Visual

Hallucinations

Suzanne

Holroyd,

Marie

M.D.,

C. Nicholson,

Objective: in patients

determine

design,

the authors

visual

patients of scores Interview

R.N.,

factors

visual

The

patients

and

family

Depression Status,

history,

and

and

medical

and

Of the associated

cognition

and

score,

history family of the

change

in vision.

among disorder.

patients The

association (Am

Conclusion:

cortical

J

Psychiatry

sensory

deprivation,

inhibition

theory.

1992;

149:1701-1706)

bilaterally

results

while

V

isual hallucinations are associated with a variety of lesions at all levels of the visual system (1-3). Weinbenger and Grant (2) reported visual hallucinations in patients with pituitary tumors pressing on the optic nerves and chiasm, noting that the hallucinations were not limited to the area of visual field loss. Lance (4) reported visual hallucinations in patients with homonymous field defects and noted that the hallucinations were confined to the area of visual field loss in all but one patient. Because the calcanine area of the occipital lobe was infarcted in many of these patients, he concluded that it was not the origin of the hallucinations and suggested that the surrounding visual association cortex was. Kolmel (5) reported that 13% of 120 patients with homonymous hemianopia and occipital lobe damage experienced complex visual hallucinations in the hemianopic field. The subjects Received

19, 1991; revision received April 1, 1992; accepted From the Department of Psychiatry and Behavioral Sciences and the Department of Ophthalmology, Johns Hopkins University School of Medicine, Baltimore. Address reprint requests to Dr. Holroyd, Department of Behavioral Medicine and Psychiatry, University of Virginia School of Medicine, Blue Ridge Hospital, Drawer D, Charlottesville, VA 22901. Copyright © I 992 American Psychiatric Association. April

AmJ

23,

Sept.

1992.

Psychiatry

149:12,

December

1992

matched

visual

indicate

that

history

degeneration

compared

Ophthalmologic

acuity.

data

visual

Hallucinations

hallucinations

and

were

visual hallucinations. living alone, lower were

disorder or with personality begun in association with

of stroke

three

in terms

Questionnaire, Telephone including demographic char-

history.

worse

a case-control to the next

were

I 00 patients, 1 3 experienced with having hallucinations:

history of psychiatric the hallucinations had

These

Using macular

subjects

with macular degeneration. They appear unrelated predisposing factors of bilaterally worse vision and

with

decreased

ofstroke, or personal 13 patients,

B.A.

of visual hallucinations phenomenologically, and

was

comparison

M.D.,

C. Wisniewski,

age-related

hallucinations

psychiatric

Finkelstein,

Method:

with

Inventory, Eysenck Personality a structured questionnaire

obtained by chart review. Results: Four variables were significantly associated with In 1 1 (84.6%)

and Sally

development.

Degeneration

Daniel

the prevalence hallucinations

patients

with

hallucinations.

Ph.D.,

to their

patient

Macular

M.P.H.,

to determine describe such

1 00 consecutive

Each

M.D.,

A. Chase,

predisposing

screened

on the Beck for Cognitive

acteristics,

Gary

was undertaken degeneration,

hallucinations. without

With

Peter V. Rabins,

This study with macular

possibly

f or

in Patients

to primary living alone worse

cognition

are

not

traits. an acute prevalent

psychiatric support support

an a

stated that the hallucinations occurred hours to days after the loss of vision and disappeared when the hemianopia resolved. He concluded that the hallucinations were “release phenomena” rather than the result of an irritative lesion. Fitzgerald (6) reported that 15% of 66 patients developed hallucinations within 1 year of becoming blind. He suggested that they were associated with “maladaptive coping” (6, p. 1534) and depression. Lepore (1) examined 104 patients with visual loss due to lesions from the retina to the occipital lobe. He found a 21% prevalence of complex hallucinations on “spontaneous visual phenomena.” The severity of the visual acuity loss correlated with hallucinations, but the presence of bilateral as opposed to unilateral disease, olden age, or other central nervous system disease did not. He doubted that these hallucinations were associated with psychiatric disorder but did not screen for this. The eponymous Charles Bonnet syndrome (7-12) has been used to label persistent complex visual hallucinations that occur in the absence of other psychopathology. This syndrome is often associated with eye disease, and insight is fully on partially retained. Most afflicted individuals who have been described were elderly. Controversy exists about whether brain lesions and/or eye

1701

VISUAL

HALLUCiNATIONS

pathology 9,

are

necessary

to produce

this

syndrome

(7,

13-15).

Many proposed.

theories Jackson

inhibiting

activity, is that

to

explain hallucinations (16) proposed that

influence

of

producing the

the

cortex

releases

hallucinations.

reduction

of

have been loss of the

the

subcortical

A related

sensory

input

to

theory specific

(17) areas

of the brain allows previous perceptions into consciousness as hallucinations. Several lines of data support this hypothesis. A review of sensory deprivation studies (18) indicated that approximately 19% of normal subjects undergoing a variety of sensory deprivation regimens develop visual hallucinations. Interestingly, long penods of isolation were not required; some hallucinations occurred within 48 hours. This theory is also supported by research showing that retinal ganglion cells discharge spontaneously. It has been suggested that decreased sensory stimulation allows these discharges to mimic normal stimuli and are misinterpreted as sensory signals (18). “Black patch psychosis” (19), a term for delirium associated with patching both eyes after cataract surgery, has been offered as further evidence of the sensory depnivation hypothesis. However, unlike patients with the other conditions discussed, these patients are often delinious, and exogenous factors such as anticholinergic eye drops have not been investigated as causes of delirium. Other data demonstrate that cortical hypenexcitability

on irritability

can

cause

visual

hallucinations.

Foer-

ster (20) found that electrical stimulation of Broadman areas 17 and 18 of the occipital lobe caused visual sensations, whereas stimulation of area 19 produced complex visual phenomena (figures, people, animals). Penfield and Perrot (21 ) produced hallucinatory expeniences in 7.7% of subjects by stimulating cortical or subcontical structures. The high prevalence of visual hallucinations among people with epilepsy also supports this hypothesis. As some of the aforementioned studies show, the occipital and temporal lobes are associated with visual hallucinations. Furthermore, hallucinations are frequently present in complex partial seizures, which often originate in the

temporal

lobe.

The

lobe

more

focus, the more complex At the neurochemical level dopaminergic and cholinergic in the

induction

of visual

posterior

the

the hallucinations the reciprocal systems may

hallucinations.

temporal

roles play

The

(22). of the a part

treatment

of Parkinson’s disease with dopamine agonists can produce visual hallucinations and other psychotic phenomena (17, 23-25). Although visual hallucinations are seen in association with a variety of disorders and occur in normal subjects under special environmental conditions, it is notable that only some people experience them in any one cmcumstance. Numerous predisposing factors have been postulated. They include psychologic stress (1 1, 26, 27),

suggestibility

(29), and cognitive personality traits some studies have

I 702

(28),

differences

in age

or

education

deficits (26, 28, 29). Predisposing have also been studied (28, 30), and shown an association between hallu-

cinations and scores on the neuroticism scale of the Eysenck Personality Questionnaire (28, 31 ). Barber (32) suggested that a small percentage of people can hallucinate at will. To further characterize the prevalence and descniption ofcomplex formed visual hallucinations in patients with visual disorders, we undertook a prevalence and case-control study of individuals with a single ophthalmologic disorder. It was hoped that features pnedisposing individuals to visual hallucinations could be determined and would suggest theories regarding possible pathophysiology. We chose to study patients with agerelated maculan degeneration because of reports that they have visual hallucinations (33). Also, age-related macular degeneration is not associated with major systemic changes of the body or brain, as are disorders such as diabetic retinopathy, so it is easier to determine whether the loss of vision is a precipitating factor in the visual

hallucinations.

eration scar

may size.

Also,

the

be measured

This

defect

by visual

allowed

for

in macular

acuity

a test

of the

larger lesion size on worse acuity the development of hallucinations.

would

and

degen-

disciform

hypothesis

that

predispose

to

METHOD One hundred seven consecutive patients who had been diagnosed as having age-related maculan degeneration by full-time faculty ophthalmologists at a university

retinal

in a study

vascular

center

would

involve

that

were

asked

answering

to participate questions

ne-

garding their vision. One hundred subjects agreed to participate and gave written informed consent. Once enrolled, each patient was screened for hallucinations by one of two interviewers (S.H., M.C.N.) with the following question: “When people have trouble with their eyes, it frequently affects their vision. It may make it difficult

to see

things

that

are

there,

but

sometimes

peo-

ple see things that really are not there on see things that other people don’t see. Has this ever happened to you?” Each subject who responded positively was asked to describe the experience so that illusions, dreams, or vivid Simple

thoughts visual

could be experiences

excluded such

by as

the interviewers. dots, colors,

or

flashes of light were not considered to be complex visual hallucinations. Any subject who experienced true complex visual hallucinations underwent a structured interview. Data were collected on age; sex; race; level of education; handedness; living situation; medical history; loss of hearing, taste, or smell; head trauma; delirium;

current

medicines;

family

history

of

neunologic

and psychiatric disorders; personal psychiatric history; and substance abuse. All subjects were given the Eysenck Personality Questionnaire (34) and the Beck Depression Inventory (35). The Beck scale was chosen because it has been shown reliable in persons over age 60 (36). The Telephone Interview for Cognitive Status (37),

a cognitive

the Mini-Mental

Am

screen

shown

State

examination

J

Psychiatry

to correlate

(38)

highly

but not

1 49:1 2, December

with

depend

1992

HOLROYD,

TABLE

1. Differences

Between

Patients

With Macular

Degeneration

W ith Hallu cinations Variable

N

Significantly different Living alone History of stroke Bilateral vision of 20/60

Score

on Telephone

or worse

Interview

Cognitive Status Score33 Score>33 Nearly significantly Hearing loss

aFishers

exact

20.5 2.6 13.3

20 19

51.3 48.7

92.3 7.7

9

69.2

15

38.5

10

76.9

20

51.3

30.4

(N=39)

Mean

SD

Analysis

X2=4.76,

df=1, p=O.OL3 =0#{149}04a X2=4.84, df=1, p=O.O3

2.6

32.8

2.9

F=6.79,

77.9 20/91.2

df=1,

SO, p=O.OI

2

X =6.93,df=1,p=0.009

different

23.7I,

df=I,

p=O.O6

po.loa

6.0 63.9

73.9 20/58.5

7.8 49.7

F=2.83, F=3.62,

df=1, df=l,

SO, p=O.lO 49, p=O.O6

test.

no

correction

for

multiple

comparisons

for the hallucinarelative

Thirteen of the 100 patients screened positive for visual hallucinations, giving a prevalence of 13%. Thirtynine hallucination-negative patients served as companison subjects. The mean age of the 52 subjects was 74.9 years (SD= were 57.7%

white were

(N=45), female

level was 113 years was 20/105 for either

J

8 I 13

12 1

RESULTS

Am

%

53.8 23.0 69.2

eye

Therefore,

cation acuity

N

7 3 9

was used. Nonadjusted relative risks were calculated variables that distinguished the patients with tions and the comparison subjects. Adjusted risks were calculated by logistic regression.

7.5); 86.6% (N=22) and

With out Hall ucinations

SD

on visual or motor capability, was also given. A structuned questionnaire was then given to further delineate the phenomenology of the visual hallucinations. A copy of the interview instrument can be obtained from the authors. The case-control method was chosen to identify predisposing factors for hallucinations because the prevalence of positive cases was unknown and a low prevalence was suspected. After each positive case was identified, the next three hallucination-negative patients were identified as comparison subjects and were given the same battery except for the questionnaire further delineating the phenomenology of the visual hallucinations. Data regarding the patient’s visual diagnosis, visual acuity, disciform scar size, and laser treatment history were abstracted from the chart by one of us, an ophthalmologist (D.F.). The data were analyzed by using the following statistics: Fisher’s exact test, chi-square analysis, analysis of variance, logistic regression, and discniminant analysis. The obtained p values were used to assess the strength of association of the variables with the presence of visual hallucinations rather than to test a formal hypothesis.

ET AL.

Who Did or Did Not Have Visual Hallucinations

(N=13)

Mean

FINKELSTEIN,

for

Femalesex Age (years) Vision in best

%

RABINS,

Psychiatry

149:12,

and 42.3% (N=30). The

(SD=2.S). The eye (SD=78.S).

December

1992

were mean

mean

male edu-

visual

As shown cantly

from

in table the

1 , the hallucinators

comparison

differed

subjects

on

the

signifi-

variables

of

living alone, having a personal history of stroke, having bilateral visual acuity of 20/60 or worse, and scone on the Telephone Interview for Cognitive Status. A score of 33 on the Telephone Interview for Cognitive Status was used to divide the groups into those with better and worse cognition. This score was chosen because the distnibution of scores was bimodal. The hallucinators were more likely to score 33 or less (table 1). Several variables showed nearly significant differences between the patients with and without hallucinations (table 1). These variables were hearing loss, female sex, age, and visual acuity in the patient’s best eye. This last variable was used as a measure of best acuity. Logistic regression and discniminant function analysis were

used

to identify

a model

of variables

that

could

best predict whether a patient with macular degeneration would or would not have visual hallucinations. A four-factor model (using the four significant variables of living alone, history of stroke, lower score on the Telephone Interview for Cognitive Status, and bilateral vision of 20/60 or worse) determined by logistic regression gave the overall best prediction of 878%. It conrectly classified 61.5% of the hallucinators and 97.2% of the comparison subjects. Discniminant analysis was performed on the four significant variables as well as the four variables that showed nearly significant differences (hearing loss, female sex, olden age, worse visual acuity in the best eye) but resulted in a lower overall predictive value than did the logistic regression. The adjusted and nonadjusted relative risks for the significant variables and the nonadjusted relative risks for the nearly significant variables are shown in table 2. Also of interest were the variables found not to be significantly different between the hallucinators and comparison subjects. These included level of education, handedness, number of concurrent medical disorders, loss of taste or smell, history of head trauma or delirium,

number

of medications,

on current), family disorder (Parkinson’s

on personal disease,

drug

and

alcohol

use

(past

history of neurologic stroke, epilepsy, or de-

1703

VISUAL

HALLUCINATIONS

TABLE lucinations

2. Nonadjusted and Adjusted Relative Risks for Visual Halin 52 Patients With Macular Degeneration Nonadjusted Relative Risk

Adjusted

TABLE 3. Characteristics Macular Degeneration

Relative

Patients Hallucination

Living History

alone of stroke

Risk

Confidence Interval

Risk

4.23 1 1.40

1.10-16.19 1.07-121.70

2.48 15.50

20/60 or worse Hearing loss Female sex Older age Worse vision in best eye

aDetermined

alone, 20/60

by logistic

history of stroke, or worse).

11.40

1.35-96.34

4.33 3.60

1.12-16.78 0.94-13.79

3.16

0.75-13.29

2.37

0.62-9.00

3.32

0.87-12.67

regression lower

Number

Percent

10 3

76.9 23.1

Normal

9

Abnormal

2 2

69.2 15.4 15.4

9 3 1

69.2 23.1 7.7

12 I

92.3 7.7

7 1

53.8 38.5 7.7

11 2

84.6 15.4

6 2

46.2 38.5 15.4

7

S3.8

Size Normal Abnormal

Confidence Interval

Color

0.47-113.04 0.89-270.16

13.05 4.59

Variable Transparency Solid Transparent Variable Definition Sharp Blurry

0.97-175.75 0.85-24.90

of edges

Movement

using

a four-variable

cognition

score,

bilateral

model

(living

vision

of

mentia), and family on personal history of psychiatric disorders (affective disorder, schizophrenia, anxiety, or other). There were no differences between the hallucinators and the comparison subjects in scones on the Beck Depression Inventory or Eysenck Personality Q uestionnaire. There were no differences in history of laser treatment to eyes on disciform scar size. Characteristics of the hallucinations are shown in table 3. The patients saw a wide variety of hallucinations; some patients saw only one form, whereas others saw many different forms. They included animals, people, both full bodies and faces, scenery, objects, and geometnc shapes. Examples include “elaborate rows of Victonan houses, with pastel colons,” “frightening faces with brown hair that would grow to coven the face,” “a collie dog,” “moving gold chains,” “red brick buildings,” “groups of brown-ned squares,” “groups of men wearing elaborate fifteenth-century garb,” and “two miniatunized teams of men playing football.” The period during which the patients had seen these hallucinations ranged from 2 to 36 months at the time of the interview. Eleven subjects (84.6%) reported an acute change in vision coincident with the beginning of the hallucinations, while two (15.4%) described an insidious onset. Three (23.1 %) noted that the hallucinations always occurred during the same time of day. Three (23.1%) found they occurred more often in bright light, two (15.4%) said they occurred more often in dim light, and eight (61.5%) found no difference. Four (30.8%) could make the hallucinations teinporanily go away by blinking, one (7.7%) could do so by trying to focus on the hallucinations, and eight (61.5%) were unable to affect the hallucinations. No patient could induce a hallucination. None of the visual hallucinations were accompanied by a hallucination in another sense (auditory, olfactory, tactile, or gustatory). Although all of the subjects believed that the hallucinations were related to their eye

1704

Characteristic

95%

Lower score on Telephone Interview for Cognitive Status Bilateral vision of

in 13 Patients With

Riska

95% Variable

of Visual Hallucinations

Moves Stands still Variable Appearance relative As real Not as real Familiarity of objects Seen before Unfamiliar Both Frequency Daily

S to other

things

S

Weekly

2

15.4

Monthly Don’t know

3 1

23.1

7 1 4 1

53.8 7.7 30.8 7.7

6

46.2

3 I 3

23.1 7.7 23.1

7

53.8

4 2

30.8 15.4

Present

frequency

relative

frequency Same

More Less

often often

Don’t

know

Duration Minutes

Hours Days Variable Presence

in area

of visual

loss

Yes No Both

Presence

in same

on different Yes No

7.7

to past

area of visual

field

occasions 12 1

92.3 7.7

disorder, three (23.1 %) had occasionally acted on the hallucination (e.g., tried to touch it, push it away). Citing reasons such as fearing “others would think [they were] crazy,” three (23i %) had never told anyone of these experiences before this study. Of the 10 (76.9%) who had told someone, five had told their doctors.

DISCUSSION The occurrence of complex visual hallucinations patients with age-related macular degeneration uncommon, and a prevalence of 13% was found

Am

J

Psychiatry

I 49:1

2, December

in is not in this

1992

HOLROYD,

consecutive group of patients. know as some patients will not their doctors, unless asked. Many lief

at knowing

that

others

had

This is important to tell anyone, including patients expressed rethis

experience

and

that

doctors were trying to study this phenomenon. The nesults of this study might reassure patients and teach physicians that having visual hallucinations with agerelated macular degeneration is not associated with depression, other primary psychiatric disorder, or abnonmat personality. Given that neurologic diseases such as epilepsy, dementia, and Parkinson’s disease are associated with visual

hallucinations,

it was

interesting

that

these

dison-

dens were not found among our hallucinators. Similanly, alcohol and drug use, number of medications, and number of medical disorders were not associated with the hallucinations. This suggests that these variables were not the cause of visual hallucinations in patients who happened to also have age-related macular degeneration. Also, factors suggested by previous studies as associated

with

hallucinations,

such

as

education,

de-

pression, and personality traits (especially score on the Eysenck Personality Questionnaire neuroticism scale), were not supported in this study. No support was found for patients’ “hallucinating at will.” The close association noted by the hallucinators between a sudden change in vision (due to laser treatment, hemorrhage, etc.) and the onset of the hallucinations also suggests that the visual hallucinations were related to the visual disorder. Further, the facts that bilateral visual

acuity

of 20/60

ciated

with

hallucinations

or

worse and

was that

significantly the

asso-

hallucinators

had somewhat worse vision in the best eye suggest a relationship between the severity of eye disease and the phenomenon of hallucinations. However, since only 13% ofthe patients with age-related maculan degeneration experienced visual hallucinations and since no risk factor distinguished 100% between the hallucinators and the nonhallucinators, the variables found to be significantly different between the hallucinatons and cornpanison subjects might best be considered predisposing factors. The theory of sensory deprivation is supported by the findings of bilateral as opposed to unilateral disease and more severe visual impairment among the subjects with hallucinations. Also, half of the hallucinations were timited to the area of visual field loss, i.e., the area of sensory deprivation. Living alone, although less cleanly related, might also be linked with less sensory stimulation. The nearly significant association between hearing loss and hallucinations also supports a sensory deprivation model, as one more route of sensory input is reduced. Two risk factors identified here, lower cognition score and personal history of stroke, support the hypothesis that decreased cortical inhibition allows subcortical on adjacent cortical areas to “release” discharges, causing hallucinations. Our results also support previous studies linking cognitive deficits with hallucinations (26, 28, 29). Furthermore, cognitive deficits in Parkinson’s disorder patients have also been associated with

Am

J

Psychiatry

149:12,

December

1992

risk

of

hallucinations

RABINS,

(25).

Charles Bonnet syndrome subsequently developed question of whether visual with age-related macular factor for or, more likely, tia.

A follow-up

study

FINKELSTEIN,

A study

of

patients

(7) revealed that dementia, which hallucinations degeneration may an early symptom

of these

patients

ET AL.

may

with

two of six raises the in patients be a risk of demenanswer

this

question. The nearly significant association between olden age and hallucinations could also indicate that greater age-related cortical atrophy is a risk factor, but we have no data to support on refute this possibility. The work of Foerster (20), who produced complex visual hallucinations by stimulating the visual association cortex, makes visual association cortex area 19 a possible candidate for the brain region “releasing” visual hallucinations. Interestingly, an abnormally high numben of neurofibnillary tangles are found in the visual association cortex of patients with Alzheirner’s disease (39), a disease in which 10% of patients have visual hallucinations,

with

relative

sparing

of the

primary

vis-

ual cortex (40). An examination of phenomena in other visual disondens and over a broader age range is now underway. This

may

help

clarify

the

importance

factor, since all our patients also help clarify whether this visual

disorders

with

of

were over phenomenon

different

age

age

pathologies

as

a risk

55. It will is present in and

further

define other factors found in this study to be associated with hallucinations. To clarify whether cortical atrophy or cortical hypenexcitability is a risk factor, it would be helpful to study brain structure (with magnetic resonance imaging and computerized tomography) and function (with EEG, visual evoked potentials, single photon emission computed tomography, and positron emission tomography).

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Visual hallucinations in patients with macular degeneration.

This study was undertaken to determine the prevalence of visual hallucinations in patients with macular degeneration, describe such hallucinations phe...
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