Cognitive and Anatomical Underpinnings of the Conceptual Knowledge for Common Objects and Familiar People: A Repetitive Transcranial Magnetic Stimulation Study

Several studies have addressed the issue of how knowledge of common objects is organized in the brain, whereas the cognitive and anatomical underpinnings of familiar people knowledge have been less explored. Here we applied repetitive transcranial magnetic stimulation (rTMS) over the left and right temporal poles before asking healthy individuals to perform a speeded word-to-picture matching task using familiar people and common objects as stimuli. We manipulated two widely used semantic variables, namely the semantic distance and the familiarity of stimuli, to assess whether the semantic organization of familiar people knowledge is similar to that of common objects. For both objects and faces we reliably found semantic distance and familiarity effects, with less accurate and slower responses for stimulus pairs that were more closely related and less familiar. However, the effects of semantic variables differed across categories, with semantic distance effects larger for objects and familiarity effects larger for faces, suggesting that objects and faces might share a partially comparable organization of their semantic representations. The application of rTMS to the left temporal pole modulated, for both categories, semantic distance, but not familiarity effects, revealing that accessing object and face concepts might rely on overlapping processes within left anterior temporal regions. Crucially, rTMS of the left temporal pole affected only the recognition of pairs of stimuli that could be discriminated at specific levels of categorization (e.g., two kitchen tools or two famous persons), with no effect for discriminations at either superordinate or individual levels. Conversely, rTMS of the right temporal pole induced an overall slowing of reaction times that positively correlated with the visual similarity of the stimuli, suggesting a more perceptual rather than semantic role of the right anterior temporal regions. Results are discussed in the light of current models of face and object semantic representations in the brain.

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

[2]  J. Démonet,et al.  Anatomical correlates for category‐specific naming of objects and actions: A brain stimulation mapping study , 2014, Human brain mapping.

[3]  E. Warrington,et al.  Spatial coding of semantic information: knowledge of country and city names depends on their geographical proximity. , 2003, Brain : a journal of neurology.

[4]  N. Kerr,et al.  Effects of contextual elaboration on face recognition , 1982, Memory & cognition.

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

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

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

[8]  T Shallice,et al.  Semantic access dyslexia. , 1979, Brain : a journal of neurology.

[9]  C. Koch,et al.  Sparse but not ‘Grandmother-cell’ coding in the medial temporal lobe , 2008, Trends in Cognitive Sciences.

[10]  Isabel Gauthier,et al.  THE INFLUENCE OF CONCEPTUAL KNOWLEDGE ON VISUAL DISCRIMINATION , 2003, Cognitive neuropsychology.

[11]  Elizabeth K. Warrington,et al.  The accessibility of proper names , 1994, Neuropsychologia.

[12]  C. Koch,et al.  Invariant visual representation by single neurons in the human brain , 2005, Nature.

[13]  Howard J. Rosen,et al.  The Anatomy of Category-specific Object Naming in Neurodegenerative Diseases , 2006, Journal of Cognitive Neuroscience.

[14]  Tim Shallice,et al.  Semantic access dysphasia resulting from left temporal lobe tumours , 2008, Brain : a journal of neurology.

[15]  J. Hodges,et al.  Progressive prosopagnosia associated with selective right temporal atrophy: a new syndrome? , 2002 .

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

[17]  E. Wassermann Risk and safety of repetitive transcranial magnetic stimulation: report and suggested guidelines from the International Workshop on the Safety of Repetitive Transcranial Magnetic Stimulation, June 5-7, 1996. , 1998, Electroencephalography and clinical neurophysiology.

[18]  T. Shallice,et al.  Deep Dyslexia: A Case Study of , 1993 .

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

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

[21]  John R. Hodges,et al.  Progressive prosopagnosia associated with selective right temporal lobe atrophy. A new syndrome? , 1995, Brain : a journal of neurology.

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

[23]  A. Damasio,et al.  A neural basis for lexical retrieval , 1996, Nature.

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

[25]  Mark S. Seidenberg,et al.  Neural Systems Underlying the Recognition of Familiar and Newly Learned Faces , 2000, The Journal of Neuroscience.

[26]  E. Warrington,et al.  Abstract and concrete concepts have structurally different representational frameworks. , 2005, Brain : a journal of neurology.

[27]  M. Tarr,et al.  The Fusiform Face Area is Part of a Network that Processes Faces at the Individual Level , 2000, Journal of Cognitive Neuroscience.

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

[29]  T. R. Dixon,et al.  Frequency and the judged familiarity of meaningful words. , 1971 .

[30]  E. Warrington,et al.  The semantic organisation of proper nouns: the case of people and brand names , 2004, Neuropsychologia.

[31]  E. Warrington,et al.  Gradients of semantic relatedness and their contrasting explanations in refractory access and storage semantic impairments , 2005, Cognitive neuropsychology.

[32]  J. Hodges,et al.  A reversal of the temporal gradient for famous person knowledge in semantic dementia: implications for the neural organisation of long-term memory , 1998, Neuropsychologia.

[33]  G Miceli,et al.  SELECTIVE DEFICIT FOR PEOPLE’S NAMES FOLLOWING LEFT TEMPORAL DAMAGE: AN IMPAIRMENT OF DOMAIN-SPECIFIC CONCEPTUAL KNOWLEDGE , 2000, Cognitive neuropsychology.

[34]  C. Semenza,et al.  Evidence from aphasia for the role of proper names as pure referring expressions , 1989, Nature.

[35]  C. Price,et al.  Identification of famous faces and buildings: a functional neuroimaging study of semantically unique items. , 2001, Brain : a journal of neurology.

[36]  E. Warrington,et al.  A circumscribed refractory access disorder: A verbal semantic impairment sparing visual semantics , 2004, Cognitive neuropsychology.

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

[38]  Guido Gainotti,et al.  What the Locus of Brain Lesion Tells us About the Nature of the Cognitive Defect Underlying Category-Specific Disorders: A Review , 2000, Cortex.

[39]  Piero Antuono,et al.  Medial temporal lobe activity for recognition of recent and remote famous names: an event-related fMRI study , 2005, Neuropsychologia.

[40]  M N Rossor,et al.  Progressive degeneration of the right temporal lobe studied with positron emission tomography. , 1990, Journal of neurology, neurosurgery, and psychiatry.

[41]  Geoffrey E. Hinton,et al.  Lesioning an attractor network: investigations of acquired dyslexia. , 1991, Psychological review.

[42]  E. Capitani,et al.  Slowly progressive aphasia: a four-year follow-up study , 2001, Neuropsychologia.

[43]  G W Humphreys,et al.  Refractory semantics in global aphasia: on semantic organisation and the access-storage distinction in neuropsychology. , 1995, Memory.

[44]  Costanza Papagno,et al.  What is the role of the uncinate fasciculus? Surgical removal and proper name retrieval. , 2011, Brain : a journal of neurology.

[45]  Guy B. Williams,et al.  Dissociating person-specific from general semantic knowledge: roles of the left and right temporal lobes , 2004, Neuropsychologia.

[46]  J. Hodges,et al.  Semantic dementia. Progressive fluent aphasia with temporal lobe atrophy. , 1992, Brain : a journal of neurology.

[47]  C. Gross Genealogy of the “Grandmother Cell” , 2002, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[48]  M. Tarr,et al.  Levels of categorization in visual recognition studied using functional magnetic resonance imaging , 1997, Current Biology.

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

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

[51]  C. Noble The familiarity-frequency relationship. , 1954, Journal of experimental psychology.

[52]  I. Gauthier,et al.  Expertise for cars and birds recruits brain areas involved in face recognition , 2000, Nature Neuroscience.

[53]  R. Nebes,et al.  Patterns of Hand Preference in a Student Population , 1975, Cortex.

[54]  E. Warrington,et al.  Word comprehension. The distinction between refractory and storage impairments. , 1996, Brain : a journal of neurology.

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

[56]  John R. Hodges,et al.  IMPAIRED KNOWLEDGE OF FAMOUS PEOPLE AND EVENTS WITH INTACT AUTOBIOGRAPHICAL MEMORY IN A CASE OF PROGRESSIVE RIGHT TEMPORAL LOBE DEGENERATION: IMPLICATIONS FOR THE ORGANISATION OF REMOTE MEMORY , 1999 .

[57]  A. Caramazza,et al.  WHAT ARE THE FACTS OF SEMANTIC CATEGORY-SPECIFIC DEFICITS? A CRITICAL REVIEW OF THE CLINICAL EVIDENCE , 2003, Cognitive neuropsychology.

[58]  T. Schormann,et al.  Functional delineation of the human occipito-temporal areas related to face and scene processing. A PET study. , 2000, Brain : a journal of neurology.

[59]  Anna M. Thornton,et al.  Corpus e Lessico di frequenza dell’Italiano Scritto (CoLFIS). , 2005 .

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

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

[62]  Á. Pascual-Leone,et al.  Transcranial magnetic stimulation: studying the brain-behaviour relationship by induction of 'virtual lesions'. , 1999, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[63]  Carlo Semenza Generating proper names: a case of selective inability , 1996 .

[64]  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.