Neuroanatomical dissociation for taxonomic and thematic knowledge in the human brain

It is thought that semantic memory represents taxonomic information differently from thematic information. This study investigated the neural basis for the taxonomic-thematic distinction in a unique way. We gathered picture-naming errors from 86 individuals with poststroke language impairment (aphasia). Error rates were determined separately for taxonomic errors (“pear” in response to apple) and thematic errors (“worm” in response to apple), and their shared variance was regressed out of each measure. With the segmented lesions normalized to a common template, we carried out voxel-based lesion-symptom mapping on each error type separately. We found that taxonomic errors localized to the left anterior temporal lobe and thematic errors localized to the left temporoparietal junction. This is an indication that the contribution of these regions to semantic memory cleaves along taxonomic-thematic lines. Our findings show that a distinction long recognized in the psychological sciences is grounded in the structure and function of the human brain.

[1]  N. Geschwind.  Disconnexion syndromes in animals and man. I. , 1965, Brain : a journal of neurology.

[2]  K. Nelson,et al.  Making sense : the acquisition of shared meaning , 1985 .

[3]  Glyn W. Humphreys,et al.  Perseverant responding in speeded naming of pictures: It's in the links. , 1991 .

[4]  Myrna F. Schwartz,et al.  The Philadelphia Naming Test: Scoring and Rationale , 1996 .

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

[6]  G. Dell,et al.  Lexical access in aphasic and nonaphasic speakers. , 1997, Psychological review.

[7]  G. Dell,et al.  Models of Impaired Lexical Access in Speech Production , 2000 .

[8]  J. Hodges,et al.  Non-verbal semantic impairment in semantic dementia , 2000, Neuropsychologia.

[9]  G. Murphy,et al.  Thematic relations in adults' concepts. , 2001, Journal of experimental psychology. General.

[10]  James L. McClelland,et al.  No Right to Speak? The Relationship between Object Naming and Semantic Impairment:Neuropsychological Evidence and a Computational Model , 2001, Journal of Cognitive Neuroscience.

[11]  A. Damasio,et al.  A role for left temporal pole in the retrieval of words for unique entities , 2001, Human brain mapping.

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

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

[14]  Thomas E. Nichols,et al.  Thresholding of Statistical Maps in Functional Neuroimaging Using the False Discovery Rate , 2002, NeuroImage.

[15]  F. Dick,et al.  Voxel-based lesion–symptom mapping , 2003, Nature Neuroscience.

[16]  James L. McClelland,et al.  Structure and deterioration of semantic memory: a neuropsychological and computational investigation. , 2004, Psychological review.

[17]  A. Meyer,et al.  Refractory effects in picture naming as assessed in a semantic blocking paradigm , 2005, The Quarterly journal of experimental psychology. A, Human experimental psychology.

[18]  John Whyte,et al.  A patient registry for cognitive rehabilitation research: a strategy for balancing patients' privacy rights with researchers' need for access. , 2005, Archives of physical medicine and rehabilitation.

[19]  Emmanuel A Stamatakis,et al.  The Anatomy of Object Processing: The Role of Anteromedial Temporal Cortex , 2005, The Quarterly journal of experimental psychology. B, Comparative and physiological psychology.

[20]  G. Dell,et al.  A Case-Series Test of the Interactive Two-Step Model of Lexical Access: Evidence from Picture Naming. , 2006 .

[21]  M. L. Lambon Ralph,et al.  Semantic impairment in stroke aphasia versus semantic dementia: a case-series comparison. , 2006, Brain : a journal of neurology.

[22]  T. Rogers,et al.  Anterior temporal cortex and semantic memory: Reconciling findings from neuropsychology and functional imaging , 2006, Cognitive, affective & behavioral neuroscience.

[23]  Anjan Chatterjee,et al.  The Functional Neuroanatomy of Thematic Role and Locative Relational Knowledge , 2007, Journal of Cognitive Neuroscience.

[24]  Daniel Y. Kimberg,et al.  Power in Voxel-based Lesion-Symptom Mapping , 2007, Journal of Cognitive Neuroscience.

[25]  R. Schubotz.  Prediction of external events with our motor system: towards a new framework , 2007, Trends in Cognitive Sciences.

[26]  Nina F. Dronkers,et al.  Neural correlates of arithmetic and language comprehension: A common substrate? , 2007, Neuropsychologia.

[27]  T. Rogers,et al.  Where do you know what you know? The representation of semantic knowledge in the human brain , 2007, Nature Reviews Neuroscience.

[28]  Alissa Melinger,et al.  When bees hamper the production of honey: lexical interference from associates in speech production. , 2007, Journal of experimental psychology. Learning, memory, and cognition.

[29]  Chris Rorden,et al.  Improving Lesion-Symptom Mapping , 2007, Journal of Cognitive Neuroscience.

[30]  David Rudrauf,et al.  Thresholding lesion overlap difference maps: Application to category-related naming and recognition deficits , 2008, NeuroImage.

[31]  Uta Noppeney,et al.  The neural systems of tool and action semantics: A perspective from functional imaging , 2008, Journal of Physiology-Paris.

[32]  M. L. Ralph,et al.  Mimicking aphasic semantic errors in normal speech production: Evidence from a novel experimental paradigm , 2008, Brain and Language.

[33]  Anjan Chatterjee,et al.  Patient Registries in Cognitive Neuroscience Research: Advantages, Challenges, and Practical Advice , 2008, Journal of Cognitive Neuroscience.

[34]  Tilo Kircher,et al.  Categorical and thematic knowledge representation in the brain: Neural correlates of taxonomic and thematic conceptual relations , 2008, Neuropsychologia.

[35]  Karalyn Patterson,et al.  Anomia: A doubly typical signature of semantic dementia , 2008, Neuropsychologia.

[36]  Lawrence W Barsalou,et al.  Simulation, situated conceptualization, and prediction , 2009, Philosophical Transactions of the Royal Society B: Biological Sciences.

[37]  Sandra Weintraub,et al.  Neurology of anomia in the semantic variant of primary progressive aphasia. , 2009, Brain : a journal of neurology.

[38]  Monica Baciu,et al.  The sensory-motor specificity of taxonomic and thematic conceptual relations: A behavioral and fMRI study , 2009, NeuroImage.

[39]  Grant M. Walker,et al.  Anterior temporal involvement in semantic word retrieval: voxel-based lesion-symptom mapping evidence from aphasia. , 2009, Brain : a journal of neurology.

[40]  Mary Hare,et al.  Activating event knowledge , 2009, Cognition.

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

[42]  Scott T. Grafton.  Embodied Cognition and the Simulation of Action to Understand Others , 2009, Annals of the New York Academy of Sciences.

[43]  Richard J. Binney,et al.  The ventral and inferolateral aspects of the anterior temporal lobe are crucial in semantic memory: evidence from a novel direct comparison of distortion-corrected fMRI, rTMS, and semantic dementia. , 2010, Cerebral cortex.

[44]  L. Buxbaum,et al.  Action knowledge, visuomotor activation, and embodiment in the two action systems , 2010, Annals of the New York Academy of Sciences.

[45]  A behavioral and anatomical analysis of associative semantic errors in picture naming , 2010 .

[46]  Laurel J Buxbaum,et al.  Critical brain regions for action recognition: lesion symptom mapping in left hemisphere stroke. , 2010, Brain : a journal of neurology.

[47]  Elizabeth Jefferies,et al.  Elucidating the Nature of Deregulated Semantic Cognition in Semantic Aphasia: Evidence for the Roles of Prefrontal and Temporo-parietal Cortices , 2010, Journal of Cognitive Neuroscience.

[48]  Z. Estes,et al.  Thematic thinking : the apprehension and consequences of thematic relations , 2011 .