The role of left inferior frontal gyrus in explicit and implicit semantic processing

Using event-related functional MRI, we examined the involvement of the left inferior frontal gyrus (LIFG) in explicit and implicit semantic processing of Chinese sentences. During scanning, Chinese readers read individually presented normal sentences with a contextually expected or unexpected target noun and were asked to perform an explicit or implicit semantic task (semantic or syntactic violation judgment). The conjunction analysis of the two tasks revealed LIFG as the critical brain region for semantic integration. Further, a cross-task comparison showed more extensive activations for the expectancy effect in the explicit task than in the implicit task in regions including bilateral anterior cingulate cortex/dorsolateral prefrontal cortex, left middle temporal gyrus, and right inferior frontal gyrus. These results indicate that LIFG is responsible for the integration process per se and that other brain regions observed in previous studies using explicit semantic tasks may be due to task-induced generic processes (e.g., cognitive control).

[1]  M. Just,et al.  Brain Activation Modulated by Sentence Comprehension , 1996, Science.

[2]  W. Levelt,et al.  The spatial and temporal signatures of word production components , 2004, Cognition.

[3]  Matthew H. Davis,et al.  The neural mechanisms of speech comprehension: fMRI studies of semantic ambiguity. , 2005, Cerebral cortex.

[4]  Peter Hagoort,et al.  The Processing Nature of the N400: Evidence from Masked Priming , 1993, Journal of Cognitive Neuroscience.

[5]  D. Swinney,et al.  Response of anterior temporal cortex to syntactic and prosodic manipulations during sentence processing , 2005, Human brain mapping.

[6]  J. Cohen,et al.  Dissociating the role of the dorsolateral prefrontal and anterior cingulate cortex in cognitive control. , 2000, Science.

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

[8]  P T Fox,et al.  Brain activation in the processing of Chinese characters and words: A functional MRI study , 2000, Human brain mapping.

[9]  C. Price The anatomy of language: a review of 100 fMRI studies published in 2009 , 2010, Annals of the New York Academy of Sciences.

[10]  Peter Hagoort,et al.  The neurocognition of syntactic processing , 1999 .

[11]  Nick F. Ramsey,et al.  Contribution of the left and right inferior frontal gyrus in recovery from aphasia. A functional MRI study in stroke patients with preserved hemodynamic responsiveness , 2010, NeuroImage.

[12]  Kuniyoshi L Sakai,et al.  An event-related fMRI study of explicit syntactic processing of normal/anomalous sentences in contrast to implicit syntactic processing. , 2003, Cerebral cortex.

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

[14]  Jian Huang,et al.  Involvement of left inferior frontal gyrus in sentence-level semantic integration , 2009, NeuroImage.

[15]  Peter Hagoort,et al.  When Elephants Fly: Differential Sensitivity of Right and Left Inferior Frontal Gyri to Discourse and World Knowledge , 2009, Journal of Cognitive Neuroscience.

[16]  Peter Hagoort,et al.  UvA-DARE (Digital Academic Repository) Unification of speaker and meaning in language comprehension: an fMRI study , 2022 .

[17]  Colin M. Macleod,et al.  Interdimensional interference in the Stroop effect: uncovering the cognitive and neural anatomy of attention , 2000, Trends in Cognitive Sciences.

[18]  Jesper Andersson,et al.  Valid conjunction inference with the minimum statistic , 2005, NeuroImage.

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

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

[21]  Gregory Hickok,et al.  Selective attention to semantic and syntactic features modulates sentence processing networks in anterior temporal cortex. , 2009, Cerebral cortex.

[22]  J. Trueswell,et al.  Cognitive control and parsing: Reexamining the role of Broca’s area in sentence comprehension , 2005, Cognitive, affective & behavioral neuroscience.

[23]  C. Büchel,et al.  Event-Related fMRI Reveals Cortical Sites Involved in Contextual Sentence Integration , 2002, NeuroImage.

[24]  S. Thompson-Schill,et al.  The frontal lobes and the regulation of mental activity , 2005, Current Opinion in Neurobiology.

[25]  Zhu Zu-de,et al.  Left Inferior Frontal Gyrus and Semantic Unification in Sentence Comprehension , 2011 .

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

[27]  Gina R. Kuperberg,et al.  Neuroanatomical distinctions within the semantic system during sentence comprehension: Evidence from functional magnetic resonance imaging , 2008, NeuroImage.

[28]  Peter F. Liddle,et al.  Reading Anomalous Sentences: An Event-Related fMRI Study of Semantic Processing , 2002, NeuroImage.

[29]  Lei Mo,et al.  Brain activation during semantic judgment of Chinese sentences: A functional MRI study , 2005, Human brain mapping.

[30]  P. Fox,et al.  The Neural System Underlying Chinese Logograph Reading , 2001, NeuroImage.

[31]  A. Dale,et al.  Distinct Patterns of Neural Modulation during the Processing of Conceptual and Syntactic Anomalies , 2003, Journal of Cognitive Neuroscience.

[32]  Angela D. Friederici,et al.  Native and non-native reading of sentences: An fMRI experiment , 2006, NeuroImage.

[33]  Stefano Cappa,et al.  Neural differences in the processing of true and false sentences: Insights into the nature of ‘truth’ in language comprehension , 2009, Cortex.

[34]  L. Tan,et al.  Functional anatomy of syntactic and semantic processing in language comprehension , 2002, Human brain mapping.

[35]  James J. Pekar,et al.  Differential components of sentence comprehension: Beyond single word reading and memory , 2006, NeuroImage.

[36]  E. Bullmore,et al.  Common and Distinct Neural Substrates for Pragmatic, Semantic, and Syntactic Processing of Spoken Sentences: An fMRI Study , 2000, Journal of Cognitive Neuroscience.

[37]  P Hagoort,et al.  Semantic, factual, and social language comprehension in adolescents with autism: an FMRI study. , 2010, Cerebral cortex.

[38]  D. Shankweiler,et al.  An Event-related Neuroimaging Study Distinguishing Form and Content in Sentence Processing , 2000, Journal of Cognitive Neuroscience.

[39]  Jonathan D. Cohen,et al.  Conflict monitoring and anterior cingulate cortex: an update , 2004, Trends in Cognitive Sciences.

[40]  Roel M. Willems,et al.  When language meets action: the neural integration of gesture and speech. , 2007, Cerebral cortex.

[41]  Colin M. Brown,et al.  Syntactic Processing in Left Prefrontal Cortex Is Independent of Lexical Meaning , 2001, NeuroImage.

[42]  A Treisman,et al.  Feature analysis in early vision: evidence from search asymmetries. , 1988, Psychological review.

[43]  Suiping Wang,et al.  Broca's area plays a role in syntactic processing during Chinese reading comprehension , 2008, Neuropsychologia.

[44]  Colin Humphries,et al.  Syntactic and Semantic Modulation of Neural Activity during Auditory Sentence Comprehension , 2006, Journal of Cognitive Neuroscience.

[45]  Roel M. Willems,et al.  Seeing and Hearing Meaning: ERP and fMRI Evidence of Word versus Picture Integration into a Sentence Context , 2008, Journal of Cognitive Neuroscience.

[46]  Kara D. Federmeier,et al.  A Rose by Any Other Name: Long-Term Memory Structure and Sentence Processing , 1999 .

[47]  Hoi-Chung Leung,et al.  Frontal activations associated with accessing and evaluating information in working memory: an fMRI study , 2003, NeuroImage.

[48]  J. Fodor The Modularity of mind. An essay on faculty psychology , 1986 .

[49]  Y. Grodzinsky,et al.  The battle for Broca’s region , 2008, Trends in Cognitive Sciences.

[50]  E. Kaan,et al.  Repair, Revision, and Complexity in Syntactic Analysis: An Electrophysiological Differentiation , 2003, Journal of Cognitive Neuroscience.

[51]  James R. Booth,et al.  Specialization of phonological and semantic processing in Chinese word reading , 2006, Brain Research.

[52]  R W Cox,et al.  AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. , 1996, Computers and biomedical research, an international journal.

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

[54]  A. Friederici Towards a neural basis of auditory sentence processing , 2002, Trends in Cognitive Sciences.

[55]  Peter Hagoort,et al.  Neural correlates of language comprehension in autism spectrum disorders: When language conflicts with world knowledge , 2011, Neuropsychologia.

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

[57]  D. Caplan,et al.  Processing of Visually Presented Sentences in Mandarin and English Studied with fMRI , 1999, Neuron.

[58]  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.

[59]  Charles D. Smith,et al.  Dissociation of Automatic and Strategic Lexical-Semantics: Functional Magnetic Resonance Imaging Evidence for Differing Roles of Multiple Frontotemporal Regions , 2006, The Journal of Neuroscience.

[60]  R. Wise,et al.  Temporal lobe regions engaged during normal speech comprehension. , 2003, Brain : a journal of neurology.

[61]  A. Nobre,et al.  The Response of Left Temporal Cortex to Sentences , 2002, Journal of Cognitive Neuroscience.

[62]  M. Jung-Beeman Bilateral brain processes for comprehending natural language , 2005, Trends in Cognitive Sciences.

[63]  M. Torrens Co-Planar Stereotaxic Atlas of the Human Brain—3-Dimensional Proportional System: An Approach to Cerebral Imaging, J. Talairach, P. Tournoux. Georg Thieme Verlag, New York (1988), 122 pp., 130 figs. DM 268 , 1990 .