The function of the left anterior temporal pole: evidence from acute stroke and infarct volume

The role of the anterior temporal lobes in cognition and language has been much debated in the literature over the last few years. Most prevailing theories argue for an important role of the anterior temporal lobe as a semantic hub or a place for the representation of unique entities such as proper names of peoples and places. Lately, a few studies have investigated the role of the most anterior part of the left anterior temporal lobe, the left temporal pole in particular, and argued that the left anterior temporal pole is the area responsible for mapping meaning on to sound through evidence from tasks such as object naming. However, another recent study indicates that bilateral anterior temporal damage is required to cause a clinically significant semantic impairment. In the present study, we tested these hypotheses by evaluating patients with acute stroke before reorganization of structure–function relationships. We compared a group of 20 patients with acute stroke with anterior temporal pole damage to a group of 28 without anterior temporal pole damage matched for infarct volume. We calculated the average percent error in auditory comprehension and naming tasks as a function of infarct volume using a non-parametric regression method. We found that infarct volume was the only predictive variable in the production of semantic errors in both auditory comprehension and object naming tasks. This finding favours the hypothesis that left unilateral anterior temporal pole lesions, even acutely, are unlikely to cause significant deficits in mapping meaning to sound by themselves, although they contribute to networks underlying both naming and comprehension of objects. Therefore, the anterior temporal lobe may be a semantic hub for object meaning, but its role must be represented bilaterally and perhaps redundantly.

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

[2]  Uta Noppeney,et al.  Temporal lobe lesions and semantic impairment: a comparison of herpes simplex virus encephalitis and semantic dementia. , 2006, Brain : a journal of neurology.

[3]  D. Tranel Impaired naming of unique landmarks is associated with left temporal polar damage. , 2006, Neuropsychology.

[4]  W. K. Simmons,et al.  The anterior temporal lobes and the functional architecture of semantic memory , 2009, Journal of the International Neuropsychological Society.

[5]  S. Cappa,et al.  Action and object naming in frontotemporal dementia, progressive supranuclear palsy, and corticobasal degeneration. , 2006, Neuropsychology.

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

[7]  Peter B Barker,et al.  Regions of neural dysfunction associated with impaired naming of actions and objects in acute stroke , 2002, Cognitive neuropsychology.

[8]  D. Pandya,et al.  Distinct Parietal and Temporal Pathways to the Homologues of Broca's Area in the Monkey , 2009, PLoS biology.

[9]  B. Miller,et al.  Classification of primary progressive aphasia and its variants , 2011, Neurology.

[10]  Elizabeth Jefferies,et al.  Deregulated Semantic Cognition Follows Prefrontal and Temporo-parietal Damage: Evidence from the Impact of Task Constraint on Nonverbal Object Use , 2011, Journal of Cognitive Neuroscience.

[11]  R. Adolphs,et al.  Neural systems behind word and concept retrieval , 2004, Cognition.

[12]  A. Caramazza,et al.  Where Do Semantic Errors Come From? , 1990, Cortex.

[13]  M. Petrides,et al.  Left mid‐ventrolateral prefrontal cortex: underlying principles of function , 2008, The European journal of neuroscience.

[14]  A. Hillis,et al.  Deterioration of naming nouns versus verbs in primary progressive aphasia , 2004, Annals of neurology.

[15]  A. Kertesz The Western Aphasia Battery , 1982 .

[16]  E. Warrington Quarterly Journal of Experimental Psychology the Selective Impairment of Semantic Memory the Selective Impairment of Semantic Memory , 2022 .

[17]  J. Hodges,et al.  Generating ‘tiger’ as an animal name or a word beginning with T: differences in brain activation , 1996, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[18]  Robert J. Zatorre,et al.  Bilingual brain organization: A functional magnetic resonance adaptation study , 2006, NeuroImage.

[19]  S. Kiebel,et al.  Training-induced brain plasticity in aphasia. , 1999, Brain : a journal of neurology.

[20]  Angela R Laird,et al.  Meta‐analyses of object naming: Effect of baseline , 2005, Human brain mapping.

[21]  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.

[22]  D. Pandya,et al.  Association fiber pathways to the frontal cortex from the superior temporal region in the rhesus monkey , 1988, The Journal of comparative neurology.

[23]  T. Shallice,et al.  Category specific semantic impairments , 1984 .

[24]  A. Hillis,et al.  Neural regions essential for distinct cognitive processes underlying picture naming. , 2007, Brain : a journal of neurology.

[25]  C. Price,et al.  Right anterior superior temporal activation predicts auditory sentence comprehension following aphasic stroke. , 2005, Brain : a journal of neurology.

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

[27]  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.

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

[29]  Peter B Barker,et al.  Restoring Cerebral Blood Flow Reveals Neural Regions Critical for Naming , 2006, The Journal of Neuroscience.

[30]  T. Rogers,et al.  Neural basis of category-specific semantic deficits for living things: evidence from semantic dementia, HSVE and a neural network model. , 2006, Brain : a journal of neurology.

[31]  M. Petrides Broca’s Area in the Human and the Nonhuman Primate Brain , 2006 .

[32]  Alfonso Caramazza,et al.  Modality-Specific Deterioration in Naming Verbs in Nonfluent Primary Progressive Aphasia , 2002, Journal of Cognitive Neuroscience.

[33]  S. Thompson-Schill,et al.  The frontal lobes and the regulation of mental activity , 2005, Current Opinion in Neurobiology.

[34]  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.

[35]  D. Tranel,et al.  Behavioral patterns and lesion sites associated with impaired processing of lexical and conceptual knowledge of actions , 2012, Cortex.

[36]  R. Wise,et al.  Listening to narrative speech after aphasic stroke: the role of the left anterior temporal lobe. , 2006, Cerebral cortex.

[37]  A R Damasio,et al.  A Neural Basis for the Retrieval of Words for Actions , 2001, Cognitive neuropsychology.

[38]  L. Tyler,et al.  Unitary vs multiple semantics: PET studies of word and picture processing , 2004, Brain and Language.

[39]  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.

[40]  Q. Lib,et al.  Nonparametric estimation of regression functions with both categorical and continuous data , 2004 .

[41]  M. Petrides,et al.  Efferent association pathways originating in the caudal prefrontal cortex in the macaque monkey , 2006, The Journal of comparative neurology.

[42]  Nathalie Tzourio-Mazoyer,et al.  New insights into the anatomo-functional connectivity of the semantic system: a study using cortico-subcortical electrostimulations. , 2005, Brain : a journal of neurology.

[43]  K. Heilman,et al.  The Significance of Body Part as Tool Errors in Limb Apraxia , 1997, Brain and Cognition.

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

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

[46]  Geoff J M Parker,et al.  Distortion correction for diffusion‐weighted MRI tractography and fMRI in the temporal lobes , 2010, Human brain mapping.

[47]  Anne L. Foundas,et al.  Anomia: Case studies with lesion localization , 1998 .

[48]  J. Ulatowski,et al.  Reperfusion of Specific Brain Regions by Raising Blood Pressure Restores Selective Language Functions in Subacute Stroke , 2001, Brain and Language.

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

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

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

[52]  J. Hodges,et al.  Kissing and dancing—a test to distinguish the lexical and conceptual contributions to noun/verb and action/object dissociation. Preliminary results in patients with frontotemporal dementia , 2003, Journal of Neurolinguistics.

[53]  M. Weiner,et al.  Cognition and anatomy in three variants of primary progressive aphasia , 2004, Annals of neurology.

[54]  Jennifer S. W. Campbell,et al.  Dissociating the Human Language Pathways with High Angular Resolution Diffusion Fiber Tractography , 2008, The Journal of Neuroscience.

[55]  I. Olson,et al.  The Enigmatic temporal pole: a review of findings on social and emotional processing. , 2007, Brain : a journal of neurology.

[56]  D. Pandya,et al.  Comparative cytoarchitectonic analysis of the human and the macaque ventrolateral prefrontal cortex and corticocortical connection patterns in the monkey , 2002, The European journal of neuroscience.

[57]  A. Caramazza,et al.  The role of the left anterior temporal lobe in language processing revisited: Evidence from an individual with ATL resection , 2011, Cortex.

[58]  Alfonso Caramazza,et al.  Selective impairment of semantics in lexical processing , 1990 .

[59]  M. Schwartz,et al.  Dissociations of language function in dementia: A case study , 1979, Brain and Language.

[60]  A. Hillis,et al.  Naming and comprehension in primary progressive aphasia: The influence of grammatical word class , 2006 .

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

[62]  Julia Thorn,et al.  Severity of Hypoperfusion in Distinct Brain Regions Predicts Severity of Hemispatial Neglect in Different Reference Frames , 2009, Stroke.

[63]  Valerie A. Carr,et al.  Spatiotemporal Dynamics of Modality-Specific and Supramodal Word Processing , 2003, Neuron.

[64]  P. Hoffman,et al.  Ventrolateral Prefrontal Cortex Plays an Executive Regulation Role in Comprehension of Abstract Words: Convergent Neuropsychological and Repetitive TMS Evidence , 2010, The Journal of Neuroscience.

[65]  Jennifer T. Crinion,et al.  Anterior temporal lobe connectivity correlates with functional outcome after aphasic stroke , 2009, Brain : a journal of neurology.

[66]  J. Gee,et al.  Neural representation of verb meaning: An fMRI study , 2002, Human brain mapping.

[67]  J R Hodges,et al.  Selective impairment of verb processing associated with pathological changes in Brodmann areas 44 and 45 in the motor neurone disease-dementia-aphasia syndrome. , 2001, Brain : a journal of neurology.

[68]  Peggy Gatignol,et al.  The role of dominant premotor cortex in language: a study using intraoperative functional mapping in awake patients , 2003, NeuroImage.

[69]  Melissa Newhart,et al.  Neural Networks Essential for Naming and Word Comprehension , 2007, Cognitive and behavioral neurology : official journal of the Society for Behavioral and Cognitive Neurology.

[70]  D. Neary,et al.  Semantic dementia: a form of circumscribed cerebral atrophy , 1995 .

[71]  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.

[72]  A. Hillis,et al.  Hypoperfusion of Wernicke's area predicts severity of semantic deficit in acute stroke , 2001, Annals of neurology.

[73]  H. White,et al.  Maximum Likelihood and the Bootstrap for Nonlinear Dynamic Models , 2000 .

[74]  Lauren L. Cloutman,et al.  Where (in the brain) do semantic errors come from? , 2009, Cortex.

[75]  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.

[76]  M. L. Lambon Ralph,et al.  The role of the anterior temporal lobes in the comprehension of concrete and abstract words: rTMS evidence , 2009, Cortex.

[77]  Kurt E. Weaver,et al.  Mapping anterior temporal lobe language areas with fMRI: A multicenter normative study , 2011, NeuroImage.

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

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

[80]  K. Amunts,et al.  Broca's region , 2006 .

[81]  Michael Petrides,et al.  The Mid-ventrolateral Prefrontal Cortex and Active Mnemonic Retrieval , 2002, Neurobiology of Learning and Memory.

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

[83]  Daniel Y. Kimberg,et al.  Support for anterior temporal involvement in semantic error production in aphasia: New evidence from VLSM , 2011, Brain and Language.

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

[85]  Karalyn Patterson,et al.  Taking both sides: do unilateral anterior temporal lobe lesions disrupt semantic memory? , 2010, Brain : a journal of neurology.