Diminished Self-Conscious Emotional Responding in Frontotemporal LobarDegeneration PatientsVirginia E. Sturm and Elizabeth A. AscherUniversity of California, BerkeleyBruce L. MillerUniversity of California, San FranciscoRobert W. LevensonUniversity of California, BerkeleyFrontotemporal lobar degeneration (FTLD) is a neurodegenerative disease that dramatically alters social andemotional behavior. Recent work has suggested that self-conscious emotions (e.g., embarrassment) may beparticularly vulnerable to disruption in this disease. Self-conscious emotions require the ability to monitor theself in relation to others. These abilities are thought to be subserved by brain regions (e.g., medial prefrontal,anterior cingulate, and insula) that are particularly vulnerable to damage in FTLD. This study examinedemotional responding (expressive behavior, peripheral physiology, and subjective experience) in 24 FTLDpatients and 16 cognitively normal control participants using a karaoke task known to elicit self-consciousemotion reliably and a nonemotional control task (isometric handgrip). Results indicated that FTLD patientsshowed diminished self-conscious emotional behavior (embarrassment and amusement) and diminishedphysiological responding while watching themselves singing. No differences were found between patients andcontrols in the nonemotional control task. These findings offer evidence of marked disruption of self-conscious emotional responding in FTLD. Diminished self-conscious emotional responding likely contributessignificantly to social inappropriateness and other behavioral abnormalities in FTLD.Keywords: dementia, self-conscious emotion, autonomic nervous systemFrontotemporal lobar degeneration (FTLD) is a neurodegenera-tive disease that selectively atrophies the frontal lobes, temporallobes, and amygdala, regions that are important for awareness ofboth self and others (Craik et al., 1999; Gusnard, Akbudak, Shul-man, & Raichle, 2001; Johnson et al., 2002; Kelley et al., 2002;Ochsner et al., 2004; Platek, Keenan, Gallup, & Mohamed, 2004;Zysset, Huber, Ferstl, & von Cramon, 2002). The prevalence ofFTLD is higher than once thought, and it is as common asAlzheimer’s disease in individuals under the age of 65 (Ratnavalli,Brayne, Dawson, & Hodges, 2002). The category of FTLD sub-sumes two clinical phenotypes that are notable for social andemotional dysfunction (Neary et al., 1998): frontotemporal demen-tia (FTD) and semantic dementia (SD). Although the consensusdiagnostic criteria proposed by Neary et al. (1998) delineate be-havioral differences between the subtypes (e.g., “decline in socialinterpersonal conduct” in FTD and “loss of sympathy and empa-thy” in SD), neuroanatomical and clinical heterogeneity oftenmake these groups difficult to dissociate (Harciarek & Jodzio,2005; Litvan et al., 1997). Although FTD tends to have atrophypredominantly in the frontal lobes and SD has atrophy primarily inthe anterior temporal lobes and amygdala, loss in the orbitofrontalcortex, insula, and anterior cingulate is often evident in bothgroups (Rosen, Gorno-Tempini, et al., 2002). The neuropatholog-ical features of FTLD are varied and do not easily map ontoclinical symptomatology, but postmortem analyses typically revealtau and/or ubiquitin inclusions in the frontal and temporal regions(Forman et al., 2006; McKhann et al., 2001).FTLD patients exhibit gradual decline in self-awareness andsocial dexterity. Clinically, FTLD patients are often socially dis-inhibited (Mendez et al., 2006; Rosen et al., 2006), a symptom thatmay be off-putting to others and is especially stressful for care-givers (de Vugt et al., 2006). Patients may become more passive,aloof, and cold than they were before disease onset (Rankin,Kramer, Mychack, & Miller, 2003), and they typically exhibitdiminished insight into and awareness of even dramatic personal-ity changes (Rankin, Baldwin, Pace-Savitsky, Kramer, & Miller,2005). Changes in hobbies, ideology, and aesthetic preferences(e.g., in food and dress) have also been reported in FTLD (Milleret al., 2001), prompting descriptions of the self as becoming “lost”in this disease (Levenson & Miller, 2007). Laboratory studies haveconsistently found that FTLD patients also fall short in their abilityto recognize others’ emotions (Keane, Calder, Hodges, & Young,2002; Lavenu, Pasquier, Lebert, Petit, & Van der Linden, 1999;Rosen, Perry, et al., 2002; Werner et al., 2007) and perspectives(Gregory et al., 2002; Lough et al., 2006; Snowden et al., 2003).These patients fail to recognize social faux pas (Gregory et al.,Virginia E. Sturm, Elizabeth A. Ascher, and Robert W. Levenson,Department of Psychology, University of California, Berkeley; Bruce L.Miller, Department of Neurology, University of California, San Francisco.We would like to acknowledge our funding sources for this work:National Institute on Aging Grants AG107766, AG19724, AG-03-006-01,and AG019724-02; National Institute of Mental Health Grant MH020006;and the State of California Alzheimer’s Disease Research Center of Cali-fornia Grant 03-75271.Correspondence concerning this article should be addressed to Robert W.Levenson, Department of Psychology, 3210 Tolman Hall, 1650; University ofCalifornia, Berkeley, CA 94720-1650. E-mail: [email protected] Copyright 2008 by the American Psychological Association2008, Vol. 8, No. 6, 861– 869 1528-3542/08/$12.00 DOI: 10.1037/a00137658612002) and are unable to rate appropriately the severity of moraland social transgressions (Lough et al., 2006). These deficitssuggest that FTLD patients may also have difficulty with the kindsof complicated emotions that arise in social interactions.In the realm of emotional functioning, laboratory-based assess-ments (Levenson et al., 2008) have indicated that FTLD patientshave intact physiological and behavioral responding in certainemotional contexts. For example, FTLD patients do not differ fromneurologically healthy controls in their emotional reactions tounexpected loud noises (Sturm, Levenson, Rosen, Allison, &Miller, 2006) or to simply themed happy, sad, and fearful emo-tional film clips (Werner et al., 2007). Thus, there is accumulatingevidence that the physiological and behavioral infrastructure that isnecessary for some aspects of simple emotional responding ispreserved in the early stages of FTLD.In contrast, emotional impairment in FTLD clearly occurs in areasof socioemotional functioning that require higher order