Brain Advance Access originally published online on January 19, 2009
Brain 2009 132(3):604-616; doi:10.1093/brain/awn343
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Social conceptual impairments in frontotemporal lobar degeneration with right anterior temporal hypometabolism
1 National Institutes of Health, National Institutes of Neurological Disorders and Stroke, Cognitive Neuroscience Section, Bethesda, MD, USA 2 Neuroscience and Aphasia Research Unit, School of Psychological Sciences, The University of Manchester, Manchester, UK 3 Cognitive and Behavioral Neuroscience Unit, LABS-D’Or Hospital Network, Rio de Janeiro, Brazil 4 The Litwin-Zucker Research Center for the Study of Alzheimer's Disease and Memory Disorders, The Feinstein Institute for Medical Research Manhasset, NY, USA
Correspondence to: Dr Jordan Grafman, NIH/NINDS, Cognitive Neuroscience Section, 10 Center Drive, Room 7D43, Bethesda, MD 20892-1440, USA. E-mail: grafmanj{at}ninds.nih.gov
Inappropriate social behaviours are early and distinctive symptoms of the temporal and frontal variants of frontotemporal lobar degeneration (FTLD). Knowledge of social behaviour is essential for appropriate social conduct. It is unknown, however, in what way this knowledge is degraded in FTLD. In a recent functional MRI study, we have identified a right-lateralized superior anterior temporal lobe (aTL) region showing selective activation for ‘social concepts’ (i.e. concepts describing social behaviour: e.g. ‘polite’, ‘stingy’) as compared with concepts describing less socially relevant animal behaviour (‘animal function concepts’: e.g. ‘trainable’, ‘nutritious’). In a further fMRI study, superior aTL activation was independent of the context of actions and feelings associated with these social concepts. Here, we investigated whether the right superior sector of the aTL is necessary for context-independent knowledge of social concepts. We assessed neuronal glucose uptake using 18-fluoro-deoxy-glucose-positron emission tomography (FDG-PET) and a novel semantic discrimination task which probed knowledge of social and animal function concepts in patients with FTLD (n = 29) and corticobasal syndrome (n = 18). FTLD and corticobasal syndrome groups performed equally poorly on animal function concepts but FTLD patients showed more pronounced impairments on social concepts than corticobasal syndrome patients. FTLD patients with right superior aTL hypometabolism, as determined on individual ROI analyses, were significantly more impaired on social concepts than on animal function concepts. FTLD patients with selective impairments for social concepts, as determined on individual neuropsychological profiles, showed higher levels of inappropriate social behaviours (‘disinhibition’) and demonstrated more pronounced hypometabolism in the right superior aTL, the left temporal pole and the right lateral orbitofrontal and dorsomedial prefrontal cortex as compared with FTLD patients showing selective impairments of animal function concepts. Combining both FTLD subgroup analyses, based on anatomical and neuropsychological criteria, by using inclusive masks, revealed the right superior aTL as associated with selective impairments of social concepts in both analyses. These results corroborate the hypothesis that the right aTL is necessary for representing conceptual social knowledge. Further, we provide first evidence for the potential importance of conceptual social knowledge impairments as contributing to behavioural symptoms of FTLD.
Key Words: frontotemporal dementia; semantics; social cognition; anterior temporal lobe; social behaviour
Abbreviations: aTL, anterior temporal lobe; CBS, corticobasal syndrome; FDG-PET, 18-fluoro-deoxy-glucose-positron emission tomography; FTLD, frontotemporal lobar degeneration; MNI, Montreal Neurological Institute; ROI, region of interest
Received April 10, 2008. Revised September 25, 2008. Accepted November 18, 2008.