Sequence learning recodes cortical representations instead of strengthening initial ones

We contrast two computational models of sequence learning. The associative learner posits that learning proceeds by strengthening existing association weights. Alternatively, recoding posits that learning creates new and more efficient representations of the learned sequences. Importantly, both models propose that humans act as optimal learners but capture different statistics of the stimuli in their internal model. Furthermore, these models make dissociable predictions as to how learning changes the neural representation of sequences. We tested these predictions by using fMRI to extract neural activity patters from the dorsal visual processing stream during a sequence recall task. We observed that only the recoding account can explain the similarity of neural activity patterns, suggesting that participants recode the learned sequences using chunks. We show that associative learning can theoretically store only very limited number of overlapping sequences, such as common in ecological working memory tasks, and hence an efficient learner should recode initial sequence representations.

[1]  Brian B. Avants,et al.  Symmetric diffeomorphic image registration with cross-correlation: Evaluating automated labeling of elderly and neurodegenerative brain , 2008, Medical Image Anal..

[2]  Z L Lu,et al.  Perceptual learning reflects external noise filtering and internal noise reduction through channel reweighting. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[3]  H. Eichenbaum,et al.  Representation of memories in the cortical–hippocampal system: Results from the application of population similarity analyses , 2016, Neurobiology of Learning and Memory.

[4]  Michael C. Frank,et al.  Modeling human performance in statistical word segmentation , 2010, Cognition.

[5]  D. Norris,et al.  Testing a positional model of the Hebb effect , 2003, Memory.

[6]  Marc W Howard,et al.  The temporal context model in spatial navigation and relational learning: toward a common explanation of medial temporal lobe function across domains. , 2005, Psychological review.

[7]  E. Rolls,et al.  Computational analysis of the role of the hippocampus in memory , 1994, Hippocampus.

[8]  A. Pouget,et al.  Perceptual learning as improved probabilistic inference in early sensory areas , 2011, Nature Neuroscience.

[9]  Peter Redgrave,et al.  Basal Ganglia , 2020, Encyclopedia of Autism Spectrum Disorders.

[10]  Neil Burgess,et al.  Representations of Serial Order , 1997, NCPW.

[11]  Stefano Fusi,et al.  Why neurons mix: high dimensionality for higher cognition , 2016, Current Opinion in Neurobiology.

[12]  Satrajit S. Ghosh,et al.  FMRIPrep: a robust preprocessing pipeline for functional MRI , 2018, bioRxiv.

[13]  Yee Whye Teh,et al.  A Hierarchical Bayesian Language Model Based On Pitman-Yor Processes , 2006, ACL.

[14]  E. Vogel,et al.  Visual working memory capacity: from psychophysics and neurobiology to individual differences , 2013, Trends in Cognitive Sciences.

[15]  Konrad Paul Kording,et al.  Bayesian integration in sensorimotor learning , 2004, Nature.

[16]  Martyn Lloyd-Kelly,et al.  What's in a Name? The Multiple Meanings of “Chunk” and “Chunking” , 2016, Front. Psychol..

[17]  R W Cox,et al.  Software tools for analysis and visualization of fMRI data , 1997, NMR in biomedicine.

[18]  Jane E. Clark,et al.  New insights into statistical learning and chunk learning in implicit sequence acquisition , 2017, Psychonomic bulletin & review.

[19]  N. Burgess,et al.  Toward a network model of the articulatory loop , 1992, Connectionist psychology: A text with readings.

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

[21]  Michael Brady,et al.  Improved Optimization for the Robust and Accurate Linear Registration and Motion Correction of Brain Images , 2002, NeuroImage.

[22]  Hugo Merchant,et al.  Interval Tuning in the Primate Medial Premotor Cortex as a General Timing Mechanism , 2013, The Journal of Neuroscience.

[23]  Matthias J. Gruber,et al.  Hippocampal Activity Patterns Carry Information about Objects in Temporal Context , 2014, Neuron.

[24]  C. Lanczos Evaluation of Noisy Data , 1964 .

[25]  Charles R Legéndy,et al.  On the ‘data stirring’ role of the dentate gyrus of the hippocampus , 2017, Reviews in the neurosciences.

[26]  G. A. Miller THE PSYCHOLOGICAL REVIEW THE MAGICAL NUMBER SEVEN, PLUS OR MINUS TWO: SOME LIMITS ON OUR CAPACITY FOR PROCESSING INFORMATION 1 , 1956 .

[27]  Kristjan Kalm,et al.  Recall is not necessary for verbal sequence learning , 2016, Memory & cognition.

[28]  Ramon Bartolo,et al.  Dynamic Representation of the Temporal and Sequential Structure of Rhythmic Movements in the Primate Medial Premotor Cortex , 2014, The Journal of Neuroscience.

[29]  E. Rolls,et al.  A computational theory of hippocampal function, and tests of the theory: New developments , 2015, Neuroscience & Biobehavioral Reviews.

[30]  Russell A. Poldrack,et al.  FMRIPrep: a robust preprocessing pipeline for functional MRI , 2018 .

[31]  P. Berkes,et al.  Statistically Optimal Perception and Learning: from Behavior to Neural Representations , 2022 .

[32]  Jörn Diedrichsen,et al.  Human premotor areas parse sequences into their spatial and temporal features , 2014, eLife.

[33]  Florent Meyniel,et al.  The Neural Representation of Sequences: From Transition Probabilities to Algebraic Patterns and Linguistic Trees , 2015, Neuron.

[34]  J. Diedrichsen,et al.  On the distribution of cross-validated Mahalanobis distances , 2016, 1607.01371.

[35]  Yves Rosseel,et al.  On the Definition of Signal-To-Noise Ratio and Contrast-To-Noise Ratio for fMRI Data , 2013, PloS one.

[36]  Li Su,et al.  A Toolbox for Representational Similarity Analysis , 2014, PLoS Comput. Biol..

[37]  H. Eichenbaum,et al.  Memory for the Order of Events in Specific Sequences: Contributions of the Hippocampus and Medial Prefrontal Cortex , 2011, The Journal of Neuroscience.

[38]  Arthur P. Shimamura,et al.  Memory for the temporal order of events in patients with frontal lobe lesions and amnesic patients , 1990, Neuropsychologia.

[39]  Anders M. Dale,et al.  Automatic parcellation of human cortical gyri and sulci using standard anatomical nomenclature , 2010, NeuroImage.

[40]  C. Almli,et al.  Unbiased nonlinear average age-appropriate brain templates from birth to adulthood , 2009, NeuroImage.

[41]  Dennis Norris,et al.  Repetition-spacing and item-overlap effects in the Hebb repetition task , 2013 .

[42]  W. Ma,et al.  Factorial comparison of working memory models. , 2014, Psychological review.

[43]  E. Todorov Optimality principles in sensorimotor control , 2004, Nature Neuroscience.

[44]  Antje Nuthmann,et al.  Memory for temporal order , 1999 .

[45]  Jörn Diedrichsen,et al.  Binding During Sequence Learning Does Not Alter Cortical Representations of Individual Actions , 2018, The Journal of Neuroscience.

[46]  Andreas Nieder,et al.  Temporal and Spatial Enumeration Processes in the Primate Parietal Cortex , 2006, Science.

[47]  Guillén Fernández,et al.  Interaction between the Human Hippocampus and the Caudate Nucleus during Route Recognition , 2004, Neuron.

[48]  J. Fiser Perceptual learning and representational learning in humans and animals , 2009, Learning & behavior.

[49]  A. Norman Redlich,et al.  Redundancy Reduction as a Strategy for Unsupervised Learning , 1993, Neural Computation.

[50]  David J. C. MacKay,et al.  Information Theory, Inference, and Learning Algorithms , 2004, IEEE Transactions on Information Theory.

[51]  Jörn Diedrichsen,et al.  The Role of Human Primary Motor Cortex in the Production of Skilled Finger Sequences , 2018, The Journal of Neuroscience.

[52]  Klaus Oberauer,et al.  The contributions of encoding, retention, and recall to the Hebb effect , 2009, Memory.

[53]  Michael J Kahana,et al.  Positional cues in serial learning: The spin-list technique , 2010, Memory & cognition.

[54]  Carl R Olson,et al.  Rank signals in four areas of macaque frontal cortex during selection of actions and objects in serial order. , 2010, Journal of neurophysiology.

[55]  G. Buzsáki,et al.  Space and Time: The Hippocampus as a Sequence Generator , 2018, Trends in Cognitive Sciences.

[56]  J. Krakauer,et al.  Consolidation of motor memory , 2006, Trends in Neurosciences.

[57]  Surya Ganguli,et al.  A theory of multineuronal dimensionality, dynamics and measurement , 2017, bioRxiv.

[58]  James L. McClelland,et al.  Considerations arising from a complementary learning systems perspective on hippocampus and neocortex , 1996, Hippocampus.

[59]  David Winzenz,et al.  Group structure and coding in serial learning. , 1972 .

[60]  Chih-Jen Lin,et al.  LIBSVM: A library for support vector machines , 2011, TIST.

[61]  Satrajit S. Ghosh,et al.  Nipype: A Flexible, Lightweight and Extensible Neuroimaging Data Processing Framework in Python , 2011, Front. Neuroinform..

[62]  A M Graybiel,et al.  The basal ganglia and adaptive motor control. , 1994, Science.

[63]  Daeyeol Lee,et al.  Activity in prefrontal cortex during dynamic selection of action sequences , 2006, Nature Neuroscience.

[64]  H. Eichenbaum,et al.  Conservation of hippocampal memory function in rats and humans , 1996, Nature.

[65]  Satrajit S. Ghosh,et al.  Mindboggling morphometry of human brains , 2016, bioRxiv.

[66]  C. Olson,et al.  Relation of ordinal position signals to the expectation of reward and passage of time in four areas of the macaque frontal cortex. , 2011, Journal of neurophysiology.

[67]  Andrew C. Heusser,et al.  Episodic sequence memory is supported by a theta-gamma phase code , 2016, Nature Neuroscience.

[68]  H. Eichenbaum,et al.  Critical role of the hippocampus in memory for sequences of events , 2002, Nature Neuroscience.

[69]  Floris P. de Lange,et al.  Statistical learning attenuates visual activity only for attended stimuli , 2019 .

[70]  Russell A. Poldrack,et al.  Deconvolving BOLD activation in event-related designs for multivoxel pattern classification analyses , 2012, NeuroImage.

[71]  Stephen M. Smith,et al.  Improved Optimization for the Robust and Accurate Linear Registration and Motion Correction of Brain Images , 2002, NeuroImage.

[72]  Ovidiu Lungu,et al.  Consolidation alters motor sequence-specific distributed representations , 2018, bioRxiv.

[73]  R. Baayen,et al.  Analyzing Reaction Times , 2010 .

[74]  A. Pouget,et al.  Probabilistic brains: knowns and unknowns , 2013, Nature Neuroscience.

[75]  Bruce Fischl,et al.  Accurate and robust brain image alignment using boundary-based registration , 2009, NeuroImage.

[76]  R. Henson Positional information in short-term memory: Relative or absolute? , 1999, Memory & cognition.

[77]  W. Estes,et al.  Item and order information in short-term memory: Evidence for multilevel perturbation processes. , 1981 .

[78]  Joshua B. Tenenbaum,et al.  Human-level concept learning through probabilistic program induction , 2015, Science.

[79]  Stephen M. Smith,et al.  Segmentation of brain MR images through a hidden Markov random field model and the expectation-maximization algorithm , 2001, IEEE Transactions on Medical Imaging.

[80]  Bryan M. Hooks,et al.  Circuit Changes in Motor Cortex During Motor Skill Learning , 2018, Neuroscience.

[81]  A. Georgopoulos,et al.  Motor cortical encoding of serial order in a context-recall task. , 1999, Science.

[82]  Andreas Nieder,et al.  Supramodal numerosity selectivity of neurons in primate prefrontal and posterior parietal cortices , 2012, Proceedings of the National Academy of Sciences.

[83]  Lila Davachi,et al.  How the hippocampus preserves order: the role of prediction and context , 2015, Trends in Cognitive Sciences.

[84]  J. Doyon,et al.  Current issues related to motor sequence learning in humans , 2018, Current Opinion in Behavioral Sciences.

[85]  S. Valdois,et al.  Sequential or simultaneous visual processing deficit in developmental dyslexia? , 2008, Vision Research.

[86]  Darren J Edwards,et al.  Task-relevant chunking in sequence learning. , 2010, Journal of experimental psychology. Human perception and performance.

[87]  Jörn Diedrichsen,et al.  Neural Organization of Hierarchical Motor Sequence Representations in the Human Neocortex , 2019, Neuron.

[88]  Jonathan D. Cohen,et al.  The effects of neural gain on attention and learning , 2013, Nature Neuroscience.

[89]  Richard N Aslin,et al.  Bayesian learning of visual chunks by human observers , 2008, Proceedings of the National Academy of Sciences.

[90]  J. Pine,et al.  Chunking mechanisms in human learning , 2001, Trends in Cognitive Sciences.

[91]  Denis G. Pelli,et al.  ECVP '07 Abstracts , 2007, Perception.

[92]  R. Henson Short-Term Memory for Serial Order: The Start-End Model , 1998, Cognitive Psychology.

[93]  Yaoda Xu,et al.  Decoding the content of visual short-term memory under distraction in occipital and parietal areas , 2015, Nature Neuroscience.

[94]  J. Tanji,et al.  Integration of temporal order and object information in the monkey lateral prefrontal cortex. , 2004, Journal of neurophysiology.

[95]  John-Dylan Haynes,et al.  Decoding the Contents of Visual Short-Term Memory from Human Visual and Parietal Cortex , 2012, The Journal of Neuroscience.

[96]  Guinevere F. Eden,et al.  Dyslexics are impaired on implicit higher-order sequence learning, but not on implicit spatial context learning , 2006, Neuropsychologia.

[97]  Jörn Diedrichsen,et al.  Binding During Sequence Learning Does Not Alter Cortical Representations of Individual Actions , 2019, The Journal of Neuroscience.

[98]  R. J. McDonald,et al.  Multiple Parallel Memory Systems in the Brain of the Rat , 2002, Neurobiology of Learning and Memory.

[99]  Andreas Nieder,et al.  Temporal and Spatial Enumeration Processes in the Primate Parietal Cortex , 2006, Science.

[100]  Scott P. Johnson,et al.  When learning goes beyond statistics: Infants represent visual sequences in terms of chunks , 2018, Cognition.

[101]  Edward F. Ester,et al.  Parietal and Frontal Cortex Encode Stimulus-Specific Mnemonic Representations during Visual Working Memory , 2015, Neuron.

[102]  Michael McCloskey,et al.  Representation of item position in immediate serial recall: Evidence from intrusion errors. , 2015, Journal of experimental psychology. Learning, memory, and cognition.

[103]  N. Hunkin,et al.  Memory for single items, word pairs, and temporal order of different kinds in a patient with selective hippocampal lesions , 2001, Cognitive neuropsychology.

[104]  T. Griffiths,et al.  A Bayesian framework for word segmentation: Exploring the effects of context , 2009, Cognition.

[105]  G. Bower,et al.  Group structure, coding, and memory for digit series , 1969 .

[106]  James L. McClelland,et al.  Why there are complementary learning systems in the hippocampus and neocortex: insights from the successes and failures of connectionist models of learning and memory. , 1995, Psychological review.

[107]  Alan D Baddeley,et al.  Memory for serial order across domains: An overview of the literature and directions for future research. , 2014, Psychological bulletin.

[108]  Jonathan D. Cohen,et al.  Facilitating open-science with realistic fMRI simulation: validation and application , 2019, bioRxiv.

[109]  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.

[110]  R. Aslin,et al.  PSYCHOLOGICAL SCIENCE Research Article UNSUPERVISED STATISTICAL LEARNING OF HIGHER-ORDER SPATIAL STRUCTURES FROM VISUAL SCENES , 2022 .

[111]  Kristjan Kalm,et al.  The Representation of Order Information in Auditory-Verbal Short-Term Memory , 2014, The Journal of Neuroscience.

[112]  Rainer Goebel,et al.  Information-based functional brain mapping. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[113]  Florent Meyniel,et al.  Brain signatures of a multiscale process of sequence learning in humans , 2019, eLife.

[114]  Jörn Diedrichsen,et al.  Skill learning strengthens cortical representations of motor sequences , 2013, eLife.

[115]  G D Brown,et al.  Oscillator-based memory for serial order. , 2000, Psychological review.

[116]  Brian B. Avants,et al.  N4ITK: Improved N3 Bias Correction , 2010, IEEE Transactions on Medical Imaging.

[117]  B. Murdock Context and mediators in a theory of distributed associative memory (TODAM2). , 1997 .

[118]  Sammi R. Chekroud,et al.  Concurrent visual and motor selection during visual working memory guided action , 2018, Nature Neuroscience.