Posterior middle temporal gyrus is involved in verbal and non-verbal semantic cognition: Evidence from rTMS

Background: Left posterior middle temporal gyrus (pMTG) is reliably activated in functional neuroimaging studies of semantic processing and is frequently damaged in patients with comprehension impairments following stroke (e.g., Wernicke's aphasia). Its precise function remains elusive, however. Some researchers take the view that pMTG is a multimodal semantic area, involved in verbal and non-verbal semantic cognition. Others ascribe a lexical-semantic function to the region, positing that it is involved in mapping between phonology and conceptual knowledge. Aims: We investigated whether pMTG was involved in non-verbal as well as verbal semantic cognition by using rTMS to induce temporary, focal “virtual lesions” to this region in healthy participants. Methods & Procedures: Participants completed picture and word versions of a semantic association test before and after receiving 10 minutes of 1-Hz offline rTMS to left pMTG. They also completed a difficulty-matched visual decision task on scrambled pictures. An occipital lobe control site was stimulated in a separate session. Outcomes & Results: TMS slowed responses to word and picture versions of the test to an equal degree. There was no slowing on a non-semantic visual-matching task, or following TMS to the control site. Conclusions: These results indicate that pMTG is involved in both verbal and non-verbal semantic cognition. This region could be key to understanding the multimodal semantic deficits often observed following stroke.

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

[2]  Ferath Kherif,et al.  Automatic Top-Down Processing Explains Common Left Occipito-Temporal Responses to Visual Words and Objects , 2010, Cerebral cortex.

[3]  D. Plaut Graded modality-specific specialisation in semantics: A computational account of optic aphasia , 2002, Cognitive neuropsychology.

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

[5]  Paul M Matthews,et al.  The Role of the Posterior Fusiform Gyrus in Reading , 2006, Journal of Cognitive Neuroscience.

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

[7]  E. Jefferies,et al.  Anterior temporal lobes mediate semantic representation: Mimicking semantic dementia by using rTMS in normal participants , 2007, Proceedings of the National Academy of Sciences.

[8]  Daniel Bub,et al.  On the Status of Object Concepts in Aphasia , 1997, Brain and Language.

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

[10]  T. Shallice,et al.  Naming manipulable objects: Anatomy of a category specific effect in left temporal tumours , 2010, Neuropsychologia.

[11]  Matthew H. Davis,et al.  Susceptibility-Induced Loss of Signal: Comparing PET and fMRI on a Semantic Task , 2000, NeuroImage.

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

[13]  A. Turken,et al.  The Neural Architecture of the Language Comprehension Network: Converging Evidence from Lesion and Connectivity Analyses , 2011, Front. Syst. Neurosci..

[14]  C Caltagirone,et al.  Drawing objects from memory in aphasia. , 1983, Brain : a journal of neurology.

[15]  S. Kosslyn,et al.  The role of area 17 in visual imagery: convergent evidence from PET and rTMS. , 1999, Science.

[16]  B. Mesquita,et al.  Adjustment to Chronic Diseases and Terminal Illness Health Psychology : Psychological Adjustment to Chronic Disease , 2006 .

[17]  D. Poeppel,et al.  The cortical organization of speech processing , 2007, Nature Reviews Neuroscience.

[18]  R. Poldrack,et al.  Dissociable Controlled Retrieval and Generalized Selection Mechanisms in Ventrolateral Prefrontal Cortex , 2005, Neuron.

[19]  M. L. Lambon Ralph,et al.  The anterior temporal lobe semantic hub is a part of the language neural network: selective disruption of irregular past tense verbs by rTMS. , 2010, Cerebral cortex.

[20]  Mbleton,et al.  The 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 .

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

[22]  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.

[23]  Bernard Mazoyer,et al.  Meta-analyzing left hemisphere language areas: Phonology, semantics, and sentence processing , 2006, NeuroImage.

[24]  Alan Cowey,et al.  Transcranial magnetic stimulation and cognitive neuroscience , 2000, Nature Reviews Neuroscience.

[25]  Elizabeth Jefferies,et al.  Heterogeneity of the Left Temporal Lobe in Semantic Representation and Control: Priming Multiple versus Single Meanings of Ambiguous Words , 2010, Cerebral cortex.

[26]  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.

[27]  E. Renzi,et al.  Impairment in associating colour to form, concomitant with aphasia. , 1972, Brain : a journal of neurology.

[28]  M. Seghier,et al.  The left superior temporal gyrus is a shared substrate for auditory short-term memory and speech comprehension: evidence from 210 patients with stroke , 2009, Brain : a journal of neurology.

[29]  Emily J. Mayberry,et al.  Coherent concepts are computed in the anterior temporal lobes , 2010, Proceedings of the National Academy of Sciences.

[30]  David Badre,et al.  Left ventrolateral prefrontal cortex and the cognitive control of memory , 2007, Neuropsychologia.

[31]  M. L. Lambon Ralph,et al.  Category-Specific versus Category-General Semantic Impairment Induced by Transcranial Magnetic Stimulation , 2010, Current Biology.

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

[33]  Stephanie Kelter,et al.  Analytical competence and language impairment in aphasia , 1980, Brain and Language.

[34]  M. Masson,et al.  Using confidence intervals in within-subject designs , 1994, Psychonomic bulletin & review.

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

[36]  A. Nobre,et al.  Dissociating Linguistic Processes in the Left Inferior Frontal Cortex with Transcranial Magnetic Stimulation , 2022 .

[37]  R J Wise,et al.  Separate neural subsystems within 'Wernicke's area'. , 2001, Brain : a journal of neurology.

[38]  Elizabeth Jefferies,et al.  Semantic Processing in the Anterior Temporal Lobes: A Meta-analysis of the Functional Neuroimaging Literature , 2010, Journal of Cognitive Neuroscience.

[39]  R. Cabeza,et al.  Imaging Cognition II: An Empirical Review of 275 PET and fMRI Studies , 2000, Journal of Cognitive Neuroscience.

[40]  F. Dick,et al.  Neural resources for processing language and environmental sounds: evidence from aphasia. , 2003, Brain : a journal of neurology.

[41]  M. L. Lambon Ralph,et al.  The Neural Organization of Semantic Control: TMS Evidence for a Distributed Network in Left Inferior Frontal and Posterior Middle Temporal Gyrus , 2010, Cerebral cortex.

[42]  M. Rushworth,et al.  A primer of magnetic stimulation as a tool for neuropsychology. , 1999, Neuropsychologia.

[43]  Guy B. Williams,et al.  What the left and right anterior fusiform gyri tell us about semantic memory. , 2010, Brain : a journal of neurology.

[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]  Charles D. Smith,et al.  Dissociation of Automatic and Strategic Lexical-Semantics: Functional Magnetic Resonance Imaging Evidence for Differing Roles of Multiple Frontotemporal Regions , 2006, The Journal of Neuroscience.

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

[47]  E. Jefferies,et al.  Amodal semantic representations depend on both anterior temporal lobes: Evidence from repetitive transcranial magnetic stimulation , 2010, Neuropsychologia.

[48]  Á. Pascual-Leone,et al.  Enhanced visual spatial attention ipsilateral to rTMS-induced 'virtual lesions' of human parietal cortex , 2001, Nature Neuroscience.

[49]  Karl J. Friston,et al.  Degeneracy and cognitive anatomy , 2002, Trends in Cognitive Sciences.

[50]  S. Thompson-Schill,et al.  Semantic adaptation and competition during word comprehension. , 2008, Cerebral cortex.

[51]  N. Dronkers,et al.  Lesion analysis of the brain areas involved in language comprehension , 2004, Cognition.

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

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

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

[55]  Elizabeth Jefferies,et al.  Different impairments of semantic cognition in semantic dementia and semantic aphasia: evidence from the non-verbal domain. , 2009, Brain : a journal of neurology.

[56]  Karl J. Friston,et al.  Anatomic Constraints on Cognitive Theories of Category Specificity , 2002, NeuroImage.

[57]  W. Levelt,et al.  The spatial and temporal signatures of word production components , 2004, Cognition.

[58]  Harold Goodglass,et al.  Interaction between phonological and semantic factors in auditory comprehension , 1981, Neuropsychologia.