The Role of Frontoparietal Cortex across the Functional Stages of Visual Search

Areas in frontoparietal cortex have been shown to be active in a range of cognitive tasks and have been proposed to play a key role in goal-driven activities (Dosenbach, N. U. F., Fair, D. A., Miezin, F. M., Cohen, A. L., Wenger, K. K., Dosenbach, R. A. T., et al. Distinct brain networks for adaptive and stable task control in humans. Proceedings of the National Academy of Sciences, U.S.A., 104, 11073–11078, 2007; Duncan, J. The multiple-demand (MD) system of the primate brain: Mental programs for intelligent behavior. Trends in Cognitive Sciences, 14, 172–179, 2010). Here, we examine the role this frontoparietal system plays in visual search. Visual search, like many complex tasks, consists of a sequence of operations: target selection, stimulus–response (SR) mapping, and response execution. We independently manipulated the difficulty of target selection and SR mapping in a novel visual search task that involved identical stimulus displays. Enhanced activity was observed in areas of frontal and parietal cortex during both difficult target selection and SR mapping. In addition, anterior insula and ACC showed preferential representation of SR-stage information, whereas the medial frontal gyrus, precuneus, and inferior parietal sulcus showed preferential representation of target selection-stage information. A connectivity analysis revealed dissociable neural circuits underlying visual search. We hypothesize that these circuits regulate distinct mental operations associated with the allocation of spatial attention, stimulus decisions, shifts of task set from selection to SR mapping, and SR mapping. Taken together, the results show frontoparietal involvement in all stages of visual search and a specialization with respect to cognitive operations.

[1]  G. Glover,et al.  Dissociable Intrinsic Connectivity Networks for Salience Processing and Executive Control , 2007, The Journal of Neuroscience.

[2]  Notger G. Müller,et al.  The functional neuroanatomy of visual conjunction search: a parametric fMRI study , 2003, NeuroImage.

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

[4]  K. Johnston,et al.  Top-Down Control-Signal Dynamics in Anterior Cingulate and Prefrontal Cortex Neurons following Task Switching , 2007, Neuron.

[5]  Anina N. Rich,et al.  Flexible Coding of Task Rules in Frontoparietal Cortex: An Adaptive System for Flexible Cognitive Control , 2015, Journal of Cognitive Neuroscience.

[6]  Russell A. Poldrack,et al.  Large-scale automated synthesis of human functional neuroimaging data , 2011, Nature Methods.

[7]  M. Corbetta,et al.  Imaging Expectations and Attentional Modulations in theHuman Brain , 2022 .

[8]  Justin L. Vincent,et al.  Distinct brain networks for adaptive and stable task control in humans , 2007, Proceedings of the National Academy of Sciences.

[9]  René Marois,et al.  Dissociation between process-based and data-based limitations for conscious perception in the human brain , 2013, NeuroImage.

[10]  Eric H. Schumacher,et al.  Neural Mechanisms for Response Selection: Representation Specific or Modality Independent? , 2003, Journal of Cognitive Neuroscience.

[11]  D G Pelli,et al.  The VideoToolbox software for visual psychophysics: transforming numbers into movies. , 1997, Spatial vision.

[12]  Patrizia Baraldi,et al.  Human parietofrontal networks related to action observation detected at rest. , 2013, Cerebral cortex.

[13]  Yuhong Jiang,et al.  Resolving dual-task interference: an fMRI study , 2004, NeuroImage.

[14]  Daniel J Mitchell,et al.  Task Encoding across the Multiple Demand Cortex Is Consistent with a Frontoparietal and Cingulo-Opercular Dual Networks Distinction , 2016, The Journal of Neuroscience.

[15]  Sean M. Polyn,et al.  Beyond mind-reading: multi-voxel pattern analysis of fMRI data , 2006, Trends in Cognitive Sciences.

[16]  H. Fukuyama,et al.  Dissociable mechanisms of attentional control within the human prefrontal cortex. , 2001, Cerebral cortex.

[17]  C. Phillips,et al.  Cross-Modal Decoding of Neural Patterns Associated with Working Memory: Evidence for Attention-Based Accounts of Working Memory. , 2016, Cerebral cortex.

[18]  Jonathan D. Cohen,et al.  Dorsal anterior cingulate cortex and the value of control , 2016, Nature Neuroscience.

[19]  M. Raichle,et al.  The anterior cingulate cortex mediates processing selection in the Stroop attentional conflict paradigm. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[20]  Jonathan D. Cohen,et al.  Conflict monitoring and anterior cingulate cortex: an update , 2004, Trends in Cognitive Sciences.

[21]  W. Krieg.  Functional Neuroanatomy , 1953, Springer Series in Experimental Entomology.

[22]  Jonathan D. Cohen,et al.  The Expected Value of Control: An Integrative Theory of Anterior Cingulate Cortex Function , 2013, Neuron.

[23]  M. D’Esposito,et al.  Frontal Networks for Learning and Executing Arbitrary Stimulus-Response Associations , 2005, The Journal of Neuroscience.

[24]  Cameron S. Carter,et al.  The neural circuitry supporting goal maintenance during cognitive control: a comparison of expectancy AX-CPT and dot probe expectancy paradigms , 2015, Cognitive, Affective, & Behavioral Neuroscience.

[25]  W. G. Koster,et al.  The psychological refractory period , 1966 .

[26]  Scott T. Grafton,et al.  Actions or Hand-Object Interactions? Human Inferior Frontal Cortex and Action Observation , 2003, Neuron.

[27]  Stefanie I. Becker,et al.  Distinct neural networks for target feature versus dimension changes in visual search, as revealed by EEG and fMRI , 2014, NeuroImage.

[28]  D H Brainard,et al.  The Psychophysics Toolbox. , 1997, Spatial vision.

[29]  P. Zelazo,et al.  What is Cognitive Control , 2013 .

[30]  D. Sharp,et al.  Contrasting network and modular perspectives on inhibitory control , 2015, Trends in Cognitive Sciences.

[31]  Aiden E. G. F. Arnold,et al.  Intraparietal sulcus activity and functional connectivity supporting spatial working memory manipulation. , 2015, Cerebral cortex.

[32]  M. Raichle.  The brain's default mode network. , 2015, Annual review of neuroscience.

[33]  Kenneth F. Valyear,et al.  Dissociating Arbitrary Stimulus-Response Mapping from Movement Planning during Preparatory Period: Evidence from Event-Related Functional Magnetic Resonance Imaging , 2006, The Journal of Neuroscience.

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

[35]  Jonathan D. Power,et al.  Multi-task connectivity reveals flexible hubs for adaptive task control , 2013, Nature Neuroscience.

[36]  Takatsune Kumada,et al.  Visual search and memory search engage extensive overlapping cerebral cortices: an fMRI study , 2004, NeuroImage.

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

[38]  Seth A. Herd,et al.  A Unified Framework for Inhibitory Control Opinion , 2022 .

[39]  T. Hanakawa,et al.  Transient Neural Activity in the Medial Superior Frontal Gyrus and Precuneus Time Locked with Attention Shift between Object Features , 1999, NeuroImage.

[40]  A. Cavanna.  The Precuneus and Consciousness , 2007, CNS Spectrums.

[41]  Yucheng Dong,et al.  A Unified Framework , 2018, Linguistic Decision Making.

[42]  Nancy Kanwisher,et al.  Broad domain generality in focal regions of frontal and parietal cortex , 2013, Proceedings of the National Academy of Sciences.

[43]  M. Smith,et al.  The Core System , 2017 .

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

[45]  M. D’Esposito,et al.  Neural Evidence for Representation-Specific Response Selection , 2003, Journal of Cognitive Neuroscience.

[46]  Walter Schneider,et al.  The cognitive control network: Integrated cortical regions with dissociable functions , 2007, NeuroImage.

[47]  M. Botvinick,et al.  Parsing executive processes: strategic vs. evaluative functions of the anterior cingulate cortex. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[48]  A. Dale,et al.  Functional Parcellation of Attentional Control Regions of the Brain , 2004, Journal of Cognitive Neuroscience.

[49]  Mark D'Esposito,et al.  Selection and maintenance of stimulus–response rules during preparation and performance of a spatial choice-reaction task , 2007, Brain Research.

[50]  A. Welford.  THE ‘PSYCHOLOGICAL REFRACTORY PERIOD’ AND THE TIMING OF HIGH‐SPEED PERFORMANCE—A REVIEW AND A THEORY , 1952 .

[51]  J. Duncan.  The multiple-demand (MD) system of the primate brain: mental programs for intelligent behaviour , 2010, Trends in Cognitive Sciences.

[52]  Thomas L. Webb,et al.  The neural basis of monitoring goal progress , 2014, Front. Hum. Neurosci..

[53]  H. Pashler.  Dual-task interference in simple tasks: data and theory. , 1994, Psychological bulletin.

[54]  M. Farah,et al.  Is anterior cingulate cortex necessary for cognitive control? , 2005, Brain : a journal of neurology.

[55]  C. Liston,et al.  Anterior Cingulate and Posterior Parietal Cortices Are Sensitive to Dissociable Forms of Conflict in a Task-Switching Paradigm , 2006, Neuron.

[56]  John Duncan,et al.  Response of the multiple-demand network during simple stimulus discriminations , 2018, NeuroImage.

[57]  H Pashler,et al.  Processing stages in overlapping tasks: evidence for a central bottleneck. , 1984, Journal of experimental psychology. Human perception and performance.

[58]  Timothy E. J. Behrens,et al.  Tools of the trade: psychophysiological interactions and functional connectivity. , 2012, Social cognitive and affective neuroscience.

[59]  A. Cavanna,et al.  The precuneus: a review of its functional anatomy and behavioural correlates. , 2006, Brain : a journal of neurology.

[60]  M. Honda,et al.  The role of rostral Brodmann area 6 in mental-operation tasks: an integrative neuroimaging approach. , 2002, Cerebral cortex.

[61]  Kristina M. Visscher,et al.  A Core System for the Implementation of Task Sets , 2006, Neuron.

[62]  N. Kanwisher,et al.  Common Neural Substrates for Response Selection across Modalities and Mapping Paradigms , 2003, Journal of Cognitive Neuroscience.

[63]  Nava Rubin,et al.  Brain areas selective for both observed and executed movements. , 2007, Journal of neurophysiology.

[64]  J. C. Johnston,et al.  Chronometric Evidence for Central Postponement in Temporally Overlapping Tasks , 2003 .

[65]  Daniel G Bobrow,et al.  On data-limited and resource-limited processes , 1975, Cognitive Psychology.

[66]  M. Posner,et al.  Cognitive and emotional influences in anterior cingulate cortex , 2000, Trends in Cognitive Sciences.

[67]  S. Petersen,et al.  Role of the anterior insula in task-level control and focal attention , 2010, Brain Structure and Function.