Fernando - Waters2014
Fernando - Waters2014
Fernando - Waters2014
S233–S245, 2014
doi:10.1093/schbul/sbu036
Flavie Waters*,1,2, Daniel Collerton3, Dominic H. ffytche4, Renaud Jardri5, Delphine Pins5, Robert Dudley6,7,
Much of the research on visual hallucinations (VHs) has review suggests that comparative studies may have poten-
been conducted in the context of eye disease and neurode- tially important clinical and theoretical implications.
generative conditions, but little is known about these phe-
nomena in psychiatric and nonclinical populations. The Key words: visual hallucinations/schizophrenia/
purpose of this article is to bring together current knowl- psychosis/cognition/imaging
edge regarding VHs in the psychosis phenotype and contrast
this data with the literature drawn from neurodegenerative
Introduction
disorders and eye disease. The evidence challenges the
traditional views that VHs are atypical or uncommon in Hallucinations are defined in different ways by different
psychosis. The weighted mean for VHs is 27% in schizo- philosophical traditions.1 In the clinical domain, a visual
phrenia, 15% in affective psychosis, and 7.3% in the general hallucination (VH) is a visual percept, experienced when
community. VHs are linked to a more severe psychopatho- awake, which is not elicited by an external stimulus. It con-
logical profile and less favorable outcome in psychosis and trasts with a visual illusion which is elicited by an external
neurodegenerative conditions. VHs typically co-occur with stimulus but differs from the percept normally associated
auditory hallucinations, suggesting a common etiological with the stimulus. VHs occur in a wide-range of organic
cause. VHs in psychosis are also remarkably complex, and psychiatric conditions, as well as in the absence of
negative in content, and are interpreted to have personal any demonstrable pathology. These experiences have been
relevance. The cognitive mechanisms of VHs in psychosis well described and researched in the context of organic
have rarely been investigated, but existing studies point disorders, particularly eye disease and neurodegenerative
to source-monitoring deficits and distortions in top-down conditions such as dementia with Lewy bodies (DLB)
mechanisms, although evidence for visual processing defi- and Parkinson’s disease (PD), but VHs have been largely
cits, which feature strongly in the organic literature, is neglected in psychiatric disorders and delirious states and
lacking. Brain imaging studies point to the activation of in nonclinical populations.
visual cortex during hallucinations on a background of Although the diagnostic manuals for mental disorders
structural and connectivity changes within wider brain list hallucinations as a primary characteristic symptom in
networks. The relationship between VHs in psychosis, eye psychotic disorders, auditory hallucinations are the symp-
disease, and neurodegeneration remains unclear, although toms that clinicians commonly ask about. One expla-
the pattern of similarities and differences described in this nation lies in the traditional beliefs that VHs are more
© The Author 2014. Published by Oxford University Press on behalf of the Maryland Psychiatric Research Center.
This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/3.0/),
which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.
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common in organic states than in psychosis.2 It is also of hallucinations, the weighted mean frequency of VH is
often difficult to decide whether the full criteria for the approximately 15% (range: 6%–27%, SD = 9). Similarly
presence of VHs have been fulfilled when a range of other to schizophrenia, the rates of VH in bipolar disorder are
perceptual abnormalities are reported. approximately half that of auditory hallucinations (28%).
In this article, we review the available evidence with Overall, these data challenge the assumption that VHs
regards to the prevalence, phenomenology, clinical char- are atypical or uncommon in psychosis.
acteristics, and assessment methods for VHs in the psy-
chosis spectrum alongside studies of cognition, brain Subclinical Symptoms in the General Community
imaging, electrophysiology, and treatment (cognitive
behavioral and pharmacological). Given the lack of Occasional hallucinatory experiences are fairly common
available literature on other psychiatric disorders, our in community-living individuals. However, community
Table 1. The Comparative Point Prevalence of Visual and Auditory Hallucinations in Schizophrenia
Modality of Hallucinations
Zarroug (1975)20 69 47 62
Ciompi and Müller (1976)21 a
18 58
McCabe (1976)18 25 20 52
Deiker and Chambers (1978)22 28 64 86
Huber (1979)23 a
33 75
Ndetei and Singh (1983)24 51 43 43
Ndetei (1984)25 141 15 41
Winokur et al (1985)26 140 32 78
Phillipson and Harris (1985)27 73 62 44
Bracha et al (1989)28 43 56 42
Owens and Slade (1989)29 a
29 63
Mueser et al (1990)30 117 14 71
Jablensky et al (1992)4 1288 30 55
Bauer et al (2011)31 1238 34 79
Total: 29 studies, n = 5873 participants Weighted mean = 27% Weighted mean = 59%
SD = 9.73 SD = 15.30
Table 2. The Comparative Prevalence of Visual Hallucinations and Auditory Hallucinations in Bipolar and Affective Disorder
Modality of Hallucinations
Table 3. The Comparative Prevalence of Visual Hallucinations and Auditory Hallucinations in the General Community (A) and After
Excluding Hallucinations Arising From Drug-Taking or Physical Illness (B)
more common in younger, compared with older, individ- hallucinations of a dead spouse are common grief reac-
uals with schizophrenia,31,53 although negative findings tions in older adults.59
exist.16 A similar inconsistency is found in the eye disease The literature in neurodegenerative disease is consis-
literature with only 3 of 9 studies investigating age and tent with this view of greater psychopathology in VH,
VHs reporting a weak association.51 with studies showing poorer response to treatment,
By contrast, in nonclinical populations, the prevalence greater mortality and morbidity, major depressive syn-
of VH is maximal in adolescence, and late adulthood, drome, and a move to institutional care.60,61
between which times the frequencies decrease.40,54 One Thus, in both younger patients with psychosis and
explanation for increased frequency of VH with age is older patients with neurodegenerative disease, VHs are
that the prevalence of most chronic disorders increases associated with poorer functioning and outcome. The
with age, as does the prevalence of neurodegenerative dis- same is not true of eye disease (eg, CBS) where the symp-
orders and age-related eye disease. In further support, the toms improve over time without progressive loss of cog-
prevalence of death-bed visions among the dying may be nitive function.
as high as 50%.55
Thus, there appears to be a bimodal distribution of Association With Other Symptoms
VH in the population with one peak in late adolescence
and early adulthood, which is associated with psychosis, In schizophrenia, VHs typically co-occur in association
and a second increase in late life associated with eye and with other hallucinations and other sensory modali-
brain disease. ties.16,28,30,62 For example, it has been reported that co-
With regards to the longitudinal course, it is believed occurring visual and auditory hallucinations occur in up
that hallucinations in schizophrenia tend to decrease as to 84% of individuals with schizophrenia.30 Furthermore,
individuals age,56 although it is important to note that the early evidence suggested VH never occurred in psychosis
risk of schizophrenia also declines with age. without the presence of auditory hallucinations (either
at the same time—multimodality hallucinations—or on
different occasions).62 In Oorschot et al’s57 sample of
Clinical Characteristics of VH individuals with mixed psychosis, VHs occurring alone
The presence of VH in psychosis has often been linked to were rarer than auditory hallucinations occurring alone.
a more severe psychopathological profile30,57 and to a less As shown in table 1, auditory hallucinations predominate
favorable prognosis.18 In patients with bipolar disorder, over VH in terms of their relative prevalence.
Baethge et al37 found that hospitalization for individuals Hallucinations in multiple modalities have also been
with hallucinations (all modalities) averaged 17% longer noted in individuals with severe depression63 and with
than those who did not hallucinate. mixed psychiatric diagnoses,64 as well as in nonclinical
In the general community, a link between VH and anx- adults and adolescents (n = 355, 11–13 years).65 Such
iety (OR = 5.0)41,58 and psychotic pathology (OR = 6.6)41 co-occurrences of auditory/VHs suggest a common hal-
has been reported. The important role of negative lucinatory mechanism which, in combination with spe-
emotions in VH is illustrated in studies showing that cific sensory dysfunctions, determines the modality of
stress and bereavement are linked to VH. For example, hallucinations.
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It is important to note, however, that “simultaneous” in PD, visions of dead people are rare, although visions
(or “fused”) auditory and VHs are not a frequent occur- of God, angels, the devil, saints, and fairies are common.
rence.16 In most cases, they are experienced at different
times (eg, an auditory hallucination one day and a VH the Reality. VHs are perceived to be real and “definitely
next). Furthermore, when simultaneous auditory/VHs do present” in a concrete sense. In further support for the
occur, they are typically unrelated66 (eg, seeing the devil subjective reality of the experience, a majority of indi-
while hearing the voice of a relative inside one’s head), viduals undertake some activity directly related to the
suggesting that the mechanisms for auditory and VHs in vision—such as moving toward the vision, hitting at the
these disorders must be partly independent, though with vision, or moving away. In the case of distressing images,
some overlap. individuals may act to keep themselves safe.
By contrast, a different pattern can be observed in
other disorders, namely frightening contents, emotional grotesque and cartoon-like (40%), landscapes or inani-
reactions, and appraisals of personal significance; a lack mate objects (20%). They are usually colorful. Unlike
of illusions (common in neurodegenerative disease) and in psychosis, VHs in CBS are not generally perceived to
simple VHs (common in eye disease) also differ. be real or to have personal meaning. Only in a third of
the cases is the content negative. Once individuals under-
Subclinical Symptoms in the General Community stand they are a common feature of poor vision, anxiety
about VH generally decreases. This differs from psycho-
Nonclinical individuals in the community report vivid sis, where lack of insight may contribute to distress about
VH, where objects are real and uncontrollable, but often these experiences. Other dimensional features related to
of brief duration.73 The features of VH in nonclinical clarity, frequency, temporal factors, and appearance are
samples are broad-ranging and include unformed VH similar to those in psychosis.76 In PD, VHs mostly con-
Fig. 1. Visual perceptual symptoms and their clinical contexts.77 A range of clinical conditions (columns) are cross-tabulated with visual
hallucination (VH) content and related phenomena (rows). For each condition, the percentage of individuals with VHs reporting a
given content is coded red (>20%), pink (10%–20%), or white (not reported or < 10%). The prevalence of each symptom in psychosis
is taken from.64 For auditory hallucinations, (+) indicates higher prevalence than VH and (−) indicates lower prevalence than VH
(figure adapted from ffytche77). Visual experiences in schizophrenia best match the phenomena reported in the red box derived from
PD, AD, DLB, and peduncular lesions—but not the green (eye and visual pathway pathology) and blue (serotonergic syndrome) boxes.
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Visual Hallucinations in the Psychosis Spectrum
and intrinsically affected, these authors proposed an exter- was at risk of harm from these snakes. CBT that included a
nal DMN interference through aberrant interactions with graded exposure approach to help reduce fear and escape
ventral and dorsal attentional networks. reaction showed some benefit which was maintained at 3
Fewer studies have investigated the electrophysiology months. Whether this is helpful with other visual experi-
of VH. Spencer and colleagues found reduced visual cor- ences is unclear, although studies show that the apprais-
tex activation as measured by a negative evoked potential als and beliefs should be a core target for treatment.70,108
component (NI) and increased gamma band phase lock- Collerton and Dudley109 developed a model drawn
ing associated with VH in schizophrenia, consistent with from a cognitive model of auditory hallucinations and
an underlying visual cortical hyperexcitability and reduced panic and which targets appraisal and reactions to VH.
responsiveness to external visual stimulation in this sub- Given that avoidance, escape and safety-seeking behav-
group.102 Indices of hyperexcitability and reduced respon- iors are common but unhelpful strategies, the aim of
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