Reduced Autonomic Responses to Faces in Capgras Delusion
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Reduced autonomic responses to faces in Capgras delusion HADYN D. ELLIS1*, ANDREW W. YOUNG1,2, ANGELA H. QUAYLE1 and KAREL W. DE PAUW3 1School of Psychology, University of Wales Cardiff, P.O. Box 901, Cardiff CF1 3YG, UK ([email protected]) 2MRC Applied Psychology Unit, 15 Chaucer Road, Cambridge CB2 2EF, UK 3Department of Psychiatry, St James’s University Hospital, Beckett Street, Leeds LS9 7TF, UK SUMMARY People experiencing the Capgras delusion claim that others, usually those quite close emotionally, have been replaced by near-identical impostors. Ellis & Young suggested in 1990 that the Capgras delusion results from damage to a neurological system involved in orienting responses to seen faces based on their personal significance. This hypothesis predicts that people suffering the Capgras delu- sion will be hyporesponsive to familiar faces. We tested this prediction in five people with Capgras delusion. Comparison data were obtained from five middle-aged members of the general public, and a psychiatric control group of five patients taking similar anti-psychotic medication. Capgras delusion patients did not reveal autonomic discrimination between familiar and unfamiliar faces, but orienting responses to auditory tones were normal in magnitude and rate of initial habituation, showing that the hyporesponsiveness is circumscribed. 1. INTRODUCTION since the double can be hated without guilt (Enoch & Trethowan 1991). Closely related to this is Berson’s The Capgras delusion (Capgras & Reboul-Lachaux (1983) idea that the precipitating event is a change 1923; Ellis et al. 1994) is characterized by the patient in crucial interpersonal relationships, producing feel- insisting that others, usually those quite close emo- ings of strangeness and eliciting previously uncon- tionally, have been replaced by doubles, impostors or scious negative feelings. These, claims Berson, lead robots. This bizarre belief can arise as a monosymp- the patient to conclude that the person who elicits tomatic delusion held with conviction despite insight such different feelings is an impostor (Berson 1983, into its irrationality and unbelievability (Alexander pp. 975–976). et al. 1979). It has been noted to follow various types A major problem for psychodynamic accounts, of brain injury (Fleminger & Burns 1993; F¨orstl et however, is that advances in brain imaging have re- al. 1991), has been reported for patients from many sulted in many of the case reports of Capgras delu- different cultures (Christodoulou 1977), and presents sion and related problems of misidentification pub- a significant risk of violence against the alleged im- lished in the last 20 years showing clear neurological postors (de Pauw & Szulecka 1988; F¨orstl et al. 1991; damage (de Pauw 1994; F¨orstl et al. 1991); these im- Silva et al. 1995). ply that, at the very least, psychodynamic accounts The Capgras delusion has long fascinated psychia- do not offer a full explanation. trists (Enoch & Trethowan 1991), and is beginning to Other attempts to explain the Capgras delusion in- attract the attention of philosophers interested in the clude the cerebral hemisphere disconnection hypoth- nature of human consciousness, beliefs and rational- esis (Joseph 1986), which proposes that each cere- ity (Dennett 1996). Although usually considered very bral hemisphere independently processes visual in- rare (Enoch & Trethowan 1991), there are grounds for thinking it may have been under-reported (F¨orstl formation from the face, and that the Capgras delu- et al. 1991). sion arises when the two processes fail to integrate; Psychodynamic accounts of the Capgras delusion the categorization failure hypothesis (Cutting 1991), are still invoked by some authors, and this possi- which suggests that the delusion reflects a distur- bility was explored by Capgras himself (Capgras & bance in the judgement of identity or uniqueness, Carrette 1924). A widely adopted hypothesis has owing to a breakdown of the normal structure of se- been that conflicting feelings of love and hate to- mantic categories; and the memory deficit hypothesis ward a close relative are resolved by the delusion, (Staton et al. 1982), which maintains that there is a failure in the updating of the patient’s mental repre- * Author for correspondence. sentations of familiar faces, and that Capgras delu- Proc. R. Soc. Lond. B (1997) 264, 1085–1092 c 1997 The Royal Society Printed in Great Britain 1085 TEX Paper 1086 H. D. Ellis and others Capgras delusion sion results from the consequent mismatch between by Tranel et al. (1995) of four patients with bilat- what is seen and its ultimately outdated representa- eral ventromedial frontal damage who could recog- tion. nize faces normally yet did not reveal discriminatory There are thus a number of theoretical accounts of SCRs to these familiar faces. The accounts given by possible functional bases for the Capgras delusion in Bauer (1984) and by Tranel et al. (1995) differ with the research literature, but these are usually gener- regard to the exact neurology of pathways mediating ated ad hoc in discussions of individual cases, and are overt and covert recognition, but concur in regarding seldom tested against systematically collected empir- them as neurologically dissociable. ical data. Ellis & Young (1990) proposed that Capgras delu- A particular focus of recent interest has been in sion is the neurological mirror image of prosopag- the hypothesis that diminished affective responses to nosia, resulting from relatively preserved overt recog- familiar visual stimuli may play a causal role. Ellis nition (the patient knows that a face is his wife’s, or & Young (1990) suggested that the Capgras delu- whoever), coupled with a loss of affective responses. sion results from damage to a neurological system in- The delusion is then a misattribution by the patient volved in orienting responses to seen faces based on of a change in his or her internal world (reduced re- their personal significance. On this hypothesis, the basis of the Capgras and other reduplicative delu- sponsiveness to stimuli with personal relevance) to a sions lies in damage to neuro-anatomical pathways change in the external world (replacement by replicas responsible for appropriate emotional reactions to or impostors) (Wright et al. 1993; Young et al. 1993). familiar visual stimuli, and represents the patient’s Such misattributions to external influences are likely attempt to make sense of the fact that these vi- in states of intense suspiciousness (Kaney & Bentall sual stimuli no longer have appropriate affective sig- 1989), known to be a common correlate of Capgras nificance. This conception can be traced back to delusion (Fleminger & Burns 1993). Brochado’s (1936) description of a thesis by Derom- On this account, Capgras delusion reflects an un- bies (1935), and has recently been emphasized by fortunate interaction of different contributory causes, several authors (Anderson 1988; Ellis & Young 1990; among which we have singled out suspiciousness and Lewis 1987; Weinstein & Burnham 1991). A pre- loss of appropriate affective responses (Young 1994). diction made by this hypothesis (and by no other The advantage of this hypothesis is that it generates existing account) is that people suffering the Cap- testable falsifiable predictions that do not follow from gras delusion will be hyporesponsive to familiar faces. other existing accounts. Consistent with this prediction, we show here that We predicted, then, that if tested with procedures Capgras delusion patients do not reveal autonomic used to investigate covert autonomic recognition in discrimination between familiar (famous) and unfa- prosopagnosia (Bauer 1984; Tranel & Damasio 1985, miliar faces. However, orienting responses to auditory 1988), people suffering the Capgras delusion will be tones were normal in magnitude and rate of initial hyporesponsive to familiar faces and will not show habituation for Capgras cases, showing that the hy- differential SCRs to familiar faces even though these poresponsiveness is circumscribed. may be overtly recognized. We tested this predic- Ellis & Young’s (1990) prediction has its origins in tion in five people with Capgras delusion. Compari- the findings of covert recognition in prosopagnosic son data were obtained from five middle-aged mem- patients by Bauer (1984) and Tranel & Damasio bers of the general public, and a psychiatric control (1985). Prosopagnosia involves an inability to recog- group of five patients taking similar anti-psychotic nize previously familiar faces after brain injury in the occipito-temporal region. Although overt recognition medication was used to rule out the possibility that of even the most familiar faces can be lost, some hyporesponsiveness might be due either to medica- prosopagnosics have been shown to reveal autonomic tion or to delusions per se. activity (skin conductance response—SCR) to faces of known individuals; this happens even though, con- 2. METHOD sciously, the prosopagnosic patient is unable to iden- tify the person (Bauer 1984; Tranel & Damasio 1985, (a) Participants 1988). Five people with Capgras delusion participated in the Covert recognition indexed by autonomic activity study. All were psychiatric patients. Table 1 summarizes in prosopagnosia, it has been argued, results from clinical information for these five individuals. In each case the continued operation of a system responsive to the they had expressed the idea that others had been sub- signal value arising from the personal emotional sig- stituted and firmly believed