Semantic Processing in the Anterior Temporal Lobes: A Meta-analysis of the Functional Neuroimaging Literature

The role of the anterior temporal lobes (ATLs) in semantic cognition is not clear from the current literature. Semantic dementia patients show a progressive and a specific semantic impairment, following bilateral atrophy of the ATLs. Neuroimaging studies of healthy participants, however, do not consistently show ATL activation during semantic tasks. Consequently, several influential theories of semantic memory do not ascribe a central role to the ATLs. We conducted a meta-analysis of 164 functional neuroimaging studies of semantic processing to investigate factors that might contribute to the inconsistency in previous results. Four factors influenced the likelihood of finding ATL activation: (1) the use of PET versus fMRI, reflecting the fact that fMRI but not PET is sensitive to distortion artifacts caused by large variations in magnetic susceptibility in the area of the ATL; (2) a field of view (FOV) of more than 15 cm, thereby ensuring whole-brain coverage; (3) the use of a high baseline task to prevent subtraction of otherwise uncontrolled semantic activation; (4) the inclusion of the ATL as an ROI. The type of stimuli or task did not influence the likelihood of ATL activation, consistent with the view that this region underpins an amodal semantic system. Spoken words, written words, and picture stimuli produced overlapping ATL peaks. On average, these were more inferior for picture-based tasks. We suggest that the specific pattern of ATL activation may be influenced by stimulus type due to variations across this region in the degree of connectivity with modality-specific areas in posterior temporal cortex.

[1]  Guy B. Williams,et al.  The human perirhinal cortex and semantic memory , 2004, The European journal of neuroscience.

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

[3]  Elizabeth Jefferies,et al.  “Pre-semantic” cognition revisited: Critical differences between semantic aphasia and semantic dementia , 2010, Neuropsychologia.

[4]  Argye E. Hillis,et al.  The function of the left anterior temporal pole: evidence from acute stroke and infarct volume , 2011, Brain : a journal of neurology.

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

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

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

[8]  Sophie K Scott,et al.  Going beyond the information given: a neural system supporting semantic interpretation , 2003, NeuroImage.

[9]  Gjm Parker,et al.  A Combined Distortion Corrected Protocol for Diffusion Weighted Tractography and fMRI , 2006 .

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

[11]  J. Desmond,et al.  The role of left prefrontal cortex in language and memory. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[12]  Marcelo L. Berthier,et al.  Unexpected brain-language relationships in aphasia: Evidence from transcortical sensory aphasia associated with frontal lobe lesions , 2001 .

[13]  P. Hoffman,et al.  Reverse concreteness effects are not a typical feature of semantic dementia: evidence for the hub-and-spoke model of conceptual representation. , 2011, Cerebral cortex.

[14]  Vincent Schmithorst,et al.  Simultaneous correction of ghost and geometric distortion artifacts in EPI using a multiecho reference scan , 2001, IEEE Transactions on Medical Imaging.

[15]  M Lowrie Neuroscience in medicine, 2nd edn , 2004 .

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

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

[18]  J. Haxby,et al.  Attribute-based neural substrates in temporal cortex for perceiving and knowing about objects , 1999, Nature Neuroscience.

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

[20]  J. Rodd,et al.  Processing Objects at Different Levels of Specificity , 2004, Journal of Cognitive Neuroscience.

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

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

[23]  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.

[24]  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.

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

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

[27]  C. Price,et al.  A functional neuroimaging study of the variables that generate category-specific object processing differences. , 1999, Brain : a journal of neurology.

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

[29]  P A Bandettini,et al.  Effects of stimulus rate on signal response during functional magnetic resonance imaging of auditory cortex. , 1994, Brain research. Cognitive brain research.

[30]  Kevin R. Smith,et al.  Word length modulates neural activity in auditory cortex during covert object naming , 2003, Neuroreport.

[31]  Matthew A. Lambon Ralph,et al.  Semantic Diversity Accounts for the “Missing” Word Frequency Effect in Stroke Aphasia: Insights Using a Novel Method to Quantify Contextual Variability in Meaning , 2011, Journal of Cognitive Neuroscience.

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

[33]  Jason B. Mattingley,et al.  Activation patterns during action observation are modulated by context in mirror system areas , 2012, NeuroImage.

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

[35]  Ana Raposo,et al.  The hierarchical organization of semantic memory: Executive function in the processing of superordinate concepts , 2012, NeuroImage.

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

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

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

[39]  Angela M. Uecker,et al.  ALE meta‐analysis: Controlling the false discovery rate and performing statistical contrasts , 2005, Human brain mapping.

[40]  Steven Graham,et al.  Word frequency and subsequent memory effects studied using event-related fMRI , 2003, NeuroImage.

[41]  M. Kiefer,et al.  Conceptual representations in mind and brain: Theoretical developments, current evidence and future directions , 2012, Cortex.

[42]  Stephen E. Rose,et al.  The structure and connectivity of semantic memory in the healthy older adult brain , 2011, NeuroImage.

[43]  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.

[44]  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.

[45]  Matthew A. Lambon Ralph,et al.  Differential Contributions of Bilateral Ventral Anterior Temporal Lobe and Left Anterior Superior Temporal Gyrus to Semantic Processes , 2011, Journal of Cognitive Neuroscience.

[46]  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.

[47]  Arne Nagels,et al.  Neural correlates of rhyming vs. lexical and semantic fluency , 2011, Brain Research.

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

[49]  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.

[50]  Stefano F Cappa,et al.  Imaging studies of semantic memory , 2008, Current opinion in neurology.

[51]  Jeffrey R. Binder,et al.  Functional MRI is a valid noninvasive alternative to Wada testing , 2011, Epilepsy & Behavior.

[52]  Giuseppe Sartori,et al.  Semantic relevance explains category effects in medial fusiform gyri , 2006, NeuroImage.

[53]  Matthew A. Lambon Ralph,et al.  Wernicke's aphasia reflects a combination of acoustic-phonological and semantic control deficits: A case-series comparison of Wernicke's aphasia, semantic dementia and semantic aphasia , 2012, Neuropsychologia.

[54]  Neil M. Borden 3D Angiographic Atlas of Neurovascular Anatomy and Pathology , 2006 .

[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]  S. Scott,et al.  The neuroanatomical and functional organization of speech perception , 2003, Trends in Neurosciences.

[57]  Manuel M. Vindiola,et al.  Patterns of brain reorganization subsequent to left fusiform damage: fMRI evidence from visual processing of words and pseudowords, faces and objects , 2011, NeuroImage.

[58]  Hanna Damasio,et al.  Naming the Same Entities from Visual or from Auditory Stimulation Engages Similar Regions of Left Inferotemporal Cortices , 2005, Journal of Cognitive Neuroscience.

[59]  M. Kubicki,et al.  Connectivity among semantic associates: An fMRI study of semantic priming , 2006, Brain and Language.

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

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

[62]  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.

[63]  Matthew A. Lambon Ralph,et al.  At the Edge of Semantic Space: The Breakdown of Coherent Concepts in Semantic Dementia Is Constrained by Typicality and Severity but Not Modality , 2011, Journal of Cognitive Neuroscience.

[64]  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.

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

[66]  C. Metzler,et al.  Effects of left frontal lesions on the selection of context-appropriate meanings. , 2001, Neuropsychology.

[67]  Karl Herholz,et al.  Staging of the cognitive decline in Alzheimer's disease: insights from a detailed neuropsychological investigation of mild cognitive impairment and mild Alzheimer's disease , 2011, International journal of geriatric psychiatry.

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

[69]  E. Denkova,et al.  Neural correlates of remembering/knowing famous people: An event-related fMRI study , 2006, Neuropsychologia.

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

[71]  K. Patterson,et al.  Deficits of knowledge vs . executive control in semantic cognition : Insights from cued naming , 2008 .

[72]  Kayoko Okada,et al.  Identification of lexical–phonological networks in the superior temporal sulcus using functional magnetic resonance imaging , 2006, Neuroreport.

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

[74]  L S Illis,et al.  Herpes simplex encephalitis: long term magnetic resonance imaging and neuropsychological profile. , 1994, Journal of neurology, neurosurgery, and psychiatry.

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

[76]  Giosuè Baggio,et al.  The balance between memory and unification in semantics: A dynamic account of the N400 , 2011 .

[77]  Richard N. A. Henson,et al.  Perception and Conception: Temporal Lobe Activity during Complex Discriminations of Familiar and Novel Faces and Objects , 2011, Journal of Cognitive Neuroscience.

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

[79]  Karl J. Friston,et al.  Hearing and saying. The functional neuro-anatomy of auditory word processing. , 1996, Brain : a journal of neurology.

[80]  Maria Luisa Gorno-Tempini,et al.  Distinct neural substrates for semantic knowledge and naming in the temporoparietal network. , 2012, Cerebral cortex.

[81]  G. Gainotti Different patterns of famous people recognition disorders in patients with right and left anterior temporal lesions: A systematic review , 2007, Neuropsychologia.

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

[83]  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.

[84]  Michele T. Diaz,et al.  The Influence of Context on Hemispheric Recruitment during Metaphor Processing , 2011, Journal of Cognitive Neuroscience.

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

[86]  Ingrid R. Olson,et al.  Sensory and semantic category subdivisions within the anterior temporal lobes , 2011, Neuropsychologia.

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

[88]  Stephen M. Smith,et al.  Functional MRI : an introduction to methods , 2002 .

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

[90]  S. Thompson-Schill Neuroimaging studies of semantic memory: inferring “how” from “where” , 2003, Neuropsychologia.

[91]  Alex Martin,et al.  Experience-dependent modulation of category-related cortical activity. , 2002, Cerebral cortex.

[92]  Timothy T Rogers,et al.  Semantic memory is impaired in patients with unilateral anterior temporal lobe resection for temporal lobe epilepsy. , 2012, Brain : a journal of neurology.

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

[94]  P. Conn Neuroscience in Medicine , 2003, Humana Press.

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

[96]  Maxime Guye,et al.  Basal functional connectivity within the anterior temporal network is associated with performance on declarative memory tasks , 2011, NeuroImage.

[97]  Gene E. Alexander,et al.  Written Language Impairments in Primary Progressive Aphasia: A Reflection of Damage to Central Semantic and Phonological Processes , 2012, Journal of Cognitive Neuroscience.

[98]  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.

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

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

[101]  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.