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

Understanding social dysfunction in the behavioural variant of frontotemporal dementia: the role of emotion and sarcasm processing
Understanding social dysfunction in the behavioural variant of frontotemporal dementia: the role of emotion and sarcasm processing
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 abnormalites 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.
592–603
Kipps, C.M.
e43be016-2dc2-45e6-9a02-ab2a0e0208d5
Nestor, P.J.
058a7998-7d59-447f-b8d3-24f7a48ae5a7
Acosta-Cabronero, J.
0a1a5bf1-64fa-4367-be51-5ad89d6fc355
Arnold, R.
d720fa07-515f-4536-9d31-9aed98e72caa
Hodges, J.R.
c17af0a9-82e7-4f5a-8a97-d50ec06bbb0a
Kipps, C.M.
e43be016-2dc2-45e6-9a02-ab2a0e0208d5
Nestor, P.J.
058a7998-7d59-447f-b8d3-24f7a48ae5a7
Acosta-Cabronero, J.
0a1a5bf1-64fa-4367-be51-5ad89d6fc355
Arnold, R.
d720fa07-515f-4536-9d31-9aed98e72caa
Hodges, J.R.
c17af0a9-82e7-4f5a-8a97-d50ec06bbb0a

Kipps, C.M., Nestor, P.J., Acosta-Cabronero, J., Arnold, R. and Hodges, J.R. (2009) Understanding social dysfunction in the behavioural variant of frontotemporal dementia: the role of emotion and sarcasm processing. Brain, 132 (3), 592–603. (doi:10.1093/brain/awn314).

Record type: Article

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 abnormalites 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.

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More information

Accepted/In Press date: 29 October 2008
e-pub ahead of print date: 6 January 2009
Published date: March 2009

Identifiers

Local EPrints ID: 489376
URI: http://eprints.soton.ac.uk/id/eprint/489376
PURE UUID: 2a789aaa-dd0a-4b07-a7bb-30541fc05b57
ORCID for C.M. Kipps: ORCID iD orcid.org/0000-0002-5205-9712

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Date deposited: 23 Apr 2024 16:31
Last modified: 24 Apr 2024 01:56

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Contributors

Author: C.M. Kipps ORCID iD
Author: P.J. Nestor
Author: J. Acosta-Cabronero
Author: R. Arnold
Author: J.R. Hodges

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