Comprehension of insincere communication in
neurodegenerative disease: Lies, sarcasm, and theory of mind
Tal Shany-Ur, Pardis Poorzand, Scott N. Grossman, Matthew E. Growdon, Jung Y. Jang,
Robin S. Ketelle, Bruce L. Miller and Katherine P. Rankin*
Department of Neurology, University of California, San Francisco, USA
a r t i c l e i n f o
Received 9 March 2011
Reviewed 7 April 2011
Revised 16 July 2011
Accepted 12 August 2011
Action editor Jordan Grafman
Published online 1 September 2011
Theory of mind
a b s t r a c t
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 e 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 comprehen-
sion 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 corre-
lated with informants’ ratings of subjects’ empathy, perspective taking and neuropsychi-
atric 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.
ª 2011 Elsevier Srl. All rights reserved.
* Corresponding author. Memory and Aging Center, Department of Neurology, University of California, 350 Parnassus Avenue, Suite 905,
San Francisco, CA 94143-1207, USA.
E-mail address: firstname.lastname@example.org (K.P. Rankin).
0010-9452/$ e see front matter ª 2011 Elsevier Srl. All rights reserved.
Available online at www.sciencedirect.com
Journal homepage: www.elsevier.com/locate/cortex
cortex 48 (2012) 1329e1341
Insincere speech is ubiquitous in everyday social interactions,
where people make jokes, speak sarcastically, intentionally
lie, or are honestly mistaken about reality (Harada et al., 2009).
The capacity to correctly interpret these forms of insincere
speech is an essential social skill, and inability to do so may
result in severely impaired communication (Winner et al.,
1998). Two common forms of insincere communication
occur when the literal content of a speaker’s message
contradicts with reality. A speaker who is lying wants to hide
their insincerity from the listener, while someone employing
sarcasmwantsthe listenerto recognize that they are speaking
insincerely. Detecting these insincere statements requires
interpretation of the speaker’s intention, a complex process
relying on integration of semantic and syntactic comprehen-
sion, contextual and paralinguistic information processing,
pragmatic knowledge, visual perspective taking, emotion
reading, and theory of mind (ToM; representing others’
beliefs, opinions and intentions).
A lie is a communicative act in which the speaker inten-
tionally withholds information from the listener in order to
cause the listener to either abandon a true belief or acquire
a false one (Chisholm and Feehan, 1977), and is often used to
protect oneself or others (Winner et al., 1998). Watching
a deceptive interaction may involve moral reasoning, since
lying violates the communication norm of truthfulness
(Harada et al., 2009). Although one may correctly identify a lie
based entirely on the fact that the truth is being withheld from
the listener, additional deliberation about the deceiver’s
intentions may require more complex emotion reading and
ToM processes. The neuroanatomic substrates of compre-
hending lies involve regions implicated with moral judgment,
including anteriortemporal and left inferiorfrontal gyrus(IFG)
regions (mediating semantic knowledge about social norms),
and rostromedial prefrontal cortex (rmPFC) (involved in
reasoning about the moral aspect of a deceptive act). Addi-
tionally, lie comprehension uniquely involves activity in
bilateral temporoparietal junction (TPJ), an area related to
perspective taking, right superior temporal sulcus (STS), and
left dorsolateral PFC, regions which may sub-serve the “ability
to detect an intent to deceive” (Harada et al., 2009). Patients
with right hemisphere lesions, especially in the medial
prefrontal cortex (MPFC), demonstrate poor ability to detect
lies, which has been attributed to impaired ToM (Stuss et al.,
2001; Winner et al., 1998).
Sarcasm is a social mechanism for indirectly conveying
criticism or covering up embarrassment in a dramatic or
humorous manner, and is perceived as less aggressive and
more polite than direct confrontation (McDonald, 1999;
Shamay-Tsoory et al., 2005; Winner et al., 1998). In both
lying and sarcasm the speaker says the opposite of what they
know to be true, and for both, comprehension requires using
contextual cues to make an accurate assessment of what the
speaker and listener think about the situation (i.e., a belief or
opinion). Both may also require additional ToM processing
and emotion reading to infer the speaker’s intention or
emotional state. However, unlike a lie, sarcasm is used to
emphasize reality rather than hide it, and the speaker is trying
to convey the truth to the listener (Channon et al., 2007; Grice,
1975). There is a unique set of paralinguistic cues in which
voice prosody and facial expression can be used to convey
sarcasm in the absence of contextual cues, however these are
not required for comprehension of sarcasm when sufficient
contextual cues are present (Channon et al., 2007; Grice, 1975;
Rockwell, 2007). The neuroanatomical substrates of sarcasm
comprehension include dorsal and ventral regions of the
MPFC including superior frontal gyri (SFG) as well as IFG (with
right IFG involved in representing the speaker’s intention and
integrating information about the speakers’ attitudes, inten-
tions and emotions and left IFG involved in integrating ToM
and language processing), the temporal poles (implicated in
social events-related knowledge and in empathy), posterior
parahippocampi (involved in assigning social salience to
auditory paralinguistic input), the STS (involved in ToM and
semantic processing) and the amygdala (related to perceiving
the implicitly conveyed feelings of the speaker) (Channon
et al., 2007; Kipps et al., 2009; McDonald and Pearce, 1996;
Rankin et al., 2009; Shamay-Tsoory et al., 2005; Uchiyama
et al., 2006, 2011).
Neurodegenerative diseases are often manifested by
a decline in social comprehension and behavior, especially
when they involve degeneration of frontal-insular, anterior
cingulate and anterior temporal regions underlying social-
cognitive processes. Individuals with the behavioral variant
of frontotemporal lobar degeneration (behavioral variant
frontotemporal dementia e bvFTD) present with a decline in
interpersonal behavior, impaired regulation of personal
conduct, emotional apathy, loss of insight (Neary et al., 1998),
and “lack of social awareness” (Miller et al., 2003). This disease
selectively targetsa networkof anteriorcingulate cortex (ACC)
and orbital fronto-insular regions involved in processing
emotional salience of stimuli (Seeley et al., 2007), and
considered to be part of the “social brain” network (Adolphs,
2010; Brothers, 1990). Correspondingly there is extensive
evidence that bvFTD patients perform poorly on tests of ToM,
(Adenzato et al., 2010; Kipps et al., 2009; Rosen et al., 2004;
Sturm et al., 2006; Zahn et al., 2009). Alzheimer’s disease
(AD), which initially targets posterior and medial temporal
regions, is associated with progressive cognitive deficits in
memory, language, perception, or attention, but not in socio-
emotional processes (McKhann et al., 1984; Seeley et al.,
preserved performance on tests of ToM, social comprehen-
sion, emotion reading and regulation, particularly when more
general effects of cognitive deficits are accounted for
(Goodkind et al., 2010; Lavenu et al., 1999; Rankin et al., 2009;
Zaitchik et al., 2004). Progressive supranuclear palsy (PSP) is
primarily a motor disorder, with characteristic subcortical
pathology resulting in a frontal-subcortical disconnection
syndrome (Litvan et al., 1996a). However, clinically this
disease often presents as a frontal dysexecutive disorder with
bvFTD-like behavioral and personality symptoms such as
social disinhibition and apathy (Donker Kaat et al., 2007;
Kertesz and McMonagle, 2010; Litvan et al., 1996b; Millar
et al., 2006). Vascular cognitive impairment (VCI) is charac-
terized primarily by impairment in attention and executive
with ADtypically have
cortex 48 (2012) 1329e1341
evidence that bvFTD specifically targets a neural network
sensitive to salient social-emotional information such as the
that this network is less affected by other neurodegenerative
diseases. Patients’ performance on these objective tests of
social cognition correlates highly with their real-life social
behavior, including their tendency to behave empathically and
totake others’perspective,suggesting suchtestsmaybeuseful
as objective measures of social functioning.
This research was supported in part by the National Institute
on Aging (NIA) grants 5-R01 AG029577, 5-P01 AG019724, and
P50 AG02350, the State of California Alzheimer’s Disease
Research Centerof California
NIH/NCRR UCSF-CTSI grant UL1 RR024131, and the Larry
L. Hillblom Foundation 2007/2I grant.
(ARCC) grant 03-75271,
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