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Show ORIGINAL CONTRIBUTION Visual Hallucinations During Prolonged Blindfolding in Sighted Subjects Lotfi B. Merabet, OD, PhD, Denise Maguire, BSc, Aisling Warde, BSc, Karin Alterescu, PhD, Robert Stickgold, PhD, andAlvaro Pascual- Leone, MD, PhD Abstract: The authors report the occurrence of visual hallucinations of varying complexity in 13 normal subjects after sudden, complete, and prolonged visual deprivation. The subjects were all healthy individuals with no history of cognitive dysfunction, psychosis, or ocular pathology. They wore a specially designed blindfold for a period of five consecutive days ( 96 hours) and were asked to record their daily experiences using a hand- held microcassette recorder. Ten ( 77%) of the subjects reported visual hallucinations, which were both simple ( bright spots of light) and complex ( faces, landscapes, ornate objects). The onset of hallucinations was generally after the first day of blindfolding. Subjects were insightful as to their unreal nature. These results indicate that rapid and complete visual deprivation is sufficient to induce visual hallucinations in normal subjects. ( JNeuro- Ophthalmol 2004; 24: 109- 113) Visual hallucinations arise under numerous conditions, such as psychiatric illness, sleep- wake transitional states, drug and medication use, and in various neurologic diseases ( 1,2). Furthermore, the deterioration of vision itself from pathology implicating the eyes or along the visual pathway can lead to visual hallucinations ( 1,2). Visual hallucinations can be generally characterized as simple or complex, formed or unformed. Simple ( or elementary) hallucinations often consist of spots of bright light generally referred to as phosphenes. In contrast, complex hallucinations consist of formed images such as faces, Laboratory for Magnetic Brain Stimulation, Department of Neurology, Beth Israel Deaconess Medical Center, Harvard Medical School, Boston, Massachusetts ( LBM, AW, KA, AP- L), and Laboratory of Neurophysiology, Department of Psychiatry, Harvard Medical School, Boston, Massachusetts ( DM, RS). Address correspondence to Alvaro Pascual- Leone, MD, PhD, Laboratory for Magnetic Brain Stimulation, Beth Israel Deaconess Medical Center, Harvard Medical School, 330 Brookline Ave., Kirstein Hall KS452, Boston, MA 02115. Supported by the National Eye Institute ( RO1EY12091), the National Institute of Mental Health ( MH- 13923, MH60734, and MH- 48832) and the General Clinical Research Center at Beth Israel Deaconess Medical Center ( NCRR MOl RR01032). people, ornate objects, or landscapes ( 2,3). In conjunction with an ongoing study investigating the effects of visual deprivation on short- term brain plasticity, we observed the occurrence of visual hallucinations after rapid, complete, and prolonged blindfolding in normally sighted individuals. METHODS Subjects The subjects of this report ( n = 13) were all part of a group ( n = 31) participating in a larger study. All experimental procedures were performed in accordance with the Declaration of Helsinki and were approved by the Beth- Israel Deaconess Medical Center Investigative Review Board and Harvard- Thorndike General Clinical Research Center. Subjects ( five male and eight female) were between the ages of 18 and 35 ( mean age, 25), medication- free, native English speakers without history of ocular, visual pathway, psychiatric, or neurologic disorder. All subjects had a normal neurologic and general physical examination performed by a physician. Subjects were randomized to one of four groups, two of which were blindfolded ( the 13 subjects reported here). Within this blindfolded cohort, one group was implicated in a tactile stimulation protocol ( n = 7) while the other received no tactile stimulation ( n = 6). Tactile stimulation included eight hours per day of activities stimulating the pads of their fingers. This involved four hours a day of intensive Braille instruction ( supervised by a professional teacher from the Caroll School for the Blind, Newton, MA), two hours engaged in non- Braille tactile stimulation ( tactile games, puzzles, clay modeling), and two hours spent in activities of daily living ( ADL), including getting dressed, eating, walking around, and going to the gym. In accordance to our study protocol, all subjects were also involved in a serial functional magnetic resonance imaging ( fMRI) to study brain activation in response to tactile stimulation of the index finger. The remaining study subjects were randomized to two non- blindfolded control groups, one with tactile stimulation ( n = 9) and one without tactile stimulation ( n = 9). The present report focuses on the experiences of the 13 subjects in the two blindfolded experimental groups. J Neuro- Ophthalmol, Vol. 24, No. 2, 2004 109 JNeuro- Ophthalmol, Vol. 24, No. 2, 2004 Merabet et al Procedure Subjects in the experimental groups were blindfolded for a period of 96 hours from 9 am on the first day until 4 pm on the fifth day. A specially designed blindfold was worn that prevented all light perception. It was held in place by a Velcro strap and further secured by Ace bandages. The blindfold permitted full motion of the eyes as well as opening and closing of eyelids. Potential tampering with the blindfold by the subjects was controlled with the use of a piece of photographic paper attached to the inside of the blindfold. All subjects were issued a hand- held microcas-sette recorder with automatic date/ time stamping and directed to report their thoughts, feelings, and perceptions related to the experiment throughout the day as frequently as they desired. Each subject was also asked to report on the content of dreams every morning on awakening. The subjects' reports were then transcribed independently by two investigators and carefully compared and reviewed for overlapping content. The subjects were not prompted to describe their experiences and were unaware of the purpose of recording them. RESULTS Ten ( 77%) of the 13 blindfolded subjects reported visual hallucinations that varied in onset, duration, and content. Generally, the visual hallucinations began between the first day and second day of blindfolding and were of sudden onset, occurred while the patient was alert ( regardless of whether the eyes were open or not), and vanished spontaneously. No subjects reported the ability to control volition-ally the appearance or disappearance of the hallucinations. In a few cases, inciting factors were apparent, such as watching television or listening to music. Other sensory experiences, such as auditory or somatosensory sensations, were not reported. In six of the 10 subjects who reported seeing hallucinations, the hallucinations were either simple ( flashing lights or phosphenes) or complex ( faces, hands, landscapes, ornate objects). In two of these six subjects, simple visual hallucinations evolved to more complex sensations as the blindfold period progressed. One subject reported seeing only simple visual hallucinations (" flashing lights") and three subjects reported seeing only complex visual hallucinations. In some instances, the hallucinations were context appropriate, reflecting the subject's psychologic state and changing in content and frequency as a function of the subject's daily activities. For example, hallucinatory experiences were often reported when subjects were engaged in activities such as walking to and from testing sites or using the restroom. Interestingly, the hallucinatory experiences were never reported during periods of tactile stimulation such as Braille reading instruction or during fMRI sessions. According to the subjects' own accounts, the hallucinations were always novel and had no relation to past experiences. All subjects who experienced hallucinations did so during the blindfolded period. With one exception, the hallucinations ceased after the blindfold was removed on the fifth day. In one subject, they continued for a few hours after the blindfold was removed. Generally, subjects were initially disoriented after blindfold removal, reporting of transitory dizziness, and difficulty focusing. Vision returned to normal approximately 30 to 60 minutes after sight restoration. There were no apparent differences in the incidence or characteristics of the hallucinations between tactile- stimulated and non- stimulated blindfolded subjects. None of the subjects ( n = 18) who were randomized to the control non- blindfolded groups experienced hallucinations. Here is a synopsis of the reported hallucinations: Subject 1, a 29- year- old woman, experienced a single hallucination 12 hours after blindfolding. It occurred while she was standing in front of what she knew to be a mirror and was of a green face with big eyes. The subject became very frightened by the experience. Subject 2, a 24- year- old man, experienced a broader range of images commencing a few hours after blindfolding and persisting for several hours after the blindfold was removed. Hallucinations at first included flashing lights, mirrors, lamps, trees, and full landscapes. At the conclusion of the second day of blindfolding, the images became more complex and he reported difficulty walking because of the " obstacles" he " saw." For example, while taking a walk outside, he reported seeing " a ground of dirt rows, mounds of pebbles, or small stones that were running from upper left to lower right field of view and between them was running a small stream of water." Over time, the images became a constant presence, and by the end of the study, he was reporting " ornate buildings of white- green marble" and " cartoon- like figures." Subject 3, a 24- year- old woman, reported one hallucinatory event. She had been napping while waiting for her sister to arrive for a visit. When her sister walked into the room, she opened her eyes and noticed a " splotch of light" in front of her eyes; " it was in the exact form of Elvis Presley.. .1 pictured Elvis toward the center, maybe a little off to the left side.. . aligned with the nose a little bit more to the left and facing my left side... it was real distinct for some reason." Subject 4, a 23- year- old man, reported seeing images as well as flashes of light within a few hours of being blindfolded. He saw outlines of puzzle pieces that, while moving, " warped into other amorphous shapes" and transformed in color from white to orange to red. He saw these perceptions " when I think about my sense of sight." On day four, he reported seeing a triangle with bold dots at each vertex of the triangle and " a large X with a light shining underneath 110 © 2004 Lippincott Williams & Wilkins Visual Hallucinations JNeuro- Ophthalmol, Vol. 24, No. 2, 2004 it." Immediately before the report, the subject was engaged in a tactile stimulation task in which he was asked to discriminate five raised dots arranged in the form of an " X" on a domino piece. Subject 5, a 29- year- old woman, reported seeing circles of light within 24 hours of blindfolding and again during the course of the week. On the second day, she reported, " I have the sensation that I can see my hands and my arms moving when I move them and leaving an illuminated trail." She had this sensation as she reached to grab an object. When she realized that she could " see" her hands, she placed them in front of her face and observed their movement for several minutes. She also reported seeing images of bright half moons that moved in space. Subject 6, a 34- year- old man, reported numerous instances of hallucinations that occurred when he would listen to the Mozart Requiem. In the first report, while listening to the music, he saw " the outline of a skull.. i t actually seemed to be turning and looking at me... sort of facing head- down and then face- down and then turning faceup. . . it seemed like it appeared in front of my eye." On a second occasion, again while listening to the Requiem, he reported another instance of hallucinosis: " it was kind of a little scary and I also saw the outline of someone wearing some sort of ceremonial mask.. i t was fairly detailed. I could tell that there was some sort of headdress.. . and the person seemed to have their face upturned and their mouth open. It was kind of brief- maybe two to three seconds or so." On a third occasion, he reported, " I was listening to the Requiem again and I had an image of an older woman with a very wrinkled face. Her look was somewhat menacing, but what was interesting ( she had white hair)... was that she was facing me. She seemed to be sitting in an airplane seat. But around her eyes she had a red eye shield similar to those that are used by people to keep out UV rays. And then the scene changed from a woman's face to a mouse- like face, not necessarily smaller but with the features of a mouse, the eyes and the nose and the mouth." In addition to the hallucinations that occurred while listening to the Requiem, he also experienced several " strobe- like images," which began on day four and reappeared several times on day five before the blindfold was removed. On one occasion he reported, " I saw on the bridge of my nose there was this strobe- like image going up my nose bridge and disappearing and coming back." Another time he reported, " I saw a barrage of these images- these strobe- like images. They lasted for 10 to 15 seconds. Earlier in the afternoon, I saw the outline of my eyes. That was fairly clear; they were fairly oval." Subject 7, a 20- ear old woman, reported simple visual hallucinations occurring on the fourth day of blindfolding. While listening to television, she would report the presence of flashing lights " as if there were two strobe lights each at the extreme of my peripheral vision. So I can just see the flashing at the corners of my eye. It is really rather annoying, that is all." She did not report any well formed visual hallucinations throughout the blindfolding period. But by the second day, she reported that her imagination skills " were vastly improving" and that she was able " to feel where things are." Subject 8, a 20- year- old woman, experienced an array of hallucinations similar to those of # 2. The hallucinations appeared suddenly 12 hours after blindfolding and evolved into a series of different images, much as in a dream. She reported seeing a butterfly that became a sunset, an otter, and finally a flower. She also reported seeing cities, skies, kaleidoscopes, lions, and sunsets so bright she could " barely look at them." " If there is a sunset or a sunrise I couldn't look at the sun... because it was too bright... it would seem like all of this light would just collect where the sun was and I just could not look there." She stressed the intensity of the hallucinations, commenting " sometimes they were much prettier, I think, than anything I have ever seen.. .1 really wish I could paint" She also reported that the hallucinated objects were always " in motion," stating " sometimes they would move fast and sometimes slower". Subject 9, a 27- year- old man, reported seeing flashes of light within 24 hours after blindfolding. Later in the week, he reported seeing images of resplendent peacock feathers and buildings. Subject 10, a 21- year- old woman, reported a single intrusive hallucination a few hours after blindfolding. She reported this image as she was eating her first meal. As she sat facing her food tray, she reached over to another table and picked up a water pitcher so she could pour herself a glass of water. She reported that as the pitcher came into what would normally have been her field of view, " I felt like I was seeing the pitcher while I was pouring the water." DISCUSSION Our study demonstrates that visual hallucinations of simple and complex types are common after sudden, complete, and prolonged visual deprivation in normal subjects. In agreement with previous reports, the hallucinations were vivid, well- defined, and consisted of simple and complex types ( 4- 7). Subjects generally described their experiences as pleasant and amusing; in only two cases were the experiences fearful or intrusive to the point of interfering with the subjects' ability to navigate within the environment. Previous studies have reported results similar to ours. Subjects wearing opaque eye goggles put in darkened rooms experienced what authors termed " meaningful" hallucinations, including images of people, objects, and scenes ( 8,9). Linn et al ( 10) reported that after a three- day period of postoperative eye- patching, 18 of 21 patients aged between 45 and 85 showed " noticeable alterations in behavior," including psychomotor disturbances, anxiety, and delusions. Ill JNeuro- Ophthalmol, Vol. 24, No. 2, 2004 Merabet et al Visual hallucinations, present in three of 21 patients, were often of other people. The hallucinations generally began within the second day of bandaging, progressed in severity on succeeding days, and disappeared once the bandages were removed. Ziskind et al ( 11) folio wed- up 98 patients aged between eight and 88 years old admitted for cataract surgery ( 88 patients patched for 24 hours) or retinal detachment ( 10 patients patched for seven to 14 days preopera-tively and 14 to 30 days postoperatively). These patients were confined to bed and denied visitation for two days. Visual hallucinations occurred in all retinal detachment patients and in 30% of cataract patients. The greater prevalence of symptoms in the retinal detachment group was attributed to the longer period of patching. A potential drawback of these latter two studies is that patients were not controlled for use of medication or psychiatric disturbances. The relatively high prevalence of hallucinations in our study may be explained by a number of reasons. First, our subjects were required to keep a microcassette recorder at hand at all times and instructed to report any unusual occurrences. Secondly, both eyes were suddenly and completely occluded for a prolonged period. Visual hallucinations have been reported to occur more frequently in acute, higher degrees of visual impairment and with bilateral rather than monocular blindness ( 12- 14). The underlying neurophysiology of visual hallucinations remains a matter of debate. However, two general mechanisms have emerged. An " irritative" process may produce excitatory discharges originating within neighboring associative cortical areas ( 7,15). Alternatively, hallucinations may arise out of a " release" mechanism because of a lack of visual input to the brain. According to this hypothesis, visual deprivation interferes with normal inhibitory circuitry, resulting in inappropriate patterns of cortical excitation and abnormal central processing ( 2,7). Blindfolding may represent a means to allow investigation of the effects of perturbing this normal inhibitory control. Activity within the visual cortex is presumed to be the product of incoming sensory signals, context- appropriate associations, and expectations that arise from multimodal cortices that feed back to unimodal areas ( 16). Feedback connections from extrastriate cortical areas appear critical for visual awareness ( 17,18). When these dominating feedback inputs into the visual cortex are visual, visual hallucinations may occur. Other " phantom sensations," such as auditory sensations in the recently deaf or phantom tactile sensations in amputees, may represent similar phenomena in different sensory domains ( 6). Several of our subjects reported hallucinations that were context- appropriate. Examples are subject l's face in the mirror and # 2' s pebbled pathways. Subject 3 " saw" Elvis when another person entered the room. Subject 5 " saw" her hands and arms when she reached to grab an object, and # 10 " saw" the water pitcher when she reached over for it and it came into what would normally have been her field of view. These context- appropriate experiences may be the result of feedback projections arising from other associative cortical areas capable of " organizing" diffuse and random input and generating a structured percept. The notion that visual hallucinations represent a condition in which a cessation of sensory inputs leads to an alteration in cortical processing has received experimental support. In the case of complete visual deprivation, Boroojerdi et al ( 19) have reported an increase in cortical excitability in the visual cortex as demonstrated with fMRI and transcranial magnetic stimulation. The effects were evident within minutes of visual deprivation. Howard et al ( 20) used fMRI during visual hallucinatory events and found that the occipital cortex manifests reduced responsiveness to exogenous stimulation, suggesting that this may underlie the disinhibition ( or " release") of endogenous visual memories whose content emerges into consciousness as hallucinations. Santhouse et al ( 7) have used fMRI and cross- correlated time series with hallucinatory events to identify associated cerebral activity during hallucinations. These authors argue that visual hallucinations are related to phasic increases in activity within visual cortical areas. Similarity between functional specializations of the activated cortical region and the content of the hallucination suggests that pathologic increases in activity within a specific component of the visual pathway lead to predictable visual hallucinatory content. For example, activation of the fusiform face area would correlate with perception of faces. Their findings also suggest that previous visual experience is an important contributor to the nature of visual hallucinations. This statement is supported by the fact that visual hallucinations have not been reported in the congenitally blind and only in the context of visual impairment ( 21). The term " Charles Bonnet Syndrome" ( CBS) has been used to describe patients with visual hallucinations with preserved intellectual function ( 4,22). Although the formal definition of the syndrome remains a matter of debate, most investigators agree that reduced or absent visual stimulation plays an integral part in the syndrome's cause. The most common associated pathology is age- related macular degeneration ( 2). The visual hallucinations described in this study fit with the current diagnostic criteria for CBS. First, the hallucinations were often vivid and complex, not associated with hallucinations in other sensory modalities, and subjects were insightful as to their unreality ( 23,24). Second, the hallucinations were the direct result of compromised visual input, a common cause for CBS ( 14,22,25). Our subjects reported restful, undisturbed sleep and stated that being blindfolded had not affected their dreams. 112 © 2004 Lippincott Williams & Wilkins Visual Hallucinations JNeuro- Ophthalmol, Vol. 24, No. 2, 2004 Given that five of our subjects reported formed hallucinations on the day of blindfolding, one might predict that nocturnal hallucinations would be very common during subsequent sleep. Indeed, the hypnagogic hallucinations seen at sleep onset bear strong similarities to the images reported here ( 26,27). The reported hallucinations bear some resemblance to objects that appear in dreams, particularly with regard to their unusual content. However, visual images reported during the study tended to be static and often context- appropriate, as opposed to the more complex and narrative visual hallucinations reported while dreaming ( 27). 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