Salience Network Activity in Perceptual Decisions

The dorsal anterior cingulate cortex (dACC) and the anterior insulae (AIs) are coactivated in various perceptual decision-making (PDM) tasks and form the salience network (SN): a key network in sensory perception and the coordination of behavioral responses. However, what the functional role of SN is, how these key SN nodes interact with each other to form a network in a perceptual decision, and how the network depends on the perceptual difficulty remain largely unknown. In the present study, we measured blood oxygen level-dependent (BOLD) signals using functional magnetic resonance imaging (fMRI). During four PDM tasks (1) face-house discrimination, (2) happy-angry face discrimination, (3) audiovisual asynchrony and synchrony perception, and a (4) random dot motion direction task, we varied the task difficulty and examined the interactions between these SN nodes. In all the experiments, behavioral accuracy decreased and response time increased with task difficulty. The BOLD signal increased in SN nodes with the ambiguity in the sensory information. We also found that there were significant directed functional connections between AIs and dACC in all four tasks and that the interactions between these nodes increased with task difficulty. The observed difficulty-dependent functional architecture of SN suggests that the dACC and AIs are part of a large-scale cognitive system that facilitates sensory integration in PDM.

[1]  Anna C Nobre,et al.  Subsecond Changes in Top–Down Control Exerted by Human Medial Frontal Cortex during Conflict and Action Selection: A Combined Transcranial Magnetic Stimulation–Electroencephalography Study , 2007, The Journal of Neuroscience.

[2]  Ziv M. Williams,et al.  Action Initiation in the Human Dorsal Anterior Cingulate Cortex , 2013, PloS one.

[3]  S. Huettel,et al.  Resolving Response, Decision, and Strategic Control: Evidence for a Functional Topography in Dorsomedial Prefrontal Cortex , 2009, The Journal of Neuroscience.

[4]  T. Paus.  Primate anterior cingulate cortex: Where motor control, drive and cognition interface , 2001, Nature Reviews Neuroscience.

[5]  J. Hirsch,et al.  A Neural Representation of Categorization Uncertainty in the Human Brain , 2006, Neuron.

[6]  M. Wallace,et al.  Multisensory temporal integration: task and stimulus dependencies , 2013, Experimental Brain Research.

[7]  Derek K. Jones,et al.  Cingulum Microstructure Predicts Cognitive Control in Older Age and Mild Cognitive Impairment , 2012, The Journal of Neuroscience.

[8]  E. Miller,et al.  Increases in Functional Connectivity between Prefrontal Cortex and Striatum during Category Learning , 2014, Neuron.

[9]  M. Dhamala,et al.  Perceptual decision-making difficulty modulates feedforward effective connectivity to the dorsolateral prefrontal cortex , 2015, Front. Hum. Neurosci..

[10]  Angela J. Yu,et al.  Bayesian Prediction and Evaluation in the Anterior Cingulate Cortex , 2013, The Journal of Neuroscience.

[11]  M. Walton,et al.  Action sets and decisions in the medial frontal cortex , 2004, Trends in Cognitive Sciences.

[12]  C. Spence,et al.  Audio-visual simultaneity judgments , 2005, Perception & psychophysics.

[13]  S. Dehaene,et al.  Dynamics of prefrontal and cingulate activity during a reward-based logical deduction task. , 2006, Cerebral cortex.

[14]  M. Mesulam,et al.  Insula of the old world monkey. II: Afferent cortical input and comments on the claustrum , 1982, The Journal of comparative neurology.

[15]  C. Li,et al.  Dissociable Roles of Right Inferior Frontal Cortex and Anterior Insula in Inhibitory Control: Evidence from Intrinsic and Task-Related Functional Parcellation, Connectivity, and Response Profile Analyses across Multiple Datasets , 2014, The Journal of Neuroscience.

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

[17]  V. Menon,et al.  A critical role for the right fronto-insular cortex in switching between central-executive and default-mode networks , 2008, Proceedings of the National Academy of Sciences.

[18]  M. Mesulam,et al.  Insula of the old world monkey. III: Efferent cortical output and comments on function , 1982, The Journal of comparative neurology.

[19]  D. Yves von Cramon,et al.  The neural implementation of multi-attribute decision making: A parametric fMRI study with human subjects , 2006, NeuroImage.

[20]  Bidhan Lamichhane,et al.  Temporal-Order Judgment of Audiovisual Events Involves Network Activity Between Parietal and Prefrontal Cortices , 2013, Brain Connect..

[21]  Bidhan Lamichhane,et al.  Amygdala Mediated Connectivity in Perceptual Decision-Making of Emotional Facial Expressions , 2013, Brain Connect..

[22]  Jean-Luc Anton,et al.  Region of interest analysis using an SPM toolbox , 2010 .

[23]  Bidhan Lamichhane,et al.  Oscillatory activity in neocortical networks during tactile discrimination near the limit of spatial acuity , 2014, NeuroImage.

[24]  E. DeYoe,et al.  A comparison of visual and auditory motion processing in human cerebral cortex. , 2000, Cerebral cortex.

[25]  Guorong Wu,et al.  A blind deconvolution approach to recover effective connectivity brain networks from resting state fMRI data , 2012, Medical Image Anal..

[26]  Viktor K. Jirsa,et al.  Multisensory integration for timing engages different brain networks , 2007, NeuroImage.

[27]  Sabine Kastner,et al.  Functional heterogeneity of conflict, error, task-switching, and unexpectedness effects within medial prefrontal cortex , 2011, NeuroImage.

[28]  Luke J. Chang,et al.  Decoding the role of the insula in human cognition: functional parcellation and large-scale reverse inference. , 2013, Cerebral cortex.

[29]  D. Lewkowicz,et al.  Infant perception of audio-visual speech synchrony in familiar and unfamiliar fluent speech. , 2014, Acta psychologica.

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

[31]  R. Blair,et al.  An alternative method for significance testing of waveform difference potentials. , 1993, Psychophysiology.

[32]  S. Bressler,et al.  Beta oscillations in a large-scale sensorimotor cortical network: directional influences revealed by Granger causality. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[33]  H. Critchley,et al.  Conjoint activity of anterior insular and anterior cingulate cortex: awareness and response , 2010, Brain Structure and Function.

[34]  G. Calvert.  Crossmodal processing in the human brain: insights from functional neuroimaging studies. , 2001, Cerebral cortex.

[35]  J. Duncan,et al.  Adaptive Coding of Task-Relevant Information in Human Frontoparietal Cortex , 2011, The Journal of Neuroscience.

[36]  J. Rieskamp,et al.  Deciding When to Decide: Time-Variant Sequential Sampling Models Explain the Emergence of Value-Based Decisions in the Human Brain , 2012, The Journal of Neuroscience.

[37]  T. Shallice,et al.  Multiple frontal systems controlling response speed , 2005, Neuropsychologia.

[38]  C. Saper.  The central autonomic nervous system: conscious visceral perception and autonomic pattern generation. , 2002, Annual review of neuroscience.

[39]  Mingzhou Ding,et al.  Analyzing information flow in brain networks with nonparametric Granger causality , 2008, NeuroImage.

[40]  Elisabeth J. Ploran,et al.  Evidence Accumulation and the Moment of Recognition: Dissociating Perceptual Recognition Processes Using fMRI , 2007, The Journal of Neuroscience.

[41]  J. Juola,et al.  Audiovisual synchrony and temporal order judgments: Effects of experimental method and stimulus type , 2008, Perception & psychophysics.

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

[43]  M. Botvinick,et al.  Conflict monitoring and cognitive control. , 2001, Psychological review.

[44]  M. Hallett,et al.  Neural Correlates of Auditory–Visual Stimulus Onset Asynchrony Detection , 2001, The Journal of Neuroscience.

[45]  R. Kahn,et al.  Functionally linked resting‐state networks reflect the underlying structural connectivity architecture of the human brain , 2009, Human brain mapping.

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

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

[48]  P. Strick,et al.  Motor areas of the medial wall: a review of their location and functional activation. , 1996, Cerebral cortex.

[49]  K. A. Hadland,et al.  The Effect of Cingulate Cortex Lesions on Task Switching and Working Memory , 2003, Journal of Cognitive Neuroscience.

[50]  Timothy Edward John Behrens,et al.  Contrasting roles for cingulate and orbitofrontal cortex in decisions and social behaviour , 2007, Trends in Cognitive Sciences.

[51]  A. Kleinschmidt,et al.  Anterior insula activations in perceptual paradigms: often observed but barely understood , 2010, Brain Structure and Function.

[52]  David A. Medler,et al.  Neural correlates of sensory and decision processes in auditory object identification , 2004, Nature Neuroscience.

[53]  H. Critchley,et al.  A common role of insula in feelings, empathy and uncertainty , 2009, Trends in Cognitive Sciences.

[54]  Mark D'Esposito,et al.  Variation of BOLD hemodynamic responses across subjects and brain regions and their effects on statistical analyses , 2004, NeuroImage.

[55]  K. Wiech,et al.  Anterior Insula Integrates Information about Salience into Perceptual Decisions about Pain , 2010, The Journal of Neuroscience.

[56]  A. T. Smith,et al.  The role of the human anterior insular cortex in time processing , 2010, Brain Structure and Function.

[57]  A. Song,et al.  The involvement of the dopaminergic midbrain and cortico-striatal-thalamic circuits in the integration of reward prospect and attentional task demands. , 2012, Cerebral cortex.

[58]  C. Spence,et al.  Audiovisual temporal order judgments , 2003, Experimental Brain Research.

[59]  Naomi B. Pitskel,et al.  Three Systems of Insular Functional Connectivity Identified with Cluster Analysis , 2010, Cerebral cortex.

[60]  L. Pessoa,et al.  Neural Correlates of Perceptual Choice and Decision Making during Fear–Disgust Discrimination , 2007, The Journal of Neuroscience.

[61]  M. D’Esposito,et al.  The Variability of Human, BOLD Hemodynamic Responses , 1998, NeuroImage.

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

[63]  A. Craig,et al.  How do you feel — now? The anterior insula and human awareness , 2009, Nature Reviews Neuroscience.

[64]  S. Rauch,et al.  Prospective long-term follow-up of 44 patients who received cingulotomy for treatment-refractory obsessive-compulsive disorder. , 2002, The American journal of psychiatry.

[65]  Jason R. Tregellas,et al.  Effect of task difficulty on the functional anatomy of temporal processing , 2006, NeuroImage.

[66]  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.

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

[68]  Katiuscia Sacco,et al.  Functional connectivity of the insula in the resting brain , 2011, NeuroImage.

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

[70]  M. Mesulam,et al.  Insula of the old world monkey. Architectonics in the insulo‐orbito‐temporal component of the paralimbic brain , 1982, The Journal of comparative neurology.

[71]  Timothy E. Ham,et al.  Cognitive Control and the Salience Network: An Investigation of Error Processing and Effective Connectivity , 2013, The Journal of Neuroscience.

[72]  Bradford C. Dickerson,et al.  Dissociable large-scale networks anchored in the right anterior insula subserve affective experience and attention , 2012, NeuroImage.

[73]  Scott D. Brown,et al.  Domain General Mechanisms of Perceptual Decision Making in Human Cortex , 2009, The Journal of Neuroscience.

[74]  E. Procyk,et al.  Behavioral Shifts and Action Valuation in the Anterior Cingulate Cortex , 2008, Neuron.

[75]  Timothy E. J. Behrens,et al.  Optimal decision making and the anterior cingulate cortex , 2006, Nature Neuroscience.

[76]  V. Menon,et al.  Saliency, switching, attention and control: a network model of insula function , 2010, Brain Structure and Function.

[77]  D. Poeppel,et al.  Temporal window of integration in auditory-visual speech perception , 2007, Neuropsychologia.

[78]  S. Lam,et al.  The Role of Right Anterior Insula and Salience Processing in Inhibitory Control , 2015, The Journal of Neuroscience.

[79]  M. Walton,et al.  Interactions between decision making and performance monitoring within prefrontal cortex , 2004, Nature Neuroscience.

[80]  Bidhan Lamichhane,et al.  The Salience Network and Its Functional Architecture in a Perceptual Decision: An Effective Connectivity Study , 2015, Brain Connect..

[81]  C. Spence,et al.  Audiovisual synchrony perception for speech and music assessed using a temporal order judgment task , 2006, Neuroscience Letters.

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

[83]  M. Botvinick.  Conflict monitoring and decision making: Reconciling two perspectives on anterior cingulate function , 2007, Cognitive, affective & behavioral neuroscience.

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

[85]  Clay B. Holroyd,et al.  Motivation of extended behaviors by anterior cingulate cortex , 2012, Trends in Cognitive Sciences.

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

[87]  M. Dhamala,et al.  The activity in the anterior insulae is modulated by perceptual decision-making difficulty , 2016, Neuroscience.