Brain, Vol. 123, No. 10, 2055-2064,
October 2000
© 2000 Oxford University Press
Visual hallucinatory syndromes and the anatomy of the visual brain
Institute of Psychiatry, London, UK
Correspondence to:
D. H. ffytche, Institute of Psychiatry, De Crespigny Park, Denmark Hill, London SE5 8AF, UK E-mail: d.ffytche{at}iop.kcl.ac.uk
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Abstract |
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We have set out to identify phenomenological correlates of cerebral functional architecture within Charles Bonnet syndrome (CBS) hallucinations by looking for associations between specific hallucination categories. Thirty-four CBS patients were examined with a structured interview/questionnaire to establish the presence of 28 different pathological visual experiences. Associations between categories of pathological experience were investigated by an exploratory factor analysis. Twelve of the pathological experiences partitioned into three segregated syndromic clusters. The first cluster consisted of hallucinations of extended landscape scenes and small figures in costumes with hats; the second, hallucinations of grotesque, disembodied and distorted faces with prominent eyes and teeth; and the third, visual perseveration and delayed palinopsia. The three visual psycho-syndromes mirror the segregation of hierarchical visual pathways into streams and suggest a novel theoretical framework for future research into the pathophysiology of neuropsychiatric syndromes.
visual hallucinations; Charles Bonnet syndrome; dorsal stream; ventral stream
CBS = Charles Bonnet syndrome; fMRI = functional MRI; SMD = senile macular degeneration; STS = superior temporal sulcus
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Introduction |
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Visual hallucinations are found in a range of neurological, psychiatric and ophthalmological conditions (Barodawala and Mulley, 1997
; Manford and Andermann, 1998), with some authors referring to their association with eye disease as the Charles Bonnet syndrome (CBS) (see ffytche and Howard, 1999). In a recent functional MRI (fMRI) study, we investigated four CBS patients while they were hallucinating (ffytche et al., 1998). The patients were asked to signal the onset and offset of each hallucination over a 5-min period and to describe their visual experiences. By cross-correlating the fMRI time series with the hallucination events, we were able to identify the cerebral activity underlying the hallucinations. We found that visual hallucinations were related to phasic increases in activity within specialized visual cortex and that the location of the increases defined the type of experience reported. Thus, colour hallucinations accompanied increased activity in cortex specialized for colour; face hallucinations, increased activity in cortex specialized for faces; object hallucinations, increased activity in cortex specialized for objects, and so forth. In an independent set of experiments reported in the same study, we found that, compared with control patients matched for age and visual impairment, patients with CBS had tonic increases in brain activity within specialized visual cortex when not hallucinating. Taken together, the imaging results implied that (i) each specialized visual area had its own associated hallucination and (ii) the pathophysiology of the hallucinations involved a localized increase in cerebral activity. In extending this work, we were interested in finding out whether the organization of the visual system as a whole influenced the phenomenology of CBS. The visual cortex is characterized by rich and complex interconnections between functionally specialized areas (see Van Essen et al., 1993; Ungerleider and Haxby, 1994) so that pathological increases in activity are unlikely to be restricted to a single specialized visual area. This raises the question: are there systematic links between visual hallucinations, i.e. hallucinatory syndromes, which reflect the anatomical connections between visual areas? The work reported below set out to answer this question using a structured interview/questionnaire method and exploring the associations and dissociations between specific hallucination categories in patients with CBS.
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Methods |
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Patients with visual hallucinations whose onset followed the development of eye disease were selected from the Visual Hallucination Case Register at the Institute of Psychiatry. The Register consists of patient volunteers from the Buckinghamshire and Kent Associations for the Blind, volunteers from the Macular Disease Society and clinical referrals to a specialist visual hallucination clinic. Patients were assessed by telephone or in the out-patient department using the Institute of Psychiatry Visual Hallucinations Interview. This structured interview/questionnaire covers phenomenology, patient demographics, ophthalmic diagnosis, current health, medication history, a measure of the patients' natural descriptive style (whether their verbal descriptions tend to be elaborate or simple) and questions related to exclusion criteria. An outline is given in the Appendix. The interview/questionnaire was developed from a previous unstructured survey (ffytche and Howard, 1999
) and included the novel hallucination categories reported in that study. In contrast to the unstructured survey, in which patients were asked to describe their hallucinations with minimal prompting, each patient was questioned systematically about each category of pathological visual experience. The assessments were all carried out by one investigator (A.S.). Inclusion criteria were: (i) age over 18 years and (ii) visual hallucinations which followed the development of eye disease. Patients were excluded from the study if: (i) there was a history of stroke, epilepsy or dementia; (ii) the hallucinations occurred in relation to sleep onset or on waking; (iii) visual hallucinations were accompanied by auditory hallucinations; (iv) the hallucinations were accompanied by symptoms suggestive of a complex partial seizure; (v) there were symptoms or a history suggestive of alcohol withdrawal syndrome; or (vi) the hallucinations formed part of a psychotic illness. The study was approved by the Bethlem and Maudsley Hospital Ethics Committee and all patients gave informed consent.
Analysis
The interview was divided into four classes of variables for further statistical testing.
- (i) Phenomenological (see Table 1 for details)—the emotional content variable was recoded into emotional (pleasant and unpleasant) and neutral.
- (ii) Aetiological—age, sex, acuity, ophthalmic diagnosis, past medical history, current medication and descriptive style. The medication variable was recoded into two categories: patients taking medications associated with visual hallucinations and those not (Barodawala and Mulley, 1997
); the past medical history variable was recoded into two categories: patients with risk factors for cerebrovascular disease (diabetes mellitus and hypertension) and those without; the diagnosis variable was recoded into two categories: patients with senile macular degeneration (SMD) and those with other ocular pathologies.
- (iii) Temporal aspects—the duration of individual hallucinations and the length of time the patients had been hallucinating.
- (iv) Miscellaneous variables—see Table 2
for details.
- (ii) Aetiological—age, sex, acuity, ophthalmic diagnosis, past medical history, current medication and descriptive style. The medication variable was recoded into two categories: patients taking medications associated with visual hallucinations and those not (Barodawala and Mulley, 1997
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Associations between different phenomenological variables were explored using a matrix of chi-squared tests and factor analysis. Apart from the transparency variable, for which all but one subject described their hallucinations as opaque, all phenomenological variables were included in the factor analysis. Factor analysis was performed using SPSS v4.0 (SPSS, Chicago, Ill., USA). The number of factors in the covariance/correlation matrix was selected by the criterion of an eigenvalue >1 and the factor matrix was optimized using varimax rotation with Kaiser normalization. Variables with a factor loading of more than 0.5 or less than –0.5 were considered core variables for a given factor. Associations between phenomenological variables and aetiological or temporal variables were tested using t- or chi-squared tests with a threshold of significance of P < 0.01.
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Results |
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Of the 128 patients on the Case Register, 39 met entry criteria and were interviewed. Of these, five patients had developed exclusion criteria since registration. The mean age of the patients included was 81 ± 10 years (range 52–101 years) and 71% were female. All were registered blind or partially sighted; 73% had a visual acuity of counting fingers or better. Sixty per cent had a diagnosis of SMD; 6% SMD plus a second diagnosis; 12% glaucoma; 3% cataract; and 18% miscellaneous ophthalmological diagnoses. Fifty-nine per cent were not taking medications thought to be associated with visual hallucinations. Ninety-one per cent of the patients had hallucinated within the past 3 months and 45% had hallucinated for >4 years. Sixty-eight per cent reported that their hallucinations occurred at least daily, with 23% hallucinating at least hourly or constantly. There was a tendency for hallucinations to last for minutes (62%), rather than seconds or hours.
Phenomenology
The percentage frequencies of phenomenological variables are given in Table 1
. The most common experiences were a simple shape, flash or tessellopsia (grid-like, latticed or network patterns; see ffytche and Howard, 1999). Facial hallucinations were generally distorted, or described as ugly, with prominent eyes and teeth (prosopometamorphopsia; see ffytche and Howard, 1999) and not infrequently as outlines or cartoon-like in quality. When figures were reported, they were typically small, wearing hats or period costume and moved in a realistic way (biological motion; Table 2). Half the patients did not have an emotional response to the hallucination and, of those who did, about half found the experiences unpleasant. The least common experiences consisted of seeing multiple copies of the same hallucinated object arranged in rows (polyopia; see ffytche and Howard, 1999), continuing to see veridical objects or patterns after looking away (visual perseveration; see Kölmel, 1982) and having veridical objects return to the field of view after a delay (delayed palinopsia; see Kölmel, 1982).
Table 2 shows that hallucinations typically were seen in more detail than real objects, faces and scenes, etc. They moved with the eyes or head but were not usually abolished by blinking. Sometimes the experiences were precipitated by being driven in a car or by other forward motion (optic flow stimulation; see de Jong et al., 1994).
The matrix of chi-squared values derived by testing each of the phenomenological variables against all others is shown in Fig. 1 [the transparency variable was excluded (see above) and emotional content recoded into a binary variable]. The chi-squared value of each test is given at the intersection of the appropriate row and column. Only chi-squared values of P < 0.01 are shown. Three main clusters of associations emerged. The first cluster consisted of hallucinations of extended landscape scenes, vehicles and small figures in costumes with hats; the second, hallucinations of grotesque, disembodied distorted faces with prominent eyes; and the third, visual perseveration and delayed palinopsia, located in the peripheral visual field. The first and third clusters had no variables in common; the first and second were linked by hallucinations of faces with prominent eyes. Of the remaining variables, only polyopia–rows and sketch-like face hallucinations–no colour showed a strong association, both pairs being linked by definition (rows are a subset of polyopia and sketch-like hallucinations imply a monochromatic drawing). Vehicles–rows and polyopia–changing visions showed a weak association.
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The factor analysis of phenomenological variables is shown in Fig. 2
. The first three factors, ranked by eigenvalues and the percentage of variance explained, corresponded to the three clusters derived from the chi-squared matrix and accounted for 40% of the total variance. The first factor (shaded red) consisted of extended landscape scenes, children and figures in costume, wearing hats. The second factor (shaded green) consisted of grotesque disembodied faces with prominent eyes and teeth. The third factor consisted of delayed palinopsia and visual perseveration in the peripheral field. Our arbitrary cut-off point (a factor loading of ±0.5) distorts the fact that there are a number of variables on the periphery of each factor. In particular, vehicles, trees/shrubs (dendropsia) and emotional content are weakly associated with factor 1, and cartoon-like and sketch-like faces are weakly associated with factor 2. As found in the chi-squared matrix, faces with prominent eyes (factor 2) are also on the periphery of factor 1. For display purposes, we have not included the row variable in the matrix as the association between polyopia and rows (linked by definition; see above) forms a fourth factor which accounts for slightly more of the variance than the peripheral visual field/perseveration/palinopsia factor (10.2% versus 9%). The omission of rows has no effect on the clustering described. Four further factors had eigenvalues >1, each accounting for 4–8% of the variance. None of these factors contained clusters of three or more core variables and consisted of paired variables linked by definition (e.g. sketch-like face hallucinations and no colour).
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Aetiology and specific hallucination categories
None of the phenomenological variables were influenced significantly by age, sex, acuity, the presence of cerebrovascular risk factors, current medication or descriptive fluency, and there was no difference in the prevalence of each variable in those patients who had taken part in our previous study (and had thus contributed to the development of the interview questionnaire) and those who had not. The only significant associations between phenomenological and aetiological or temporal variables were an association between coloured hallucinations and a diagnosis of SMD [
2(1) = 8.25, P < 0.01], and an association between longer duration hallucinations and perceived unpleasantness [2(1) = 7.22, P < 0.01]. |
Discussion |
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The results allow us to describe the typical CBS hallucination. It is a single constant and solid object, appearing in the central visual field `seen' in more detail than veridical objects. While most commonly a flash, it is often a complex grid, a disembodied distorted face, a small costumed figure with a hat or a branching structure. Our analysis revealed associations between hallucinations which formed segregated syndrome-like clusters. The three visual psycho-syndromes were unrelated to demographic or aetiological factors. We argue below that they reflect the anatomical and neurophysiological organization of the visual system.
Visual streams and hallucinatory syndromes
In man, as in the monkey, the visual brain consists of multiple map-like cortical representations of external space, each specialized for a different visual attribute (Zeki et al., 1991). The specialized cortical regions are interconnected, forming a hierarchy, with low level areas projecting to higher level ones (Van Essen et al., 1993). The hierarchy divides into two pathway streams, one ventral leading to the ventral temporal lobe and one dorsal leading to the parietal lobe (Van Essen et al., 1993; Ungerleider and Haxby, 1994). A third projection along the superior temporal sulcus is connected to both streams (Young, 1992; Ungerleider and Haxby, 1994).
Ventral temporal lobe
Single-cell neurophysiological recordings in the monkey and fMRI experiments in man have shown that the anterior ventral temporal lobe is specialized for complex features related to objects and landscapes (Kanwisher et al., 1996; Tanaka, 1996; Epstein and Kanwisher, 1998; Halgren et al., 1999). The region lies in close proximity to the amygdala which is activated by emotional stimuli (Morris et al., 1996). The functional specializations of the region match the categories of hallucination which together form the first syndromic cluster in our patient group: landscapes, figures and, to a lesser extent, vehicles, trees/shrubs (dendropsia), and emotional content. The similarity between the functional specializations of the region and the content of the hallucination cluster suggests a relationship between the two and leads us to propose that pathological increases in activity within the anterior temporal projection of the ventral pathway underly the first visual psycho-syndrome (Fig. 3, red).
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Superior temporal sulcus
In man, functional imaging studies have identified several cortical regions activated by face stimuli. Puce and colleagues and Kanwisher and colleagues (Puce et al., 1996
; Kanwisher et al., 1997) described an area in the fusiform gyrus selectively activated by face stimuli (the fusiform face area), while Puce and colleagues (Puce et al., 1998) and Wicker and colleagues (Wicker et al., 1998) have described an area in the superior temporal sulcus (STS) sensitive to eye movements and gaze in face stimuli. In the monkey, the homologous region contains subsets of neurones sensitive to eyes, eye movements and direction of gaze (Perrett et al., 1982, 1985). More recently, Hoffman and Haxby have added to these findings by showing that the fusiform face area underlies facial recognition while the STS underlies the processing of facial expression, in particular those expressive features related to the eyes (Hoffman and Haxby, 2000). Furthermore, evoked potential studies have found that the face-specific component recorded over the STS is maximal when eye stimuli are presented alone or within distorted face stimuli where the facial features have been rearranged (Bentin et al., 1996).
In our previous fMRI study, we described activation of the fusiform face area in a CBS patient with face hallucinations (ffytche et al., 1998). The face hallucinations reported were cartoon-like and sketch-like but otherwise unremarkable, in striking contrast to the distorted, grotesque faces with prominent staring eyes in the typical face hallucinations described in this study. We would argue that the grotesque distorted faces which form the second cluster of hallucination categories are unlikely to have arisen from pathological increases of activity in the fusiform face area. The prominence of the eyes and the indifference to the position of facial features implicit in the distortions reported is more in accord with the specializations of the STS face region. We therefore propose that the second visual psycho-syndrome relates to pathological increases in activity within the STS (Fig. 3, green).
Visual parietal lobe
In the monkey, the parietal lobe contains representations of space in a variety of different reference frames (Colby, 1998), helping maintain the stability of the visual world across successive eye movements (Duhamel et al., 1992). We argue that the pathological visual experiences of perseveration and delayed palinopsia (objects remaining in the field of view after the patient has looked away or returning after a short delay) imply functional abnormalities within parietal reference frames and that the third visual psycho-syndrome relates to pathological increases of activity in the parietal projection of the dorsal pathway (Fig. 3, yellow).
There is further evidence to link the three hallucinatory syndromes and visual pathway streams. A well-described organizational feature of the dorsal projection to the parietal lobe in the monkey is the predominant representation of the peripheral visual field while, in contrast, the ventral temporal lobe contains a predominant representation of the central visual field (Baizer et al., 1991). If our hypothesis were correct, one would expect the dorsal stream hallucinatory syndrome to be associated with the peripheral visual field and the ventral stream hallucinatory syndrome to be associated with the central visual field. This is exactly what we found—perseveration and delayed palinopsia were located in the peripheral visual field while hallucinations of figures, vehicles and landscapes were located in the central visual field.
Other evidence linking the hallucinatory syndromes to pathway streams stems from the fact that the anatomical connections of the STS place it in an intermediate position between the dorsal and ventral pathways (Young, 1992) so that, if our hypothesis were correct, one might expect links between the STS syndrome and the dorsal and ventral syndromes. In fact, we only found one such link, with hallucinations of faces with prominent eyes forming a phenomenological bridge between ventral and STS syndromes. Finally, the hypothesis that the third visual psycho-syndrome relates to the parietal projection of the dorsal stream is supported by the fact that delayed palinopsia and visual perseveration are associated with lesions in the parietal lobe (Critchley, 1951).
Methodological issues
The content of our visual psycho-syndromes depends on the phenomenological variables we have included in the structured interview/questionnaire and on the statistical methods used to explore the data. We will discuss each of these issues in turn.
Choice of phenomenological variables
Our structured interview/questionnaire was based on clinical experience, the results of our previous unstructured survey and the known specializations of the visual brain. While we have tried to be as comprehensive as possible, there are likely to be many further visual symptoms, yet to be described, which will fall into one or other of the clusters we have identified. An obvious omission in our choice of variables is visual motion, a known specialization of the human brain (Zeki et al., 1991). While our structured interview asked about motion, two-thirds of the patients felt that their hallucinations moved with their eyes, suggesting that the interview was not detecting hallucinations with intrinsic `true' motion. We therefore did not include the motion variables in our correlation matrix.
Factor analysis
We used factor analysis to explore our data set. The method has been criticized on the grounds that the answer obtained can be influenced by the investigator through the choice of matrix rotation (for a review, see Everitt and Dunn, 1991). In order to avoid this potential source of bias, we used standard factor extraction and rotation methods and confirmed that the associations reported were not statistical artefacts by examining the matrix of chi-squared tests. Since our aim in the factor analysis was to look for associations between several variables, we have ignored the lower ranking factors which contained variable pairs, linked by definition.
Chi-squared matrix
The chi-squared matrix quantifies the relative strengths of associations between different variables rather than testing the null hypothesis of independence for each pair of variables. Since our aim was to show the clustering of associations, we have not applied a Bonferroni correction for multiple comparisons. The clustering remains the same even if a Bonferroni correction is applied, the only difference being the significance associated with each test.
Tessellopsia
Our structured interview/questionnaire also contained specific questions about the size and perceived distance of individual elements in the grid-like hallucinations described in our previous study (ffytche and Howard, 1999). In that study, we suggested that tessellopsia might be related to the zig-zag fortifications of migraine aura, although we did not have phenomenological data to test the hypothesis directly. Migrainous zig-zags increase in size the more peripherally they are located in the visual field, making a direct comparison difficult. However, at a similar eccentricity to the tesselloptic grids in our patient group, the degrees of visual angle of migrainous zig-zags given by Richards (Richards, 1971) matches the degrees of visual angle of individual tesselloptic elements (see Fig. 4: 2.5 ± 1°, n = 127 in Richards, versus 3.7 ± 2°, range 1–8°, n = 17 in our patient group; t = 2.0 P > 0.05). The size of the smallest migrainous and tesselloptic elements also matches the critical grid size in the grid-like block portraits of the artist Chuck Close (Pelli, 1999). This critical grid size determines whether a viewer perceives Close's portraits as flat surfaces or as realistic faces. The convergence of the three sets of data from normal subjects, patients with eye disease and patients with migraine suggests that all three phenomena may be related. We have argued that they are linked to long-range cortical connections in early visual areas whose cortical extent and connectivity match the spatial extent and geometry of the perceptual phenomena (ffytche and Howard, 1999), although how the anatomy and perceptual experience relate are questions for further study.
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Coloured hallucinations and SMD
Apart from the clustering of hallucinations into specific syndromes, we also found an association between colour hallucinations and SMD. The association was not predicted a priori and can be criticized on the grounds that the significance of the association does not withstand correction for multiple comparisons. However, it sheds some light on the question as to why pathological activity might influence some pathways in the visual system and not others. Colour vision is impaired early in SMD (Bowman, 1980
) and becomes worse as the disease progresses. Colour loss results from the fact that the cones serving colour vision are located predominantly in the macular region affected by the disease. Signals related to colour vision pass to the parvocellular layers of the lateral geniculate nucleus and, thence, through areas V1 and V2, to the colour area in the ventral pathway (Zeki and Shipp, 1988). Clarke found evidence for degeneration throughout the ventral colour pathway in a post-mortem study of a patient with SMD (Clarke, 1994) and we would argue that the association between SMD and colour hallucinations is the result of selective de-afferentation with localized hyper-excitability within the colour area resulting in coloured hallucinations. Our fMRI evidence provides some support for the theory as the colour area was tonically hyperactive in CBS patients with SMD (ffytche et al., 1998).
Models of syndrome formation
How are we to interpret the similarities that we have found between, on the one hand, clusters of visual hallucinations which segregate into visual psycho-syndromes and, on the other hand, the known segregation of anatomical connections in the visual cortex into extended hierarchical pathway streams? The question that prompted the study was whether pathological activity from one cortical area might propagate along anatomical interconnections to another area and be reflected in an association between different types of hallucination. In such a model, extended pathways of interconnected areas result in syndromes of connected symptoms, i.e. segregated pathways leading to segregated syndromes. However, since many classes of hallucination fell outside the three clustered syndromes, the mechanism of syndrome formation may not be so straightforward. If anatomical connectivity underlies phenomenological connectivity then why are many hallucinations isolated and independent in nature? The answer may lie in the fact that the areas that correspond to syndromic clusters are positioned at the top of the visual hierarchy while the areas that seem to correspond to independent hallucinations are positioned at the bottom. While this may mean that areas at the top of the hierarchy have stronger anatomical connections and hence lead to stronger links between their associated hallucinations, another interpretation relates to the fact that the complexity of visual information increases as one ascends the visual hierarchy (Ungerleider and Haxby, 1994). Low level areas represent simple visual features and are likely to be associated with simple hallucinations. High level areas represent complex visual features by integrating different low level inputs, and thus pathological activity restricted to a single high level area is likely to result in multiple hallucination categories apparent as a symptom cluster. Without specific imaging studies to test the different hypotheses, the exact mechanism of syndrome formation remains speculative.
Conclusion
The apparent neurobiologically based clustering of visual hallucinations in CBS has implications which extend beyond visual science. It suggests that syndromic links between specific pathological mental experiences are not random or arbitrary details, but clues as to the cerebral location of functional pathology. CBS visual hallucinations provide a model with which to generate and test hypotheses about hallucinations in general and, given the wealth of neurobiologically based research into the visual system over the last two decades, an opportunity to study the detailed relationship between psychopathology and the brain. The challenge for neuropsychiatry is to develop the neurobiology of the auditory system, of delusion formation and of disordered thinking to interpret the associations between psychotic symptoms encountered clinically.
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Appendix: Outline of the Institute of Psychiatry Visual Hallucinations Interview |
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When did your visual experiences begin?
When was your last vision?
How often do they occur?
How long typically do they last?
Are they pleasant, unpleasant or neutral?
Do you see them in front of you, or out of the corner of your eye?
Do you see them in your blind area?
Are they in more detail than the real objects around you?
Can you see through them?
Do you see them with your eyes closed?
Do the visions go away if you move your eyes or blink?
Do the visions move when you move your eyes or move your head?
Are they in colour and, if so, is the colour normal, vivid or dull?
Are the visions like whole scenes, or individual objects/figures?
Do visions usually change from one thing into another?
Flashes, lines, colours, zig-zags, Catherine wheels?
A complete figure/group of figures? (if so, were they small, in costume or uniform, wearing a hat?)
A face without a body? (if so, was it realistic or caricature, ugly, prominent eyes or teeth?)
Words, letters, musical notes or numbers?
Vehicles?
Regular patterns (brickwork, netting, honeycombs, latticework, etc.)?
Irregular patterns (maps, hedges, bushes, etc.)?
Field of view covered with small particles (rain drops, snowflakes, hundreds and thousands etc.)?
Multiple copies of an image at the same time (if so, did they form a row?)
Surfaces filled with objects, patterns or shapes?
Looked at something and found that its image persisted even after you looked away?
Looked at something and found that its image returned some time later?
Visions brought on by motion (being driven, on a train, etc.)?
Exclusion questions
Visions associated with sound or talking?
Visions associated with dizziness, strange smells or other unusual sensations?
Occurrence only in bed or on waking from sleep?
History of stroke, major psychiatric illness, epilepsy?
Frightening visions of small animals, spiders, snakes, maggots, etc.?
Descriptive fluency
Describe a Christmas tree.
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Acknowledgments |
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We thank Dr Pak Sham for statistical advice. This work was supported by the Wellcome Trust; D.H.ff is a Wellcome Trust Clinician Scientist Fellow.
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Received January 27, 2000. Revised May 19, 2000. Accepted June 12, 2000.
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  E. J. Abbott, G. B. Connor, P. H. Artes, and R. V. Abadi Visual Loss and Visual Hallucinations in Patients with Age-Related Macular Degeneration (Charles Bonnet Syndrome) Invest. Ophthalmol. Vis. Sci., March 1, 2007; 48(3): 1416 - 1423. [Abstract] [Full Text] [PDF]
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 U. P. Mosimann, E. N. Rowan, C. E. Partington, D. Collerton, E. Littlewood, J. T. O'Brien, D. J. Burn, and I. G. McKeith Characteristics of Visual Hallucinations in Parkinson Disease Dementia and Dementia With Lewy Bodies Am J Geriatr Psychiatry, February 1, 2006; 14(2): 153 - 160. [Abstract] [Full Text] [PDF]
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 N. Oishi, F. Udaka, M. Kameyama, N. Sawamoto, K. Hashikawa, and H. Fukuyama Regional cerebral blood flow in Parkinson disease with nonpsychotic visual hallucinations Neurology, December 13, 2005; 65(11): 1708 - 1715. [Abstract] [Full Text] [PDF]
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 S A Madill, D H Ffytche, and C. S. Tan Charles Bonnet syndrome in patients with glaucoma and good acuity Br. J. Ophthalmol., June 1, 2005; 89(6): 785 - 786. [Full Text] [PDF]
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 G. J. Menon Complex Visual Hallucinations in the Visually Impaired: A Structured History-Taking Approach Arch Ophthalmol, March 1, 2005; 123(3): 349 - 355. [Abstract] [Full Text] [PDF]
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 C. Frith The pathology of experience Brain, February 1, 2004; 127(2): 239 - 242. [Full Text] [PDF]
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 D H ffytche, J M Lappin, and M Philpot Visual command hallucinations in a patient with pure alexia J. Neurol. Neurosurg. Psychiatry, January 1, 2004; 75(1): 80 - 86. [Abstract] [Full Text] [PDF]
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P. Soros, O. Vo, I.-W. Husstedt, S. Evers, and H. Gerding Phantom eye syndrome: Its prevalence, phenomenology, and putative mechanisms Neurology, May 13, 2003; 60(9): 1542 - 1543. [Abstract] [Full Text] [PDF]
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W Burke The neural basis of Charles Bonnet hallucinations: a hypothesis J. Neurol. Neurosurg. Psychiatry, November 1, 2002; 73(5): 535 - 541. [Abstract] [Full Text] [PDF]
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A. J. Harding, E. Stimson, J. M. Henderson, and G. M. Halliday Clinical correlates of selective pathology in the amygdala of patients with Parkinson's disease Brain, November 1, 2002; 125(11): 2431 - 2445. [Abstract] [Full Text] [PDF]
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A. J. Harding, G. A. Broe, and G. M. Halliday Visual hallucinations in Lewy body disease relate to Lewy bodies in the temporal lobe Brain, February 1, 2002; 125(2): 391 - 403. [Abstract] [Full Text] [PDF]
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