Context-dependent interpretation of words: Evidence for interactive neural processes

The meaning of a word usually depends on the context in which it occurs. This study investigated the neural mechanisms involved in computing word meanings that change as a function of syntactic context. Current semantic processing theories suggest that word meanings are retrieved from diverse cortical regions storing sensory-motor and other types of semantic information and are further integrated with context in left inferior frontal gyrus (LIFG). Our fMRI data indicate that brain activity in an area sensitive to motion and action semantics--the posterior middle temporal gyrus (PMTG)--is modulated by a word's syntactic context. Ambiguous words such as bowl were presented in minimal disambiguating contexts indicating object (the bowl) or action (to bowl) meanings and were compared to low-ambiguity controls. Ambiguous words elicited more activity than low-ambiguity controls in LIFG and various meaning-related areas such as PMTG. Critically, ambiguous words also elicited more activity in to--contexts than the--contexts in PMTG and LIFG, suggesting that contextual integration strengthened the action meaning in both areas. The pattern of results suggests that the activation of lexical information in PMTG was sensitive to contextual disambiguating information and that processing context-dependent meanings may involve interactions between frontal and posterior areas.

[1]  A. Damasioa,et al.  Neural systems behind word and concept retrieval , 2004 .

[2]  Karl J. Friston,et al.  Action selectivity in parietal and temporal cortex. , 2005, Brain research. Cognitive brain research.

[3]  R. Adolphs,et al.  Neural systems behind word and concept retrieval , 2004, Cognition.

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

[5]  P. Tabossi Effects of context on the immediate interpretation of unambiguous nouns. , 1988 .

[6]  A. Damasio,et al.  Neural Correlates of Naming Actions and of Naming Spatial Relations , 2001, NeuroImage.

[7]  W. Marslen-Wilson,et al.  Making Sense of Semantic Ambiguity: Semantic Competition in Lexical Access , 2002 .

[8]  Sharon L. Thompson-Schill,et al.  Conceptual Representations of Action in the Lateral Temporal Cortex , 2005, Journal of Cognitive Neuroscience.

[9]  E E Smith,et al.  The neural substrate and temporal dynamics of interference effects in working memory as revealed by event-related functional MRI. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[10]  Alfonso Caramazza,et al.  All Talk and No Action: A Transcranial Magnetic Stimulation Study of Motor Cortex Activation during Action Word Production , 2004, Journal of Cognitive Neuroscience.

[11]  Stefano F. Cappa,et al.  Word and picture matching: a PET study of semantic category effects , 1999, Neuropsychologia.

[12]  Alfonso Caramazza,et al.  Dissociating neural correlates for nouns and verbs , 2005, NeuroImage.

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

[14]  J. Haxby,et al.  fMRI Responses to Video and Point-Light Displays of Moving Humans and Manipulable Objects , 2003, Journal of Cognitive Neuroscience.

[15]  M. Pickering,et al.  Architectures and Mechanisms for Language Processing , 1999 .

[16]  Yishi Jin,et al.  Getting a GRIP on Liprins , 2002, Neuron.

[17]  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 .

[18]  Frank R. Abate,et al.  The new Oxford American dictionary , 2001 .

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

[20]  J. Desmond,et al.  The role of left prefrontal cortex in language and memory. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[21]  Matthew A. Lambon Ralph,et al.  Lateralization of ventral and dorsal auditory-language pathways in the human brain , 2005, NeuroImage.

[22]  John Sinclair,et al.  Collins COBUILD English Language Dictionary , 1987 .

[23]  C. Fiebach,et al.  Modulation of Inferotemporal Cortex Activation during Verbal Working Memory Maintenance , 2006, Neuron.

[24]  Marcel Adam Just,et al.  Ambiguity in the brain: what brain imaging reveals about the processing of syntactically ambiguous sentences. , 2003, Journal of experimental psychology. Learning, memory, and cognition.

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

[26]  S. Bookheimer,et al.  Form and Content Dissociating Syntax and Semantics in Sentence Comprehension , 1999, Neuron.

[27]  B. Horwitz,et al.  Functional Interactions of the Inferior Frontal Cortex during the Processing of Words and Word-like Stimuli , 2001, Neuron.

[28]  M. D’Esposito,et al.  A Trial-Based Experimental Design for fMRI , 1997, NeuroImage.

[29]  Abraham Z Snyder,et al.  Reliability of functional localization using fMRI , 2003, NeuroImage.

[30]  Alex Martin,et al.  Representation of Manipulable Man-Made Objects in the Dorsal Stream , 2000, NeuroImage.

[31]  D. Swinney Lexical access during sentence comprehension: (Re)consideration of context effects , 1979 .

[32]  David Badre,et al.  Semantic retrieval, mnemonic control, and prefrontal cortex. , 2002, Behavioral and cognitive neuroscience reviews.

[33]  Morten L. Kringelbach,et al.  Visual word recognition: the first half second , 2004, NeuroImage.

[34]  A. Damasio,et al.  Nouns and verbs are retrieved with differently distributed neural systems. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[35]  Scott T. Grafton,et al.  A distributed left hemisphere network active during planning of everyday tool use skills. , 2004, Cerebral cortex.

[36]  R. Woods Modeling for Intergroup Comparisons of Imaging Data , 1996, NeuroImage.

[37]  C. Fiebach,et al.  The role of left inferior frontal and superior temporal cortex in sentence comprehension: localizing syntactic and semantic processes. , 2003, Cerebral cortex.

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

[39]  Karl J. Friston,et al.  Dynamic Diaschisis: Anatomically Remote and Context-Sensitive Human Brain Lesions , 2001, Journal of Cognitive Neuroscience.

[40]  J. Kable,et al.  Neural Substrates of Action Event Knowledge , 2002, Journal of Cognitive Neuroscience.

[41]  Alan C. Evans,et al.  A new anatomical landmark for reliable identification of human area V5/MT: a quantitative analysis of sulcal patterning. , 2000, Cerebral cortex.

[42]  Olaf B. Paulson,et al.  When Action Turns into Words. Activation of Motor-Based Knowledge during Categorization of Manipulable Objects , 2002, Journal of Cognitive Neuroscience.

[43]  B. Postle,et al.  Using event-related fMRI to assess delay-period activity during performance of spatial and nonspatial working memory tasks. , 2000, Brain research. Brain research protocols.

[44]  I. Johnsrude,et al.  Somatotopic Representation of Action Words in Human Motor and Premotor Cortex , 2004, Neuron.

[45]  H. Lüders,et al.  Functional connectivity in the human language system: a cortico-cortical evoked potential study. , 2004, Brain : a journal of neurology.

[46]  I. Johnsrude,et al.  The problem of functional localization in the human brain , 2002, Nature Reviews Neuroscience.

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

[48]  P. Fletcher,et al.  Neural processing of nouns and verbs: the role of inflectional morphology , 2004, Neuropsychologia.

[49]  S. Thompson-Schill Neuroimaging studies of semantic memory: inferring “how” from “where” , 2003, Neuropsychologia.

[50]  M. Brett,et al.  Actions Speak Louder Than Functions: The Importance of Manipulability and Action in Tool Representation , 2003, Journal of Cognitive Neuroscience.

[51]  Lorraine K. Tyler,et al.  Objects and their actions: evidence for a neurally distributed semantic system , 2003, NeuroImage.

[52]  C. Price,et al.  A functional neuroimaging study of the variables that generate category-specific object processing differences. , 1999, Brain : a journal of neurology.

[53]  David Caplan,et al.  Effects of Syntactic Structure and Propositional Number on Patterns of Regional Cerebral Blood Flow , 1998, Journal of Cognitive Neuroscience.

[54]  Mark S. Seidenberg,et al.  Evidence for Multiple Stages in the Processing of Ambiguous Words in Syntactic Contexts. , 1979 .

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

[56]  U Noppeney,et al.  The neural areas that control the retrieval and selection of semantics , 2004, Neuropsychologia.

[57]  B. Postle,et al.  Prefrontal cortex and the mediation of proactive interference in working memory , 2004, Cognitive, affective & behavioral neuroscience.

[58]  S. Petersen,et al.  PET activation of posterior temporal regions during auditory word presentation and verb generation. , 1996, Cerebral cortex.

[59]  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.

[60]  Scott T. Grafton,et al.  Premotor Cortex Activation during Observation and Naming of Familiar Tools , 1997, NeuroImage.

[61]  Kara D. Federmeier,et al.  Brain responses to nouns, verbs and class-ambiguous words in context. , 2000, Brain : a journal of neurology.

[62]  C Dohle,et al.  Human anterior intraparietal area subserves prehension , 1998, Neurology.

[63]  Jia-Hong Gao,et al.  Neural systems for word meaning modulated by semantic ambiguity , 2004, NeuroImage.

[64]  H. Damasio,et al.  Effects of noun–verb homonymy on the neural correlates of naming concrete entities and actions , 2005, Brain and Language.

[65]  Kathy Rooney,et al.  Encarta world English dictionary , 1999 .

[66]  Anne Cutler,et al.  The access and processing of idiomatic expressions , 1979 .

[67]  Alex Martin,et al.  Semantic memory and the brain: structure and processes , 2001, Current Opinion in Neurobiology.

[68]  A. Friederici,et al.  The brain basis of syntactic processes: functional imaging and lesion studies , 2003, NeuroImage.

[69]  D. Perani,et al.  The neural correlates of verb and noun processing. A PET study. , 1999, Brain : a journal of neurology.

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

[71]  E. Halgren,et al.  Dynamic Statistical Parametric Mapping Combining fMRI and MEG for High-Resolution Imaging of Cortical Activity , 2000, Neuron.

[72]  M. Just,et al.  The neural bases of sentence comprehension: a fMRI examination of syntactic and lexical processing. , 2001, Cerebral cortex.

[73]  C. Price The anatomy of language: contributions from functional neuroimaging , 2000, Journal of anatomy.

[74]  F. Pulvermüller Brain reflections of words and their meaning , 2001, Trends in Cognitive Sciences.

[75]  D. Poeppel,et al.  Dorsal and ventral streams: a framework for understanding aspects of the functional anatomy of language , 2004, Cognition.

[76]  F. Pulvermüller,et al.  Words in the brain's language , 1999, Behavioral and Brain Sciences.

[77]  J. Haxby,et al.  Attribute-based neural substrates in temporal cortex for perceiving and knowing about objects , 1999, Nature Neuroscience.

[78]  J. Haxby,et al.  Parallel Visual Motion Processing Streams for Manipulable Objects and Human Movements , 2002, Neuron.

[79]  François Lazeyras,et al.  Anatomical variability of the lateral frontal lobe surface: implication for intersubject variability in language neuroimaging , 2005, NeuroImage.

[80]  R. Adolphs,et al.  NEURAL CORRELATES OF CONCEPTUAL KNOWLEDGE FOR ACTIONS , 2003, Cognitive neuropsychology.