Probing the cortical network underlying the psychological refractory period: A combined EEG–fMRI study

Human performance exhibits strong multi-tasking limitations in simple response time tasks. In the psychological refractory period (PRP) paradigm, where two tasks have to be performed in brief succession, central processing of the second task is delayed when the two tasks are performed at short time intervals. Here, we aimed to probe the cortical network underlying this postponement of central processing by simultaneously recording electroencephalography (EEG) and functional magnetic resonance imaging (fMRI) data while 12 subjects performed two simple number-comparison tasks. Behavioral data showed a significant slowing of response times to the second target stimulus at short stimulus-onset asynchronies, together with significant correlations between response times to the first and second target stimulus, i.e., the hallmarks of the PRP effect. The analysis of EEG data showed a significant delay of the post-perceptual P3 component evoked by the second target, which was of similar magnitude as the effect on response times. fMRI data revealed an involvement of parietal and prefrontal regions in dual-task processing. The combined analysis of fMRI and EEG data-based on the trial-by-trial variability of the P3-revealed that BOLD signals in two bilateral regions in the inferior parietal lobe and precentral gyrus significantly covaried with P3 related activity. Our results show that combining neuroimaging methods of high spatial and temporal resolutions can help to identify cortical regions underlying the central bottleneck of information processing, and strengthen the conclusion that fronto-parietal cortical regions participate in a distributed "global neuronal workspace" system that underlies the generation of the P3 component and may be one of the key cerebral underpinnings of the PRP bottleneck.

[1]  S. Geisser,et al.  On methods in the analysis of profile data , 1959 .

[2]  Robert Turner,et al.  A Method for Removing Imaging Artifact from Continuous EEG Recorded during Functional MRI , 2000, NeuroImage.

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

[4]  E. Vogel,et al.  Electrophysiological Evidence for a Postperceptual Locus of Suppression during the Attentional Blink Time-based Attention and the Attentional Blink , 1998 .

[5]  R. D. de Jong,et al.  Multiple bottlenecks in overlapping task performance. , 1993, Journal of experimental psychology. Human perception and performance.

[6]  Benoit Brisson,et al.  Electrophysiological evidence of central interference in the control of visuospatial attention , 2007, Psychonomic bulletin & review.

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

[8]  K. Amunts,et al.  Neural correlates of dual task interference can be dissociated from those of divided attention: an fMRI study. , 2001, Cerebral cortex.

[9]  Karl J. Friston,et al.  Statistical parametric mapping , 2013 .

[10]  D. Lehmann,et al.  Reference-free identification of components of checkerboard-evoked multichannel potential fields. , 1980, Electroencephalography and clinical neurophysiology.

[11]  Mark E Nelson,et al.  Brain maps and parallel computers , 1990, Trends in Neurosciences.

[12]  Kin Fai Ellick Wong.  The Relationship between Attentional Blink and Psychological Refractory Period , 2002 .

[13]  A. Engel,et al.  Trial-by-Trial Coupling of Concurrent Electroencephalogram and Functional Magnetic Resonance Imaging Identifies the Dynamics of Performance Monitoring , 2005, The Journal of Neuroscience.

[14]  G D Logan,et al.  Parallel memory retrieval in dual-task situations: I. Semantic memory. , 2000, Journal of experimental psychology. Human perception and performance.

[15]  J. Grafman,et al.  Dissociating the roles of the rostral anterior cingulate and the lateral prefrontal cortices in performing two tasks simultaneously or successively. , 2003, Cerebral cortex.

[16]  P. Jolicoeur,et al.  Central processing overlap modulates P3 latency , 2005, Experimental Brain Research.

[17]  R. Quian Quiroga,et al.  Single-trial event-related potentials with wavelet denoising , 2003, Clinical Neurophysiology.

[18]  Matthias M. Müller,et al.  Probing the functional brain state during P300-evocation , 1992 .

[19]  H. Pashler.  The Psychology of Attention , 1997 .

[20]  Rami K. Niazy,et al.  Simultaneous recording of laser-evoked brain potentials and continuous, high-field functional magnetic resonance imaging in humans , 2005, NeuroImage.

[21]  P. Jolicoeur,et al.  A central capacity sharing model of dual-task performance. , 2003, Journal of experimental psychology. Human perception and performance.

[22]  Hermann J. Müller,et al.  How to test for dual-task-specific effects in brain imaging studies — An evaluation of potential analysis methods , 2011, NeuroImage.

[23]  S. Dehaene,et al.  Brain Dynamics Underlying the Nonlinear Threshold for Access to Consciousness , 2007, PLoS biology.

[24]  Christopher L. Asplund,et al.  Isolation of a Central Bottleneck of Information Processing with Time-Resolved fMRI , 2006, Neuron.

[25]  A. Engel,et al.  Opinion TRENDS in Cognitive Sciences Vol.10 No.12 Single-trial EEG–fMRI reveals the dynamics of cognitive function , 2022 .

[26]  C. Eriksen,et al.  A psychophysiological investigation of the continuous flow model of human information processing. , 1985, Journal of experimental psychology. Human perception and performance.

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

[28]  R. Marois,et al.  Capacity limits of information processing in the brain , 2005, Trends in Cognitive Sciences.

[29]  Pieter R. Roelfsema,et al.  The Brain's Router: A Cortical Network Model of Serial Processing in the Primate Brain , 2010, PLoS Comput. Biol..

[30]  R. Andersen,et al.  Functional analysis of human MT and related visual cortical areas using magnetic resonance imaging , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[31]  David E. Kieras,et al.  A computational theory of executive cognitive processes and multiple-task performance: Part 2. Accounts of psychological refractory-period phenomena. , 1997 .

[32]  C. W. Telford.  The refractory phase of voluntary and associative responses , 1931 .

[33]  Valerie Kirsch,et al.  Separating distinct aspects of the voluntary selection between response alternatives: N2- and P3-related BOLD responses , 2010, NeuroImage.

[34]  E. John,et al.  Evoked-Potential Correlates of Stimulus Uncertainty , 1965, Science.

[35]  F. Tong,et al.  Training Improves Multitasking Performance by Increasing the Speed of Information Processing in Human Prefrontal Cortex , 2009, Neuron.

[36]  T W Picton,et al.  The P300 Wave of the Human Event‐Related Potential , 1992, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[37]  Maurizio Corbetta,et al.  Large-scale brain networks account for sustained and transient activity during target detection , 2009, NeuroImage.

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

[39]  Bettina Sorger,et al.  Novelty and target processing during an auditory novelty oddball: A simultaneous event-related potential and functional magnetic resonance imaging study , 2008, NeuroImage.

[40]  Arnaud Delorme,et al.  EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis , 2004, Journal of Neuroscience Methods.

[41]  S. Dehaene,et al.  Semantic processing of neglected numbers , 2008, Cortex.

[42]  Alicia M. Helion,et al.  Dissociating sources of dual-task interference using human electrophysiology , 2004, Psychonomic bulletin & review.

[43]  A. Dove,et al.  Prefrontal cortex activation in task switching: an event-related fMRI study. , 2000, Brain research. Cognitive brain research.

[44]  Sabine Van Huffel,et al.  Removal of BCG artifacts from EEG recordings inside the MR scanner: A comparison of methodological and validation-related aspects , 2010, NeuroImage.

[45]  Terrence J. Sejnowski,et al.  An Information-Maximization Approach to Blind Separation and Blind Deconvolution , 1995, Neural Computation.

[46]  A. Mognon,et al.  ADJUST: An automatic EEG artifact detector based on the joint use of spatial and temporal features. , 2011, Psychophysiology.

[47]  S. Luck.  Sources of Dual-Task Interference: Evidence From Human Electrophysiology , 1998 .

[48]  D. J. Felleman,et al.  Distributed hierarchical processing in the primate cerebral cortex. , 1991, Cerebral cortex.

[49]  Jeff Miller,et al.  Backward crosstalk effects in psychological refractory period paradigms: effects of second-task response types on first-task response latencies , 2006, Psychological research.

[50]  Rolf Ulrich,et al.  Decomposing sources of response slowing in the PRP paradigm. , 2007, Journal of experimental psychology. Human perception and performance.

[51]  S. Dehaene,et al.  Timing of the brain events underlying access to consciousness during the attentional blink , 2005, Nature Neuroscience.

[52]  D. Friedman,et al.  The novelty P3: an event-related brain potential (ERP) sign of the brain's evaluation of novelty , 2001, Neuroscience & Biobehavioral Reviews.

[53]  J. Palva,et al.  Very Slow EEG Fluctuations Predict the Dynamics of Stimulus Detection and Oscillation Amplitudes in Humans , 2008, The Journal of Neuroscience.

[54]  Andreas Kleinschmidt,et al.  Recent advances in recording electrophysiological data simultaneously with magnetic resonance imaging , 2008, NeuroImage.

[55]  W. K. Simmons,et al.  Circular analysis in systems neuroscience: the dangers of double dipping , 2009, Nature Neuroscience.

[56]  Andreas Kleinschmidt,et al.  Ongoing Activity Fluctuations in hMT+ Bias the Perception of Coherent Visual Motion , 2008, The Journal of Neuroscience.

[57]  Torsten Schubert,et al.  Response activation in overlapping tasks and the response-selection bottleneck. , 2008, Journal of experimental psychology. Human perception and performance.

[58]  D. Navon,et al.  Queuing or Sharing? A Critical Evaluation of the Single-Bottleneck Notion , 2002, Cognitive Psychology.

[59]  Gordon D. Logan,et al.  Parallel memory retrieval in dual-task situations: II. Episodic memory. , 2001 .

[60]  Torsten Schubert,et al.  The central attentional limitation and executive control. , 2008, Frontiers in bioscience : a journal and virtual library.

[61]  M. Sigman,et al.  Parsing a Cognitive Task: A Characterization of the Mind's Bottleneck , 2005, PLoS biology.

[62]  Nadim Joni Shah,et al.  Single-trial P3 amplitude and latency informed event-related fMRI models yield different BOLD response patterns to a target detection task , 2009, NeuroImage.

[63]  Torsten Schubert,et al.  Functional neuroanatomy of interference in overlapping dual tasks: an fMRI study. , 2003, Brain research. Cognitive brain research.

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

[65]  R. D. Gordon,et al.  Executive control of visual attention in dual-task situations. , 2001, Psychological review.

[66]  J. Duncan,et al.  Separate and Shared Sources of Dual-Task Cost in Stimulus Identification and Response Selection , 2002, Cognitive Psychology.

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

[68]  G. Woodman,et al.  Event-related potential studies of attention , 2000, Trends in Cognitive Sciences.

[69]  S. Debener,et al.  Simultaneous recording of EEG and BOLD responses: a historical perspective. , 2008, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[70]  D E Kieras,et al.  A computational theory of executive cognitive processes and multiple-task performance: Part 1. Basic mechanisms. , 1997, Psychological review.

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

[72]  S. Dehaene,et al.  Imaging unconscious semantic priming , 1998, Nature.

[73]  E. Donchin,et al.  Is the P300 component a manifestation of context updating? , 1988, Behavioral and Brain Sciences.

[74]  M. Sigman,et al.  Dynamics of the Central Bottleneck: Dual-Task and Task Uncertainty , 2006, PLoS biology.

[75]  Daniel Brandeis,et al.  Synchronization facilitates removal of MRI artefacts from concurrent EEG recordings and increases usable bandwidth , 2006, NeuroImage.

[76]  S. Dehaene,et al.  Towards a cognitive neuroscience of consciousness: basic evidence and a workspace framework , 2001, Cognition.

[77]  G D Logan,et al.  Parallel memory retrieval in dual-task situations: II. Episodic memory. , 2001, Journal of experimental psychology. Learning, memory, and cognition.

[78]  Torsten Schubert,et al.  Task-order coordination in dual-task performance and the lateral prefrontal cortex: an event-related fMRI study , 2006, Psychological research.

[79]  Andreas Kleinschmidt,et al.  Spontaneous local variations in ongoing neural activity bias perceptual decisions , 2008, Proceedings of the National Academy of Sciences.

[80]  N. Kanwisher,et al.  Functional Magnetic Resonance Imaging Provides New Constraints on Theories of the Psychological Refractory Period , 2004, Psychological science.

[81]  Simon B. Eickhoff,et al.  A new SPM toolbox for combining probabilistic cytoarchitectonic maps and functional imaging data , 2005, NeuroImage.

[82]  Piotr Jaskowski,et al.  Evidence for an Integrative Role of P3b in Linking Reaction to Perception , 2005 .

[83]  S. Dehaene,et al.  Unconscious semantic priming extends to novel unseen stimuli , 2001, Cognition.

[84]  S. Debener,et al.  Trial-by-Trial Fluctuations in the Event-Related Electroencephalogram Reflect Dynamic Changes in the Degree of Surprise , 2008, The Journal of Neuroscience.

[85]  Mariano Sigman,et al.  Parsing a sequence of brain activations at psychological times using fMRI , 2007, NeuroImage.

[86]  Arno Villringer,et al.  Visual evoked potentials recovered from fMRI scan periods , 2005, Human brain mapping.

[87]  Tom Eichele,et al.  Semi-automatic identification of independent components representing EEG artifact , 2009, Clinical Neurophysiology.

[88]  Pierre Jolickur.  Concurrent Response-Selection Demands Modulate the Attentional Blink , 1999 .

[89]  M. Sigman,et al.  Brain Mechanisms of Serial and Parallel Processing during Dual-Task Performance , 2008, The Journal of Neuroscience.

[90]  Rami K. Niazy,et al.  Removal of FMRI environment artifacts from EEG data using optimal basis sets , 2005, NeuroImage.

[91]  W. Singer,et al.  The constructive nature of vision: direct evidence from functional magnetic resonance imaging studies of apparent motion and motion imagery , 1998, The European journal of neuroscience.