Nouns and verbs in the intact brain: evidence from event-related potentials and high-frequency cortical responses.

Lesion evidence indicates that words from different lexical categories, such as nouns and verbs, may have different cortical counterparts. In this study, processing of nouns and verbs was investigated in the intact brain using (i) behavioral measures, (ii) stimulus-triggered event-related potentials and (iii) high-frequency electrocortical responses in the gamma band. Nouns and verbs carefully matched for various variables, including word frequency, length, arousal and valence, were presented in a lexical decision task while electrocortical responses were recorded. In addition, information about cognitive processing of these stimuli was obtained using questionnaires and reaction times. As soon as approximately 200 ms after stimulus onset, event-related potentials disclosed electrocortical differences between nouns and verbs over widespread cortical areas. In a later time window, 500-800 ms after stimulus onset, there was a significant difference between high-frequency responses in the 30 Hz range. Difference maps obtained from both event-related potentials and high-frequency responses revealed strong between-category differences of signals recorded above motor and visual cortices. Behavioral data suggest that these different physiological responses are related to semantic associations (motor or visual) elicited by these word groups. Our results are consistent with a neurobiological model of language representation postulating cell assemblies with distinct cortical topographies as biological counterparts of words. Assemblies representing nouns referring to visually perceived objects may include neurons in visual cortices, and assemblies representing action verbs may include additional neurons in motor, premotor and prefrontal cortices. Event-related potentials and high-frequency responses are proposed to indicate two different functional states of cell assemblies: initial full activation ('ignition') and continuous reverberatory activity.

[1]  E. Fetz,et al.  Coherent 25- to 35-Hz oscillations in the sensorimotor cortex of awake behaving monkeys. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[2]  R. Sternbach,et al.  Principles of Psychophysiology , 1966 .

[3]  F. Perrin,et al.  Spherical splines for scalp potential and current density mapping. , 1989, Electroencephalography and clinical neurophysiology.

[4]  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.

[5]  E. Fetz,et al.  Synchronization of neurons during local field potential oscillations in sensorimotor cortex of awake monkeys. , 1996, Journal of neurophysiology.

[6]  J. Pernier,et al.  Gamma‐range Activity Evoked by Coherent Visual Stimuli in Humans , 1995, The European journal of neuroscience.

[7]  S Dehaene,et al.  Electrophysiological evidence for category-specific word processing in the normal human brain. , 1995, Neuroreport.

[8]  Prof. Dr. Valentino Braitenberg,et al.  Anatomy of the Cortex , 1991, Studies of Brain Function.

[9]  T. Allison,et al.  Word recognition in the human inferior temporal lobe , 1994, Nature.

[10]  D. Lehmann,et al.  Verb and Noun Meaning of Homophone Words Activate Different Cortical Generators: A Topographical Study of Evoked Potential Fields , 1979 .

[11]  G. Gainotti,et al.  Evidence for a possible neuroanatomical basis for lexical processing of nouns and verbs , 1994, Neuropsychologia.

[12]  F. D. Silva Neural mechanisms underlying brain waves: from neural membranes to networks. , 1991 .

[13]  J. Fuster Memory in the cerebral cortex : an empirical approach to neural networks in the human and nonhuman primate , 1996 .

[14]  J. Fuster Memory in the cerebral cortex , 1994 .

[15]  Leslie G. Ungerleider,et al.  Discrete Cortical Regions Associated with Knowledge of Color and Knowledge of Action , 1995, Science.

[16]  Werner Lutzenberger,et al.  Words and pseudowords elicit distinct patterns of 30-Hz EEG responses in humans , 1994, Neuroscience Letters.

[17]  B. Hjorth An on-line transformation of EEG scalp potentials into orthogonal source derivations. , 1975, Electroencephalography and clinical neurophysiology.

[18]  A. Caramazza,et al.  Representation of Grammatical Categories of Words in the Brain , 1995, Journal of Cognitive Neuroscience.

[19]  T. Elbert,et al.  Visual stimulation alters local 40-Hz responses in humans: an EEG-study , 1995, Neuroscience Letters.

[20]  N. Birbaumer,et al.  Electrocortical distinction of vocabulary types. , 1995, Electroencephalography and clinical neurophysiology.

[21]  Friedemann Pulvermüller,et al.  A cell assembly model of language , 1991 .

[22]  Gerald P. Berent,et al.  The syntactic priming effect: Evoked response evidence for a prelexical locus , 1986, Brain and Language.

[23]  B. Rockstroh Slow cortical potentials and behavior , 1989 .

[24]  A. Caramazza,et al.  On the Basis for the Agrammatic's Difficulty in Producing Main Verbs , 1984, Cortex.

[25]  A. J. Fridlund,et al.  The Skeletomotor System , 1990 .

[26]  H. Jasper Report of the committee on methods of clinical examination in electroencephalography , 1958 .

[27]  F. Attneave,et al.  The Organization of Behavior: A Neuropsychological Theory , 1949 .

[28]  N Birbaumer,et al.  Spectral responses in the gamma-band: physiological signs of higher cognitive processes? , 1995, Neuroreport.

[29]  J. Kounios,et al.  Concreteness effects in semantic processing: ERP evidence supporting dual-coding theory. , 1994, Journal of experimental psychology. Learning, memory, and cognition.

[30]  N. Birbaumer,et al.  Brain Rhythms of Language: Nouns Versus Verbs , 1996, The European journal of neuroscience.

[31]  Leslie G. Ungerleider,et al.  Neural correlates of category-specific knowledge , 1996, Nature.

[32]  M. Coles Modern mind-brain reading: psychophysiology, physiology, and cognition. , 1989, Psychophysiology.

[33]  A. Aertsen,et al.  Neuronal assemblies , 1989, IEEE Transactions on Biomedical Engineering.

[34]  J. Rohrbaugh,et al.  Improving spatial and temporal resolution in evoked EEG responses using surface Laplacians. , 1993, Electroencephalography and clinical neurophysiology.

[35]  M. Posner,et al.  Positron Emission Tomographic Studies of the Processing of Singe Words , 1989, Journal of Cognitive Neuroscience.

[36]  D. O. Hebb,et al.  The organization of behavior , 1988 .

[37]  H. Neville,et al.  Fractionating language: different neural subsystems with different sensitive periods. , 1992, Cerebral cortex.

[38]  Werner Lutzenberger,et al.  Evoked potentials distinguish between nouns and verbs , 1995, Neuroscience Letters.

[39]  K. K. Tan,et al.  The spatial location of EEG electrodes: locating the best-fitting sphere relative to cortical anatomy. , 1993, Electroencephalography and clinical neurophysiology.

[40]  Olivier Bertrand,et al.  Scalp Current Density Mapping: Value and Estimation from Potential Data , 1987, IEEE Transactions on Biomedical Engineering.

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

[42]  C. Jack,et al.  Determination of 10-20 system electrode locations using magnetic resonance image scanning with markers. , 1993, Electroencephalography and clinical neurophysiology.

[43]  E Donchin,et al.  A new method for off-line removal of ocular artifact. , 1983, Electroencephalography and clinical neurophysiology.

[44]  H. Goodglass,et al.  Specific Semantic Word Categories in Aphasia , 1966 .

[45]  V. Braitenberg Cell Assemblies in the Cerebral Cortex , 1978 .

[46]  F Pulvermüller,et al.  Hebb's concept of cell assemblies and the psychophysiology of word processing. , 1996, Psychophysiology.

[47]  G. McCarthy,et al.  Language-Related ERPs: Scalp Distributions and Modulation by Word Type and Semantic Priming , 1994, Journal of Cognitive Neuroscience.

[48]  A. Aertsen,et al.  Response synchronization in the visual cortex , 1993, Current Opinion in Neurobiology.

[49]  F. Perrin,et al.  Comments on article by Biggins et al. , 1992, Electroencephalography and clinical neurophysiology.

[50]  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.

[51]  Michael Bersick,et al.  Brain potentials elicited by words: word length and frequency predict the latency of an early negativity , 1997, Biological Psychology.

[52]  Karl J. Friston,et al.  Distribution of cortical neural networks involved in word comprehension and word retrieval. , 1991, Brain : a journal of neurology.

[53]  Alfonso Caramazza,et al.  Patterns of dissociation in comprehension and production of nouns and verbs , 1988 .

[54]  Richard S. J. Frackowiak,et al.  Noun and verb retrieval by normal subjects. Studies with PET. , 1996, Brain : a journal of neurology.

[55]  W Singer,et al.  Visual feature integration and the temporal correlation hypothesis. , 1995, Annual review of neuroscience.

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

[57]  R. C. Oldfield The assessment and analysis of handedness: the Edinburgh inventory. , 1971, Neuropsychologia.

[58]  N Birbaumer,et al.  High-frequency cortical responses: do they not exist if they are small? , 1997, Electroencephalography and clinical neurophysiology.

[59]  Jordan Grafman,et al.  Handbook of Neuropsychology , 1991 .

[60]  G Pfurtscheller,et al.  Event-related desynchronization during motor behavior and visual information processing. , 1991, Electroencephalography and clinical neurophysiology. Supplement.

[61]  E. Warrington,et al.  Categories of knowledge. Further fractionations and an attempted integration. , 1987, Brain : a journal of neurology.

[62]  N. Birbaumer,et al.  High-frequency brain activity: Its possible role in attention, perception and language processing , 1997, Progress in Neurobiology.