siology 63 (2007) 146–151www.elsevier.com/locate/ijpsycho

International Journal of Psychophy

Delusions: A suitable case for imaging?

Hadyn D. Ellis

School of Psychology, Cardiff University, Cardiff CF10 3AT, UK

Received 1 February 2006; received in revised form 1 March 2006; accepted 30 March 2006Available online 21 June 2006

Abstract

This review is intended to outline the need/opportunities for imaging research in the area of delusions. In particular, delusions ofmisidentification are offered as possible examples of how both spatial and temporal brain imaging may throw light upon the theoretical, parallelprocesses of identification and emotional arousal occurring when a familiar face is encountered. Other types of Delusional Misidentifications arealso briefly explored. The review then turns to related phenomena, including the ways imaging may help elucidate different types of covert facerecognition; and also further explain the distinctive (but not entirely independent) processes underlying face, voice and object recognition.Throughout the review the aim is to emphasise the potential value to cognitive neuropsychiatry of good imaging techniques.© 2006 Elsevier B.V. All rights reserved.

Keywords: Cognitive neuropsychiatry; Delusions; fMRI; Brain imaging

1. Introduction

The title to this paper includes an obvious rhetoricalquestion. Delusions (or at least some forms of them) areeminent candidates for imaging analysis. Indeed, some successin this regard has recently been claimed, for example, byBlackwood et al. (2004) who, in a fMRI study, found that,compared with matched controls, people diagnosed withschizophrenia with persecutory delusions, when asked aboutthe self-relevance of certain either ambiguous or non-ambigu-ous threat statements, revealed a significant absence of rostral-ventral anterior cingulate activation combined with an increasein activation within the posterior cingulate gyrus.

Compared with the efforts that have gone into analysingmany other cognitive phenomena, however, the use oftechniques such as SPECT, PET, MRI, fMRI and MEG toexplore the structures underlying delusions (and, by implica-tion, beliefs in general) has been limited. The field is clearlyready for a more systematic approach, and in this paper I shallendeavour both to outline some reasons for doing so and to addthe stricture that imaging research must be based upon goodmodels of information processing. In order to do this I shallfocus on a particular set of monothematic delusions, each of

E-mail address: ellish@cardiff.ac.uk.

0167-8760/$ - see front matter © 2006 Elsevier B.V. All rights reserved.doi:10.1016/j.ijpsycho.2006.03.015

which involves inappropriate beliefs about the identity of otherpeople or objects, that have already received extensive analysisusing cognitive neuropsychiatric principles (Ellis, 1998).

1.1. Delusions

First, however, it is necessary to define “delusions”. Inclinical terms, the DSM-IV definition detailed in Table 1 isusually adequate: it emphasises the incorrectness and impossi-bility of the belief — the certainty with which it is held, itsincorrigibility and its cultural atypicality (i.e. beliefs not held bya significant number of others).

While it is possible to unpick each and every one of thesecriteria (Bell, 2006), they do provide a sufficient workingdefinition that has had undeniable pragmatic value and willsuffice here. The group of delusions that will form theremaining focus of this paper exemplify each of the abovecriteria.

1.2. Delusions of misidentifications

The delusions of misidentification (DMS) comprise aninteresting and theoretically challenging set of bizarre beliefsthat have been of particular interest to cognitive neuropsychia-trists over the last 15 years. Each involves a distinct alteration in

Table 1DSM-IV definition of delusions

A fixed false belief based on incorrect inference about external reality that isfirmly sustained despite what almost everybody else believes and despitewhat constitutes incontrovertible and obvious proof or evidence to thecontrary. The belief is not one ordinarily accepted by other members of theperson’s culture or subculture (e.g. it is not an article of religious faith).

Fig. 1. The modal model of face recognition, together with putative sites for theorigin of paraprosopia, intermetamorphosis and the Frégoli delusion.

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the way others are perceived or identified (see Table 2); and, forevery one, cogent explanations have been advanced that linkeach to some putative mechanism of normal informationprocessing — which, of course, is the essential precept ofcognitive neuropsychiatry (Ellis, 1991, 1998; David, 1993).

2. The modal model of face recognition

Ellis and Young (1990) attempted to explain most of theDMSs within an established model of face processing (Bruceand Young, 1986). Over subsequent years this model of facerecognition has been extensively revised (e.g. Burton et al.,1990; Young and Burton, 1999), but, for present purposes, itserves the useful purpose of showing how a facial image iseventually identified by positing three distinct stages: an initial,structural encoding phase where basic visual information isprocessed via mechanisms that extract view-centred descrip-tions independent of expressions; the resulting description isthen passed to a system containing a stored record of all facesknown to the perceiver; these are called the Face RecognitionUnits (FRUs); the final stage is where connections are made toepisodic/biographical information about the individual (i.e.where identity, and subsequently name, are established); this iscalled the Person Identity Nodes (PINs) stage.

Fig. 1 indicates that, potentially, these three stages may eachbe associated with a different DMS (Ellis and Young, 1990;Ellis, 1997; Ellis and Lewis, 2001)— although, in truth, exactly

Table 2The four delusions of misidentification

Paraprosopia Faces transform into a grotesque mask (monster, vampire,werewolf ).‘Autoparaprosopia’ occurs when the transformationappears to the patient's own face when looking into amirror (Ellis, 1997).

Intermetamorphosis Faces (and objects) temporally change into that of someother, known person; some other parts of the body do notchange (Courbon and Tusques, 1923).

Frégoli delusion Named after the celebrated Italian mimic, LéopoldoFrégoli, the delusion involves the belief that significantothers can disguise themselves, usually but not always, inorder to persecute the patient. Essentially, there is no beliefof any physical change in the person: instead the patientbelieves s/he is the disguised version of someone else(Courbon and Fail, 1927).

Capgras delusion The most common delusion of misidentification (1-3% ofthe psychiatric population) involves the belief that othersusually, but not necessarily close to the patient, have beenreplaced by impostors, doubles, robots, etc. (Capgras andReboul-Lachaux, 1923).Capgras-type delusions for objects and voices have alsobeen described (Ellis et al., 1996; Lewis et al., 2001).

how these operate in practice has not yet been established. Atbest one could say that there is at least a superficial plausibilitythat paraprosopia represents disruption at the structural encod-ing stage; intermetamorphosis results from excitation of thewrong FRU; and the Frégoli delusion may happen when,despite being excited by the correct FRU, an inappropriate PINbecomes activated, giving rise to the belief that the person,although veridically perceived, is actually someone else.

The important point to note here is that, howeversuperficially the identification of delusion and face-processingstage has been identified, and acknowledging the lack ofempirical support for these associations, three of the four DMSspotentially can be explained within a model of normal facerecognition and thus fulfil one of the precepts of cognitiveneuropsychiatry. The model, however, does not admit anexplanation of the most prevalent DMS, the Capgras delusion,whereby patients normally have a reasonably veridical perceptfrom which they could infer identity — instead of which theyinsist that the individual is an impostor, a double or whatever.

It should be noted that more recent models of facerecognition have emphasised its distributed nature sharingearly processing features of other objects within both theoccipital and the temporal cortex (Haxby et al., 2001; Ishai etal., 2000). As Haxby et al. (2001) have pointed out, however,this approach is not incompatible with more modular models,such as Bruce and Young's, but, as we shall see later, it mayhave significance for imaging predictions.

2.1. Capgras delusion

In order to account for the Capgras delusion Ellis and Young(1990) stepped out of the psychiatric arena to considerneurological cases of prosopagnosia (Bodamer, 1947; Mea-dows, 1974), where, usually following specific brain injury,there is an almost absolute inability to recognise faces (leavingidentification by voice, gait, dress, etc. unaffected). Someindividuals with prosopagnosia, however, have been shown toreveal what has been termed covert face recognition (Bauer,1984; Young and Ellis, 2000), suggesting that, at an unconscious

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level, some facial information can affect either cognitive orautonomic activity. Bauer (1984), using a technique normallyemployed in forensic lie detection, noted that the prosopagnosicpatient, L.F., revealed elevated skin-conductance responses topreviously-familiar faces even though he could not consciouslyidentify them.

The subsequent use of SCRs to investigate responses to facesand other stimuli by those with prosopagnosia and healthyindividuals has proved quite illuminating (Tranel and Damasio,1985), prompting Ellis and Young (1990) to suggest that peoplewith the Capgras delusion would demonstrate the oppositeeffects to those shown by L.F. and others with prosopagnosia,i.e. reveal overt identification but not covert recognition.Normal individuals show reduced SCR to familiar comparedwith unfamiliar faces (Tranel and Damasio, 1985; Ellis et al.,1993), familiar voices (Reid et al., 1993; Lewis et al., 2001),familiar landmarks (Sherwood, 2004), but, interestingly, notfamiliar names (Ellis et al., 1999). Just what these phenomenasignify is open to speculation, but it is widely accepted asindicating the registered significance/emotional familiarity ofcertain classes of stimuli.

According to Ellis and Young (1990), people with theCapgras delusion lack the usual input regarding a face's personalsignificance; but, where the face is of someone particularlyclose, the absence of this information can be the precursor to thedelusion. That is to say, normally the emotional significance of aface is automatically integratedwith input regarding the person'sidentity: when the former is absent problems may ensue.

This argument led to the obvious prediction that those withthe Capgras delusion, shown a series of familiar and unfamiliarfaces, would not reveal differential SCRs to the two types ofstimuli. This predicted result was confirmed by two indepen-dent studies (Ellis et al., 1997; Hirstein and Ramachandran,1997). Ellis et al. found that five patients with Capgras delusion,when shown a series of familiar and unfamiliar faces, did notdemonstrate the same SCR differences as either matchedpsychiatric patients or normal controls (see Fig. 2). The study byHirstein and Ramachandran involved a neurological patient

Fig. 2. Skin conductance response to familiar and unfamiliar faces by fiveindividuals with the Capgras delusion and matched psychiatric and normalcontrols. Adapted from Ellis et al. (1997), Proc. R. Soc. B.

who developed Capgras delusion for his parents following a caraccident. His SCRs, too, failed to differentiate unfamiliar fromfamiliar faces (some of which were of personally known people,rather than of famous people).

3. Revised model of face recognition

These results provide strong, albeit circumstantial, evidencefor the idea that face recognition involves more than one route(Bauer, 1984), which itself necessitates a significant modifica-tion to models based upon the notion of a single route. Bauersuggested these routes as serving: (1) overt recognition: aventral route (from visual cortex to limbic system via theinferior longitudinal fasciculus); and (2) covert face recognition:a dorsal route via the superior temporal sulcus and inferiorparietal lobule.

Breen et al. (2000) then offered an alternative model that wasnot based upon what they demonstrated to be Bauer'sinappropriate neuroanatomy, which was further modified byEllis and Lewis (2001). (See Fig. 3) The essence of this newmodel is that, while the left side is, essentially, no different fromthat offered by Bruce and Young (1986) and is also compatiblewith the distributed model of Haxby et al. (2001), the right sideof the diagram includes a box representing affective responsesto familiar faces that processes outputs from the FRU stage inparallel with the PIN stage. A subsequent stage involves anintegration of the information provided by the PIN stage and theaffective-response stage: any significant discrepancy betweenthe two registers as an anomalous experience that, under somecircumstances, leads to the Capgras delusion. It is worth notingthat the absence of an appropriate affective response to afamiliar face cannot itself account for the delusion. Tranel et al.(1995) showed that patients with fronto-ventro-medial lesionsalso failed to show the normal SCR discrepancy betweenfamiliar and unfamiliar faces— but did not develop the Capgrasdelusion.

4. Imaging the capgras delusion

So far, so good. But, however cogent the model may appearto be, it requires corroboration from functional imaging and thatexercise has yet to be undertaken systematically.

Only one imaging study of a patient with Capgras delusionhas been published. This SPECT analysis was carried out byLebert et al. (1994) and revealed gross hemispheric changes inblood flow, viz. a 20% reduction in right parietal activity. Thiswas consistent with a study by Ellis et al. (1993) who foundthat a group of individuals with the Capgras delusion showedmarkedly slower RTs than controls when deciding whether twofaces tachistoscopically shown in the left visual field (i.e.going first to the right hemisphere) were the same or different;no such difference was observed when both stimuli fell in theright visual field (i.e. initially arriving at the left cerebralhemisphere).

However, in order more adequately to inform our under-standing of the Capgras delusion and also to provide invaluableinformation about normal face processing, more detailed,

Fig. 3. The revised face-recognition model by Ellis and Lewis (2001). An abnormality at Awill lead to prosopagnosia. An abnormality at B will lead to the Capgrasdelusion. An abnormality at C, however, will produce a reduced SCR for familiar faces but no delusion.

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sophisticated systematic investigations are required. ManyfMRI studies have already revealed the role in face processingof structures such as the lateral fusiform gyrus (Kanwisher et al.,1997) and temporal cortex (retrosplenial) (Shah et al., 2001).These studies, however valuable, with the exception of theapproach taken by Haxby et al. (2001), have not been expresslyinformed by the kinds of model illustrated in Fig. 3; and nonehas attempted systematically to examine the putative role ofaffective responses in the process of normal face recognition,where structures such as the amygdala are likely to be involved.Zald (2003) has reviewed the role of the amygdala in theemotional evaluation of sensory stimuli, though there is moreevidence for its part in assessing aversive as opposed topositively balanced stimuli (See also Green and Phillips, 2004.)Just how this difference might reveal itself in the Capgrasdelusion is impossible to guess. Imaging, however, may wellprovide the answer. The amygdala does have a role to play inSCR, but those having undergone bilateral amygdalectomy stillshow differential SCRs to stimuli suggesting that the amygdalais not solely responsible for this autonomic manifestation ofarousal (Zald, 2003).

There are a number of other questions raised by DMSresearch that would also yield answers by appropriate imaging.These include: stimulus type; and the very nature of covertrecognition itself. These will be examined in turn.

4.1. Stimuli

As was briefly mentioned earlier, both intermetamorphosisand the Capgras delusion have been observed for stimuli otherthan faces. This has only been explored empirically for theCapgras delusion.

4.1.1. ObjectsAnderson (1988) was the first to describe a case of Capgras

delusion for objects. Here the patient developed the belief that

his wife and her nephew were stealing his tools andsystematically replacing each one with an inferior copy.Eventually some 300 items were believed by him to havebeen changed — but, importantly, he never evinced any suchdelusion for people.

Ellis et al. (1996) reported two similar cases. Eachinvolved middle-aged women who believed that personaland household items had mysteriously been replaced bysimilar items. Again, neither woman held any such beliefsabout people being impostors. It would be parsimonious, tosay the least, to argue that whatever mechanism(s) underliethe Capgras delusion for faces (i.e. absence of the usualemotional recognition) should apply equally to the samedelusion for objects. However, a common mechanism isunlikely. Instead it is necessary to posit a distinct one,whereby emotional recognition for objects is enabled inparallel to conscious recognition. Van Lancker (1991) hasargued persuasively for such a mechanism that imbuesparticular, familiar objects with affective significance. Func-tional imaging may well also help further to distinguish thosebrain areas involved in recognising familiar faces from thoseprimarily tuned to familiar objects — sometimes conflatedinto a single mechanism based upon expertise (e.g. Gauthieret al., 2000). Ishai et al. (2000) and Haxby et al. (2000) haveshown how brain structures involved in face recognition andman-made objects share common features, but, nonetheless,however distributed these may be, areas of the brain areespecially tuned to different types of visual input.

4.1.2. VoicesThe same conclusion may be drawn between the processing

of familiar voices and faces. Ellis et al. (1997), using primingtechniques, showed that the two systems were similar in manyways but are parallel, with no overlapping mechanisms.Following his car accident, Hirstein and Ramachandran's(1997) Capgras delusion patient thought his parents were

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impostors when confronted with them directly, but, on thetelephone, they sounded normal. This observation wasreinforced by Lewis et al. (2001) in a study of a woman whodeclared her son to be an impostor based upon his voice — i.e.the opposite signs from those revealed by Hirstein andRamachandran's patient.

Again, it may be surmised that functional imaging offers anexcellent means of establishing how identity is normallyestablished via faces and voices and how the processes canbreak down independently in different forms of the Capgrasdelusion.

4.1.3. NamesAt this point it is worthwhile mentioning that, while the

general rule seems to be that familiar stimuli produce largerSCRs compared with those elicited by unfamiliar stimuli, thereis at least one exception: names do not follow this pattern. Intwo experiments Ellis et al. (1999) found no such SCR effectswhen famous and unknown names were shown to participants.

This finding has no bearing on the discussion regardingdelusions but it does reinforce the general point that differentsystems underlie the process of recognition. In the case ofperson identification the same ultimate conclusion (“it is x?”)may be reached via face, voice or name but it seems that eachinvolves quite distinct mechanisms that can be superficiallyestablished by conventional, behavioural experiments butrequire detailed functional imaging exactly to locate thesupporting brain structures, together with temporal analysisusing, say, magnetic electroencephalography to determine, ineach case, the sequence of operations, and how, eventually, theyconverge towards the same end point (i.e. identification of anindividual).

5. Unconscious recognition

As has been said, people with the Capgras delusion do notreveal the usual familiar>unfamiliar faces SCRs (Ellis, 1997).They appear to lack the normally automatic affective input thatfamiliar faces engender — an omission most significant for thefaces of those personally close to them.

It was also pointed out that people with prosopagnosia notonly reveal covert recognition through differential SCRs forpreviously familiar faces (Bauer, 1984) but have also beenshown to do so using a number of other methods (see Youngand Ellis, 2000). For example, they learn correct face–namepairings more easily when the stimuli are personally known(Bruyer et al., 1983); they reveal face–name or self-priming(i.e. a “known” face preceding its name that has to beclassified as familiar or unfamiliar is responded to faster (DeHaan et al., 1987)); when a name is shown to be classified(say, either pop star or politician) the presence of apreviously-known face from the other category interfereswith the process and increases response times (De Haan et al.,1987). All of these methods, as well as others, have shownthat, up to a point before conscious awareness, people withprosopagnosia can correctly process information aboutpreviously known faces.

De Haan et al. (1992) decided to test L.F., the first individualwith prosopagnosia in whom autonomic covert recognition hadbeen observed, with both an interference task and a self-primingtask. L.F. revealed covert recognition in each, leading De Haanet al. to conclude that “… autonomic and behavioural indices ofcovert recognition reflect the same, or similar neuropsycholog-ical phenomena”.

The obvious question to ask is: given that L.F. showed bothautonomic and behavioural covert face recognition, would thosewith the Capgras delusion show neither? To answer thisquestion Ellis et al. (2000) tested B.P., a 69-year-old womanwith Capgras delusion, together with six non-psychiatriccontrols. Each was given a standard familiar/unfamiliar faceSCR test; a self-priming task (names to be classified forfamiliarity preceded by same face or another's face); and aninterference test (incidental faces present while names wereclassified by occupation).

The results were unequivocal: unlike all the controls, B.P.'sSCRs did not differentiate between familiar and unfamiliarfaces. However, B.P. showed exactly the same behaviouralcovert recognition effects as the controls. In other words,different kinds of covert face recognition are not mediated bythe same mechanism as De Haan et al. concluded. Rather theremust be at least two different processes, one governingautonomic ‘recognition’ and the other behavioural ‘recogni-tion’. Again, one cannot avoid the thought that studies usingfMRI/MEG will provide further illumination.

6. Conclusion

Green and Gazzaniga (2001) have made a persuasive case forlinking neuroimaging and cognitive neuropsychiatry – espe-cially for the study of schizophrenia – yet imaging delusions ofbelief have yet to be fully embraced by the imaging community.

The area of delusions in general and delusions ofmisidentification in particular are ideal candidates for imaginganalyses — both spatial and temporal. These would not onlyhelp us to understand how these anomalous states occur but alsocast important light on how beliefs develop and, specificallyfrom studies of DMS, either validate and extend the model inFig. 3 or, if the analyses prove not to be consistent with it,suggest new ways of understanding face processing. What willbe essential is that imaging studies are informed by the data onnormal information processing gathered over the last 50 years,together with the theoretical insights they have generated. Alltoo often sophisticated imaging studies have been limited bytheir failing to be firmly grounded upon good cognitive models.Future imaging studies of delusions and belief should not makethe same mistake.

Acknowledgements

I should like to thank Professor Peter Halligan, Dr. MichaelLewis and Diane Ellis, Cardiff University, for their commentson an earlier draft of the paper; and the helpful comments of ananonymous referee are also gratefully acknowledged. Email:EllisH@cardiff.ac.uk.

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