Review

Of Roman chariots and goats in overcoats: The syndromeof Charles Bonnet

Chris Plummer

a,*

, Anne Kleinitz

, Patrick Vroomen

, Roger Watts

Department of Neurology, Austin Hospital, Melbourne, Victoria

Department of Medicine, Mersey Campus Hospital, La Trobe, Tasmania

Received 1 June 2006; accepted 3 August 2006

Abstract

Charles Bonnet syndrome (CBS) is a widely under-recognised disorder typically characterised by complex visual hallucinations in thevisually impaired. The lack of consensus over a uniform definition for CBS has much to do with the unresolved pathophysiology of thedisorder. A leading hypothesis proposes that complex hallucinations arise from visual association cortical areas following their de-affer-entation from the central visual pathway. While treatment aimed at improving the visual deficit can limit the symptoms of CBS, at pres-ent there is no reliably effective pharmacotherapy for the disorder. Once correctly recognised, a key management principle is to reassurethe patient that CBS is a well-documented clinical entity that is not a harbinger of psychiatric illness.

Keywords:

Charles bonnet syndrome; Hallucination; Visual; Visually impaired persons; Macular degeneration

1. Introduction

A diagnosis of Charles Bonnet syndrome (CBS) in thesetting of visual impairment infers that insight into the illu-sory nature of complex visual hallucinations is retained,that other sensory hallucinatory phenomena are absent,

and that alternative conditions known to give rise to hallu-cinations such as migraine, occipital lobe epilepsy, and psy-chiatric disease have been excluded. Closeto 250 years haspassed since Bonnet’s index case report

of the complexvisual hallucinations experienced by his grandfather whowas blinded by cataract disease. Since then, such hallucina-tions have been documented with lesions seated anywherealong the central visual pathway, from the orbit to the cal-carine ﬁssure. This has contributed to a now 70-year-long

controversy surrounding the deﬁnition of CBS. In defer-ence to Bonnet’s original case description and consideringthat key studies in CBS have thus far been based on pa-tients with ocular disease, we apply the term in this reviewto patients with complex visual hallucinations associatedwith pathology of the eye.Suspicion that CBS prevalence estimates are spuriouslylow has as much to do with the suﬀerer’s fear of being la-belled insane upon symptom disclosure, as with a lack of awarenessof the disorder in the broader medicalcommunity.

4,5

Weprefaceourreviewoftheclinicalcharacteristics,path-ophysiology,andmanagementofCBSwiththepresentationof two quite remarkable and particularly instructive exam-plesofthesyndrome.Bothpatientshadseverevisualimpair-ment from end-stage age-related macular degeneration.

2. Clinical characteristics

2.1. Patient 1

A 73-year-old woman who lived alone presented withanxiety-provoking visual hallucinations. Inch-long blackants scurried across her kitchen ﬂoor, walls and windows.

0967-5868/$ - see front matter

Corresponding author. Present address. Centre for Neurosciences andNeurological Research, St Vincent’s Hospital, 5th Floor Daly Wing, 35Victoria Parade, Fitzroy, Victoria 3650, Australia. Tel.: +61 3 92883045;fax: +61 3 92883350.

E-mail address:

chris.plummer@svhm.org.au(C. Plummer).

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Journal of Clinical Neuroscience 14 (2007) 709–714

In desperation, she began spraying insecticide throughoutthe house. Her neighbour, whose features were seeminglymasked by the insects, called an ambulance. Floating sea-horses and featherless chickens joined the colonies of antsin the Emergency Department. A Roman chariot, the riderdressed in gold, flashed across the curtain several times. Onthe ward, tropical vines grew from the foot of her bed. Aman stood with thick brown tree trunks for legs and thickgreen branches for arms. Nurses’ heads would shrink andthen expand before melting into the floor. Brightly col-oured fairies carrying wands invited her for walks aroundthe hospital grounds. She once caught herself telling themto get off a road at which point they donned diamondcoats, jumped into a wooden carriage, and rode up to herbedside. Ants in the mirror were at times replaced by anelephant’s trunk blotting out half her face. Her hair inthe reflection flowed with cobwebs and the basin was mat-ted with hair and whiskers. Cobwebs spilled from her cer-eal bowl at breakfast. The bathroom floor was coveredwith water that vanished whenever she tried to mop itup. The carpet in the room would lift away from the floor,roll up in the form of a snake, and slither out the door. Alittle girl and boy with a black and white dog stood next tothe bed, as did extraterrestrial-like beings with largedomed-shaped heads and slitted black eyes. Twisted headswith grotesque faces and bulbous eyes peered out from thewall, while little red carriages, trains and push bikes disap-peared into it. Further history revealed an experience of ‘ant’ hallucinations 4 months previously but the images dis-appeared after 2 weeks. She did not seek medical advice atthat time fearing that she might be considered ‘a bit odd’.Throughout the hospital admission she was rarely freefrom hallucinations and would repeatedly ask for reassur-ance that she was ‘not going mad’. Two months after dis-charge the hallucinations were still intrusive. She owned asmall black dog but would see several dogs resemblingoversized greyhounds with unusually long snouts in herdaughter’s yard. A man and a goat, both wearing grey hatsand overcoats, often stood beside her before wandering off together down a crooked road. She grew accustomed toseeing a baby seated on the lounge chair wearing greyclothes. It smiled but made no sounds. Caterpillars and treefrogs began joining her for the evening bath. She began tonotice that distractions, such as listening to the radio andattending to household chores, dampened the hallucina-tions, while solitude, particularly during the evening hours,tended to heighten them. At follow-up 1 year later, she wasexperiencing very much the same hallucinations but wasmore cognisant of their unreality and less anxious as a re-sult. The only new hallucination that had since appearedwas that of a bright kaleidoscopic array which would tran-siently emanate from her central field of vision.

2.2. Patient 2

A 90-year-old man who lived with his wife woke to finda bright pink handkerchief on the floor of his bedroom.Every time he tried to pick the cloth up it seemed to moveout of reach. He followed it from room to room but wasdistracted by the appearance of rows of bearded humanfaces with bulging eyes jutting out from the lounge-roomwall. Through the window he saw a large brown Ayrshirecow in the front yard and, beyond it, he made out a redsports car racing up the street towards his house. Heopened the front door only to be greeted by a trio of police-man dressed like American highway patrol officers totinglarge guns. Fearing at this point that he was losing his fac-ulties he summoned his wife and an ambulance was called.In the Emergency Department of the local hospital he sawa draught horse pulling a cart loaded with wooden logs.The cart transformed into a Roman chariot and spedacross the hospital curtain with a rider at the helm. Largetree trunks appeared at the foot of the bed and begancracking down the middle one by one. The cubicle curtainwas replaced by rows of neatly arranged wooden palings.He was soon convinced that the visions were imaginedand his anxiety was replaced by a sense of amusement.At follow-up 2 years later the patient was still experiencingfrequent visual hallucinations. Grazing Ayrshire cows con-tinued to appear in the front yard. Little children in redoutfits ran around the house. People of various shapesand sizes wore raincoats and trudged through pools of water inside the house. Three years later he was virtuallyhallucination-free, reporting only very occasional episodesof visions of cows and children.

2.3. Clinical ﬁndings

Both patients had features of end-stage neovascular(‘wet’) age-related macular degeneration (AMD) on indi-rect fundoscopy. Central scotomas encompassing the blindspot were present bilaterally in Patient 2 and on the left inPatient 1. Corresponding visual acuities were limited to fin-ger-counting peripherally, though Patient 1 retained aright-sided acuity of 6/18. Both estimated that their visionhad been thus affected for at least 2 years. This was corrob-orated by their respective ophthalmology records. Patient 1underwent unsuccessful laser photocoagulation 3 monthsprior to presentation. Patient 2 had cataract disease at pre-sentation but surgery, which was performed well after hishallucinations began remitting, made little impact on eitherhis visual acuity (movement only appreciated in the worstaffected eye by this stage) or on the pattern of his persistingCBS symptoms.

3. Diagnosis and syndrome origins

What is remarkable about the clinical features is that,despite the rich detail and variety of images reported bythe patients, there are themes and indeed ﬁgures commonto both (viz. Roman chariots, tree trunks, grotesque faces,pools of water). The image descriptions typify the syn-drome of Charles Bonnet, eponymously coined by de Mor-sier

in honour of the Swiss philosopher who ﬁrst

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documented the disorder in 1760. In what stands as the ﬁrstdescription of hallucinatory phenomena in the scientiﬁc lit-erature,

Bonnet’s account relates a series of complex visualimages perceived by his then 89-year-oldgrandfather,Charles Lullin, who had cataract disease.

While awareof their illusory nature, Lullin perceived vivid images of people, birds, tapestries and buildings. It was recentlynoted

that Bonnet signiﬁcantly underplayed the sophisti-cation of his grandfather’s hallucinations in his report.For instance, Lullin’s ‘women’ were actually young danc-ing girls ‘dressed in yellow silks with rose coloured ribbons,pearl collars, golden buckles, and diamond pendants’, andLullin’s ‘carriage’ was ‘a coach complete with drivers andhorses, expanded in correct proportion to the size of ahouse’.

Curiously, it seems that Bonnet himself experi-encedvisual hallucinations as his vision dimmed withage.

To this day, CBS is known for this very flavour of imagery, namely, extended landscapes, human and animalfigures and ornate structures. The term ‘pseudo-hallucina-tion’ is often strictly applied to indicate that the suffereris aware that the images are not real.

4. Categorisation of the images

Characterisation of the hallucinatory phenomena in CBShas previously been hampered by the limited number of published cases. Indeed, as few as 46 cases were countedin the literature from the time of Bonnet’s original descrip-tion up to as recently as 1989.

A 1996 case series by Teu-nisse et al.,

still the largest to date, sheds significant lighton the clinical spectrum of CBS. Characteristics of theimages reported by the 63 patients, drawn from 505 individ-uals with visual impairment secondary to eye disease, variedgreatly in terms of colour, movement, clarity and bizarre-ness. Specific examples featured a dragon, a shining angel,and a humorous police arrest played out in miniature. Asis typical, additional sensory phenomena such as auditoryand olfactory hallucinations were invariably absent. Thewide range of visual hallucinations experienced in CBS issimilarly reflected in case studies.

9–13

Ffytche and How-ard,

extrapolating the earlier clinical observations of Klu-ver,

classiﬁed their patients’ hallucinations into eightcategories: tessellopsia (regular, overlapping patterns);hyperchromatopsia; prosopometamorphopsia (facial dis-tortion); dendropsia (branching forms); perseveration; illu-sory visual spread; polyopia; and micro/macropsia. Ourpatients’ visual experiences match this system of classiﬁca-tion quite well: tessellopsia (cobwebs, rows of trees); hyper-chromatopsia (caterpillars, kaleidoscopes, bright redvehicles, gold chariots); prosopometamorphopsia (gro-tesque faces, extraterrestrial-like heads); dendropsia (vines,roads); polyopia (ant colonies, wooden palings); micropsia(trains, push-bikes, fairies); and macropsia (greyhounds,nurses’ heads). The clinical validity of this method of imagecategorisation is yet to be established but, as later discussed,it does go some way in respecting the known specialisationof the visual association cortex.

5. The patient’s perspective

The images of CBS tend to appear within theboundariesof the negative scotoma in the partially sighted.

The pre-dominantly central projection of imagery in patients withAMD is in keeping with the central ﬁeld loss typical of macular disease. Dimly lit conditions, states of drowsinessand physical isolation, and circumstances of relative socialisolation have been noted as factors favouring the recur-rence of hallucinations.

Conversely, rapid blinking, sus-tained eye closure, diversionary activities, or simplywalking away may relieve them.

Suﬀerers typically regardthemselves as the onlooker, and it is unusual for them tofeel as though they are part of the panorama. The ﬁrst pa-tient’s impression of being invited to tour the hospitalgrounds by fairies might therefore be considered atypical.However, it is clear that she was initially drawn in by thelife-like nature of the images. This initial deception is notuncommon

and patients do ultimately appreciate thatthe visions are not real. Despite this, suﬀerers are generallyreluctant to report the problem for fear of being labelledmad.

4,5

Indeed, patients with CBS have been erroneouslyadmitted to psychiatric institutions on one level,

whileon another, have had their experiences dismissed as ‘silly’by medical practitioners.

6. Prevalence and confounders in CBS

Reluctance by suﬀerers to disclose their hallucinatoryexperiences, along with the relative lack of awareness of the condition in general medical circles, has led to the sus-picion that prevalence estimates of CBS are spuriously low.Estimates have rangedwidely from 0.4% to 63% in thevisually impaired.

4,5,16,18

A clearer view of the epidemiol-ogy is also hamstrung by sub-specialty recruitment bias,prevalence ﬁndings varying across the disciplines of geriat-ricmedicine, neurology, ophthalmology, and psychia-try.

16,19–21

Elements of this bias might relate topotentially different pathogenetic contributions made byacuity loss vis-a`-vis field loss in defining CBS risk. The rel-ative import of the ageing brain on the genesis of hallucina-tions is also unclear. Mean age of onset data from largerseries demonstrate clustering across the eighth and ninthdecades.

4,5,18,20,21

The Mini Mental State Exam score, usedas evidence against dementia in many CBS studies, may notdetect subtler higher order cognitive deﬁcits. De Morsierhimself stressed the potential contribution of age to syn-drome onsetand de-emphasised visual loss as a diagnosticpre-requisite.

Indeed, the man who coined the syndromelater confessed that it was never his intention to link thesymptoms to eye disease. De Morsier argued until his deaththat his later reference to CBS as a ‘senile syndrome withlesions of the eyes’was misconstrued but the connectionhad already stuck.

It seems then that the eponym wasfraught with confusion from the outset.A further confounding factor in regard to the prevalencedata is the manner in which sight-impaired patients are

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