et al.  Integration of emotion and cognition in the lateral prefrontal cortex , 2002, Proceedings of the National Academy of Sciences of the United States of America.

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

[10]  Maurizio Corbetta,et al.  The human brain is intrinsically organized into dynamic, anticorrelated functional networks. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[11]  Jon Driver,et al.  Integration of Goal- and Stimulus-Related Visual Signals Revealed by Damage to Human Parietal Cortex , 2010, The Journal of Neuroscience.

[12]  Abhishek Datta,et al.  Neuroplastic changes following rehabilitative training correlate with regional electrical field induced with tDCS , 2011, NeuroImage.

[13]  Claus C. Hilgetag,et al.  Restoration of visual orienting into a cortically blind hemifield by reversible deactivation of posterior parietal cortex or the superior colliculus , 2002, Experimental Brain Research.

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

[15]  Bertram R. Payne,et al.  Functional circuitry underlying natural and interventional cancellation of visual neglect , 2003, Experimental Brain Research.

[16]  L. Cohen,et al.  Transcranial direct current stimulation: State of the art 2008 , 2008, Brain Stimulation.

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

[18]  J. Theeuwes,et al.  Top-down versus bottom-up attentional control: a failed theoretical dichotomy , 2012, Trends in Cognitive Sciences.

[19]  Walter Paulus,et al.  Transcranial direct current stimulation over the primary motor cortex during fMRI , 2011, NeuroImage.

[20]  Jeffrey M. Zacks,et al.  Coherent spontaneous activity accounts for trial-to-trial variability in human evoked brain responses , 2006, Nature Neuroscience.

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

[22]  C. Frith,et al.  Neural Correlates of Attentional Capture in Visual Search , 2004, Journal of Cognitive Neuroscience.

[23]  Joy J. Geng,et al.  Neuroscience and Biobehavioral Reviews Review Re-evaluating the Role of Tpj in Attentional Control: Contextual Updating? , 2022 .

[24]  M. Nitsche,et al.  Safety criteria for transcranial direct current stimulation (tDCS) in humans , 2003, Clinical Neurophysiology.

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

[26]  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.

[27]  S. Yantis,et al.  A Domain-Independent Source of Cognitive Control for Task Sets: Shifting Spatial Attention and Switching Categorization Rules , 2009, The Journal of Neuroscience.

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

[29]  J. Gottlieb Attention, Learning, and the Value of Information , 2012, Neuron.

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

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

[32]  Paolo Bartolomeo,et al.  Dorsal and Ventral Parietal Contributions to Spatial Orienting in the Human Brain , 2011, The Journal of Neuroscience.

[33]  Mark W Greenlee,et al.  Cathodal stimulation of human MT+ leads to elevated fMRI signal: a tDCS-fMRI study. , 2012, Restorative neurology and neuroscience.

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

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

[36]  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.

[37]  Giulio Cossu,et al.  Magic-Factor 1, a Partial Agonist of Met, Induces Muscle Hypertrophy by Protecting Myogenic Progenitors from Apoptosis , 2008, PloS one.

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

[39]  E. Viding,et al.  Load theory of selective attention and cognitive control. , 2004, Journal of experimental psychology. General.

[40]  Jin Fan,et al.  Cognitive Control in Majority Search: A Computational Modeling Approach , 2011, Front. Hum. Neurosci..

[41]  Jin Fan,et al.  Cognition-emotion integration in the anterior insular cortex. , 2013, Cerebral cortex.

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

[43]  Satoshi Tanaka,et al.  A rat model for measuring the effectiveness of transcranial direct current stimulation using fMRI , 2011, Neuroscience Letters.

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

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

[46]  Violeta Dimova,et al.  Electrified minds: Transcranial direct current stimulation (tDCS) and Galvanic Vestibular Stimulation (GVS) as methods of non-invasive brain stimulation in neuropsychology—A review of current data and future implications , 2010, Neuropsychologia.

[47]  A. Valero-Cabré,et al.  Cathodal transcranial direct current stimulation on posterior parietal cortex disrupts visuo-spatial processing in the contralateral visual field , 2008, Experimental Brain Research.

[48]  M. Raichle,et al.  Localization of a human system for sustained attention by positron emission tomography , 1991, Nature.

[49]  Jin Fan,et al.  An information theory account of cognitive control , 2014, Front. Hum. Neurosci..

[50]  Neil G. Muggleton,et al.  Modulating inhibitory control with direct current stimulation of the superior medial frontal cortex , 2011, NeuroImage.

[51]  Franziska M. Korb,et al.  Priming of Control: Implicit Contextual Cuing of Top-down Attentional Set , 2012, The Journal of Neuroscience.

[52]  Carles Falcón,et al.  Modulation of verbal fluency networks by transcranial direct current stimulation (tDCS) in Parkinson’s disease , 2013, Brain Stimulation.

[53]  Jin Fan,et al.  Quantitative Characterization of Functional Anatomical Contributions to Cognitive Control under Uncertainty , 2014, Journal of Cognitive Neuroscience.

[54]  L. Yao,et al.  Causal Interactions in Attention Networks Predict Behavioral Performance , 2012, The Journal of Neuroscience.

[55]  R. Marois,et al.  Visual Short-Term Memory Load Suppresses Temporo-Parietal Junction Activity and Induces Inattentional Blindness , 2005, Psychological science.

[56]  Shihui Han,et al.  Attentional capture is contingent on the interaction between task demand and stimulus salience , 2009, Attention, perception & psychophysics.

[57]  G. Fink,et al.  Bidirectional alterations of interhemispheric parietal balance by non-invasive cortical stimulation. , 2009, Brain : a journal of neurology.

[58]  Karl J. Friston,et al.  Anterior insular cortex and emotional awareness , 2013, The Journal of comparative neurology.

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

[60]  Men-Tzung Lo,et al.  Revealing the brain's adaptability and the transcranial direct current stimulation facilitating effect in inhibitory control by multiscale entropy , 2014, NeuroImage.

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

[62]  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.

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

[64]  O. Tzeng,et al.  Unleashing Potential: Transcranial Direct Current Stimulation over the Right Posterior Parietal Cortex Improves Change Detection in Low-Performing Individuals , 2012, The Journal of Neuroscience.

[65]  J. Gottlieb,et al.  Distinct neural mechanisms of distractor suppression in the frontal and parietal lobe , 2012, Nature Neuroscience.

[66]  Christopher L. Asplund,et al.  A central role for the lateral prefrontal cortex in goal-directed and stimulus-driven attention , 2010, Nature Neuroscience.

[67]  Joseph B. Hopfinger,et al.  Interactions between endogenous and exogenous attention on cortical visual processing , 2006, NeuroImage.

[68]  Mi Young Lee,et al.  The effect of transcranial direct current stimulation on the cortical activation by motor task in the human brain: An fMRI study , 2009, Neuroscience Letters.