The Neuroanatomical Basis of Understanding Sarcasm and Its Relationshipto Social Cognition
S. G. Shamay-Tsoory and R. Tomer
Rambam Medical Center and University of Haifa
J. Aharon-Peretz
Rambam Medical Center
The authors explored the neurobiology of sarcasm and the cognitive processes underlying it byexamining the performance of participants with focal lesions on tasks that required understanding of sarcasm and social cognition. Participants with prefrontal damage (
n
25) showed impaired perfor-mance on the sarcasm task, whereas participants with posterior damage (
n
16) and healthy controls(
n
17) performed the same task without difficulty. Within the prefrontal group, right ventromediallesions were associated with the most profound deficit in comprehending sarcasm. In addition, althoughthe prefrontal damage was associated with deficits in theory of mind and right hemisphere damage wasassociated with deficits in identifying emotions, these 2 abilities were related to the ability to understandsarcasm. This suggests that the right frontal lobe mediates understanding of sarcasm by integratingaffective processing with perspective taking.
Irony
is an indirect form of speech used to convey feelings in anindirect way. Ironic utterances are characterized by oppositionbetween the literal meaning of the sentence and the speaker’smeaning (Winner, 1988). One form of irony is
sarcasm
. Sarcasmis usually used to communicate implicit criticism about the listeneror the situation. It is usually used in situations provoking negativeaffect and is accompanied by disapproval, contempt, and scorn(Sperber & Wilson, 1986). For example, a boss catching hisemployee taking a nap may remark “Joe, don’t work too hard!” toexpress his disapproval. The listener must identify the oppositionbetween the literal meaning of this sentence (Joe is working toohard) and the boss’s intention to criticize Joe (Joe is a lazy worker).The ironic speaker intends that the listener detect the deliberatefalseness; he makes a statement that violates the context andintends the listener to recognize this statement (Dennis, Purvis,Barnes, Wilkinson, & Winner, 2001). The interpretation of sar-casm thus involves understanding of the intentions expressed inthe situation and may include processes of social cognition andtheory of mind.
SARCASM AND SOCIAL COGNITION
It has been demonstrated that the use of sarcasm has severalsocial communicative functions, such as increasing the perceivedpoliteness of the criticism (Brown & Levinson, 1978), decreasingthe perceived threat and aggressiveness of the criticism (Dews &Winner, 1995), and creating a humorous atmosphere (Dews &Winner, 1995). It appears that a deficit in understanding sarcasticutterances may reflect an impaired ability to understand social cuessuch as intentions, beliefs, and emotions. In concordance, recenttheories explaining irony have argued that sarcastic comments areinterpreted in the light of their relevance to the situation. Sperberand Wilson’s (1981) relevance theory advocates that the interpre-tation of ironic utterances may require recognition of the speaker’sattitude and thus requires shared knowledge between the speakerand the listener.A key aspect of social cognition is the ability to infer otherpeople’s mental state, thoughts, and feelings, commonly referredto as the
theory of mind
(ToM). Although irony has been investi-gated from a psycholinguistic perspective (e.g., Grice, 1978; Sper-ber & Wilson, 1981), recent findings in developmental and neu-ropsychological research suggest that understanding irony in-volves the understanding of social cues and requires ToM. Irony isonly gradually mastered by young children. Developmental re-search studies have suggested that the difficulty that small childrenmay have in understanding irony is related to their difficultiesinferring the speaker’s belief and intentions (Sullivan, Winner, &Hopfied, 1995; Winner & Leekam, 1991). Understanding ironyrequires first-order intentionality about the speaker’s belief (toavoid interpreting irony as a mistake), as well as second-orderintentionality about the speaker’s beliefs about the listener’s be-liefs, to avoid interpreting irony as a lie (Dews & Winner, 1997).Happe (1993) has reported that among autistic children, impairedability to attribute mental states relates to impaired ability tointerpret irony. The same pattern of impairment has been reportedin clinical populations of individuals with brain injury (Dennis etal., 2001). Winner, Brownell, Happe, Blum, and Pincus (1998)have suggested that individuals with right hemisphere brain dam-age are unable to distinguish lies from jokes and that this inabilityis related to a difficulty in attributing second-order mental states(Winner et al., 1998). Shamay, Tomer, and Aharon-Peretz (2002)have reported that prefrontal brain damage was associated withboth impaired empathic ability and impaired ability to interpretironic utterances, and these abilities were highly correlated in agroup of frontal lobe-lesioned patients (Shamay et al., 2002).
S. G. Shamay-Tsoory and R. Tomer, Cognitive Neurology Unit, Ram-bam Medical Center, Haifa, Israel, and Department of Psychology andBrain and Behavior Center, University of Haifa, Haifa; J. Aharon-Peretz,Cognitive Neurology Unit, Rambam Medical Center.S. G. Shamay-Tsoory was supported by a doctoral research grant fromthe Israel Foundation Trustees. We are grateful to Margo Lapidot for theHebrew version of the Irony test.Correspondence concerning this article should be addressed to S. G.Shamay-Tsoory, Department of Psychology and Brain and Behavior Cen-ter, University of Haifa, Haifa 31905, Israel. E-mail: sshamay@psy.haifa.ac.il
Neuropsychology Copyright 2005 by the American Psychological Association2005, Vol. 19, No. 3, 288–300 0894-4105/05/$12.00 DOI: 10.1037/0894-4105.19.3.288
288
THE ANATOMICAL BASIS OF SARCASM
Previous research investigating the effects of brain damage onsarcasm has pointed to the role of the right hemisphere in prag-matic understanding (McDonald, 1999). Considerable research onadult participants has shown that the right hemisphere predomi-nates in influencing the interpretation of conversation (Caplan &Dapretto, 2001; Rehak, Kaplan, & Gardner, 1992) and in under-standing irony in particular (Brownell, Simpson, Bihrle, Potter, &Gardner, 1990). Winner et al. (1998) have found that right hemi-sphere patients have difficulty interpreting inferential questionsregarding counterfactual end comments of stories. With qualitativeobservations, researchers have also suggested that right hemi-sphere patients attribute the listener with perceiving the literalmeaning of the utterance (Kaplan, Brownell, Jacobs, & Gardner,1990). It has been suggested that the right hemisphere is involvedin several paralinguistic domains, such as the prosodic elements of language (Ross, 1981), proverb interpretation (Benton, 1968), andindirect requests (Weylman, Brownell, Roman, & Gardner, 1989).The right hemisphere has also been implicated in the appreciationof humor. For example, Wapner, Hamby, and Gardner (1981)suggested that right hemisphere patients have difficulty in fullyinterpreting a joke’s content. In addition, the right hemisphere isdominant for both the comprehension and expression of emotion inall modalities (Tucker, Luu, & Pribram, 1995).Although the right hemisphere is clearly implicated in detectionof irony and sarcasm, there are indications that the frontal lobesmay also be involved in interpretation of sarcastic utterances. Thefrontal lobes have long been considered to play a special role insocial cognition, with damage in this region affecting not onlyhigh-level cognitive functions but also social behavior (Adolphs,1999; Eslinger, 1998) and personality (A. R. Damasio, 1994).Alexander, Benson, and Stuss (1989) suggested that damage to thefrontal lobes area may impair analysis, planning, and monitoringof language. Understanding of sarcastic utterances by patients withprefrontal lesions has been directly tested in controlled experi-ments only once (McDonald & Pearce, 1996); the authors foundthat compared with healthy controls, these patients could notinterpret sarcasm. In concordance with this, we also reported adeficit in interpretation of sarcasm in patients with prefrontaldamage (Shamay et al., 2002). In these studies, however, patientswith unilateral right and left frontal damage, or patients withlesions in nonfrontal brain regions, were not included.Although the above-mentioned studies imply involvement of different brain regions in the comprehension of sarcasm, they donot indicate which areas are necessary for such comprehension.These studies fail to establish accurate localization because they donot examine the relative contribution of the side (right vs. left) andsite (anterior vs. posterior) of lesions. This distinction is of highimportance, as evidence from patients with frontal lobe damagesuggests that the right frontal lobe is involved in nonliteral lan-guage functions (Alexander et al., 1989), humor appreciation(Shammi & Stuss, 1999), self-awareness (Stuss & Benson, 1986),and ToM (Stuss, Gallup, & Alexander, 2001), all of which arebelieved to be related to interpretation of sarcasm. It is thuspossible that whereas either the right hemisphere or the frontallobes play a role in mediating sarcasm, the right frontal lobe has aunique role in the understanding of sarcastic utterances.The social communicative function of irony suggests a distinctrole for ventromedial (VM) regions within the frontal lobes, asopposed to dorsolateral (DL) regions. Whereas DL prefrontalregions have been associated with executive functions, VM lesionshave been shown to result in impaired social skills, such as social judgment (Eslinger & Damasio, 1985) and decision making (Be-chara, Damasio, Tranel, & Anderson, 1998). Thus, if patients withlesions in subregions of the prefrontal cortex differ in their deficitin understanding sarcasm, this would suggest that specific areaswithin the prefrontal cortex are crucial to the mediation of com-prehension of sarcastic utterances. To the best of our knowledge,no study to date has directly examined deficits in the interpretationof sarcasm in patients with limited focal lesions in distinct pre-frontal and posterior regions of the brain or examined the contri-bution of asymmetry and exact localization of the lesion within thefrontal lobes. The purpose of the present study was thus twofold:first, to examine the neural basis of understanding sarcasm, andsecond, to explore the relationship between deficits in the compre-hension of sarcasm and social cognition. We therefore examinedthe relationships between performance on tasks that assess theunderstanding of sarcasm and performance on tasks that assessToM (the “faux pas” task) and affect recognition (facial expres-sion, affective prosody) in patients with well-defined localizedbrain lesions.
METHODParticipants
Patients with well-defined, localized, acquired cortical lesions, who werereferred for a cognitive assessment at the Cognitive Neurology Unit, wererecruited for participation in this study. Etiology of lesions included braincontusions and hematomas following traumatic head injury (
n
30), braintumors (
n
7), and cerebrovascular accident (CVA) (
n
4). All patientsgave informed consent for participation in the study. Testing of participantsrequired two meetings (1 hr each). Neurologic and neuropsychologicalscreening were conducted in the first session, and the tasks assessingsarcasm, ToM, and recognition of affect were administered during thesecond session. Anatomical classification was based on current (within 6months) magnetic resonance (MR) or computerized axial tomography (CT)data. For inclusion, lesions had to be localized to either frontal or non-frontal cortical regions. Frontal lesions included cases with gray and whitematter lesions. Lesions extending to the basal ganglia were excluded. Forpatients with head injury, the acute neuroradiological studies were exam-ined, and all patients with characteristics of diffuse axonal injury wereexcluded. Lesion location was classified as frontal (prefrontal cortex[PFC],
n
25) and posterior (posterior cortex [PC],
n
16) subgroups onthe basis of the location of the lesion. Seventeen aged-matched healthyvolunteers served as controls (healthy controls; HC).The PFC group consisted of 12 patients with unilateral lesions (lefthemisphere
6, right hemisphere
6) and 13 patients with bilaterallesions. The PC subgroup included 16 patients with unilateral lesions (lefthemisphere
9, right hemisphere
7).No patient had an aphasic disturbance. Testing and lesion localizationwere undertaken at least 6 months (average time: 19.34 [
SD
16.32]months) after the acute onset. All participants were free of history of significant alcohol or substance abuse, psychiatric disorder, or other illnessaffecting the central nervous system. All participants completed theRaven’s Progressive Matrices (Raven, Court, & Raven, 1992) so that wecould assess reasoning and obtain an estimate of general intellectualfunctioning. The following measures were used to evaluate the partici-
289
NEUROBIOLOGY OF SARCASM
Table 1
Detailed Description of the Patients With Frontal Lesions
Participant Lesion site and etiologySize of lesion
a
Participant Lesion site and etiologySize of lesion
a
Left Right Left Right1. 1 0Ventromedial
dorsolateralsubarachnoid hematoma2. 0 .125Ventromedial contusion3. 0 1.38Ventromedial contusion4. .31 4.00Dorsolateral hematoma5. .25 .25Ventromedial contusion6. 0 5Dorsolateral meningioma7. 7.5 4.75Ventromedial
dorsolateralsubarachnoid hematoma8. 0 2.00Dorsolateral subarachnoidhematoma9. 6.00 12.5Ventromedial
dorsolateralcontusion10. 1.00 3.125Ventromedial contusion11. 4 3.63Ventromedial contusion12. 16.00 17.00Ventromedial
dorsolateralencephalomacia13. 0 2.00Ventromedialencephalomacia14. 6.5 0Dorsolateral contusion15. 3.5 8.00Ventromedial
dorsolateralcontusion16. 0 .625Dorsolateral aneurysm17. .75 0Ventromedial
dorsolateralmeningioma18. 8.25 2.5Ventromedial contusion19. 2.6125 3.25Ventromedial contusion20. 0 2.5Dorsolateral meningioma21. 7.5 .125Ventromedial contusion22. 1 0Dorsolateral hematoma
290
SHAMAY-TSOORY, TOMER, AND AHARON-PERETZ
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