Understanding social dysfunction in the behavioural variant of frontotemporal dementia: the role of emotion and sarcasm processing

Abstract

Social interaction is profoundly affected in the behavioural form of frontotemporal dementia (bvFTD) yet there are few means of objectively assessing this. Diagnosis of bvFTD is based on informant report, however a number of individuals with a clinical profile consistent with the disease have no imaging abnormality and seem to remain stable, with doubt about the presence of underlying neurodegenerative pathology. We aimed to quantify aspects of the behavioural disorder and link it to the underlying level of atrophy in socially relevant brain regions. We tested individuals with either bvFTD (N = 26) or Alzheimer's disease (N = 9) and 16 controls using The Awareness of Social Inference Test (TASIT) to assess their ability to identify emotion and sarcasm in video vignettes. A subset of bvFTD patients (N = 21) and controls (N = 12) were scanned using MRI within 6 months of assessment. There was marked impairment in the ability of bvFTD patients whose scans showed abnormalities to recognize sarcastic, but not sincere statements. Their capacity to interpret negative emotion was also impaired, and this appeared to be a major factor underlying the deficit in sarcasm recognition. Clinically diagnosed bvFTD patients whose scans were normal, Alzheimer's disease patients and controls had no difficulty in appreciating both types of statement. In a multivariate imaging analysis it was shown that the sarcasm (and emotion recognition) deficit was dependent on a circuit involving the lateral orbitofrontal cortex, insula, amygdala and temporal pole, particularly on the right. Performance on a more global test of cognitive function, the Addenbrooke's Cognitive Examination did not have a unique association with these regions. The TASIT is an objective test of social dysfunction in bvFTD which indexes the frontotemporal volume loss in bvFTD patients and provides an objective measure for separating behavioural patients who are likely to decline from those who may remain stable. These results provide additional evidence for the role of the orbitofrontal cortex and related structures in the processing of socially relevant signals, particularly those where negative emotion recognition is important.

How preserved is episodic memory in behavioral variant frontotemporal dementia?

“…The 2 patient groups can be discriminated on MRI and PET findings despite exhibiting equivalent degrees of behavioral disturbance. [8][9][10] This heterogeneity of bvFTD might explain previous findings: if only the progressive group shows brain atrophy, then this group is more likely to exhibit memory deficits, while the so-called phenocopy group will present little or no memory dysfunction.…”

“…The predominant and characteristic behavioral disturbances are still the best indicator of bvFTD, although such behavioral disturbances are difficult to quantify and reliable informants are not always available. There is also growing evidence that patients with bvFTD show disproportionate impairment on tests of theory of mind and social cognition, involving detection of faux pas, 24 sarcasm, 25 and emotion discrimination. 26,27 According to our data, it is also possible to distinguish AD and bvFTD on the orientation scores of the ACE, in that patients with AD have more impaired orientation, while even patients with progressive bvFTD had preserved orientation for time and place.…”

“…35 Other indicators of progressive bvFTD are impairment in activities of daily living, 12 executive function, 33 and social cognition. 25 The fact that the phenocopy group also showed reduced memory performance across most tests in comparison to healthy controls was a surprise and is difficult to explain. Subtle memory deficits can be an indicator of prefrontal cortex damage; however, previous studies report that phenocopy cases show no or very subtle executive function impairment 33 and little cortical prefrontal cortex atrophy.…”

“…8,9,12,13,25,33 The nosology of these patients is a matter of ongoing debate. It seems unlikely that they have progressive FTD but rather a phenocopy, which mimics the behavioral symptoms of bvFTD.…”

“…[5][6][7] To date, surprisingly few studies have investigated episodic memory in bvFTD, with inconsistent results. Such inconsistency could, at least in part, be explained by recent studies which have shown that clinically diagnosed patients with bvFTD vary in their prognosis [8][9][10] ; some show rapid progression while others show little or no progression over a decade. The 2 patient groups can be discriminated on MRI and PET findings despite exhibiting equivalent degrees of behavioral disturbance.…”