Tracking cognitive processing stages with MEG: A spatio-temporal model of associative recognition in the brain

In this study, we investigated the cognitive processing stages underlying associative recognition using MEG. Over the last four decades, a model of associative recognition has been developed in the ACT-R cognitive architecture. This model was first exclusively based on behavior, but was later evaluated and improved based on fMRI and EEG data. Unfortunately, the limited spatial resolution of EEG and the limited temporal resolution of fMRI have made it difficult to fully understand the spatiotemporal dynamics of associative recognition. We therefore conducted an associative recognition experiment with MEG, which combines excellent temporal resolution with reasonable spatial resolution. To analyze the data, we applied non-parametric cluster analyses and a multivariate classifier. This resulted in a detailed spatio-temporal model of associative recognition. After the visual encoding of the stimuli in occipital regions, three separable memory processes took place: a familiarity process (temporal cortex), a recollection process (temporal cortex and supramarginal gyrus), and a representational process (dorsolateral prefrontal cortex). A late decision process (superior parietal cortex) then acted upon the recollected information represented in the prefrontal cortex, culminating in a late response process (motor cortex). We conclude that existing theories of associative recognition, including the ACT-R model, should be adapted to include these processes.

[1]  Myeong-Ho Sohn,et al.  An information-processing model of three cortical regions: evidence in episodic memory retrieval , 2005, NeuroImage.

[2]  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.

[3]  Robert Oostenveld,et al.  FieldTrip: Open Source Software for Advanced Analysis of MEG, EEG, and Invasive Electrophysiological Data , 2010, Comput. Intell. Neurosci..

[4]  Michael Wilson MRC Psycholinguistic Database , 2001 .

[5]  Rachel A. Diana,et al.  Imaging recollection and familiarity in the medial temporal lobe: a three-component model , 2007, Trends in Cognitive Sciences.

[6]  John R. Anderson,et al.  Using model-based functional MRI to locate working memory updates and declarative memory retrievals in the fronto-parietal network , 2013, Proceedings of the National Academy of Sciences.

[7]  Anders M. Dale,et al.  An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest , 2006, NeuroImage.

[8]  G Sandini,et al.  Topography of brain electrical activity: a bioengineering approach. , 1983, Medical progress through technology.

[9]  John R. Anderson,et al.  The fan effect: New results and new theories. , 1999 .

[10]  K. Norman,et al.  Memory Strength and Repetition Suppression: Multimodal Imaging of Medial Temporal Cortical Contributions to Recognition , 2005, Neuron.

[11]  Marcia K. Johnson,et al.  Prefrontal Cortex Activity Associated with Source Monitoring in a Working Memory Task , 2004, Journal of Cognitive Neuroscience.

[12]  Julie A Fiez,et al.  Decoding and disrupting left midfusiform gyrus activity during word reading , 2016, Proceedings of the National Academy of Sciences.

[13]  Anders M. Dale,et al.  Cortical Surface-Based Analysis I. Segmentation and Surface Reconstruction , 1999, NeuroImage.

[14]  John R Anderson,et al.  The discovery of processing stages: Extension of Sternberg's method. , 2016, Psychological review.

[15]  Alberto Pisoni,et al.  Separating Recognition Processes of Declarative Memory via Anodal tDCS: Boosting Old Item Recognition by Temporal and New Item Detection by Parietal Stimulation , 2015, PloS one.

[16]  John R. Anderson,et al.  Using fMRI to Test Models of Complex Cognition , 2008, Cogn. Sci..

[17]  Jens Frahm,et al.  Equivalent Responses to Lexical and Nonlexical Visual Stimuli in Occipital Cortex: A Functional Magnetic Resonance Imaging Study , 1997, NeuroImage.

[18]  Pat Gunn,et al.  A rational account of memory predicts left prefrontal activation during controlled retrieval. , 2008, Cerebral cortex.

[19]  John R. Anderson,et al.  Competition and representation during memory retrieval: Roles of the prefrontal cortex and the posterior parietal cortex , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[20]  Moritz Grosse-Wentrup,et al.  Multisubject Learning for Common Spatial Patterns in Motor-Imagery BCI , 2011, Comput. Intell. Neurosci..

[21]  R. Shiffrin,et al.  A retrieval model for both recognition and recall. , 1984, Psychological review.

[22]  Caren M. Rotello,et al.  Recall-to-Reject in Recognition: Evidence from ROC Curves ☆ ☆☆ , 2000 .

[23]  Martin Luessi,et al.  MNE software for processing MEG and EEG data , 2014, NeuroImage.

[24]  Miguel P. Eckstein,et al.  Predicting variations of perceptual performance across individuals from neural activity using pattern classifiers , 2010, NeuroImage.

[25]  Michael Burke,et al.  Topography and Dynamics of Associative Long-term Memory Retrieval in Humans , 2007, Journal of Cognitive Neuroscience.

[26]  M. Brodeur,et al.  Prefrontal cortex contribution to associative recognition memory in humans: an event-related functional magnetic resonance imaging study , 2003, Neuroscience Letters.

[27]  Kenneth J. Malmberg,et al.  Recognition memory: A review of the critical findings and an integrated theory for relating them , 2008, Cognitive Psychology.

[28]  Friedemann Pulvermüller,et al.  Early influences of word length and frequency: a group study using MEG , 2003, Neuroreport.

[29]  Douglas L. Hintzman,et al.  Judgments of frequency and recognition memory in a multiple-trace memory model. , 1988 .

[30]  R. Henson A Mini-Review of fMRI Studies of Human Medial Temporal Lobe Activity Associated with Recognition Memory , 2005, The Quarterly journal of experimental psychology. B, Comparative and physiological psychology.

[31]  Riitta Salmelin,et al.  Tracking neural coding of perceptual and semantic features of concrete nouns , 2012, NeuroImage.

[32]  Tim Curran,et al.  ERP correlates of familiarity and recollection processes in visual associative recognition , 2007, Brain Research.

[33]  F. Pulvermüller,et al.  Effects of word length and frequency on the human event-related potential , 2004, Clinical Neurophysiology.

[34]  Niels Taatgen,et al.  Contrasting single and multi-component working-memory systems in dual tasking , 2016, Cognitive Psychology.

[35]  William D. Marslen-Wilson,et al.  The time course of visual word recognition as revealed by linear regression analysis of ERP data , 2006, NeuroImage.

[36]  Max Coltheart,et al.  The MRC Psycholinguistic Database , 1981 .

[37]  Martin Lepage,et al.  Dorsolateral prefrontal cortex involvement in memory post-retrieval monitoring revealed in both item and associative recognition tests , 2005, NeuroImage.

[38]  John R. Anderson The Architecture of Cognition , 1983 .

[39]  John A. Pyles,et al.  Dynamic Encoding of Face Information in the Human Fusiform Gyrus , 2014, Nature Communications.

[40]  Rupert Lanzenberger,et al.  Magnetoencephalography indicates finger motor somatotopy , 2004, The European journal of neuroscience.

[41]  Mitsuo Ochi,et al.  Motor somatotopy of extensor indicis proprius and extensor pollicis longus , 2011, Neuroreport.

[42]  Akira Hashizume,et al.  Somatosensory mechanical response and digit somatotopy within cortical areas of the postcentral gyrus in humans: An MEG study , 2013, Human brain mapping.

[43]  J. Wixted Dual-process theory and signal-detection theory of recognition memory. , 2007, Psychological review.

[44]  John R. Anderson How Can the Human Mind Occur in the Physical Universe , 2007 .

[45]  Pierluigi Zoccolotti,et al.  Length Effect in Word Naming in Reading: Role of Reading Experience and Reading Deficit in Italian Readers , 2005, Developmental neuropsychology.

[46]  Raymond P. Kesner,et al.  Prefrontal and hippocampal contributions to encoding and retrieval of spatial memory , 2010, Neurobiology of Learning and Memory.

[47]  M. Bar,et al.  The effects of priming on frontal-temporal communication , 2008, Proceedings of the National Academy of Sciences.

[48]  G. Rees,et al.  Neuroimaging: Decoding mental states from brain activity in humans , 2006, Nature Reviews Neuroscience.

[49]  Tom M. Mitchell,et al.  Machine learning classifiers and fMRI: A tutorial overview , 2009, NeuroImage.

[50]  Darryl W. Schneider,et al.  Modeling fan effects on the time course of associative recognition , 2012, Cognitive Psychology.

[51]  M. Kutas,et al.  Interactions between sentence context and word frequencyinevent-related brainpotentials , 1990, Memory & cognition.

[52]  T. Curran,et al.  Semantic and perceptual effects on recognition memory: Evidence from ERP , 2009, Brain Research.

[53]  G. Bower,et al.  Human Associative Memory , 1973 .

[54]  Tom Heskes,et al.  Interpreting single trial data using groupwise regularisation , 2009, NeuroImage.

[55]  B B Murdock,et al.  TODAM2: a model for the storage and retrieval of item, associative, and serial-order information. , 1993, Psychological review.

[56]  E. Heit,et al.  Associative Recognition: a Case of Recall-to-reject Processing , 2022 .

[57]  John R. Anderson,et al.  Using Data-Driven Model-Brain Mappings to Constrain Formal Models of Cognition , 2015, PloS one.

[58]  John T Wixted,et al.  In defense of the signal detection interpretation of remember/know judgments , 2004, Psychonomic bulletin & review.

[59]  A. Wagner,et al.  Prefrontal and hippocampal contributions to visual associative recognition: Interactions between cognitive control and episodic retrieval , 2004, Brain and Cognition.

[60]  Trevor Hastie,et al.  The Elements of Statistical Learning , 2001 .

[61]  R. Oostenveld,et al.  Nonparametric statistical testing of EEG- and MEG-data , 2007, Journal of Neuroscience Methods.

[62]  Sydney S. Cash,et al.  Decoding word and category-specific spatiotemporal representations from MEG and EEG , 2011, NeuroImage.

[63]  Lynne M. Reder,et al.  Models of recognition: A review of arguments in favor of a dual-process account , 2006, Psychonomic bulletin & review.

[64]  R. Henson,et al.  Neural correlates of retrieval processing in the prefrontal cortex during recognition and exclusion tasks , 2003, Neuropsychologia.

[65]  Michael A. Ford,et al.  Can I have a quick word? Early electrophysiological manifestations of psycholinguistic processes revealed by event-related regression analysis of the EEG , 2009, Biological Psychology.

[66]  Frank Rösler,et al.  Topography of brain electrical activity dissociates the retrieval of spatial versus verbal information from episodic long-term memory in humans , 1997, Neuroscience Letters.

[67]  John R. Anderson,et al.  Stages of Processing in Associative Recognition: Evidence from Behavior, EEG, and Classification , 2013, Journal of Cognitive Neuroscience.

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

[69]  M. Rugg,et al.  Human recognition memory: a cognitive neuroscience perspective , 2003, Trends in Cognitive Sciences.

[70]  Keith Rayner,et al.  Investigating the effects of a set of intercorrelated variables on eye fixation durations in reading. , 2003, Journal of experimental psychology. Learning, memory, and cognition.

[71]  M. Rugg,et al.  Event-related potentials and recognition memory , 2007, Trends in Cognitive Sciences.

[72]  John R. Anderson,et al.  The discovery of processing stages: Analyzing EEG data with hidden semi-Markov models , 2015, NeuroImage.

[73]  A. Yonelinas The Nature of Recollection and Familiarity: A Review of 30 Years of Research , 2002 .

[74]  L. Squire,et al.  Simple and associative recognition memory in the hippocampal region. , 2001, Learning & memory.