Annals of the New York Academy of Sciences Graded Specialization within and between the Anterior Temporal Lobes

Considerable evidence from different methodologies has identified the anterior temporal lobes (ATLs) as key regions for the representation of semantic knowledge. Research interest is now shifting to investigate the roles of different ATL subregions in semantic representation, with particular emphasis on the functions of the left versus right ATLs. In this review, we provide evidence for graded specializations both between and within the ATLs. We argue (1) that multimodal, pan-category semantic representations are supported jointly by both left and right ATLs, yet (2) that the ATLs are not homogeneous in their function. Instead, subtle functional gradations both between and within the ATLs emerge as a consequence of differential connectivity with primary sensory/motor/limbic regions. This graded specialization account of semantic representation provides a compromise between theories that posit no differences between the functions of the left and right ATLs and those that posit that the left and right ATLs are entirely segregated in function. Evidence for this graded account comes from converging sources, and its benefits have been exemplified in formal computational models. We propose that this graded principle is not only a defining feature of the ATLs but is also a more general neurocomputational principle found throughout the temporal lobes.

[1]  D. Plaut,et al.  Annals of the New York Academy of Sciences a Vision of Graded Hemispheric Specialization , 2022 .

[2]  Richard J. Binney,et al.  Using a combination of fMRI and anterior temporal lobe rTMS to measure intrinsic and induced activation changes across the semantic cognition network , 2015, Neuropsychologia.

[3]  T. Rogers,et al.  Disorders of representation and control in semantic cognition: Effects of familiarity, typicality, and specificity , 2015, Neuropsychologia.

[4]  Claude J. Bajada,et al.  Transport for language south of the Sylvian fissure: The routes and history of the main tracts and stations in the ventral language network , 2015, Cortex.

[5]  Gina F. Humphreys,et al.  Establishing task- and modality-dependent dissociations between the semantic and default mode networks , 2015, Proceedings of the National Academy of Sciences.

[6]  Hugues Duffau,et al.  Stimulation mapping of white matter tracts to study brain functional connectivity , 2015, Nature Reviews Neurology.

[7]  G. Alarcón,et al.  Incidence of functional bi-temporal connections in the human brain in vivo and their relevance to epilepsy surgery , 2015, Cortex.

[8]  Régine Kolinsky,et al.  Illiterate to literate: behavioural and cerebral changes induced by reading acquisition , 2015, Nature Reviews Neuroscience.

[9]  P. Hoffman,et al.  The Roles of Left Versus Right Anterior Temporal Lobes in Conceptual Knowledge: An ALE Meta-analysis of 97 Functional Neuroimaging Studies , 2015, Cerebral cortex.

[10]  Nikos Makris,et al.  Large-scale brain networks of the human left temporal pole: a functional connectivity MRI study. , 2015, Cerebral cortex.

[11]  Richard J. Binney,et al.  Differing contributions of inferior prefrontal and anterior temporal cortex to concrete and abstract conceptual knowledge , 2015, Cortex.

[12]  Rebecca L. Jackson,et al.  The Nature and Neural Correlates of Semantic Association versus Conceptual Similarity , 2015, Cerebral cortex.

[13]  P. Hoffman,et al.  Direct Exploration of the Role of the Ventral Anterior Temporal Lobe in Semantic Memory: Cortical Stimulation and Local Field Potential Evidence From Subdural Grid Electrodes , 2014, Cerebral cortex.

[14]  S. Dehaene,et al.  Anatomical Connections of the Visual Word Form Area , 2014, The Journal of Neuroscience.

[15]  Ingrid R. Olson,et al.  Beyond the FFA: The role of the ventral anterior temporal lobes in face processing , 2014, Neuropsychologia.

[16]  K. Embleton,et al.  A comparison of dual gradient‐echo and spin‐echo fMRI of the inferior temporal lobe , 2014, Human brain mapping.

[17]  F. Hadj-Bouziane,et al.  Selective dissociation between core and extended regions of the face processing network in congenital prosopagnosia. , 2014, Cerebral cortex.

[18]  Guido Gainotti,et al.  Why Are the Right and Left Hemisphere Conceptual Representations Different? , 2014, Behavioural neurology.

[19]  Matthew A. Lambon Ralph,et al.  Neurocognitive insights on conceptual knowledge and its breakdown , 2014, Philosophical Transactions of the Royal Society B: Biological Sciences.

[20]  James L. McClelland,et al.  Why Bilateral Damage Is Worse than Unilateral Damage to the Brain , 2013, Journal of Cognitive Neuroscience.

[21]  Galit Yovel,et al.  The challenge of localizing the anterior temporal face area: A possible solution , 2013, NeuroImage.

[22]  G. Gainotti Laterality effects in normal subjects' recognition of familiar faces, voices and names. Perceptual and representational components , 2013, Neuropsychologia.

[23]  G. Ojemann,et al.  Famous face identification in temporal lobe epilepsy: Support for a multimodal integration model of semantic memory , 2013, Cortex.

[24]  John S. Duncan,et al.  Memory reorganization following anterior temporal lobe resection: a longitudinal functional MRI study , 2013, Brain : a journal of neurology.

[25]  D. Plaut,et al.  Distributed circuits, not circumscribed centers, mediate visual recognition , 2013, Trends in Cognitive Sciences.

[26]  G. Gainotti Is the Right Anterior Temporal Variant of Prosopagnosia a Form of ‘Associative Prosopagnosia’ or a Form of ‘Multimodal Person Recognition Disorder’? , 2013, Neuropsychology Review.

[27]  Lars A. Ross,et al.  Social cognition and the anterior temporal lobes: a review and theoretical framework. , 2013, Social cognitive and affective neuroscience.

[28]  I. Olson,et al.  Anterior temporal face patches: a meta-analysis and empirical study , 2013, Front. Hum. Neurosci..

[29]  A. Caramazza,et al.  Conceptual Object Representations in Human Anterior Temporal Cortex , 2012, The Journal of Neuroscience.

[30]  Matthew A. Lambon Ralph,et al.  Convergent Connectivity and Graded Specialization in the Rostral Human Temporal Lobe as Revealed by Diffusion-Weighted Imaging Probabilistic Tractography , 2012, Journal of Cognitive Neuroscience.

[31]  Steven Z. Rapcsak,et al.  Efficient Visual Object and Word Recognition Relies on High Spatial Frequency Coding in the Left Posterior Fusiform Gyrus: Evidence from a Case-Series of Patients with Ventral Occipito-Temporal Cortex Damage , 2012, Cerebral cortex.

[32]  Elizabeth Jefferies,et al.  Both the Middle Temporal Gyrus and the Ventral Anterior Temporal Area Are Crucial for Multimodal Semantic Processing: Distortion-corrected fMRI Evidence for a Double Gradient of Information Convergence in the Temporal Lobes , 2012, Journal of Cognitive Neuroscience.

[33]  G. Gainotti The format of conceptual representations disrupted in semantic dementia: A position paper , 2012, Cortex.

[34]  Cara L. Wong,et al.  The function of the anterior temporal lobe: A review of the empirical evidence , 2012, Brain Research.

[35]  Christian Vollmar,et al.  Imaging language networks before and after anterior temporal lobe resection: Results of a longitudinal fMRI study , 2012, Epilepsia.

[36]  D. Neary,et al.  Famous People Knowledge and the Right and Left Temporal Lobes , 2011, Behavioural neurology.

[37]  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.

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

[39]  D. Plaut,et al.  Complementary neural representations for faces and words: A computational exploration , 2011, Cognitive neuropsychology.

[40]  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.

[41]  Allan Snyder,et al.  Noninvasive brain stimulation reduces prejudice scores on an implicit association test. , 2011, Neuropsychology.

[42]  M. Walshe,et al.  Atlasing location, asymmetry and inter-subject variability of white matter tracts in the human brain with MR diffusion tractography , 2011, NeuroImage.

[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]  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.

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

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

[48]  Matthew A. Lambon Ralph,et al.  Solving the paradox of the equipotential and modular brain: A neurocomputational model of stroke vs. slow-growing glioma , 2010, Neuropsychologia.

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

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

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

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

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

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

[55]  W. K. Simmons,et al.  The Selectivity and Functional Connectivity of the Anterior Temporal Lobes , 2009, Cerebral cortex.

[56]  L. Tyler,et al.  Complementary hemispheric asymmetries in object naming and recognition: A voxel-based correlational study , 2009, Neuropsychologia.

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

[58]  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.

[59]  M. Ashtari,et al.  Development and aging of the healthy human brain uncinate fasciculus across the lifespan using diffusion tensor tractography , 2009, Brain Research.

[60]  B. Miller,et al.  The Neural Correlates of Verbal and Nonverbal Semantic Processing Deficits in Neurodegenerative Disease , 2009, Cognitive and behavioral neurology : official journal of the Society for Behavioral and Cognitive Neurology.

[61]  T. Mihara,et al.  NEURAL CONNECTION BETWEEN BILATERAL BASAL TEMPORAL REGIONS: CORTICO‐CORTICAL EVOKED POTENTIAL ANALYSIS IN PATIENTS WITH TEMPORAL LOBE EPILEPSY , 2009, Neurosurgery.

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

[63]  Jordan Grafman,et al.  Social conceptual impairments in frontotemporal lobar degeneration with right anterior temporal hypometabolism. , 2009, Brain : a journal of neurology.

[64]  M. Saling,et al.  Verbal memory in mesial temporal lobe epilepsy: beyond material specificity. , 2009, Brain : a journal of neurology.

[65]  G. Ojemann,et al.  Category-specific naming and recognition deficits in temporal lobe epilepsy surgical patients , 2008, Neuropsychologia.

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

[67]  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.

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

[69]  Derek K. Jones,et al.  Symmetries in human brain language pathways correlate with verbal recall , 2007, Proceedings of the National Academy of Sciences.

[70]  Galia Avidan,et al.  Structural imaging reveals anatomical alterations in inferotemporal cortex in congenital prosopagnosia. , 2007, Cerebral cortex.

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

[72]  Jordan Grafman,et al.  Social concepts are represented in the superior anterior temporal cortex , 2007, Proceedings of the National Academy of Sciences.

[73]  D. Pandya,et al.  Association fibre pathways of the brain: parallel observations from diffusion spectrum imaging and autoradiography. , 2007, Brain : a journal of neurology.

[74]  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.

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

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

[77]  Philip Scheltens,et al.  The clinical profile of right temporal lobe atrophy. , 2004, Brain : a journal of neurology.

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

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

[80]  Guido Gainotti,et al.  Slowly progressive defect in recognition of familiar people in a patient with right anterior temporal atrophy. , 2003, Brain : a journal of neurology.

[81]  C. Frith,et al.  Development and neurophysiology of mentalizing. , 2003, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[82]  Randall Griffith,et al.  Recognition and identification of famous faces in patients with unilateral temporal lobe epilepsy , 2002, Neuropsychologia.

[83]  Paul J. Harrison,et al.  Asymmetry of the uncinate fasciculus: a post-mortem study of normal subjects and patients with schizophrenia. , 2002, Cerebral cortex.

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

[85]  Kevin Murphy,et al.  Speech production: Wernicke, Broca and beyond. , 2002, Brain : a journal of neurology.

[86]  S. Scott,et al.  A physiological change in the homotopic cortex following left posterior temporal lobe infarction , 2002, Annals of neurology.

[87]  R. Kikinis,et al.  Uncinate fasciculus findings in schizophrenia: a magnetic resonance diffusion tensor imaging study. , 2002, The American journal of psychiatry.

[88]  M. Jones-Gotman,et al.  Memory Deficits after Resection from Left or Right Anterior Temporal Lobe in Humans: A Meta‐Analytic Review , 2002, Epilepsia.

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

[90]  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.

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

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

[93]  C J Price,et al.  The neural systems sustaining face and proper-name processing. , 1998, Brain : a journal of neurology.

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

[95]  O. Devinsky The Temporal Lobe and Limbic System , 1998 .

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

[97]  N. Kanwisher,et al.  The Fusiform Face Area: A Module in Human Extrastriate Cortex Specialized for Face Perception , 1997, The Journal of Neuroscience.

[98]  Gerald L. Russell,et al.  The temporal variant of frontotemporal dementia. , 1997, Brain : a journal of neurology.

[99]  B. Miller,et al.  Aggressive, socially disruptive and antisocial behaviour associated with fronto-temporal dementia , 1997, British Journal of Psychiatry.

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

[101]  H. Terzian Syndrome of Kluver and Bucy reproduced in man by bilateral removal of the temporal lobes , 1996 .

[102]  J. Sergent,et al.  Functional neuroanatomy of face and object processing. A positron emission tomography study. , 1992, Brain : a journal of neurology.

[103]  E M Critchley,et al.  Loss of memory for people following temporal lobe damage. , 1989, Brain : a journal of neurology.

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

[105]  Morris Moscovitch,et al.  Selective impairment of semantic memory after temporal lobectomy , 1978, Neuropsychologia.

[106]  W. Scoville,et al.  LOSS OF RECENT MEMORY AFTER BILATERAL HIPPOCAMPAL LESIONS , 1957, Journal of neurology, neurosurgery, and psychiatry.

[107]  H. Klüver,et al.  PRELIMINARY ANALYSIS OF FUNCTIONS OF THE TEMPORAL LOBES IN MONKEYS , 1939 .

[108]  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.

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

[110]  John R. Hodges Semantic dementia: progressive fluent aphasia with temporal lobe atrophy , 1995 .

[111]  H. Klüver,et al.  "Psychic blindness" and other symptoms following bilateral temporal lobectomy in Rhesus monkeys. , 1937 .

[112]  Sanger Brown,et al.  An Investigation into the Functions of the Occipital and Temporal Lobes of the Monkey's Brain , 1888 .

[113]  D. Plaut,et al.  Cerebral Cortex Advance Access published December 18, 2012 Bilateral Hemispheric Processing of Words and Faces: Evidence from Word Impairments in Prosopagnosia and Face Impairments in Pure Alexia , 2022 .