Neural dynamics of semantic composition

Significance The rapid comprehension of speech is a remarkable but poorly understood human capacity. Central to this process is the integration of the meaning of each word, as it is heard, into the listener’s interpretation of the utterance. Here we focus on the real-time flow of neural activity that underpins this combinatorial process, using multivariate pattern analysis and computational semantic models to discover the contextual constraints that are constructed as each word is heard, and to determine how these constraints guide the interpretation of future words in the utterance. This combination of methods reveals a continuous information flow across the left-hemisphere language system, strongly constraining the immediate activation of word meanings and providing a neural substrate for seamless real-time speech comprehension. Human speech comprehension is remarkable for its immediacy and rapidity. The listener interprets an incrementally delivered auditory input, millisecond by millisecond as it is heard, in terms of complex multilevel representations of relevant linguistic and nonlinguistic knowledge. Central to this process are the neural computations involved in semantic combination, whereby the meanings of words are combined into more complex representations, as in the combination of a verb and its following direct object (DO) noun (e.g., “eat the apple”). These combinatorial processes form the backbone for incremental interpretation, enabling listeners to integrate the meaning of each word as it is heard into their dynamic interpretation of the current utterance. Focusing on the verb-DO noun relationship in simple spoken sentences, we applied multivariate pattern analysis and computational semantic modeling to source-localized electro/magnetoencephalographic data to map out the specific representational constraints that are constructed as each word is heard, and to determine how these constraints guide the interpretation of subsequent words in the utterance. Comparing context-independent semantic models of the DO noun with contextually constrained noun models reflecting the semantic properties of the preceding verb, we found that only the contextually constrained model showed a significant fit to the brain data. Pattern-based measures of directed connectivity across the left hemisphere language network revealed a continuous information flow among temporal, inferior frontal, and inferior parietal regions, underpinning the verb’s modification of the DO noun’s activated semantics. These results provide a plausible neural substrate for seamless real-time incremental interpretation on the observed millisecond time scales.

[1]  Radoslaw Martin Cichy,et al.  Multivariate pattern analysis for MEG: A comparison of dissimilarity measures , 2018, NeuroImage.

[2]  Nikolaus Kriegeskorte,et al.  Frontiers in Systems Neuroscience Systems Neuroscience , 2022 .

[3]  G. Murphy,et al.  Feature Availability in Conceptual Combination , 1992 .

[4]  W Tecumseh Fitch,et al.  Preface to the Special Issue on the Biology and Evolution of Language , 2017, Psychonomic bulletin & review.

[5]  L. Tyler,et al.  Understanding What We See: How We Derive Meaning From Vision , 2015, Trends in Cognitive Sciences.

[6]  P. Hagoort On Broca, brain, and binding: a new framework , 2005, Trends in Cognitive Sciences.

[7]  L K Tyler,et al.  Is gating an on-line task? Evidence from naming latency data , 1985, Perception & psychophysics.

[8]  Jeffrey L. Elman,et al.  A novel integrated MEG and EEG analysis method for dipolar sources , 2007, NeuroImage.

[9]  F Grosjean,et al.  Spoken word recognition processes and the gating paradigm , 1980, Perception & psychophysics.

[10]  Alessandro Lenci,et al.  Distributional Memory: A General Framework for Corpus-Based Semantics , 2010, CL.

[11]  Alexander Borst,et al.  How does Nature Program Neuron Types? , 2008, Front. Neurosci..

[12]  Thomas A. Carlson,et al.  Representational dynamics of object recognition: Feedforward and feedback information flows , 2016, NeuroImage.

[13]  Lawrence W. Barsalou,et al.  Are Automatic Conceptual Cores the Gold Standard of Semantic Processing? The Context-Dependence of Spatial Meaning in Grounded Congruency Effects , 2015, Cogn. Sci..

[14]  Peter Hagoort,et al.  MUC (Memory, Unification, Control) and beyond , 2013, Front. Psychol..

[15]  P. Fletcher,et al.  Selecting among competing alternatives: selection and retrieval in the left inferior frontal gyrus. , 2005, Cerebral cortex.

[16]  R. Ilmoniemi,et al.  Interpreting magnetic fields of the brain: minimum norm estimates , 2006, Medical and Biological Engineering and Computing.

[17]  Peter,et al.  Semantic Unification , 2008 .

[18]  Bernard Mazoyer,et al.  Meta-analyzing left hemisphere language areas: Phonology, semantics, and sentence processing , 2006, NeuroImage.

[19]  G. Miller,et al.  Contextual correlates of semantic similarity , 1991 .

[20]  William W. Graves,et al.  Where is the semantic system? A critical review and meta-analysis of 120 functional neuroimaging studies. , 2009, Cerebral cortex.

[21]  L. Pylkkänen,et al.  Basic linguistic composition recruits the left anterior temporal lobe and left angular gyrus during both listening and reading. , 2013, Cerebral cortex.

[22]  L. Tyler,et al.  Decoding the Cortical Dynamics of Sound-Meaning Mapping , 2017, The Journal of Neuroscience.

[23]  N. Tzourio-Mazoyer,et al.  Automated Anatomical Labeling of Activations in SPM Using a Macroscopic Anatomical Parcellation of the MNI MRI Single-Subject Brain , 2002, NeuroImage.

[24]  Giosuè Baggio,et al.  The balance between memory and unification in semantics: A dynamic account of the N400 , 2011 .

[25]  Angela D. Friederici,et al.  Evolution of the neural language network , 2016, Psychonomic Bulletin & Review.

[26]  Liina Pylkkänen,et al.  Mismatching Meanings in Brain and Behavior , 2008, Lang. Linguistics Compass.

[27]  R. Leahy,et al.  EEG and MEG: forward solutions for inverse methods , 1999, IEEE Transactions on Biomedical Engineering.

[28]  Karl J. Friston,et al.  MEG and EEG data fusion: Simultaneous localisation of face-evoked responses , 2009, NeuroImage.

[29]  J. Elman On the Meaning of Words and Dinosaur Bones: Lexical Knowledge Without a Lexicon , 2009, Cogn. Sci..

[30]  Li Su,et al.  Spatiotemporal Searchlight Representational Similarity Analysis in EMEG Source Space , 2012, 2012 Second International Workshop on Pattern Recognition in NeuroImaging.

[31]  Rsenl A. FaulcoNpR Understanding Noun Phrases , 2005 .

[32]  R. H. Baayen,et al.  The CELEX Lexical Database (CD-ROM) , 1996 .

[33]  W. Marslen-Wilson Functional parallelism in spoken word-recognition , 1987, Cognition.

[34]  D. Poeppel,et al.  The cortical organization of speech processing , 2007, Nature Reviews Neuroscience.

[35]  S. Greenspan,et al.  Semantic flexibility and referential specificity of concrete nouns , 1986 .

[36]  S. Taulu,et al.  Spatiotemporal signal space separation method for rejecting nearby interference in MEG measurements , 2006, Physics in medicine and biology.

[37]  J. Sarvas Basic mathematical and electromagnetic concepts of the biomagnetic inverse problem. , 1987, Physics in medicine and biology.

[38]  L. Pylkkänen,et al.  Semantic composition of sentences word by word: MEG evidence for shared processing of conceptual and logical elements , 2018, Neuropsychologia.

[39]  Billi Randall,et al.  From perception to conception: how meaningful objects are processed over time. , 2013, Cerebral cortex.

[40]  Zellig S. Harris,et al.  Distributional Structure , 1954 .

[41]  Roger B. H. Tootell,et al.  The advantage of combining MEG and EEG: Comparison to fMRI in focally stimulated visual cortex , 2007, NeuroImage.

[42]  Ted Briscoe,et al.  A Large Subcategorization Lexicon for Natural Language Processing Applications , 2006, LREC.

[43]  Michael F. Bonner,et al.  Converging Evidence for the Neuroanatomic Basis of Combinatorial Semantics in the Angular Gyrus , 2015, The Journal of Neuroscience.

[44]  Liina Pylkkänen,et al.  The time-course and spatial distribution of brain activity associated with sentence processing , 2012, NeuroImage.

[45]  Billi Randall,et al.  Balancing Prediction and Sensory Input in Speech Comprehension: The Spatiotemporal Dynamics of Word Recognition in Context , 2018, The Journal of Neuroscience.

[46]  P. Johnson-Laird The mental representation of the meaning of words , 1987, Cognition.

[47]  Liina Pylkkänen,et al.  Simple Composition: A Magnetoencephalography Investigation into the Comprehension of Minimal Linguistic Phrases , 2011, The Journal of Neuroscience.

[48]  Nikolaus Kriegeskorte,et al.  Recurrence is required to capture the representational dynamics of the human visual system , 2019, Proceedings of the National Academy of Sciences.

[49]  Peter Hagoort,et al.  Frequency-specific directed interactions in the human brain network for language , 2017 .

[50]  Randy L Buckner,et al.  Common and dissociable activation patterns associated with controlled semantic and phonological processing: evidence from FMRI adaptation. , 2005, Cerebral cortex.

[51]  James A. Hampton,et al.  Compositionality and Concepts in Linguistics and Psychology , 2017 .

[52]  Michael Wilson,et al.  MRC psycholinguistic database: Machine-usable dictionary, version 2.00 , 1988 .

[53]  Thomas E. Nichols,et al.  Nonparametric permutation tests for functional neuroimaging: A primer with examples , 2002, Human brain mapping.

[54]  John C. Trueswell,et al.  Compositionality and the angular gyrus: A multi-voxel similarity analysis of the semantic composition of nouns and verbs , 2015, Neuropsychologia.

[55]  C. Granger Investigating Causal Relations by Econometric Models and Cross-Spectral Methods , 1969 .

[56]  Peter Hagoort,et al.  How the brain makes sense beyond the processing of single words – An MEG study , 2019, NeuroImage.

[57]  Liina Pylkkänen,et al.  MEG Evidence for Incremental Sentence Composition in the Anterior Temporal Lobe. , 2017, Cognitive science.

[58]  L. Barsalou Cognitively Plausible Theories of Concept Composition , 2017 .

[59]  David M. Blei,et al.  Probabilistic topic models , 2012, Commun. ACM.

[60]  Michael I. Jordan,et al.  Latent Dirichlet Allocation , 2001, J. Mach. Learn. Res..

[61]  Ellen F. Lau,et al.  A cortical network for semantics: (de)constructing the N400 , 2008, Nature Reviews Neuroscience.

[62]  Mary C. Potter,et al.  Understanding noun phrases , 1979 .

[63]  Liina Pylkkänen,et al.  The role of the left anterior temporal lobe in semantic composition vs. semantic memory , 2014, Neuropsychologia.

[64]  L. Garnero,et al.  Combined MEG and EEG source imaging by minimization of mutual information , 1999, IEEE Transactions on Biomedical Engineering.

[65]  R. Poldrack,et al.  Recovering Meaning Left Prefrontal Cortex Guides Controlled Semantic Retrieval , 2001, Neuron.

[66]  A. Friederici,et al.  Differential cortical contribution of syntax and semantics: An fMRI study on two-word phrasal processing , 2017, Cortex.

[67]  M. Farah,et al.  Role of left inferior prefrontal cortex in retrieval of semantic knowledge: a reevaluation. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[68]  Cathy J. Price,et al.  A review and synthesis of the first 20 years of PET and fMRI studies of heard speech, spoken language and reading , 2012, NeuroImage.

[69]  S. Thompson-Schill,et al.  Putting concepts into context , 2016, Psychonomic bulletin & review.

[70]  W. Marslen-Wilson,et al.  Access to word meanings during spoken language comprehension: effects of sentential semantic context. , 1993, Journal of experimental psychology. Learning, memory, and cognition.

[71]  L. Barsalou Context-independent and context-dependent information in concepts , 1982, Memory & cognition.

[72]  A. Friederici The cortical language circuit: from auditory perception to sentence comprehension , 2012, Trends in Cognitive Sciences.

[73]  R. Poldrack,et al.  Dissociable Controlled Retrieval and Generalized Selection Mechanisms in Ventrolateral Prefrontal Cortex , 2005, Neuron.

[74]  C. Granger Investigating causal relations by econometric models and cross-spectral methods , 1969 .

[75]  Colin Humphries,et al.  Time course of semantic processes during sentence comprehension: An fMRI study , 2007, NeuroImage.