Similar neural correlates for language and sequential learning: Evidence from event-related brain potentials

We used event-related potentials (ERPs) to investigate the time course and distribution of brain activity while adults performed (1) a sequential learning task involving complex structured sequences and (2) a language processing task. The same positive ERP deflection, the P600 effect, typically linked to difficult or ungrammatical syntactic processing, was found for structural incongruencies in both sequential learning as well as natural language and with similar topographical distributions. Additionally, a left anterior negativity (LAN) was observed for language but not for sequential learning. These results are interpreted as an indication that the P600 provides an index of violations and the cost of integration of expectations for upcoming material when processing complex sequential structure. We conclude that the same neural mechanisms may be recruited for both syntactic processing of linguistic stimuli and sequential learning of structured sequence patterns more generally.

[1]  Roger W. Schvaneveldt,et al.  Attention and probabilistic sequence learning , 1998 .

[2]  D. Caplan,et al.  The role of animacy and thematic relationships in processing active English sentences: Evidence from event-related potentials , 2007, Brain and Language.

[3]  Kristine H. Onishi,et al.  Infants learn phonotactic regularities from brief auditory experience , 2003, Cognition.

[4]  C. Petten,et al.  A special role for the right hemisphere in metaphor comprehension? ERP evidence from hemifield presentation , 2007, Brain Research.

[5]  Peter Hagoort,et al.  Brain responses to lexical ambiguity resolution and parsing. , 1994 .

[6]  Benjamin Martin Bly,et al.  Event-related potential markers of expectation violation in an artificial grammar learning task , 2007, Neuroreport.

[7]  Benjamin A Clegg,et al.  Sequence learning , 1998, Trends in Cognitive Sciences.

[8]  Christopher M. Conway,et al.  Implicit statistical learning in language processing: Word predictability is the key , 2010, Cognition.

[9]  M Eimer,et al.  Explicit and implicit learning of event sequences: evidence from event-related brain potentials. , 1996, Journal of experimental psychology. Learning, memory, and cognition.

[10]  Martin Eimer,et al.  Chunking processes in the learning of event sequences: Electrophysiological indicators , 2000, Memory & cognition.

[11]  M. Kutas,et al.  Who Did What and When? Using Word- and Clause-Level ERPs to Monitor Working Memory Usage in Reading , 1995, Journal of Cognitive Neuroscience.

[12]  Morten H. Christiansen,et al.  Language as shaped by the brain. , 2008, The Behavioral and brain sciences.

[13]  Marco Baroni,et al.  Generalizable distributional regularities aid fluent language processing , 2008 .

[14]  Jutta L. Mueller,et al.  The Role of Pause Cues in Language Learning: The Emergence of Event-related Potentials Related to Sequence Processing , 2008, Journal of Cognitive Neuroscience.

[15]  M. Kutas,et al.  An ERP analysis of implicit structured sequence learning. , 1997, Psychophysiology.

[16]  A. Reber Implicit learning of artificial grammars , 1967 .

[17]  Peter Ford Dominey,et al.  ERP analysis of cognitive sequencing: a left anterior negativity related to structural transformation processing , 2000, Neuroreport.

[18]  Todd M. Bailey,et al.  The role of similarity in artificial grammar learning. , 2000, Journal of experimental psychology. Learning, memory, and cognition.

[19]  Axel Cleeremans,et al.  Implicit learning out of the lab: the case of orthographic regularities. , 2001, Journal of experimental psychology. General.

[20]  Matthias Schlesewsky,et al.  An alternative perspective on “semantic P600” effects in language comprehension , 2008, Brain Research Reviews.

[21]  Dawn G. Blasko,et al.  ERP and behavioral evidence of individual differences in metaphor comprehension , 2003, Memory & cognition.

[22]  Marshall R. Mayberry,et al.  Situated sentence processing: The coordinated interplay account and a neurobehavioral model , 2010, Brain and Language.

[23]  Thomas F. Mnte,et al.  Brain Activity Associated with Syntactic Incongruencies in Words and Pseudo-Words , 1997, Journal of Cognitive Neuroscience.

[24]  Karsten Steinhauer,et al.  Brain signatures of artificial language processing: Evidence challenging the critical period hypothesis , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[25]  Virginia Valian,et al.  Anchor points in language learning: The role of marker frequency ☆ , 1988 .

[26]  John F. Connolly,et al.  CHAPTER 9 – Event-Related Potentials in the Study of Language , 2008 .

[27]  John R. Vokey,et al.  Salience of Item Knowledge in Learning Artificial Grammars , 1992 .

[28]  C. Fiebach,et al.  Separating syntactic memory costs and syntactic integration costs during parsing: the processing of German WH-questions , 2002 .

[29]  Yuki Kamide,et al.  Anticipatory Processes in Sentence Processing , 2008, Lang. Linguistics Compass.

[30]  John C. Trueswell,et al.  Chapter 7 – Sentence Comprehension , 1995 .

[31]  Nick Chater,et al.  Reduction of Uncertainty in Human Sequential Learning: Evidence from Artificial Grammar Learning , 2003 .

[32]  Morten H. Christiansen,et al.  Sequential Expectations: The Role of Prediction-Based Learning in Language , 2010, Top. Cogn. Sci..

[33]  Peter Hagoort,et al.  Word-category violations in patients with Broca’s aphasia: An ERP study , 2005, Brain and Language.

[34]  S. Coulson,et al.  Handedness, hemispheric asymmetries, and joke comprehension. , 2004, Brain research. Cognitive brain research.

[35]  C. Phillips,et al.  ERP effects of the processing of syntactic long-distance dependencies. , 2005, Brain research. Cognitive brain research.

[36]  Angela D. Friederici,et al.  Isn't It Ironic? An Electrophysiological Exploration of Figurative Language Processing , 2011, Journal of Cognitive Neuroscience.

[37]  Thomas F Münte,et al.  Differences in incidental and intentional learning of sensorimotor sequences as revealed by event-related brain potentials. , 2003, Brain research. Cognitive brain research.

[38]  L L Elliott,et al.  Development of a test of speech intelligibility in noise using sentence materials with controlled word predictability. , 1977, The Journal of the Acoustical Society of America.

[39]  C. Felser,et al.  Storage and integration in the processing of filler-gap dependencies: An ERP study of topicalization and wh-movement in German , 2003, Brain and Language.

[40]  E. Newport,et al.  Learning at a distance I. Statistical learning of non-adjacent dependencies , 2004, Cognitive Psychology.

[41]  M. Goldsmith,et al.  Statistical Learning by 8-Month-Old Infants , 1996 .

[42]  A. Friederici,et al.  Semantic and syntactic processing in Chinese sentence comprehension: Evidence from event-related potentials , 2006, Brain Research.

[43]  Thomas R. G. Green,et al.  The necessity of syntax markers: Two experiments with artificial languages , 1979 .

[44]  Peter Hagoort,et al.  How the brain solves the binding problem for language: a neurocomputational model of syntactic processing , 2003, NeuroImage.

[45]  Elissa L Newport,et al.  Structural packaging in the input to language learning: Contributions of prosodic and morphological marking of phrases to the acquisition of language , 1987, Cognitive Psychology.

[46]  A Hahne,et al.  What's Different in Second-Language Processing? Evidence from Event-Related Brain Potentials , 2001, Journal of psycholinguistic research.

[47]  M. Pickering,et al.  Do people use language production to make predictions during comprehension? , 2007, Trends in Cognitive Sciences.

[48]  Christopher M. Conway,et al.  Contribution of implicit sequence learning to spoken language processing: some preliminary findings with hearing adults. , 2007, Journal of deaf studies and deaf education.

[49]  J. Saffran Statistical Language Learning , 2003 .

[50]  R. Aslin,et al.  Statistical learning of higher-order temporal structure from visual shape sequences. , 2002, Journal of experimental psychology. Learning, memory, and cognition.

[51]  M. Nissen,et al.  Attentional requirements of learning: Evidence from performance measures , 1987, Cognitive Psychology.

[52]  S. Edelman,et al.  Learn locally, act globally: Learning language from variation set cues , 2008, Cognition.

[53]  C. Phillips,et al.  The role of feature-number and feature-type in processing Hindi verb agreement violations , 2007, Brain Research.

[54]  R. C. Oldfield The assessment and analysis of handedness: the Edinburgh inventory. , 1971, Neuropsychologia.

[55]  K. Rayner,et al.  Effects of contextual constraint on eye movements in reading: A further examination , 1996, Psychonomic bulletin & review.

[56]  Stefan Koelsch,et al.  Musical training modulates the development of syntax processing in children , 2009, NeuroImage.

[57]  S L Wolf,et al.  An Alternative Perspective , 1999, Applied psychophysiology and biofeedback.

[58]  G. Dell,et al.  Speech errors, phonotactic constraints, and implicit learning: a study of the role of experience in language production. , 2000, Journal of experimental psychology. Learning, memory, and cognition.

[59]  Gina R. Kuperberg,et al.  Neural mechanisms of language comprehension: Challenges to syntax , 2007, Brain Research.

[60]  E. Newport,et al.  PSYCHOLOGICAL SCIENCE Research Article INCIDENTAL LANGUAGE LEARNING: Ustening (and Learning) out of the Comer of Your Ear , 2022 .

[61]  Angela D. Friederici,et al.  Hierarchical and Linear Sequence Processing: An Electrophysiological Exploration of Two Different Grammar Types , 2006, Journal of Cognitive Neuroscience.

[62]  Tim Curran,et al.  Attentional and Nonattentional Forms of Sequence Learning , 1993 .

[63]  E. Pothos Theories of artificial grammar learning. , 2007, Psychological bulletin.

[64]  Kara D. Federmeier Thinking ahead: the role and roots of prediction in language comprehension. , 2007, Psychophysiology.

[65]  R. Gómez Variability and Detection of Invariant Structure , 2002, Psychological science.

[66]  David Swinney,et al.  Brain potentials elicited by garden-path sentences: evidence of the application of verb information during parsing , 1994 .

[67]  A. Friederici,et al.  Temporal structure of syntactic parsing: early and late event-related brain potential effects. , 1996, Journal of experimental psychology. Learning, memory, and cognition.

[68]  P. Holcomb,et al.  Event-related brain potentials elicited by syntactic anomaly , 1992 .

[69]  D. Poeppel,et al.  The linguistic processes underlying the P600 , 2010 .

[70]  M. Kutas,et al.  Getting it: human event-related brain response to jokes in good and poor comprehenders , 2001, Neuroscience Letters.

[71]  B. Scholl,et al.  The Automaticity of Visual Statistical Learning Statistical Learning , 2005 .

[72]  M. Bar The proactive brain: using analogies and associations to generate predictions , 2007, Trends in Cognitive Sciences.

[73]  J. Elman,et al.  Networks are not ‘hidden rules’ , 1999, Trends in Cognitive Sciences.

[74]  Scott Sinnett,et al.  Speech segmentation by statistical learning depends on attention , 2005, Cognition.

[75]  James L. McClelland,et al.  Learning the structure of event sequences. , 1991, Journal of experimental psychology. General.

[76]  Angela D. Friederici,et al.  When word category information encounters morphosyntax: An ERP study , 2005, Neuroscience Letters.

[77]  Morten H. Christiansen,et al.  Sequential learning in non-human primates , 2001, Trends in Cognitive Sciences.

[78]  Marina Nespor,et al.  Signal-Driven Computations in Speech Processing , 2002, Science.

[79]  Jenny R Saffran,et al.  Words in a sea of sounds: the output of infant statistical learning , 2001, Cognition.

[80]  M. Ferguson,et al.  How social perception can automatically influence behavior , 2004, Trends in Cognitive Sciences.

[81]  M. Kutas,et al.  Bridging the Gap: Evidence from ERPs on the Processing of Unbounded Dependencies , 1993, Journal of Cognitive Neuroscience.

[82]  D. Caplan,et al.  Electrophysiological distinctions in processing conceptual relationships within simple sentences. , 2003, Brain research. Cognitive brain research.

[83]  Frank Rösler,et al.  Response Anticipation Processes in the Learning of a Sensorimotor Sequence: Evidence from the Latera , 2001 .

[84]  L. Osterhout,et al.  Event-Related Brain Potentials Elicited by Failure to Agree , 1995 .

[85]  Peter Ford Dominey,et al.  Training with cognitive sequences improves syntactic comprehension in agrammatic aphasics , 2003, Neuroreport.

[86]  Angela D. Friederici,et al.  Learning : rule extraction and representation , 1999 .

[87]  L R Squire,et al.  The information acquired during artificial grammar learning. , 1994, Journal of experimental psychology. Learning, memory, and cognition.

[88]  A. Friederici The Time Course of Syntactic Activation During Language Processing: A Model Based on Neuropsychological and Neurophysiological Data , 1995, Brain and Language.

[89]  Elizabeth K. Johnson,et al.  Statistical learning of tone sequences by human infants and adults , 1999, Cognition.

[90]  P. Perruchet,et al.  Implicit learning and statistical learning: one phenomenon, two approaches , 2006, Trends in Cognitive Sciences.

[91]  Spatz Wb Unipolar brush cells in marmoset cerebellum and cochlear nuclei express calbindin. , 2000 .

[92]  Morten H. Christiansen,et al.  Impaired artificial grammar learning in agrammatism , 2010, Cognition.

[93]  Maryellen C. MacDonald,et al.  The lexical nature of syntactic ambiguity resolution , 1994 .

[94]  D. Swinney,et al.  Brain potentials elicited by garden-path sentences: evidence of the application of verb information during parsing. , 1994, Journal of experimental psychology. Learning, memory, and cognition.

[95]  D. Tucker Spatial sampling of head electrical fields: the geodesic sensor net. , 1993, Electroencephalography and clinical neurophysiology.

[96]  Morten H. Christiansen,et al.  When Less is Less and When Less is More: Starting Small with Staged Input , 2003 .

[97]  F Rösler,et al.  Implicit and explicit learning of event sequences: evidence for distinct coding of perceptual and motor representations. , 2000, Acta psychologica.

[98]  Peter Neri,et al.  Meaningful interactions can enhance visual discrimination of human agents , 2006, Nature Neuroscience.

[99]  D. Tucker,et al.  Scalp electrode impedance, infection risk, and EEG data quality , 2001, Clinical Neurophysiology.

[100]  M. Kutas,et al.  Reading senseless sentences: brain potentials reflect semantic incongruity. , 1980, Science.

[101]  Peter M. Vishton,et al.  Rule learning by seven-month-old infants. , 1999, Science.

[102]  Morten H. Christiansen,et al.  PSYCHOLOGICAL SCIENCE Research Article Statistical Learning Within and Between Modalities Pitting Abstract Against Stimulus-Specific Representations , 2022 .

[103]  Van Berkum,et al.  Understanding Sentences in Context What Brain Waves Can Tell Us , 2008 .

[104]  Peter Hagoort,et al.  Reflections on the neurobiology of syntax , 2009 .

[105]  L. Osterhout,et al.  The independence of combinatory semantic processing: Evidence from event-related potentials , 2005 .

[106]  Tomifusa Kuboki,et al.  Explicit knowledge and intention to learn in sequence learning: an event-related potential study , 2005, Neuroreport.

[107]  Morten H. Christiansen,et al.  Modality-constrained statistical learning of tactile, visual, and auditory sequences. , 2005, Journal of experimental psychology. Learning, memory, and cognition.

[108]  Patricia J. Brooks,et al.  Acquisition of Gender-like Noun Subclasses in an Artificial Language: The Contribution of Phonological Markers to Learning , 1993 .

[109]  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.

[110]  Morten H. Christiansen,et al.  A Connectionist Single-Mechanism Account of Rule-Like Behavior in Infancy , 2000 .

[111]  M. Linden,et al.  Associative chunk strength in artificial grammar learning. , 1997 .

[112]  Janet L. McDonald,et al.  Properties of Phonological Markers That Affect the Acquisition of Gender-Like Subclasses☆☆☆★ , 1998 .

[113]  L. Osterhout,et al.  Morphological analysis in sentence processing: An ERP study , 2003 .

[114]  L. L. Elliott,et al.  Verbal auditory closure and the speech perception in noise (SPIN) Test. , 1995, Journal of speech and hearing research.

[115]  H. Neville,et al.  Maturational Constraints on Functional Specializations for Language Processing: ERP and Behavioral Evidence in Bilingual Speakers , 1996, Journal of Cognitive Neuroscience.

[116]  Colin M. Brown,et al.  The syntactic positive shift (sps) as an erp measure of syntactic processing , 1993 .

[117]  J. Saffran Constraints on Statistical Language Learning , 2002 .

[118]  E. Kaan,et al.  Electrophysiological evidence for serial sentence processing: a comparison between non-preferred and ungrammatical continuations. , 2003, Brain research. Cognitive brain research.

[119]  R. Gómez,et al.  Infant artificial language learning and language acquisition , 2000, Trends in Cognitive Sciences.

[120]  Aniruddh D. Patel,et al.  Processing Syntactic Relations in Language and Music: An Event-Related Potential Study , 1998, Journal of Cognitive Neuroscience.

[121]  Z. Dienes,et al.  Rule learning by seven-month-old infants and neural networks , 1999 .

[122]  Simon Kirby,et al.  Biological Foundations and Origin of Syntax , 2009 .

[123]  Y. Niv,et al.  Dialogues on prediction errors , 2008, Trends in Cognitive Sciences.

[124]  A. Friederici,et al.  Event-related brain potentials during natural speech processing: effects of semantic, morphological and syntactic violations. , 1993, Brain research. Cognitive brain research.

[125]  Ellen F. Lau,et al.  The role of structural prediction in rapid syntactic analysis , 2006, Brain and Language.

[126]  Peter Ford Dominey,et al.  COGNITIVE NEUROSCIENCE: Dissociable ERP profiles for processing rules vs instances in a cognitive sequencing task , 2000 .

[127]  N. Chater,et al.  Transfer in artificial grammar learning : A reevaluation , 1996 .

[128]  D. Shanks,et al.  Two mechanisms in implicit artificial grammar learning? Comment on Meulemans and Van der Linden (1997). , 1999 .

[129]  R. C. Oldfield THE ASSESSMENT AND ANALYSIS OF HANDEDNESS , 1971 .

[130]  Manuel Carreiras,et al.  Grammatical Gender and Number Agreement in Spanish: An ERP Comparison , 2005, Journal of Cognitive Neuroscience.

[131]  Michael A. Stadler,et al.  Statistical structure and implicit serial learning. , 1992 .

[132]  Axel Mecklinger,et al.  Error and Deviance Processing in Implicit and Explicit Sequence Learning , 2008, Journal of Cognitive Neuroscience.

[133]  Frank Rösler,et al.  5. Representation and Learning of Structure in Perceptuo-Motor Event-Sequences , 1999 .

[134]  M. Kutas,et al.  Expect the Unexpected: Event-related Brain Response to Morphosyntactic Violations , 1998 .

[135]  Jutta L. Mueller,et al.  Native and Nonnative Speakers' Processing of a Miniature Version of Japanese as Revealed by ERPs , 2005, Journal of Cognitive Neuroscience.

[136]  M. Garrett,et al.  Syntactically Based Sentence Processing Classes: Evidence from Event-Related Brain Potentials , 1991, Journal of Cognitive Neuroscience.

[137]  T. Gunter,et al.  The communicative style of a speaker can affect language comprehension? ERP evidence from the comprehension of irony , 2010, Brain Research.

[138]  E. Gibson,et al.  The P600 as an index of syntactic integration difficulty , 2000 .

[139]  Kaan Edith Fundamental Syntactic Phenomena and Their Putative Relation to the Brain , 2009 .

[140]  Peder J. Johnson,et al.  Assessing implicit learning with indirect tests: Determining what is learned about sequence structure. , 1994 .

[141]  G. Mulder,et al.  When syntax meets semantics. , 1997, Psychophysiology.

[142]  Axel Cleeremans,et al.  Implicit learning: news from the front , 1998, Trends in Cognitive Sciences.

[143]  R. Aslin,et al.  Statistical learning in a serial reaction time task: access to separable statistical cues by individual learners. , 2001, Journal of experimental psychology. General.

[144]  R. Gómez,et al.  Sensitivity to word order cues by normal and language/learning disabled adults. , 2002, Journal of communication disorders.

[145]  S. Coulson,et al.  Hemispheric asymmetries and joke comprehension , 2005, Neuropsychologia.

[146]  P. Hagoort,et al.  A superficial resemblance does not necessarily mean you are part of the family : Counterarguments to Coulson, King and Kutas (1998) in the P600/SPS-P300 debate , 1999 .

[147]  C. Petten,et al.  Conceptual integration and metaphor: An event-related potential study , 2002, Memory & cognition.

[148]  Patricia K. Kuhl,et al.  Grammatical Processing without Semantics? An Event-related Brain Potential Study of Preschoolers using Jabberwocky Sentences , 2007, Journal of Cognitive Neuroscience.

[149]  Sarah C. Creel,et al.  Distant melodies: statistical learning of nonadjacent dependencies in tone sequences. , 2004, Journal of experimental psychology. Learning, memory, and cognition.

[150]  J. Bruce Tomblin,et al.  Procedural Learning in Adolescents With and Without Specific Language Impairment , 2007 .

[151]  E. Newport,et al.  Computation of Conditional Probability Statistics by 8-Month-Old Infants , 1998 .