Frontotemporal lobar degeneration and social behaviour: Dissociation between the knowledge of its consequences and its conceptual meaning

Jorge Moll,Diana Caine,Roland Zahn,Helen Beaumont,Benjamin Shaw,Alistair Burns,Matthew A. Lambon Ralph,Paul Hoffman,Jordan Grafman,Sophie Green,Alexander Gerhard

doi:10.1016/j.cortex.2017.05.009

Abstract

Inappropriate social behaviour is an early symptom of frontotemporal lobar degeneration (FTLD) in both behavioural variant frontotemporal dementia (bvFTD) and semantic dementia (SD) subtypes. Knowledge of social behaviour is essential for appropriate social conduct. The superior anterior temporal lobe (ATL) has been identified as one key neural component for the conceptual knowledge of social behaviour, but it is unknown whether this is dissociable from knowledge of the consequences of social behaviour. Here, we used a newly-developed test of knowledge about long-term and short-term consequences of social behaviour to investigate its impairment in patients with FTLD relative to a previously-developed test of social conceptual knowledge. We included 19 healthy elderly control participants and 19 consecutive patients with features of bvFTD or SD and defined dissociations as performance differences between tasks for each patient (Bonferroni-corrected p < .05). Knowledge of long-term consequences was selectively impaired relative to short-term consequences in five patients and the reverse dissociation occurred in one patient. Six patients showed a selective impairment of social concepts relative to long-term consequences with the reverse dissociation occurring in one patient. These results corroborate the hypothesis that knowledge of long-term consequences of social behaviour is dissociable from knowledge of short-term consequences, as well as of social conceptual knowledge. Confirming our hypothesis, we found that patients with more marked grey matter (GM) volume loss in frontopolar relative to right superior ATL regions of interest exhibited poorer knowledge of the long-term consequences of social behaviour relative to the knowledge of its conceptual meaning and vice versa (n = 15). These findings support the hypothesis that frontopolar and ATL regions represent distinct aspects of social knowledge. This suggests that rather than being unable to suppress urges to behave inappropriately, FTLD patients often lose the knowledge of what appropriate social behaviour is and can therefore not be expected to behave accordingly.

Highlights

Social knowledge has been defined as knowledge of one's own and other people's minds (Adolphs, 2009)
Using fMRI and transcranial magnetic stimulation (TMS) methods, we have demonstrated that this abstract conceptual social knowledge, which is independent of the context of actions (Zahn, Moll, Paiva et al, 2009) and emotions (Zahn et al, 2007; Zahn, Moll, Paiva et al, 2009), is represented in the superior anterior temporal lobe [ATL: (Pobric, Lambon Ralph, & Zahn, 2016)]
Group comparisons of our patients with healthy control participants (Table 1) showed that general semantic and social conceptual impairments were consistently observed in our Frontotemporal lobar degeneration (FTLD) group, whereas more variability existed in performance on the sequential social knowledge task

Summary

Introduction

Social knowledge has been defined as knowledge of one's own and other people's minds (Adolphs, 2009). Two rare cases with selective right and left ATL atrophy respectively showed selective impairments on social versus non-social concepts in the right ATL and an impairment of both types of concepts in the left ATL case (Pobric et al, 2016) These results were in keeping with repetitive TMS of the right and left superior ATL, showing a selective slowing of social relative to non-social concepts in the right superior ATL, as well as a slowing of social and non-social conceptual task responses relative to a nonsemantic control condition in the left superior ATL (Pobric et al, 2016). These findings were in keeping with a larger body of evidence on graded hemispheric and regional specialisation within the ATLs for different conceptual content (Rice, Hoffman, & Lambon Ralph, 2015; Rice, Lambon Ralph, & Hoffman, 2015)

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Discussion

Conclusion