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.

Although there is an emerging consensus that the anterior temporal lobes (ATLs) are involved in semantic memory, it is currently unclear which specific parts of this region are implicated in semantic representation. Answers to this question are difficult to glean from the existing literature for 3 reasons: 1) lesions of relevant patient groups tend to encompass the whole ATL region; 2) while local effects of repetitive transcranial magnetic stimulation (rTMS) are spatially more specific, only the lateral aspects of the ATL are available to stimulation; and 3) until recently, functional magnetic resonance imaging (fMRI) studies were hindered by technical limitations such as signal distortion and dropout due to magnetic inhomogeneities and also, in some cases, by methodological factors, including a restricted field of view and the choice of baseline contrast for subtraction analysis. By utilizing the same semantic task across semantic dementia, rTMS, and distortion-corrected fMRI in normal participants, we directly compared the results across the 3 methods for the first time. The findings were highly convergent and indicated that crucial regions within the ATL for semantic representation include the anterior inferior temporal gyrus, anterior fusiform gyrus, and the anterior superior temporal sulcus.

[1]  Jelliffe.  Vergleichende Lokalisationslehre der Grosshirnrinde , 1910 .

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

[3]  D. Pandya,et al.  Afferent cortical connections and architectonics of the superior temporal sulcus and surrounding cortex in the rhesus monkey , 1978, Brain Research.

[4]  R. Desimone,et al.  Visual properties of neurons in a polysensory area in superior temporal sulcus of the macaque. , 1981, Journal of neurophysiology.

[5]  R P Lesser,et al.  Basal temporal language area demonstrated by electrical stimulation , 1986, Neurology.

[6]  M. Mesulam,et al.  Neural inputs into the temporopolar cortex of the rhesus monkey , 1987, The Journal of comparative neurology.

[7]  R P Lesser,et al.  Characterization of the basal temporal language area in patients with left temporal lobe epilepsy , 1990, Neurology.

[8]  V E Amassian,et al.  Mapping of motor cortex gyral sites non-invasively by transcranial magnetic stimulation in normal subjects and patients. , 1991, Electroencephalography and clinical neurophysiology. Supplement.

[9]  H. Lüders,et al.  Basal temporal language area. , 1991, Brain : a journal of neurology.

[10]  D. J. Felleman,et al.  Distributed hierarchical processing in the primate cerebral cortex. , 1991, Cerebral cortex.

[11]  E. Rolls.  Neural organization of higher visual functions , 1991, Current Opinion in Neurobiology.

[12]  J. Hodges,et al.  Semantic dementia. Progressive fluent aphasia with temporal lobe atrophy. , 1992 .

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

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

[15]  Richard S. J. Frackowiak,et al.  Functional anatomy of a common semantic system for words and pictures , 1996, Nature.

[16]  John C. Rothwell,et al.  The cortical topography of human swallowing musculature in health and disease , 1996, Nature Medicine.

[17]  Karl J. Friston,et al.  Detecting Activations in PET and fMRI: Levels of Inference and Power , 1996, NeuroImage.

[18]  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.

[19]  M. Mesulam,et al.  From sensation to cognition. , 1998, Brain : a journal of neurology.

[20]  D G von Keyserlingk,et al.  Representation of cortical motor function as revealed by stereotactic transcranial magnetic stimulation. , 1998, Electroencephalography and clinical neurophysiology.

[21]  J. Hodges,et al.  Is a Picture Worth a Thousand Words? Evidence from Concept Definitions by Patients with Semantic Dementia , 1999, Brain and Language.

[22]  J. Desmond,et al.  Functional Specialization for Semantic and Phonological Processing in the Left Inferior Prefrontal Cortex , 1999, NeuroImage.

[23]  J. A. Frost,et al.  Conceptual Processing during the Conscious Resting State: A Functional MRI Study , 1999, Journal of Cognitive Neuroscience.

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

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

[26]  J. Guérit,et al.  The temporal lobe and the limbic system, P. Gloor (Ed.). Oxford University Press (1997), 865 , 2000 .

[27]  E. Stein,et al.  A parametric manipulation of central executive functioning. , 2000, Cerebral cortex.

[28]  Richard S. J. Frackowiak,et al.  A voxel‐based morphometry study of semantic dementia: Relationship between temporal lobe atrophy and semantic memory , 2000, Annals of neurology.

[29]  S. Scott,et al.  Identification of a pathway for intelligible speech in the left temporal lobe. , 2000, Brain : a journal of neurology.

[30]  M N Rossor,et al.  Patterns of temporal lobe atrophy in semantic dementia and Alzheimer's disease , 2001, Annals of neurology.

[31]  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.

[32]  R. Poldrack,et al.  Recovering Meaning Left Prefrontal Cortex Guides Controlled Semantic Retrieval , 2001, Neuron.

[33]  B. Sahakian,et al.  Differing patterns of temporal atrophy in Alzheimer’s disease and semantic dementia , 2001, Neurology.

[34]  N. Tzourio-Mazoyer,et al.  Automated Anatomical Labeling of Activations in SPM Using a Macroscopic Anatomical Parcellation of the MNI MRI Single-Subject Brain , 2002, NeuroImage.

[35]  M. Martinez,et al.  Mapping of the human visual cortex using image-guided transcranial magnetic stimulation. , 2002, Brain research. Brain research protocols.

[36]  J. Hodges,et al.  When objects lose their meaning: What happens to their use? , 2002, Cognitive, affective & behavioral neuroscience.

[37]  C. Price,et al.  A PET Study of Stimulus- and Task-Induced Semantic Processing , 2002, NeuroImage.

[38]  R. Wise,et al.  Temporal lobe regions engaged during normal speech comprehension. , 2003, Brain : a journal of neurology.

[39]  R. Wise,et al.  Language systems in normal and aphasic human subjects: functional imaging studies and inferences from animal studies. , 2003, British medical bulletin.

[40]  M. D’Esposito,et al.  Neural Evidence for Representation-Specific Response Selection , 2003, Journal of Cognitive Neuroscience.

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

[42]  P. Matthews,et al.  Semantic Processing in the Left Inferior Prefrontal Cortex: A Combined Functional Magnetic Resonance Imaging and Transcranial Magnetic Stimulation Study , 2003, Journal of Cognitive Neuroscience.

[43]  Paul J. Laurienti,et al.  An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets , 2003, NeuroImage.

[44]  M. Mishkin,et al.  Functional Mapping of the Primate Auditory System , 2003, Science.

[45]  T. Rogers,et al.  A duck with four legs: Investigating the structure of conceptual knowledge using picture drawing in semantic dementia , 2003, Cognitive neuropsychology.

[46]  E. Rolls,et al.  A Neurodynamical cortical model of visual attention and invariant object recognition , 2004, Vision Research.

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

[48]  D. Neary,et al.  Knowledge of famous faces and names in semantic dementia. , 2004, Brain : a journal of neurology.

[49]  Simona Luzzi,et al.  Semantic memory is an amodal, dynamic system: Evidence from the interaction of naming and object use in semantic dementia , 2004, Cognitive neuropsychology.

[50]  S. Scott,et al.  Retrieving meaning after temporal lobe infarction: The role of the basal language area , 2004, Annals of neurology.

[51]  Norbert Schuff,et al.  Deformation tensor morphometry of semantic dementia with quantitative validation , 2004, NeuroImage.

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

[53]  R. Bowtell,et al.  Correction of spatial distortion in EPI due to inhomogeneous static magnetic fields using the reversed gradient method , 2004, Journal of magnetic resonance imaging : JMRI.

[54]  James L. McClelland,et al.  Semantic Cognition: A Parallel Distributed Processing Approach , 2004 .

[55]  A. Wagner,et al.  Domain-general and domain-sensitive prefrontal mechanisms for recollecting events and detecting novelty. , 2005, Cerebral cortex.

[56]  John Duncan,et al.  Attentional functions of parietal and frontal cortex. , 2005, Cerebral cortex.

[57]  H. Shibasaki,et al.  Neural mechanisms underlying the processing of Chinese words: An fMRI study , 2005, Neuroscience Research.

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

[59]  M. Catani,et al.  The rises and falls of disconnection syndromes. , 2005, Brain : a journal of neurology.

[60]  Nikolaus Weiskopf,et al.  Optimal EPI parameters for reduction of susceptibility-induced BOLD sensitivity losses: A whole-brain analysis at 3 T and 1.5 T , 2006, NeuroImage.

[61]  Gary W. Thickbroom,et al.  Differential activation of frontal lobe areas by lexical and semantic language tasks: A functional magnetic resonance imaging study , 2006, Journal of Clinical Neuroscience.

[62]  S. Scott,et al.  Converging Language Streams in the Human Temporal Lobe , 2006, The Journal of Neuroscience.

[63]  Tim D. Fryer,et al.  Declarative memory impairments in Alzheimer's disease and semantic dementia , 2006, NeuroImage.

[64]  István Ulbert,et al.  Processing stages underlying word recognition in the anteroventral temporal lobe , 2006, NeuroImage.

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

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

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

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

[69]  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.

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

[71]  D. Neary,et al.  Distinct patterns of olfactory impairment in Alzheimer's disease, semantic dementia, frontotemporal dementia, and corticobasal degeneration , 2007, Neuropsychologia.

[72]  E. Jefferies,et al.  Refractory effects in stroke aphasia: A consequence of poor semantic control , 2007, Neuropsychologia.

[73]  Pascale Piolino,et al.  Anatomical and functional alterations in semantic dementia: A voxel-based MRI and PET study , 2007, Neurobiology of Aging.

[74]  M. L. Lambon Ralph,et al.  Generalization and Differentiation in Semantic Memory , 2008, Annals of the New York Academy of Sciences.

[75]  Rainer Goebel,et al.  Functional MRI investigation of verbal selection mechanisms in lateral prefrontal cortex , 2008, NeuroImage.

[76]  G. Kreiman,et al.  Timing, Timing, Timing: Fast Decoding of Object Information from Intracranial Field Potentials in Human Visual Cortex , 2009, Neuron.

[77]  M. L. Lambon Ralph,et al.  Conceptual knowledge is underpinned by the temporal pole bilaterally: convergent evidence from rTMS. , 2009, Cerebral cortex.

[78]  John Duncan,et al.  Evidence for long-range feedback in target detection: Detection of semantic targets modulates activity in early visual areas , 2009, Neuropsychologia.

[79]  N. Stanietsky,et al.  The interaction of TIGIT with PVR and PVRL2 inhibits human NK cell cytotoxicity , 2009, Proceedings of the National Academy of Sciences.

[80]  J. Rauschecker,et al.  Maps and streams in the auditory cortex: nonhuman primates illuminate human speech processing , 2009, Nature Neuroscience.

[81]  Roy W Jones,et al.  Comprehension of concrete and abstract words in semantic dementia. , 2009, Neuropsychology.

[82]  Song-Lin Ding,et al.  Parcellation of human temporal polar cortex: A combined analysis of multiple cytoarchitectonic, chemoarchitectonic, and pathological markers , 2009, The Journal of comparative neurology.

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

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

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

[86]  Jean-Luc Anton,et al.  Region of interest analysis using an SPM toolbox , 2010 .

[87]  M. A. Lambon Ralph,et al.  The inferior, anterior temporal lobes and semantic memory clarified: Novel evidence from distortion-corrected fMRI , 2010, Neuropsychologia.

[88]  J. Warren,et al.  Flavour processing in semantic dementia , 2010, Cortex.

[89]  Ingrid R. Olson,et al.  Social cognition and the anterior temporal lobes , 2010, NeuroImage.

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

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