Gamma Oscillatory Activity Related to Language Prediction

Using magnetoencephalography, the current study examined gamma activity associated with language prediction. Participants read high- and low-constraining sentences in which the final word of the sentence was either expected or unexpected. Although no consistent gamma power difference induced by the sentence-final words was found between the expected and unexpected conditions, the correlation of gamma power during the prediction and activation intervals of the sentence-final words was larger when the presented words matched with the prediction compared with when the prediction was violated or when no prediction was available. This suggests that gamma magnitude relates to the match between predicted and perceived words. Moreover, the expected words induced activity with a slower gamma frequency compared with that induced by unexpected words. Overall, the current study establishes that prediction is related to gamma power correlations and a slowing of the gamma frequency.

[1]  A. Borst Seeing smells: imaging olfactory learning in bees , 1999, Nature Neuroscience.

[2]  E. Maris,et al.  Prior Expectation Mediates Neural Adaptation to Repeated Sounds in the Auditory Cortex: An MEG Study , 2011, The Journal of Neuroscience.

[3]  Gina R Kuperberg,et al.  What do we mean by prediction in language comprehension? , 2016, Language, cognition and neuroscience.

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

[5]  Elkan G. Akyürek,et al.  Dynamic hidden states underlying working memory guided behaviour , 2017, Nature Neuroscience.

[6]  M. Bastiaansen,et al.  A predictive coding framework for rapid neural dynamics during sentence-level language comprehension , 2015, Cortex.

[7]  J. Schoffelen,et al.  Beta oscillations relate to the N400m during language comprehension , 2012, Human brain mapping.

[8]  S. Hanslmayr,et al.  Temporal-Pattern Similarity Analysis Reveals the Beneficial and Detrimental Effects of Context Reinstatement on Human Memory , 2015, The Journal of Neuroscience.

[9]  Marcel Bastiaansen,et al.  Integration or Predictability? A Further Specification of the Functional Role of Gamma Oscillations in Language Comprehension , 2012, Front. Psychology.

[10]  A. Clark Whatever next? Predictive brains, situated agents, and the future of cognitive science. , 2013, The Behavioral and brain sciences.

[11]  P. Mitra,et al.  Analysis of dynamic brain imaging data. , 1998, Biophysical journal.

[12]  E. Maris,et al.  Beta oscillations reflect memory and motor aspects of spoken word production , 2015, Human brain mapping.

[13]  B. Staresina,et al.  Gamma Power Reductions Accompany Stimulus-Specific Representations of Dynamic Events , 2015, Current Biology.

[14]  L. Colgin,et al.  Slow and Fast Gamma Rhythms Coordinate Different Spatial Coding Modes in Hippocampal Place Cells , 2014, Neuron.

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

[16]  R. Oostenveld,et al.  Tactile Spatial Attention Enhances Gamma-Band Activity in Somatosensory Cortex and Reduces Low-Frequency Activity in Parieto-Occipital Areas , 2006, The Journal of Neuroscience.

[17]  P. Hagoort,et al.  Integration of Word Meaning and World Knowledge in Language Comprehension , 2004, Science.

[18]  Walter Paulus,et al.  Noninvasively Decoding the Contents of Visual Working Memory in the Human Prefrontal Cortex within High-gamma Oscillatory Patterns , 2012, Journal of Cognitive Neuroscience.

[19]  M. Traxler,et al.  Effects of prediction and contextual support on lexical processing: Prediction takes precedence , 2015, Cognition.

[20]  Ton Dijkstra,et al.  Context-dependent Semantic Processing in the Human Brain: Evidence from Idiom Comprehension , 2013, Journal of Cognitive Neuroscience.

[21]  W. Singer,et al.  Dynamic predictions: Oscillations and synchrony in top–down processing , 2001, Nature Reviews Neuroscience.

[22]  D. Roehm,et al.  The costs of being certain: Brain potential evidence for linguistic preactivation in sentence processing. , 2017, Psychophysiology.

[23]  C. Summerfield,et al.  Expectation in perceptual decision making: neural and computational mechanisms , 2014, Nature Reviews Neuroscience.

[24]  Karl J. Friston What Is Optimal about Motor Control? , 2011, Neuron.

[25]  Kara D. Federmeier,et al.  The N400 as a snapshot of interactive processing: Evidence from regression analyses of orthographic neighbor and lexical associate effects. , 2011, Psychophysiology.

[26]  Thomas R Knösche,et al.  Tangential derivative mapping of axial MEG applied to event-related desynchronization research , 2000, Clinical Neurophysiology.

[27]  Kara D. Federmeier,et al.  Alpha and theta band dynamics related to sentential constraint and word expectancy , 2017, Language, cognition and neuroscience.

[28]  Karl J. Friston,et al.  LFP and oscillations—what do they tell us? , 2015, Current Opinion in Neurobiology.

[29]  Katherine A. DeLong,et al.  Probabilistic word pre-activation during language comprehension inferred from electrical brain activity , 2005, Nature Neuroscience.

[30]  Robert Oostenveld,et al.  Online and offline tools for head movement compensation in MEG , 2013, NeuroImage.

[31]  P. Fries A mechanism for cognitive dynamics: neuronal communication through neuronal coherence , 2005, Trends in Cognitive Sciences.

[32]  E. Moser,et al.  Gamma oscillations in the hippocampus. , 2010, Physiology.

[33]  Terrence J. Sejnowski,et al.  The “independent components” of natural scenes are edge filters , 1997, Vision Research.

[34]  Albert Kim,et al.  Rapid Interactions between Lexical Semantic and Word Form Analysis during Word Recognition in Context: Evidence from ERPs , 2012, Journal of Cognitive Neuroscience.

[35]  Luc H. Arnal,et al.  Transitions in neural oscillations reflect prediction errors generated in audiovisual speech , 2011, Nature Neuroscience.

[36]  A. Rodríguez-Fornells,et al.  Electrophysiological correlates of semantic anticipation during speech comprehension , 2017, Neuropsychologia.

[37]  Lucia Melloni,et al.  Brain Oscillations during Spoken Sentence Processing , 2012, Journal of Cognitive Neuroscience.

[38]  Colin M. Brown,et al.  Anticipating upcoming words in discourse: evidence from ERPs and reading times. , 2005, Journal of experimental psychology. Learning, memory, and cognition.

[39]  Friedemann Pulvermüller,et al.  Behavioral / Cognitive Neural Correlates of Semantic Prediction and Resolution in Sentence Processing , 2017 .

[40]  H. Bowman,et al.  The Temporal Signature of Memories: Identification of a General Mechanism for Dynamic Memory Replay in Humans , 2016, PLoS biology.

[41]  Luc H. Arnal,et al.  Cortical oscillations and sensory predictions , 2012, Trends in Cognitive Sciences.

[42]  Suzanne Dikker,et al.  Before the N400: Effects of lexical–semantic violations in visual cortex , 2011, Brain and Language.

[43]  H. Kennedy,et al.  Visual Areas Exert Feedforward and Feedback Influences through Distinct Frequency Channels , 2014, Neuron.

[44]  Alejandro Pérez,et al.  Item parameters dissociate between expectation formats: a regression analysis of time-frequency decomposed EEG data , 2014, Front. Psychol..

[45]  Jack J. Lin,et al.  Direct brain recordings reveal hippocampal rhythm underpinnings of language processing , 2016, Proceedings of the National Academy of Sciences.

[46]  P. Hagoort,et al.  EEG theta and gamma responses to semantic violations in online sentence processing , 2006, Brain and Language.

[47]  Angela D. Friederici,et al.  Prediction Signatures in the Brain: Semantic Pre-Activation during Language Comprehension , 2016, Front. Hum. Neurosci..

[48]  Axel Mecklinger,et al.  Gamma activity in human EEG is related to highspeed memory comparisons during object selective attention , 2001 .

[49]  Alessandro Angrilli,et al.  Gamma EEG activity induced by semantic violation during sentence reading , 2009, Neuroscience Letters.

[50]  J. Martinerie,et al.  The brainweb: Phase synchronization and large-scale integration , 2001, Nature Reviews Neuroscience.

[51]  Lin Wang,et al.  Language Prediction Is Reflected by Coupling between Frontal Gamma and Posterior Alpha Oscillations , 2018, Journal of Cognitive Neuroscience.

[52]  Burkhard Maess,et al.  Memory-matches evoke human gamma-responses , 2004, BMC Neuroscience.

[53]  Suzanne Dikker,et al.  Predicting language: MEG evidence for lexical preactivation , 2013, Brain and Language.

[54]  E. Maris,et al.  Oscillatory brain responses in spoken word production reflect lexical frequency and sentential constraint , 2014, Neuropsychologia.

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

[56]  T. Sejnowski,et al.  Removal of eye activity artifacts from visual event-related potentials in normal and clinical subjects , 2000, Clinical Neurophysiology.

[57]  Eric Halgren,et al.  Neural stages of spoken, written, and signed word processing in beginning second language learners , 2013, Front. Hum. Neurosci..

[58]  Matthias M. Müller,et al.  Selective visual-spatial attention alters induced gamma band responses in the human EEG , 1999, Clinical Neurophysiology.

[59]  O. Jensen,et al.  Cross-frequency coupling between neuronal oscillations , 2007, Trends in Cognitive Sciences.

[60]  O. Bertrand,et al.  Oscillatory gamma activity in humans and its role in object representation , 1999, Trends in Cognitive Sciences.

[61]  Manuel Carreiras,et al.  Long-range neural synchronization supports fast and efficient reading: EEG correlates of processing expected words in sentences , 2013, NeuroImage.

[62]  M. Bastiaansen,et al.  Fast oscillatory dynamics during language comprehension: Unification versus maintenance and prediction? , 2015, Brain and Language.

[63]  R. Oostenveld,et al.  Theta and Gamma Oscillations Predict Encoding and Retrieval of Declarative Memory , 2006, The Journal of Neuroscience.

[64]  T. Hafting,et al.  Frequency of gamma oscillations routes flow of information in the hippocampus , 2009, Nature.

[65]  Kara D. Federmeier,et al.  Thirty years and counting: finding meaning in the N400 component of the event-related brain potential (ERP). , 2011, Annual review of psychology.