Brain activity during automatic semantic priming revealed by event-related functional magnetic resonance imaging

Semantic priming occurs when a subject is faster in recognising a target word when it is preceded by a related word compared to an unrelated word. The effect is attributed to automatic or controlled processing mechanisms elicited by short or long interstimulus intervals (ISIs) between primes and targets. We employed event-related functional magnetic resonance imaging (fMRI) to investigate blood oxygen level dependent (BOLD) responses associated with automatic semantic priming using an experimental design identical to that used in standard behavioural priming tasks. Prime-target semantic strength was manipulated by using lexical ambiguity primes (e.g., bank) and target words related to dominant or subordinate meaning of the ambiguity. Subjects made speeded lexical decisions (word/nonword) on dominant related, subordinate related, and unrelated word pairs presented randomly with a short ISI. The major finding was a pattern of reduced activity in middle temporal and inferior prefrontal regions for dominant versus unrelated and subordinate versus unrelated comparisons, respectively. These findings are consistent with both a dual process model of semantic priming and recent repetition priming data that suggest that reductions in BOLD responses represent neural priming associated with automatic semantic activation and implicate the left middle temporal cortex and inferior prefrontal cortex in more automatic aspects of semantic processing.

[1]  John Hart,et al.  Delineation of single‐word semantic comprehension deficits in aphasia, with anatomical correlation , 1990, Annals of neurology.

[2]  Irene P. Kan,et al.  Effects of Repetition and Competition on Activity in Left Prefrontal Cortex during Word Generation , 1999, Neuron.

[3]  Karl J. Friston,et al.  A unified statistical approach for determining significant signals in images of cerebral activation , 1996, Human brain mapping.

[4]  Karl J. Friston,et al.  How Many Subjects Constitute a Study? , 1999, NeuroImage.

[5]  G. Humphreys,et al.  Basic processes in reading : visual word recognition , 1993 .

[6]  Michael W. L. Chee,et al.  Frequency of Concrete Words Modulates Prefrontal Activation during Semantic Judgments , 2002, NeuroImage.

[7]  T. Shallice,et al.  Neuroimaging evidence for dissociable forms of repetition priming. , 2000, Science.

[8]  Jia Fc,et al.  [Event-related functional magnetic resonance imaging]. , 2001, Sheng li ke xue jin zhan [Progress in physiology].

[9]  Daniel L. Schacter,et al.  On the Relations among Priming, Conscious Recollection, and Intentional Retrieval: Evidence from Neuroimaging Research , 1998, Neurobiology of Learning and Memory.

[10]  R. Schvaneveldt,et al.  Facilitation in recognizing pairs of words: evidence of a dependence between retrieval operations. , 1971, Journal of experimental psychology.

[11]  J. Fiez Phonology, Semantics, and the Role of the Left Inferior Prefrontal Cortex , 2022 .

[12]  Richard S. J. Frackowiak,et al.  Functional anatomy of a common semantic system for words and pictures , 1996, Nature.

[13]  D. Nelson,et al.  The University of South Florida homograph norms , 1980 .

[14]  G. Simpson Lexical ambiguity and its role in models of word recognition. , 1984, Psychological bulletin.

[15]  M. Albert,et al.  The speed of constituent mental operations and its relationship to neuronal representation: An hypothesis , 1991 .

[16]  Stephen M. Rao,et al.  Human Brain Language Areas Identified by Functional Magnetic Resonance Imaging , 1997, The Journal of Neuroscience.

[17]  S. Blumstein,et al.  Semantic Facutation in Aphasia: Effects of Time and Expectancy , 1995, Journal of Cognitive Neuroscience.

[18]  Karl J. Friston,et al.  Event-related fMRI , 1997 .

[19]  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.

[20]  Karl J. Friston,et al.  Analysis of fMRI Time-Series Revisited , 1995, NeuroImage.

[21]  J. Hodges,et al.  Semantic dementia. Progressive fluent aphasia with temporal lobe atrophy. , 1992 .

[22]  Lee Ryan,et al.  Masked word repetition results in increased fMRI signal: a framework for understanding signal changes in priming , 2002, Neuroreport.

[23]  Randy L. Buckner,et al.  Event Related Functional MRI , 1999 .

[24]  G Mulder,et al.  Sentence comprehension and word repetition: a positron emission tomography investigation. , 1999, Psychophysiology.

[25]  P. Dixon,et al.  University of Alberta norms of relative meaning frequency for 566 homographs , 1994, Memory & cognition.

[26]  D. Schacter,et al.  Task-specific repetition priming in left inferior prefrontal cortex. , 2000, Cerebral cortex.

[27]  Curt Burgess,et al.  Activation and selection processes in the recognition of ambiguous words. , 1985 .

[28]  Daniel L. Schacter,et al.  Neuroimaging of priming , 2001 .

[29]  Karl J. Friston,et al.  Spatial registration and normalization of images , 1995 .

[30]  C. Fiebach,et al.  fMRI Evidence for Dual Routes to the Mental Lexicon in Visual Word Recognition , 2002, Journal of Cognitive Neuroscience.

[31]  L. K. Tyler,et al.  Automatic Access to Lexical Semantics in Aphasia: Evidence from Semantic and Associative Priming , 1993, Brain and Language.

[32]  Joel R. Meyer,et al.  Modality independence of word comprehension , 2002, Human brain mapping.

[33]  Allan Collins,et al.  A spreading-activation theory of semantic processing , 1975 .

[34]  H. Kucera,et al.  Computational analysis of present-day American English , 1967 .

[35]  E Halgren,et al.  Cognitive evoked potentials as modulatory processes in human memory formation and retrieval. , 1987, Human neurobiology.

[36]  Karl J. Friston,et al.  Analysis of fMRI Time-Series Revisited—Again , 1995, NeuroImage.

[37]  Stephen M. Smith,et al.  Functional MRI : an introduction to methods , 2002 .

[38]  D. Tank,et al.  Brain magnetic resonance imaging with contrast dependent on blood oxygenation. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[39]  Sheila E. Blumstein,et al.  Semantic processing in aphasia: Evidence from an auditory lexical decision task , 1982, Brain and Language.

[40]  F. Guillem,et al.  Short-and Long-Delay Intracranial ERP Repetition Effects Dissociate Memory Systems in the Human Brain , 1999, Journal of Cognitive Neuroscience.

[41]  Alan C. Evans,et al.  An MRI-Based Probabilistic Atlas of Neuroanatomy , 1994 .

[42]  T. Shallice,et al.  Dual-Process Model in Semantic Priming: A Functional Imaging Perspective , 1999, NeuroImage.

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

[44]  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.

[45]  E. Bullmore,et al.  Brain activation during automatic and controlled processing of semantic relations: a priming experiment using lexical-decision , 2001, Neuropsychologia.

[46]  P. Hagoort Impairments of Lexical-Semantic Processing in Aphasia: Evidence from the Processing of Lexical Ambiguities , 1993, Brain and Language.

[47]  J. H. Neely Semantic priming effects in visual word recognition: A selective review of current findings and theories. , 1991 .

[48]  Harry A. Whitaker,et al.  Brain and Language , 1994 .

[49]  Avishai Henik,et al.  Differential Effects of Semantic and Identity Priming in Patients with Left and Right Hemisphere Lesions , 1993, Journal of Cognitive Neuroscience.

[50]  Karl J. Friston,et al.  Event‐related f MRI , 1997, Human brain mapping.

[51]  M. D’Esposito,et al.  The Variability of Human, BOLD Hemodynamic Responses , 1998, NeuroImage.

[52]  E Zarahn,et al.  Event-related functional MRI: implications for cognitive psychology. , 1999, Psychological bulletin.

[53]  L. K. Tyler,et al.  Automatic Access of Lexical Information in Broca′s Aphasics: Against the Automaticity Hypothesis , 1995, Brain and Language.

[54]  D. Schacter,et al.  Neuroimaging of Priming: New Perspectives on Implicit and Explicit Memory , 2001 .

[55]  O Josephs,et al.  Event-related functional magnetic resonance imaging: modelling, inference and optimization. , 1999, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[56]  A M Dale,et al.  Optimal experimental design for event‐related fMRI , 1999, Human brain mapping.

[57]  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 .

[58]  C. C. Wood,et al.  Event-related potentials, lexical decision and semantic priming. , 1985, Electroencephalography and clinical neurophysiology.

[59]  P. Matthews,et al.  Effective Paradigm Design , 2001 .

[60]  Jemett L. Desmond,et al.  Semantic encoding and retrieval in the left inferior prefrontal cortex: a functional MRI study of task difficulty and process specificity , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[61]  Andrew C Papanicolaou,et al.  Source localization of the N400 response in a sentence-reading paradigm using evoked magnetic fields and magnetic resonance imaging , 1997, Brain Research.

[62]  J. Ashburner,et al.  Nonlinear spatial normalization using basis functions , 1999, Human brain mapping.

[63]  P. Holcomb Automatic and attentional processing: An event-related brain potential analysis of semantic priming , 1988, Brain and Language.

[64]  E. Halgren,et al.  Human medial temporal lobe potentials evoked in memory and language tasks. , 1986, Electroencephalography and clinical neurophysiology.

[65]  Colin M. Brown,et al.  An Event-Related Brain Potential Analysis of Visual Word Priming Effects , 2000, Brain and Language.

[66]  G. McCarthy,et al.  Language-related field potentials in the anterior-medial temporal lobe: II. Effects of word type and semantic priming , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[67]  G I de Zubicaray,et al.  The semantic interference effect in the picture‐word paradigm: An event‐related fMRI study employing overt responses , 2001, Human brain mapping.

[68]  P. Hagoort Semantic Priming in Broca's Aphasics at a Short SOA: No Support for an Automatic Access Deficit , 1997, Brain and Language.