A Neural Basis for the Retrieval of Words for Actions

Although much has been learned in recent years about the neural basis for retrieving words denoting concrete entities, the neural basis for retrieving words denoting actions remains poorly understood. We addressed this issue by testing two specific anatomical hypotheses. (1) Naming of actions depends not only on the classical implementation structures of the left frontal operculum, but also on mediational structures located in left premotor/prefrontal areas. (2) The neural systems subserving naming of actions and naming of concrete entities are segregated. The study used the lesion method and involved 75 subjects with focal, stable lesions in the left or right hemispheres, whose magnetic resonance data were analysed with a three-dimensional reconstruction method. The experimental tasks were standardised procedures for measuring action and object naming. The findings offered partial support for the hypotheses, in that: (1) lesions related to impaired action naming overlapped maximally in the left frontal operculum and in the underlying white matter and anterior insula; and (2) lesions of the left anterior temporal and inferotemporal regions, which produce impairments in naming of concrete entities, did not cause action naming deficits. A follow-up analysis indicated that action naming impairments, especially when they were disproportionate relative to concrete entity naming impairments, were not only associated with premotor/prefrontal lesions, but also with lesions of the left mesial occipital cortex and of the paraventricular white matter underneath the supramarginal and posterior temporal regions.

[1]  H. Goodglass,et al.  Judgments of Concept Similarity by Normal and Aphasic Subjects: Relation to Naming and Comprehension , 1997, Brain and Language.

[2]  W. Nelson Francis,et al.  FREQUENCY ANALYSIS OF ENGLISH USAGE: LEXICON AND GRAMMAR , 1983 .

[3]  S. Petersen,et al.  Memory's echo: vivid remembering reactivates sensory-specific cortex. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[4]  S. Cappa,et al.  Object and action naming in Alzheimer's disease and frontotemporal dementia , 1998, Neurology.

[5]  Emer M. E. Forde,et al.  Category specific recognition impairments: a review of important case studies and influential theories , 1999 .

[6]  G. Gainotti,et al.  Neuroanatomical correlates of category-specific semantic disorders: a critical survey. , 1995, Memory.

[7]  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.

[8]  Randi C. Martin,et al.  Patterns of Verb Impairment in Aphasia: An Analysis of Four Cases. , 1996, Cognitive neuropsychology.

[9]  M. Schwartz,et al.  DISSOCIATIONS OF LANGUAGE IN APHASIA: IMPLICATIONS FOR NORMAL FUNCTION * , 1976, Annals of the New York Academy of Sciences.

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

[11]  Randall J. Frank,et al.  Explaining category-related effects in the retrieval of conceptual and lexical knowledge for concrete entities: operationalization and analysis of factors , 1997, Neuropsychologia.

[12]  D. Neary,et al.  Progressive language disorder associated with frontal lobe degeneration , 1996 .

[13]  A. Damasio,et al.  The neurobiology of knowledge retrieval , 1999, Behavioral and Brain Sciences.

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

[15]  A. Damasio,et al.  Neural regionalization of knowledge access: preliminary evidence. , 1990, Cold Spring Harbor symposia on quantitative biology.

[16]  J. A. Pruszynski,et al.  Neural correlates , 2023 .

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

[18]  Hanna Damasio,et al.  On the Neurology of Naming , 1997 .

[19]  P. T. Fox,et al.  Positron emission tomographic studies of the cortical anatomy of single-word processing , 1988, Nature.

[20]  Daniel Tranel,et al.  Verb Retrieval in Brain-Damaged Subjects: 1. Analysis of Stimulus, Lexical, and Conceptual Factors , 2000, Brain and Language.

[21]  J. Fiez,et al.  Standardized stimuli and procedures for investigating the retrieval of lexical and conceptual knowledge for actions , 1997, Memory & cognition.

[22]  A. Chatterjee,et al.  Verbs, events and spatial representations , 1999, Neuropsychologia.

[23]  R. Berndt,et al.  Grammatical class and context effects in a case of pure anomia: Implications for models of language production , 1988 .

[24]  Karl J. Friston,et al.  A PET study of word finding , 1991, Neuropsychologia.

[25]  S L Small,et al.  Distributed representations of semantic knowledge in the brain. , 1995, Brain : a journal of neurology.

[26]  S. Petersen,et al.  Practice-related changes in human brain functional anatomy during nonmotor learning. , 1994, Cerebral cortex.

[27]  Martin Arguin,et al.  The Interaction of Object Form and Object M eaning in the Identification Performance of a Patient with Category-specific Visual Agnosia , 1997 .

[28]  A. Damasio,et al.  A neural basis for lexical retrieval , 1996, Nature.

[29]  F. Pulvermüller,et al.  Neurophysiological distinction of verb categories , 2000, Neuroreport.

[30]  Alan C. Evans,et al.  Lateralization of phonetic and pitch discrimination in speech processing. , 1992, Science.

[31]  D. Tranel,et al.  Patterns of dissociation in the processing of verb meanings in brain-damaged subjects , 2001 .

[32]  R Myerson,et al.  Transformational Grammars of Three Agrammatic Patients , 1972, Language and speech.

[33]  M. Grossman,et al.  Not all words are created equal Category‐specific deficits in central nervous system disease , 1998, Neurology.

[34]  Eleanor M. Saffran,et al.  Clues to the functional and neural architecture of word meaning , 2000 .

[35]  Harold Goodglass,et al.  Contrasting cases of Italian agrammatic aphasia without comprehension disorder , 1983, Brain and Language.

[36]  K. Laws,et al.  A ‘normal’ category-specific advantage for naming living things , 1999, Neuropsychologia.

[37]  J. Hodges,et al.  Progressive loss of access to spoken word forms in a case of Alzheimer’s disease , 1991, Proceedings of the Royal Society of London. Series B: Biological Sciences.

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

[39]  M. D’Esposito,et al.  Category-specific difficulty naming with verbs in Alzheimer's disease , 1996, Neurology.

[40]  D. Neary Lesion Analysis in Neuropsychology , 1990 .

[41]  J. G. Snodgrass,et al.  A standardized set of 260 pictures: norms for name agreement, image agreement, familiarity, and visual complexity. , 1980, Journal of experimental psychology. Human learning and memory.

[42]  R. Buckner,et al.  Dissociation of human prefrontal cortical areas across different speech production tasks and gender groups. , 1995, Journal of neurophysiology.

[43]  Stefano F. Cappa,et al.  Pure anomia with spared action naming due to a left temporal lesion , 1994, Neuropsychologia.

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

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

[46]  T. Shallice,et al.  Category specific semantic impairments. , 1998, Brain : a journal of neurology.

[47]  Elizabeth K. Warrington,et al.  Category specificity in an agrammatic patient: The relative impairment of verb retrieval and comprehension , 1985, Neuropsychologia.

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

[49]  A. Caramazza,et al.  Domain-Specific Knowledge Systems in the Brain: The Animate-Inanimate Distinction , 1998, Journal of Cognitive Neuroscience.

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

[51]  Irene P. Kan,et al.  Verb generation in patients with focal frontal lesions: a neuropsychological test of neuroimaging findings. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[52]  G. Miller,et al.  Semantic networks of english , 1991, Cognition.

[53]  Harold Goodglass,et al.  Syntatic constructions used by agrammatic speakers: Comparison with conduction aphasics and normals. , 1994 .

[54]  R. J. Frank,et al.  Reliability of PET activation across statistical methods, subject groups, and sample sizes , 1996, Human brain mapping.

[55]  A. Damasio Time-locked multiregional retroactivation: A systems-level proposal for the neural substrates of recall and recognition , 1989, Cognition.

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

[57]  D. Tranel,et al.  Verb Retrieval in Brain-Damaged Subjects: 2. Analysis of Errors , 2000, Brain and Language.

[58]  W. Krieg Functional Neuroanatomy , 1953, Springer Series in Experimental Entomology.

[59]  R. J. Frank,et al.  Three-dimensional in vivo mapping of brain lesions in humans. , 1992, Archives of neurology.

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

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

[62]  R. Berndt,et al.  Retrieval of nouns and verbs in agrammatism and anomia , 1990, Brain and Language.

[63]  D. Howard,et al.  Why Is a Verb Like an Inanimate Object? Grammatical Category and Semantic Category Deficits , 2000, Brain and Language.

[64]  H. Goodglass,et al.  Deep dysphasia: Analysis of a rare form of repetition disorder , 1990, Brain and Language.

[65]  R. Adolphs,et al.  A Role for Somatosensory Cortices in the Visual Recognition of Emotion as Revealed by Three-Dimensional Lesion Mapping , 2000, The Journal of Neuroscience.

[66]  A. Caramazza,et al.  Lexical organization of nouns and verbs in the brain , 1991, Nature.

[67]  F Pulvermüller,et al.  Nouns and verbs in the intact brain: evidence from event-related potentials and high-frequency cortical responses. , 1999, Cerebral cortex.

[68]  D Klein,et al.  Cerebral organization in bilinguals: a PET study of Chinese-English verb generation. , 1999, Neuroreport.

[69]  K Ugurbil,et al.  Functional magnetic resonance imaging of Broca's area during internal speech. , 1993, Neuroreport.

[70]  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.

[71]  E. Bullmore,et al.  The functional neuroanatomy of implicit-motion perception or ‘representational momentum’ , 2000, Current Biology.

[72]  T. Schweizer,et al.  Musical instrument naming impairments: the crucial exception to the living/nonliving dichotomy in category-specific agnosia. , 2000, Brain and cognition.

[73]  Joel L. Davis,et al.  Large-Scale Neuronal Theories of the Brain , 1994 .

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

[75]  D. Medin,et al.  Family resemblance, conceptual cohesiveness, and category construction , 1987, Cognitive Psychology.

[76]  Richard S. J. Frackowiak,et al.  The anatomy of phonological and semantic processing in normal subjects. , 1992, Brain : a journal of neurology.

[77]  J. Mazziotta,et al.  Mapping motor representations with positron emission tomography , 1994, Nature.

[78]  A. Damasio,et al.  A neural basis for the retrieval of conceptual knowledge , 1997, Neuropsychologia.

[79]  Willem J. M. Levelt,et al.  A theory of lexical access in speech production , 1999, Behavioral and Brain Sciences.

[80]  R. J. Frank,et al.  Brainvox: An Interactive, Multimodal Visualization and Analysis System for Neuroanatomical Imaging , 1997, NeuroImage.

[81]  S. Pinker Learnability and Cognition: The Acquisition of Argument Structure , 1989 .

[82]  B. Gordon Models of Naming , 1997 .

[83]  A. Caramazza How many levels of processing are there in lexical access , 1997 .

[84]  A. Damasio,et al.  Cortical systems for retrieval of concrete knowledge: The convergence zone framework , 1994 .

[85]  G W Humphreys,et al.  Top-down processes in object identification: evidence from experimental psychology, neuropsychology and functional anatomy. , 1997, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.