Journal of Neuro-Ophthalmology, September 1990, Volume 10, Issue 3

The Charles Bonnet syndrome. Visual perceptive dysfunction in sensory deprivation.

We present a series of four patients with the Charles Bonnet syndrome, which is characterized by recurrent vivid visual hallucinations in the presence of normal cognition and insight. It usually occurs in elderly people with ophthalmic pathology causing severe visual sensory deprivation. Our experience suggests that this syndrome is frequently overlooked or misdiagnosed by both ophthalmologists and psychiatrists. To our knowledge this is only the second series of cases of the syndrome in the American literature.

JOUTllQI of Clinical Neuro- ophthalmology 10( 3): 215- 218, 1990. The Charles Bonnet Syndrome Visual Perceptive Dysfunction in Sensory Deprivation R. Michael Siatkowski, M. D., Ben Zimmer, M. D., and Paul R. Rosenberg, M. D. « ;> 1990 Raven Press, Ltd., New York We present a series of four patients with the Charles Bonnet syndrome, which is characterized by recurrent vivid visual hallucinations in the presence of normal cognition and insight. It usually occurs in elderly people with ophthalmic pathology causing severe visual sen­sory deprivation. Our experience suggests that this syn­drome is frequently overlooked or misdiagnosed by both ophthalmologists and psychiatrists. To our knowledge this is only the second series of cases of the syndrome in the American literature. Key Words: Charles Bonnet syndrome- Release phe­nomenon- Visual hallucinations. From the Department of Ophthalmology, St. Francis Medical Center ( R. M. S., P. RR), Pittsburgh, Pennsylvania, and the ~ e­gheny Neuropsychiatric Institute ( B. Z.), Oakdale, Pennsylvarua. Address correspondence and reprint requests to Dr. Paul R Rosenberg at the Ophthalmology Residency Training ~ rogram, St. Francis Medical Center, 4401 Penn Avenue, SUite 1060, Pittsburgh, PA 15224, U. S. A. 215 The entity which Morsier termed the Charles Bonnet syndrome in 1936 was first described by the Swiss naturalist Charles Bonnet in 1760 ( 1). Bonnet reported the case of his 89- year- old grand­father who had severe visual loss due to advanced cataracts, and visions of figures, people, and ani­mals ( 2). Apart from the ocular problems, the pa­tient was in good physical and mental health. We present four similar patients with ocular pathology and visual hallucinations. CASE REPORTS Case One An 87- year- old retired male truck driver had age related macular degeneration and difficulty read­ing. His visual acuity was hand motions in the right eye and 20/ 100 in the left eye. Examination of the fundus revealed an old macular scar in the right eye and an active subretinal neovascular membrane in an untreatable location in the left eye. The patient noted that over the last several weeks he had been seeing vivid and sharply col­ored images of oil wells, bouquets of flowers, and road maps. These images lasted for approximately 5 min each. They disappeared with eyelid closure, and occurred more frequently at night. The patient was never frightened by these images, but rather " amused and entertained." He clearly stated he realized that they were not actually present. Other than the visual hallucinations, the psychiatric and neurologic evaluation was normal. He was taking Isordil, Tenormin, and aspirin. Magnetic reso­nance imaging ( MRI) of the brain revealed a few scattered ischemic infarcts of the frontal and pari­etal lobes. No temporal or occipital lesions were noted. The patient was placed on a trial of Haldol with resolution of the visual hallucinations. When 216 R. M. SIATKOWSKI ET AI. Haldol was discontinued, the visual hallucinations reoccurred. als of antipsychotic medications were u in ceasing the visual hallucinations. Case Two An 84- year- old white woman with a history of poor vision due to amblyopia in the left eye pre­sented with a complaint of decreased vision and flashing lights in the right eye. Visual acuity was 8/ 200 in the right eye and count fingers at 3 ft in the left eye. There was a 55 prism diopter left exotro­pia. Examination of the right eye revealed an at­tached retina with no areas of traction, and a large, active subfoveal neovascular membrane. The left eye had a dense cataract. In a detailed interview, the patient described a two- month period of vi­sions of " vivid, moving, red and blue streaks" cre­ating geometric patterns " like in a kaleidoscope." Later, she began having visions of people sitting and sewing garments. The visions were more prevalent at night and came without warning. The images were " crystal clear." The patient never heard voices associated with the visions. She stated that she always knew that they were not actually present and that they never really both­ered her. Other than the above visions, the psy­chiatric and neurologic evaluation was normal. List of medications was unavailable. MRI of the brain revealed no mass lesions or areas of isch­emia. The visual hallucinations persisted until her death 1 year later. Case Three A 78- year- old white man had a history of mac­ular degeneration and complained of bothersome visual hallucinations of several months duration. Visual acuities were 2/ 200 in both eyes. Retinal ex­amination revealed bilateral disciform scars. The patient stated that every night he had visions of workers remodeling his house. He observed them moving furniture, painting the walls, and recon­structing a fireplace. The images were quite clear and he could see them " over my regular blurry vision." There were no associated voices, and the patient was aware that the people were not truly present. He felt no particular emotional reaction to them but stated that they made it difficult to con­centrate on whatever he was doing. These visions were never present during daylight. Psychiatric and neurologic evaluation was normal, other than for the visual hallucinations. He was on no medi­cations. Computed tomography of the brain re­vealed mild, diffuse age- related cortical atrophy. There were no inf,"' ct~ O[ mass lesions. Several tri- Case Four A 39- year- old black man with a history of prolif­erative diabetic retinopathy complained of visual hallucinations of 2 months duration. Visual acu­ities were count fingers at 5 ft and hand motions in the right and left eyes, respectively. Fundus exam­ination revealed severe proliferative diabetic reti­nopathy in both eyes with bilateral traction retinal detachments that included the macula. His visions occurred only at night, or while wearing sun glasses, and they lasted 10 min to several hours. The patient saw " vivid white clouds over snow­capped mountains." He also described " clear brick buildings" which " changed from one psychedelic color to another." The patient was always able to distinguish these appearances from his usual blurred vision. He denied any associated fear, but rather described the visions as " annoying." The patient reported no previous personal or family psychiatric history and he refused psychiatric eval­uation. Neurologic evaluation was unremarkable. The patient was on insulin for his diabetic control. Subsequently, the patient underwent pars plana vitrectomy, membrane peeling, and air- fluid ex­change in the right eye. The macula was reat­tached and vision improved to 20/ 200. The patient reported concomitant disappearance of his visual hallucinations. DISCUSSION The Charles Bonnet syndrome consists of visual hallucinatory phenomena in the presence of oph­thalmic pathology. The hallucinations are charac­terized by the following criteria ( 3). They occur in a state of clear consciousness, and are not accom­panied by any other disorders of sensory- percep­tion; they coexist with normal visual perceptions and the individual retains the ability to differenti­ate them from the latter; the visions appear sud­denly and unexpectedly, and tend to disappear on closing the eyes; and they are not accompanied by any particular emotional reaction. The content of the visual hallucinations is well organized and defined, as opposed to the normally blurred perception of real objects in patients with ocular pathology. Their detail and dynamic char­acter serves to differentiate them from the points or amorphous patterns that comprise the so- called " photisms" that commonly occur in patients with ocular pathology ( 4). The visions always Occur in I Clin r: \ I" 1. 1~ 90 CHARLES BONNET SYNDROME 217 external space and the patients show insight that the perceived objects are unreal. Concomitant hal­lucinations of other sensory modalities or impaired cognition or insight will, by definition, exclude the diagnosis of Charles Bonnet syndrome. The cause of visual hallucinations in the pres­ence of decreased visual acuity is unknown, but it is likely that sensory deprivation is the initiating factor. Two similar phenomena have been well de­scribed. The first is visual hallucinations confined to a specific area of field defect ( 5). The other is phantom pain after a limb amputation, which is thought to be a hallucinatory phenomenon of the thalamus ( 6). In both phenomena the common de­nominator is the absence of afferent sensory input to the part of the brain concerned. It seems likely that a similar mechanism operates in the Charles Bonnet syndrome. In support of this, Heron et al. have shown that after prolonged visual depriva­tion followed by return to a normal environment, humans experience distortions in object size, shape, and color, as well as apparent movement of stationary objects ( 7). It is unclear whether the hallucinations are a re­sult of so- called " release phenomena" or are sec­ondary to local cortical irritation. Release phenom­ena result from the brain's constant bombardment with stimuli, most of which are excluded from con­sciousness by customary sensory input. Removal of sensory input ( by lesions of the visual system in the Charles Bonnet syndrome) " releases" these hallucinations ( 8). Cogan has postulated that these hallucinations tend to be more continuous and nonstereotypic than those of the irritative variety ( 9). In addition, since the images vary from un­formed phosphenes to sharply outlined objects, release phenomena are not useful in localizing the area of cortex responsible ( 10,11). Release phenomena also tend to disappear with closure of the eyes or altering of the sensory input, i. e., by directed gaze. Coexisting central nervous system pathology, such as infarcts or cortical atro­phy, may further lower the threshold for occur­rence of release phenomena. Antipsychotics may be helpful in these cases by virtue of their central dopaminergic blocking activity. Most authors feel that release phenomena are the mechanisms at play in the Charles Bonnet syndrome, and they cite a normal visual evoked potential and electro­encephalogram in these patients as supporting ev­idence ( 12). However, the fact that the hallucina­tions in Charles Bonnet syndrome can be more of­ten episodic than continuous has led some to believe that cortical irritation plays a role. Rosen­baum et al. postulate that cells of the visual cortex are more likely to discharge spontaneously when normal afferent input is reduced. At least one case has been reported in which anticonvulsants abol­ished the hallucinations in a patient with the syn­drome ( 13). Perhaps both mechanisms playa role in the pathogensis of the hallucinatory phenom­ena. The exact prevalence of the Charles Bonnet syn­drome is unknown. Berrios and Brook diagnosed it in 2/ 150 ( 1.3%) patients referred to a psychiatrist for visual hallicinations ( 14). Nortin- Willison and Munir made the diagnosis in 8/ 434 ( 1.8%) patients referred to a psychogeriatric unit for routine eval­uation. The mean age of all patients was greater than 65, and it was more common in women than men ( 15). It has been described in association with bereavement and with auditory hallucinations in a patient with impaired hearing ( 16,17). ( These au­ditory hallucinations in patients with decreased hearing are probably analgous to the visual hallu­cinations in the Charles Bonnet syndrome.) We are concerned that the Charles Bonnet syn­drome may often be overlooked or misdiagnosed. Reports in the literature describing conditions that are most likely the Charles Bonnet syndrome have been labeled intracranial complications of temporal arteritis, occipital lobe seizures ( 18), or atheroscle­rotic cerebrovascular disease ( 19). In addition, pa­tients may also be reluctant to recount a history of hallucinations, even on persistent questioning, lest they be considered to have psychiatric disease. The prognosis in the Charles Bonnet syndrome varies with the nature of the visual dysfunction. It is possible to " cure" some patients with the Charles Bonnet syndrome by restoring or improv­ing normal sensory input, e. g., cataract removal ( see case four). On the other hand, some patients may observe that the hallucinations will cease as their eye disease progresses to total blindness ( 13). Some investigators have reported the efficacy of anticonvulsants such as carbamazepine or neuro­leptics for this condition ( see case one), but there are no proven trials of such therapy. Nevertheless, for the vast majority of cases, treatment will con­sist of physician recognition and expression of sen­sitivity, and reassurance and education of the pa­tient. In summary, the Charles Bonnet syndrome is a clinical condition occurring in elderly patients with peripheral ocular pathology and preserved intel­lect and cognition. It is characterized by vivid, elaborate, and dynamic recurrent visual hallucina­tory phenomena of a neutral nature. Neurologic, psychiatric, and neuroimaging examinations fail to reveal any focus of pathology responsible for these , Clin Neuro- ophthalmol, Vol. 10, No. 3, 1990 218 R. M. SIATKOWSKl ET AI. hallucinations, which are most likely the result of ~ ortical release phenomena from impaired sensory mput. The incidence of the Charles Bonnet syndrome is surely higher than currently diagnosed due to lack of knowledge of the syndrome, and patient reluctance to recount a history of visual hallucina­tions. The Charles Bonnet syndrome may resolve with either restoration or loss of normal visual function, or with anticonvulsant or neuroleptic therapy. It is a condition that requires compassion­ate reassurance of the patient. REFERENCES 1. Berrice GE, Brook P. The Charles Bonnet syndrome and the problem of visual perceptive disorders in the elderly. Age Ageing 1982; 11: 17- 23. 2. Olbrich HM, Engelmeier MP, Pauleikhoff D, Waubke T. Visual hallucinations in ophthalmology. Graefes Arch Clin Exp Ophthalmol 1987; 225: 217- 20. 3. Damas- Mora J, Skelton- Robinson M, Jenner FA. The Charles Bonnet syndrome in perspective. Psychol Med 1982; 12: 251-- 61. 4. White NJ. Complex visual hallucinations in partial blind­ness due to eye disease. Br I Psychiatry 1980; 136: 284-- 6. 5. Winberger L, Grant FC. 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