Comprehension of insincere communication in neurodegenerative disease: Lies, sarcasm, and theory of mind

Department of Neurology, University of California, San Francisco, USA.
Cortex (Impact Factor: 5.13). 09/2011; 48(10):1329-41. DOI: 10.1016/j.cortex.2011.08.003
Source: PubMed


Comprehension of insincere communication is an important aspect of social cognition requiring visual perspective taking, emotion reading, and understanding others' thoughts, opinions, and intentions. Someone who is lying intends to hide their insincerity from the listener, while a sarcastic speaker wants the listener to recognize they are speaking insincerely. We investigated whether face-to-face testing of comprehending insincere communication would effectively discriminate among neurodegenerative disease patients with different patterns of real-life social deficits. We examined ability to comprehend lies and sarcasm from a third-person perspective, using contextual cues, in 102 patients with one of four neurodegenerative diseases (behavioral variant frontotemporal dementia [bvFTD], Alzheimer's disease [AD], progressive supranuclear palsy [PSP], and vascular cognitive impairment) and 77 healthy older adults (normal controls - NCs). Participants answered questions about videos depicting social interactions involving deceptive, sarcastic, or sincere speech using The Awareness of Social Inference Test. All subjects equally understood sincere remarks, but bvFTD patients displayed impaired comprehension of lies and sarcasm compared with NCs. In other groups, impairment was not disease-specific but was proportionate to general cognitive impairment. Analysis of the task components revealed that only bvFTD patients were impaired on perspective taking and emotion reading elements and that both bvFTD and PSP patients had impaired ability to represent others' opinions and intentions (i.e., theory of mind). Test performance correlated with informants' ratings of subjects' empathy, perspective taking and neuropsychiatric symptoms in everyday life. Comprehending insincere communication is complex and requires multiple cognitive and emotional processes vulnerable across neurodegenerative diseases. However, bvFTD patients show uniquely focal and severe impairments at every level of theory of mind and emotion reading, leading to an inability to identify obvious examples of deception and sarcasm. This is consistent with studies suggesting this disease targets a specific neural network necessary for perceiving social salience and predicting negative social outcomes.

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    • "Emotion deficits in FTLD are diverse and multidimensional: deficits may affect the cognitive processing of emotional cues in the verbal, visual, auditory or chemosensory modalities and extend across emotion categories (Snowden et al., 2001; Keane et al., 2002; Rosen et al., 2002; Werner et al., 2007; Bedoin et al., 2009; Omar et al., 2011a,b; Kumfor et al., 2011; Rohrer et al., 2012; Hsieh et al., 2012a; Kumfor and Piguet, 2012) and the processing of both elementary emotions and more complex prosocial sentiments (Moll et al., 2011). Impaired processing of emotional signals is often mirrored by abnormal emotional behaviours exhibited by patients themselves and correlates both with impaired understanding of others' mental states (Snowden et al., 2001; Kipps et al., 2009; Shany-Ur et al., 2012) and with altered autonomic reactivity (Werner et al., 2007; Eckart et al., 2012; Balconi et al., 2015), consistent with the targeting of distributed neural networks that process emotion by the proteinopathies that underpin FTLD (Omar et al., 2011a,b; Virani et al., 2013; Woolley et al., 2015). Limited evidence suggests that particular emotion categories or emotion modalities may be differentially affected in FTLD (Snowden et al., 2001; Kumfor et al., 2013; Lindquist et al., 2014; Oliver et al., 2015). "
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    ABSTRACT: art may signal emotions independently of a biological or social carrier: it might therefore constitute a test case for defining brain mechanisms of generic emotion decoding and the impact of disease states on those mechanisms. This is potentially of particular relevance to diseases in the frontotemporal lobar degeneration (FTLD) spectrum. These diseases are often led by emotional impairment despite retained or enhanced artistic interest in at least some patients. However, the processing of emotion from art has not been studied systematically in FTLD. Here we addressed this issue using a novel emotional valence matching task on abstract paintings in patients representing major syndromes of FTLD (behavioural variant frontotemporal dementia, n=11; sematic variant primary progressive aphasia (svPPA), n=7; nonfluent variant primary progressive aphasia (nfvPPA), n=6) relative to healthy older individuals (n=39). Performance on art emotion valence matching was compared between groups taking account of perceptual matching performance and assessed in relation to facial emotion matching using customised control tasks. Neuroanatomical correlates of art emotion processing were assessed using voxel-based morphometry of patients' brain MR images. All patient groups had a deficit of art emotion processing relative to healthy controls; there were no significant interactions between syndromic group and emotion modality. Poorer art emotion valence matching performance was associated with reduced grey matter volume in right lateral occopitotemporal cortex in proximity to regions previously implicated in the processing of dynamic visual signals. Our findings suggest that abstract art may be a useful model system for investigating mechanisms of generic emotion decoding and aesthetic processing in neurodegenerative diseases.
    Full-text · Article · Jan 2016 · Neuropsychologia
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    • "If there are age-related changes in the comprehension of sarcasm , it is of interest to explore whether this relates to emotion perception and theory of mind. The ability to detect and interpret sarcasm has been found to relate to emotion recognition in people with brain injury (Shamay-Tsoory et al., 2005), and dementia (Kipps et al., 2009; Rankin et al., 2009; Shany-Ur et al., 2012). There is also evidence that theory of mind abilities are related to sarcasm comprehension in brain injured samples (e.g., McDonald & Flanagan, 2004; Channon, Pellijeff & Rule, 2005; Shamay- Tsoory et al., 2005; Winner, Brownell, Happé, Blum, & Pincus, 1998). "
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    ABSTRACT: Younger and older adults differ in performance on a range of social-cognitive skills, with older adults having difficulties in decoding nonverbal cues to emotion and intentions. Such skills are likely to be important when deciding whether someone is being sarcastic. In the current study we investigated in a life span sample whether there are age-related differences in the interpretation of sarcastic statements. Using both video and verbal materials, 116 participants aged between 18 and 86 completed judgments about whether statements should be interpreted literally or sarcastically. For the verbal stories task, older adults were poorer at understanding sarcastic intent compared with younger and middle-aged participants, but there was no age difference in interpreting control stories. For the video task, older adults showed poorer understanding of sarcastic exchanges compared with younger and middle-aged counterparts, but there was no age difference in understanding the meaning of sincere interactions. For the videos task, the age differences were mediated by the ability to perceive facial expressions of emotion. Age effects could not be explained in terms of variance in working memory. These results indicate that increased age is associated with specific difficulties in using nonverbal and contextual cues to understand sarcastic intent. (PsycINFO Database Record
    Full-text · Article · Oct 2015 · Developmental Psychology
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    • "From the perspective, it is not unreasonable to propose that the different instances of pragmatic inferences share the same basic mechanisms . Studies of the comprehension of figurative language in bvFTD patients (e.g., Rankin et al., 2009; Shany-Ur et al., 2012), usually ask participants to interpret an utterance without explicitly providing the pragmatic/figurative interpretation as we did in Experiment 1. Therefore, it is possible that bvFTD patients' difficulty in interpreting figurative language derives not from an inability to interpret metaphoric or ironic language per se, but instead from their difficulty in generating relevant alternative interpretations as well as to their greater tolerance of pragmatic violations as we propose for the case of scalar implicature. "
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    Full-text · Article · Jul 2015 · Neuropsychologia
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