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pilepsy Research (2009) 85, 162—171
journa l homepage: www.e lsev ier .com/ locate /ep i lepsyres
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elusions, illusions and hallucinations in epilepsy:. Elementary phenomena
rent Elliotta, Eileen Joyceb, Simon Shorvonb,∗
National Hospital for Neurology and Neurosurgery, United KingdomUCL Institute of Neurology, University College London, United Kingdom
eceived 31 October 2008; received in revised form 8 March 2009; accepted 15 March 2009vailable online 6 May 2009
KEYWORDSEpilepsy;Hallucinations;Delusions;Illusions;SEEG;Cerebral localisation
Summary The purpose of this paper and its pair is to provide a comprehensive review, from thedifferent perspectives of neurology and neuropsychiatry, of the phenomenology and mechanismsof hallucinatory experience in epilepsy. We emphasise the clinical and electrophysiological fea-tures, and make comparisons with the primary psychoses. In this paper, we consider definitionsand elementary hallucinatory phenomena. Regarding definition, there is a clearly divergentevolution in meaning of the terms delusion, illusion and hallucination in the separate traditionsof neurology and psychiatry. Psychiatry makes clear distinctions between the terms and hasfocussed on the empirical use of descriptive psychopathology in order to delineate the variouspsychiatric syndromes, including those in epilepsy. These distinctions in psychiatry have stoodthe test of time and are useful in clinical descriptive terms, but do not help to understand thebasic mechanisms. The focus of neurology has been to regard delusions, illusions and hallucina-tions in epilepsy as a result of localised or network based neuronal epileptic activity that canbe investigated especially using intracranial stereoelectroencephalography (SEEG). The neu-rological approach leads to a more synoptical definition of ‘hallucination’ than in psychiatryand to the conclusion that there is little point in differentiating hallucination from illusion ordelusion in view of the overlap in the physiological bases of the phenomena. The semiologi-cally derived differentiation of these terms in psychiatry is not supported by similarly discreteelectrophysiological signatures. However, as discussed in the second paper, some psychotic
states are associated with similar electrophysiological changes. The wide range of hallucina-tory symptoms occurring during epileptic seizures recorded during intracranial SEEG and brainstimulation are reviewed here, including: experiential and interpretive phenomena, affectivesymptoms, as well as auditory, olfactory, gustatory, somatic and visual hallucinatory phenom-ena. Several conclusions can be drawn. First, it is clear that there is only limited anatomicalspecificity of many hallucinatory states. Repeated seizures or stimulation of a single area,even within the same patient can produce different psychic responses, whilst stimulation of∗ Corresponding author at: Department of Clinical and Experimental Epilepsy, National Hospital for Neurology and Neurosurgery,ueen Square, London, WC1N 3BG, United Kingdom. Tel.: +44 845 155 5000x4194; fax: +44 207 676 2155.
E-mail address: [email protected] (S. Shorvon).
920-1211/$ — see front matter © 2009 Elsevier B.V. All rights reserved.oi:10.1016/j.eplepsyres.2009.03.018
Delusions, illusions and hallucinations in epilepsy
widely distinct areas (especiallyremarkably similar phenomena. Tincluding experiential phenomenspecific areas from this point ofvisual and auditory cortices. Invorence of complex hallucinatory strecognised at least since the 1960the mesial temporal lobe, insula
networks.© 2009 Elsevier B.V. All rights reserved.Contents
Definitions ............................................................................................................... 164Experiential mental phenomena evoked by brain stimulation............................................................. 164SEEG correlates of hallucinatory symptoms recorded during seizures in patients with epilepsy ........................... 166Discussion................................................................................................................ 170References ............................................................................................................... 170
‘If sensitive nerves are enough to make a poet I should beworth more than Shakespeare and Homer. . . I who haveheard through closed doors people talking in low tonesthirty paces away, across whose abdomen one may seethe viscera throbbing, and who have sometimes felt inthe space of a minute a million thoughts, images andcombinations of all kinds throwing themselves into mybrain at once, as it were the lighted squibs of fireworks.’Correspondence of Flaubert, (Lombroso 1891).
The term ‘lighted squibs of fireworks’ is a pertinent wayof describing the disordered bursts of energy which under-pin at least some of the hallucinatory experiences seen inepilepsy.
Historically, much of the research in this area derivesfrom the field of psychiatry, with its emphasis on the empiri-cal use of descriptive psychopathology in order to delineatethe various psychiatric syndromes and determine to whatextent the psychopathology (i.e., abnormalities of affect,thought, and perception) seen in epilepsy is similar to, ordiffers from that seen in the major mental disorders, forexample schizophrenia.
By contrast, there has been an almost entirely sepa-rate tradition within neurology. The central theorem ofthis school is that hallucinations occur as a consequence ofthe activation of a localised group of neurones which canbe investigated by cerebral recording and cerebral stim-ulation, and the ‘Gold Standard’ investigation has beenintracranial stereoelectroencephalography (SEEG). Over thepast 50 years this application has greatly clarified someof the details regarding the anatomical basis and physio-logical mechanisms underpinning hallucinations in epilepsy.Throughout this period psychiatry has tended to echo theview of Hughlings Jackson that compound mental states‘cannot be owing to an epileptic discharge’ (Jackson, 1958),however, whilst it is true that complex psychic states as seen
view into question and it appears, in at least some cases,that complex psychotic symptoms are directly due to theeffects of non-convulsive epileptic activity (limbic status) orto the indirect after-effects of chronic epileptic discharges.
The purpose of this set of two papers is to provide a com-prehensive review of the phenomenonology of hallucinationsin epilepsy from a specifically neurological and neuropsy-chiatric standpoint, and to draw distinctions between thisapproach and that of clinical psychiatry. The term ‘halluci-nation’ is here taken to encompass a range of phenomenagiving it a very different usage to that seen in psychia-try. Based as it is on electrophysiological findings, our mainthrust is to present SEEG evidence which demonstrates thathallucinations often have an electrophysiological basis, usu-ally involving widely disseminated limbic structures. In thisfirst paper, we begin with a brief review of definitions and ofthe different meanings assigned to key terms such as ‘hal-lucination’ and ‘psychosis’ that have emerged as a resultof the divergent evolution of very separate neurologicaland psychiatric traditions. We then consider the elemen-tary hallucinatory states which are observed during brainstimulation, and during spontaneous brief epileptic seizures.
In the second paper we consider the more complex andprolonged states associated with complex partial statusepilepticus, postictal and interictal psychosis. The similarityof these latter states to the primary psychoses raises inter-esting questions about the pathophysiology of psychosis.
It is important to recognise that SEEG does have a majorlimitation, namely sampling bias, which we would like tomention at the outset. The electrodes record activity fromonly a very small area in the vicinity of the electrode(measured in millimetres), and activity in areas beyondthis will be overlooked. This is important as there aremany indications that limbic functional (and dysfunctional)activity is often a widely distributed network phenomenoninvolving disparate interconnected neuronal areas. Gloor for
in the ‘functional’ psychoses have less often been correlatedwith abnormalities on SEEG, as Trimble (1991) points out‘specific Schneiderian phenomena have not been recordedbut in all probability have not been examined for.’ There isnow a considerable body of SEEG evidence which calls this
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163
in the limbic system) within the same individual can producehis lack of specificity applies particularly to psychic symptoms,a, and complex hallucinatory states. The most anatomicallyview are the elementary hallucinations arising from primarylvement of the limbic cortex is a pre-requisite for the occur-ates. It is clear that on the basis of these findings, as has beens, that even apparently focal epileptic seizures, (especially in
and limbic cortices), must involve widely distributed neuronal
nstance, has shown repeatedly that the concept of a smalliscrete limbic epileptic focus is inaccurate and that limbiceizures (even with focal pathology, such as hippocampalclerosis) may involve simultaneously a wide network ofeuronal activation, not necessarily even contiguous. This
164 B. Elliott et al.
Table 1 Summary of the conventional definitions as used commonly in psychiatry.
Hallucination (David, 2004) ‘A sensory experience which occurs in the absence of corresponding external stimulation ofthe relevant sensory organ, has sufficient sense of reality resemble a veridical perception,over which the subject does not feel direct and voluntary control, and which occurs in theawake state’.
Illusion These are false perceptions of a real external stimulus, for example a change in shape, size,colour or texture. In some cases, where the external stimulus is minimal, the differentiationnosologically from hallucination can be difficult, although illusions carry different aetiologicaland diagnostic implications.
Delusion Delusions are abnormalities of thought rather than perception (although they may developfrom the latter) and may be defined as ‘fixed false beliefs, strongly held and immutable in theface of refuting evidence, that are not consonant with the person’s education, social andcultural background.’ (Sadock and Sadock, 2000). As with hallucination, this term has aninteresting history (Berrios and Dening, 1996) and its exact meaning and usage have evolvedcontinuously, reflecting trends in psychology. Delusional themes commonly include: guilt,worthlessness, ill-health, persecution, reference, grandeur, love, jealousy, poverty,infestation, and religion. A range of beliefs are also recognised that lie somewhere between
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ame limitation almost certainly applies to the productionf complex psychological symptoms. Since the scalp EEGs often normal despite widespread activity on SEEG, weegard this investigation as an unreliable indicator of ongo-ng ictal activity and it is not considered any further.
This series of papers provides no definitive answers touestions about mechanisms of hallucinatory or psychotictates, nor do we that all psychiatric states have the samehysiological basis, but we intend our review to provide aramework for future investigation into the potential phys-ological causes of psychosis and more clearly to define theverlap that is undoubtedly present between epilepsy andsychosis.
efinitions
he thesis within neurology that delusions, illusions andallucinations in epilepsy are a symptom of localised oretwork-based neuronal spike or spike-wave activity pointso a fundamental distinction between the approaches ofeurology and psychiatry.
An exemplar of this problem can be viewed in the classicescription given by Williams (1959) of an hallucination: ‘byopular usage an hallucination, which is a percept withoutstimulus, may be organic or psychotic. An organic halluci-ation occurs when through brain disease the patient has aercept without stimulus, into the nature of which he usu-lly has insight. Local disturbance of the brain has evokedperceptual response. . . But percepts may arise within the
ody—–be proprioceptive as well as exteroceptive, and therean be no fundamental difference between sensations feltn a limb or through the eye as a result of a local epilepticischarge. . . For the physiological changes in the cerebrumesponsible for both are similar. They can all be considered
rganic hallucinations, caused by the epileptic discharge. . .he feelings called fear, depression or pleasure arising in thettack [also] have no local reference, in other regards theyre similar, and for physiological purposes can be consideredo be organic hallucinations.’
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, these ‘overvalued ideas’ are often best considered asccupations, the unlikely validity of which the holder has
From the psychiatric perspective, the definition of hal-ucination is broadly similar (Table 1), but the usage isuite different. Whilst most psychiatrists would consider theatient experiencing complex auditory hallucinations or per-ecutory delusions to be ‘psychotic’, probably none wouldxtend this term to include those experiencing ictal affectsuch as fear, depression, pleasure, deja vu, rage or indeedn epigastric rising sensation. The electrophysiological basisf these phenomena are not considered due to the histori-al emphasis of descriptive psychopathologists on providingsystem of empirically derived, phenomenologically based
ategories, without reference to causation. The meticu-ous but empirical categorization of hallucinatory symptomsn psychiatry has served the discipline well, but does notdvance an understanding of the cerebral mechanisms. Weope that the neurological approach, embedded in physiol-gy, will illuminate at least some of these interesting andhallenging clinical hallucinatory phenomena.
Distinction between these diverse categories in epilepsys not possible at the electrophysiological level. Repeatedeizures or stimulation of a single area, even within the sameatient can produce different psychic responses (Baldwin,960; Weingarten et al., 1976; Horowitz et al., 1968) whilsttimulation of widely distinct areas within the same individ-al can produce remarkably similar phenomena (Horowitzt al., 1968; Penfield and Perot, 1963; Fish et al., 1993). Yetsychiatry must remain reliant on the distinction betweenhese phenomena in order to produce reliable diagnoses ando advise on treatment and prognosis as well as to manageisk. This semiological approach need not detract from anppreciation of the electrographic basis, thus, in the rest ofhis paper, we use the term hallucination broadly, to refero all these phenomena.
xperiential mental phenomena evoked by
rain stimulationhe first major study of auras (a simple partial seizure occur-ng within seconds before a complex partial or secondarily
165
Table 2 Experiential illusions and hallucinations observedwith stereotaxic exploration of the temporal lobes.
Experience No. ofobservations
No. ofpatients
Visual illusions 9 3Elementary visual
hallucinations (phosphenes)15a 3
Complex visual hallucinations 18 5Elementary auditory
hallucinations0 0
Complex auditoryhallucinations
3 2
Olfactory hallucinations 2 1Familiarity (déjà vu) 23 4Unfamiliarity (jamais vu) 0 0Forced thinking 10 2Fear >49 7Anger 1b 1Irritation >3 1Emotional distress (depression,
guilt etc.)6c 3
Thirst 10 2Feeling of bodily distortion 2 1
Adapted from Gloor et al. (1982).a All induced by electrical stimulation.
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Delusions, illusions and hallucinations in epilepsy
generalized tonic-clonic seizure) was that of Gowers (1901)who reported psychical auras in 4.6% of over 2000 cases.By 1938 Penfield had discovered that such mental phenom-ena could also be reproduced by electrical stimulation ofthe temporal lobe in epileptic patients during surgical pro-cedures performed for intractable epilepsy (Penfield, 1938).His particular interest was in the evocation of memory andhe subsequently made a distinction between what he called‘experiential’ and ‘interpretive’ mental phenomena. Thesehave received remarkably little attention from subsequentresearchers and are therefore briefly reviewed here.
Experiential phenomena were said to represent men-tal events from the patient’s personal past; they may beespecially vivid and combine elements of perception, mem-ory and affect in a unified subjective experience (Glooret al., 1982). Interpretive phenomena had to do with thepresent circumstances of the patient and included illusionsand emotions. Gloor (1990) summarises the key featuresof ‘experiential responses’ as follows: (a) there may be avivid or intrusive recall of a past event; (b) there is a feel-ing of familiarity or reminiscence (déjà vu, deja vécu); (c)the characteristic sensation of dreaminess; (d) the patientis said to be always aware of the incongruity and illusorynature of the experience; (e) affective states such as fear,sadness, guilt, anger or sexual excitement are common; (f)these responses typically lack certain features such as for-ward motion in time (with the exception possibly of musicalhallucinations) and scenes do not evolve; and (g) auditoryhallucinations are said to be almost entirely without seman-tic content (i.e., they lack coherent meaning).
Penfield and Jasper (1954) subdivided psychical seizuresinto four groups: (1) illusions, (2) emotions, (3) halluci-nations and (4) forced thinking. For Penfield, who wasessentially a localisationist, hallucinations were in factmemory images with the particular memory evoked depend-ing on which engram happened to be closest to the siteof stimulating electrode. A key element of Penfield’s laterthinking was the idea that experiential responses occur vir-tually only in seizures arising from the lateral temporalisocortex, where the stimulus was strong enough to pro-voke an after-discharge (in stimulation-induced seizures an‘after-discharge’ is the term used to describe the contin-uation of neuronal activity which outlasts the stimulationtrain. This may indicate spread to other structures; Penfieldand Perot, 1963). The localisation to the lateral cortex hasbeen shown to be incorrect, and we go into further detailhere, to emphasise the fundamental point that much ofthe complex hallucinatory experience in epilepsy cannot bewell localised — this ‘phrenological’ conceptualisation is notbacked up by the electrophysiological data — although as wewill see below the more elementary the phenomenon themore localised it tends to be.
Halgren et al. (1978) reported the results of 3495 stim-ulations of the medial temporal lobe of 36 patients withpsychomotor epilepsy. Just 267 (7.6%) elicited a mentalresponse which included hallucinations of complete scenes,déjà vu, anxiety and visceral sensations. Like Penfield they
found that the presence of an after-discharge was neces-sary but not sufficient for an experiential response to occur,whilst also suggesting that mental phenomena evoked bymedial temporal lobe stimulation were idiosyncratic andrelated to the personality of the patient. Others have takenp
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b Angry mood and facial expression (no aggression).c In one instance may have been caused by strong nausea.
p this point and attempted to integrate personality fac-ors by arguing that hallucinations are symbolically relatedo ongoing psychodynamic processes (Mahl et al., 1964;ayport and Ferguson, 1974; Ferguson et al., 1969). Theseactors were not addressed in Penfield’s earlier studies,or were attempts made to check the veracity of patientsvoked ‘memories’ (Trimble, 1991).
The anatomical basis was revised further by Gloor etl. (1982) who imputed a key role for limbic structuresather than temporal neocortex. In his study he attemptedo reproduce fragments of experiential seizure phenomenay electrical stimulation of intra-cerebral depth electrodesn 35 patients with medically intractable epilepsy. Psycho-ensory symptoms were elicited in 18 (52%) and had usuallyccurred as part of the patients previous seizure experience.timulation of limbic structures produced experiential phe-omena far more frequently than stimulation of temporaleocortex or white matter with the amygdala producing theost responses (n = 44), followed by hippocampus (n = 26)
nd parahippocampal gyrus (n = 12). Even complex visualallucinations were reported with limbic stimulation alone,hilst stimulation of temporal neocortex and white matter
esulted in only five elementary visual hallucinations whichere most likely caused by stimulation of optic radiationbres. In only two instances was the temporal neocortexlone involved in the production of a response. The seizurehenomena elicited are outlined above in Table 2.
More recent work (Gloor, 1990; Fish et al., 1993) con-inues to cast doubt on Penfield’s original emphasis on theole of the temporal neocortex, and indeed on the con-ept that the symptoms have a well-localised basis. Fish et
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l. (1993) studied the clinical responses obtained by elec-rical stimulation of the temporal and frontal lobes in 75atients undergoing pre-surgical evaluation using chronicntra-cerebral EEG recording. Responses were subdividednto: (1) complex perceptual illusions and hallucinations;2) mnemonic phenomena (flashbacks of personal memoriesnd déjà vu) and (3) affective responses. Experiential phe-omena (without an after-discharge or one limited to thetimulation site) were elicited in 20 patients. Auditory hal-ucinations occurred in two (in both cases combined withisual hallucinations), visual hallucinations and illusions inight, fear also in eight and affective responses other thanear in four. In common with previous findings stimulation ofhe amygdala produced the most responses, followed lessften by the hippocampus and only rarely from the tempo-al neocortex. The same phenomenon could be elicited bytimulation of widely varying areas even within the sameatient, and the habitual auras could in some cases belicited by stimulation of different areas. The authors alsoonclude that unless limbic structures are activated experi-ntial phenomena (including emotional responses, illusionsf familiarity and both complex auditory and visual halluci-ations) do not occur. They speculate that limbic activationy means of a seizure discharge may add an affective dimen-ion to perceptual data processed by the temporal neocortexhich ‘may be required for endowing them with emotional
mmediacy.’ Vignall et al. (2007) provided an elegant SEEGtudy of the ‘dreamy state’ as originally described by Jack-on. 40 stimulations were carried out in 16 subjects and 15eizures in 5 subjects. A total of 15 sensations of déjà vecu,5 visual hallucinations and 5 feelings of strangeness wereecorded. 45% of the dreamy states were evoked by stimula-ion of the amygdale, 37.5% of the hippocampus and 17.5%f the parahippocampal gyrus. There was no involvement ofhe temporal neocortex in any of the dreamy states recordedn spontaneous seizures or by stimulation and indeed theuthors considered that spread to the lateral cortex inhib-ted the state. It was also thought that the déjà vecu andisual hallucinations were part of a clinical continuum con-isting of a memory relived by the patient, and that thetudy demonstrated the existence of large neural networksnderpinning memory recall which could be activated viahe hippocampus, amygdala and rhinal cortex.
Gloor (1990) evolved what he called the ‘matrix the-ry’ to try to explain these findings. He considered that thexperiential phenomena in temporal lobe epilepsy were nothe result of loss of inhibitory control, as Hughlings Jack-on (Jackson, 1958) and Halgren et al. (1978) believed, butere the result of positive activation of limbic structures.e hypothesised that: ‘evocation of an experience dependsn the formation of a specifically patterned matrix madep of excited and inhibited neurons dispersed within widelyistributed neuronal populations in large areas of isocor-ex and of the limbic system. Such a matrix which encodests perceptual, mnemonic and affective information can behought of as ‘representing’ an experience and to be specificor it. What carries the specific information is not the activ-
ty of any single cell within this population, but the specificattern of connectivity woven between the neurons whichreates a distributed matrix of excitation and inhibition ands specific for the experience it ‘represents’. . . [He proposedhat] an epileptic discharge within the temporal lobe at theB. Elliott et al.
nset of a seizure, when it has not yet become too diffuse oroo intense, may be able to recreate a specific matrix thatay be similar or identical to that normally encoding a natu-
al experience. Repeated discharge through mechanisms ofynaptic plasticity known to be affected by epileptic dis-harge may have strengthened the interconnectivity of theeurons constituting such a matrix.’
This hypothesis would require the requisite structureso be reciprocally interconnected and this would appear toe the case (e.g., Van Hoesen, 1982). If these phenomenao arise from activation of matrices in distributed neu-onal networks, then they could presumably be elicited fromifferent areas of the temporal lobe including temporal iso-ortex, thus allowing reconciliation with Penfield’s earlierbservations. Similarly, it would not be surprising that stim-lation of the limbic ‘receiving end’ could elicit responseshat reflect functions of the areas from which these connec-ions originate.
It is also clear that these ‘experiential’ states differarkedly from the complex psychotic symptoms seen in
he functional psychoses or in the psychoses of epilepsy,lthough it is not clear to what extent this sort of spe-ific psychopathology was examined for. However, the keyhemes that do emerge are that complex hallucinations andrange of abnormal affective states do occur in response
o stimulation of predominantly limbic structures with rela-ively limited localisational specificity, at least compared torimary neocortex.
EEG correlates of hallucinatory symptomsecorded during seizures in patients withpilepsy
wo vital technical developments underpin much of theork cited in this review. These are the ability to recordEG activity from deep structures (particularly deep lim-ic structures) via SEEG and the ability to make long-termecordings via EEG telemetry. These developments permithe study of ictal and interictal phenomena. The data reduc-ion and storage needed, require advanced computing andlectrode technologies, as well as atlases for electrodelacement. The first studies were conducted in the 1950snd the technologies are now used on a worldwide basis.hese data provide the most convincing evidence concern-
ng the anatomical bases of hallucinatory phenomena; heree review some examples from what is a large literature.
a) Affective and related psychological symptomsThe studies of Penfield, Gloor and others are men-
tioned above. Other groups have elaborated upon thiswork. Wieser and colleagues have provided a num-ber of illuminating and very detailed SEEG studies inpatients being evaluated for epilepsy surgery. At thecore of this work lies a detailed review of 213 seizuresin 29 patients (Wieser, 1983), using arrays of record-ing electrodes typically placed in the hippocampus,
parahippocampal gyrus, amygdala and cingulate gyrus.A wide variety of psychological symptoms have beenrecorded during periods of ongoing epileptic seizureactivity (as recorded by these deep electrodes), particu-larly if this activity was prolonged, therefore amounting
Delusions, illusions and hallucinations in epilepsy 167
Flc
Figure 1 Long lasting clonic discharge in the left periamyg-dalar region during a rage attack (Wieser, 1983).
to limbic status epilepticus. Five examples are providedbelow:
An intracranial EEG recorded during a rage attack isshown in Fig. 1 and another recorded during a laughingfit can be seen in Fig. 2, both showing left periamygdaladischarges.
SEEG recordings in a further patient who demon-strated markedly fluctuating symptoms (comprisingfugue states, visual distortions, visual hallucinations,anxiety and visceral sensations) correlated with deep,predominantly right temporal (lingual gyrus, gyrus ofHeschl, hippocampus and amygdala) discharges (Wieseret al., 1985). Wieser (1980) reports a fourth case of a22-year-old female in whom fifty-three seizures were
recorded of which forty-nine were accompanied by clin-ical signs in various forms: (1) right sided hippocampaldischarge was associated with feelings of anxiety andvisceral sensations which were more pronounced if theanterior temporal lobe and in particular the amygdala(
Figure 3 ‘Visual delusion’ during a temporo-occipital discharge (mthe bottom shows enlarged portions of the record between the hopositioning for this patient. (Wieser, 1983).
igure 2 Laughing fit accompanied by rhythmic discharges ineft periamygdalar region (electrode 1) slowing down to 0.5 somplexes. (Wieser, 1983).
were the site of seizure discharge, (2) more elaboratesymptoms were associated with spread of the dischargeto lateral temporal cortex so modifying activity in thelingual gyrus when visual experiences were prominentand to the right gyrus of Heschl during musical halluci-nations.
The final example is an episode captured on SEEGwhich Wieser calls a ‘visual delusion’. During a spon-taneous epileptic discharge from the temporo—occipitalcortex the patient believed for a short time that hermedicine cabinet was in fact her neighbours stove
(Fig. 3; Wieser, 1983).b) AuditoryIctal auditory hallucinations have a particularly spe-
cific localisation to discharges in or near Heschl’s
ost prominent in 4/8—9, also visible in 5/1—2). The insert atrizontal bars. On the right is a brain map with the electrode
168 B. Elliott et al.
Table 3 Distribution of the main subjective symptoms at seizure onset according to electrophysiologic subtype (Maillard et al.(2004)). n = number in each subgroup; (%) percentage of those in subgroup experiencing each hallucinatory type.
Ictal features Medial n = 24 Medial—lateral n = 18 Lateral n = 13 Degree of significance
Auditory hallucination or illusion 1 (4.2) 2 (11.1) 6 (46.2) P = 0.005a
Visual hallucination or illusion 2 (8.3) 3 (16.7) 4 (30.8) P = 0.21Sensory hallucination or illusion
(visual, auditory or vestibular)3 (12.5) 6 (33.3) 11 (84.6) P < 0.0001a
Gustatory hallucination 2 (8.3) 1 (5.6) 0 P = 0.78Fear 9 (37.5) 4 (22.2) 0 P = 0.026a
50)
(
(
(
Viscerosensory symptoms 19 (79.2) 9 (a Significant.
gyrus and the auditory association areas (Wieser,1980, 1983). Maillard et al. (2004) using stereoelec-troencephalography (SEEG), analysed 187 spontaneousseizures recorded from 55 patients with medicallyintractable TLE. Patients were classified into medial(M; n = 24), lateral (L; n = 13) and medio-lateral (ML;n = 18) groups on the basis of the electrophysiologicalfindings. Viscerosensory symptoms, fear and the dreamystate were significantly more frequent in the M andML groups. Whereas only auditory hallucinations andillusions significantly differentiated the L from the Mor ML groups (46.2% in L vs. 4.2% and 11.1% in Mand ML respectively). The results are summarised inTable 3 and are consistent with the localising value ofthese symptoms namely Heschl’s gyrus for primary audi-tory hallucinations, more extended and lateral partsof the superior temporal gyrus for complex auditoryhallucinations and basal—temporal gyri and temporo-occipital junction for complex visual hallucinations(Bancaud and Talairach, 1993).
Auditory auras appear to have a similar localisa-tion, and possibly even lateralisation. Clarke et al.(2003) describe the phenomenon of ‘ear-plugging’ inlocalisation-related epilepsy. In their series, three chil-dren who demonstrated unilateral or bilateral earplugging (i.e., placing their hands over an ear in whatis probably an attempt to block out an auditory halluci-nation) at the onset of partial seizures were investigatedwith scalp video electroencephalography (VEEG), mag-netoencephalography (MEG) and MRI. All three pluggedtheir ears during auditory hallucinations which werelocalised to the superior temporal gyrus, and appearedto lateralise the site of seizure onset to the contralateraltemporal lobe. Mohamed et al. (2006) later investi-gated auditory hallucinations in 6 children using MEG.Three patients had elementary hallucinations, one hada complex hallucination and two had both complex andelementary hallucinations. Sounds heard included stam-peding elephants, unbearable and buzzing sounds as wellas rushing water. Two patients complained of amplifica-tion of sound whilst another at age eleven heard friend’svoices talking about him. All 6 patients demonstrated
clustered MEG spike sources in the superior temporalgyrus; two had scattered spikes in the superior tempo-ral gyrus as well as clustered MEG spike sources in theleft inferior and middle frontal gyri or parieto-occipitalregion.3 (23.1) P = 0.004a
It is also interesting to observe that hallucinations oflanguage or speech can arise from both dominant andnon-dominant epileptic foci.
c) OlfactoryAlthough every medical student associates TLE with
‘olfactory hallucinations’, they are in fact relativelyinfrequent in epilepsy. Chen et al. (2003) examinedcase-notes of 217 patients who underwent temporallobectomy for medically intractable TLE. Just twelve(5.5%) reported olfactory auras, with lesions affectingmesial temporal structures in eleven. Diagnosis on his-tology included gliosis (n = 7, 58.3%), neoplasm (n = 4,33.3%) and a single arteriovenous malformation (8.3%).This supports the view that olfactory auras are rare inTLE as well as the finding by Acharya et al. (1998) thattumour is the most likely aetiology. The only SEEG studywe were able to identify was that quoted by Wieser(1983) in combination with gustatory hallucinations—–seebelow.
d) GustatoryGustatory hallucinations are also considered rare in
epilepsy. Gowers (1909) found only one case in a seriesof 1102 patients. Gibbs et al. (1948) and Currie et al.(1971) reported prevalence rates of just 1.3% and 3%respectively and the most recent series by Hausser-Hauwand Bancaud (1987) reported a prevalence rate of 4%.In the latter study gustatory hallucinations were inves-tigated using SEEG and found to occur in 10 patients(50%) during temporal lobe seizures, in six (30%) duringparietal seizures and in four (20%) during parietotem-poral seizures. Isolated brief gustatory hallucinationscould be elicited from stimulation of: the right rolandicoperculum, parietal operculum, amygdala, hippocam-pus, medial temporal gyrus and the anterior part of theright temporal gyrus. Seizures with gustatory manifes-tations could be induced by electrical stimulation ofthe right hippocampus and amygdala and left hippocam-pus and indeed Wieser (1983) gives an example of lefthippocampal status recorded on SEEG resulting in botholfactory and gustatory hallucinations.
e) SomaticBaldeweg et al. (1998) using SEEG demonstrated an
association between somatic hallucinations and activityin the post-central gyrus, parietal operculum, insula andinferior parietal lobule. The insula is a key relay sta-tion between frontotemporal cortical areas and limbicregions. Penfield was the first investigator to underline
Delusions, illusions and hallucinations in epilepsy
the similarity between symptoms observed during tem-poral lobe seizures and those evoked by insular cortexstimulation (Penfield and Jasper, 1954). His early worknoted that focal insula lobe seizures produced abdominalsensations and gastro-intestinal movement, findings sub-stantiated by later electrical stimulation experimentsunder local anaesthesia (Penfield and Rasmussen, 1950;Penfield and Kristiansen, 1951; Penfield and Jasper,1954). In a later study, Penfield and Faulk (1955)stimulated the insula cortex of 6 patients undergo-ing craniotomy for focal epilepsy. In four, stimulationproduced effects on the stomach which varied frominhibited gastric motility, to the production of violentactivity with a marked increase in tone. The issue ofwhether abdominal and epigastric sensations were rep-resented in this region was left an ‘open question’, withmany of the sensory responses thought be secondary tomotor changes in the gastro-intestinal tract.
Despite these early findings, the role of the insulain TLE has remained more or less unexplored, largelydue to its relative inaccessibility to depth EEG record-ing. Recent improvements in SEEG technology such assmaller electrodes and greater accuracy of localisationusing MRI, now permit chronic insular cortex record-ings to be taken. Isnard and Mauguiere (2005) providea description of the clinical features of insular lobeseizures in 50 patients. These began as simple par-tial seizures occurring in full consciousness, followedby a sensation of laryngeal constriction, parasthesia,dysarthric speech and/or elementary auditory hallu-cinations. Other authors however, have shown thatthe symptomatology of insula seizures may reflectwidespread propagation or distribution and argue thatthe symptomatology may not be very anatomically spe-cific, with Ryvlin et al. (2006), for example, describingnocturnal hypermotor seizures suggestive of frontal lobeepilepsy arising in the insular cortex, and a similar casewas reported by Nguyen et al. (2008) in which insularseizures were diagnosed by SEEG and insular resectionresulted in seizure freedom.
(f) Visual hallucinations and illusionsIctal elementary visual phenomena are common in
occipital seizures with estimated prevalence rates rang-ing from 8% (Marques-Assis et al., 1971) to 72% (Salanovaet al., 1992). In a review by Taylor et al. (2003), elemen-tary hallucinations were divided into positive (simplyshaped flashes of colour or light, phosphenes) and nega-tive (scotoma, hemianopia, amaurosis) manifestations.Simple illusions may also occur where objects mayappear to change in size (macropsia and micropsia),shape (metamorphopsia), or lose colour (achromatop-sia). Panayiotopoulos (1999) provides a qualitativeanalysis of ictal visual symptoms in 9 patients withidiopathic occipital epilepsy with visual hallucinations(IOEVH). He found that elementary ictal visual halluci-nations comprised mostly multiple bright coloured spots,circles, or balls lasting for between 5 and 30 s, although
in one patient up to 10 min. Their onset was usually uni-lateral, appearing in the temporal hemifields and thenmoving horizontally to the contralateral side. Whilstthey may multiply, flash and change in size, occipitalparoxysms were only present on the scalp EEG in three.169
Palmini et al. (1993) investigated 8 patients, in whomit was unclear whether the seizure originated in theoccipital or temporal lobes, with depth electrodes. Onesuffered sudden loss of vision as the aura, anotherreported colours of discrete objects blurring together,and a third described blurred vision affecting the entirevisual field. All three of these had an occipital focus onSEEG, and in all cases the seizure propagated to theipsilateral mesial temporal lobe and neocortex. Rightoccipital lobe supra- and infra-calcarine structures wereinvolved in 93% of ictal onset in the first patient. Seizuresbegan mesially in right infra-calcarine region in the sec-ond, and in the third, 80% originated on the mesialsurface of the left supra- and infra-calcarine regions.In the fourth patient who reported loss of vision and asense of freezing in the left eye, 75% of the seizures atonset occurred simultaneously in the right mesial andlateral occipital lobe as well as in ipsilateral temporalneocortex and hippocampus. Intra-cerebral recordingsin proven occipital lobe epilepsy show rapid spread toposterior temporal, parietal and frontal regions (Tayloret al., 2003; Bancaud, 1969; Takeda et al., 1970). Suchcases emphasise the observation that seizures in primarycortex may be quite localised, in contrast to the widelydistributed seizures of association or limbic cortex, andpropagation through the corpus-callosum to the oppo-site occipital lobe in occipital lobe epilepsy is often alate finding in adults (Williamson and Spencer, 1986).
Involvement of the occipito-temporal cortex rendersthe hallucinations more complex and colourful. Ictalcomplex visual hallucinations tend to last a few secondsto minutes with the patient retaining insight into theunreality of the experience (Taylor et al., 2003). There isa reported high association with parieto-occipital lesions(Lance and Smee, 1989) but lesions of the temporal lobehave also been identified (David et al., 1945). Palinop-sia is a rather characteristic epileptic feature, in whichimages persist or reduplicate, and has been localisedto the right posterior cerebral region. In the rare phe-nomena of autoscopia, subjects perceive mirror imagesof themselves of normal size, shape and density, theymay be in situations from their past or performing com-plex tasks. This may arise from seizures affecting theoccipital-temporal junction zone (Sveinbjornsdottir andDuncan, 1993; Dewhurst and Pearson, 1955; Ionasescu,1960).
Complex visual hallucinations have a much more dif-fuse anatomical basis than simple hallucinations. In thestudy of Panayiotopoulos (1999) of idiopathic occipi-tal epilepsy for example, only one patient experienceda complex visual hallucination, whereas Palmini et al.(1993) report that their patient with coloured flashesaffecting particularly the left upper field and associatedwith unmotivated fear, nausea and formed visual andauditory hallucinations had a seizure onset in the righttemporal lobe in all cases. Several other examples havealready been cited above including the findings of Gloor
(1982) of complex visual hallucinations resulting fromlimbic stimulation alone, and the findings of Fish et al.(1993) that unless limbic structures are activated com-plex visual hallucinations do not occur. It would seemthat as with more complex auditory hallucinations, a
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more diffuse network of activation is required for theiraetiogenesis and the involvement of limbic structures iskey.
iscussion
ere we have adopted the neurological definition of ‘hallu-ination’ which includes affects such as fear, depression,nger and déjà vu within its rubric as well as includinghe more traditional forms of hallucination described bysychiatrists. What does emerge from the above reviews that, in epilepsy, any distinction between the variousbnormalities of affect, thought (delusions) and perceptionillusions and hallucinations) is not mirrored by differ-nces at the anatomical and electrophysiological level.lectrical stimulation of the same area within the lim-ic system can produce symptoms belonging to each orll of these categories, whereas stimulation of widely seg-egated areas can produce a remarkably similar mentalesponse. This lack of strict anatomical specificity withinhe limbic system for the various types of hallucinatoryhenomenon induced by electrical stimulation or electro-raphic seizure activity is striking, and can be explainednly by invoking theories of widely distributed neuronal net-orks.
There is however, greater anatomical specificity whenne considers elementary hallucinatory phenomena inducedy stimulation of primary sensory areas (visual, auditory,ther sensory and somatic), this is again mirrored by theften well-localised phenomenology of seizures arising fromhese areas (viz. auditory hallucinations to Heschl’s gyrusnd visual illusions to the temporal and occipital neocor-ex). Having said this, visual symptomatology is in itself aoor anatomical discriminator, especially if complex, andan occur in seizures apparently with origin in occipital,emporal (mesial and neocortical), other limbic and parietalortex.
A wide variety of psychological symptoms (includingallucinations in most sensory modalities) have now beenecorded during periods of ongoing epileptic seizure activ-ty using intracranial EEG techniques. As Gloor suggested,nvolvement of limbic structures once again appears to beey in complex hallucinatory symptomatology, and it is per-aps not surprising that stimulation of the limbic ‘receivingnd’ may elicit a range of responses that reflect the func-ion of areas from which these cortico-limbic connectionsriginate.
This finding is of particular interest when we come toonsider the electrophysiological correlates of complex psy-hotic states in the second paper, where the implication ofhese observations for understanding mechanisms underpin-ing psychiatric states is explored. Whilst it is clear that thehort lived hallucinations described in this paper bear littleesemblance to those encountered in the functional psy-
hoses, limbic seizure activity, particularly when prolonged,i.e., amounting to complex partial status epilepticus), cannduce complex hallucinatory states which are remarkablyimilar to those observed in disorders such as schizophreniand it is to these that we turn our attention in the secondaper.H
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