by Oliver Sacks
Typically the hallucinations would appear suddenly and spontaneously, then disappear just as suddenly after seconds or minutes—although in one subject, hallucination became almost continuous by the third day. The subjects reported a range from simple hallucinations (flashing lights, phosphenes, geometrical patterns) to complex ones (figures, faces, hands, animals, buildings, and landscapes). In general, the hallucinations appeared full-fledged, without warning—they never seemed to be built up slowly, piecemeal, like voluntary imagery or recall. For the most part, the hallucinations aroused little emotion and were regarded as “amusing.” Two subjects had hallucinations which correlated with their own movements and actions: “I have the sensation that I can see my hands and my arms moving when I move them and leaving an illuminated trail,” said one subject. “I felt like I was seeing the pitcher while I was pouring the water,” said another.
Several subjects spoke of the brilliance and colors of their hallucinations; one described “resplendent peacock feathers and buildings.” Another saw sunsets almost too bright to bear and luminous landscapes of extraordinary beauty, “much prettier, I think, than anything I have ever seen. I really wish I could paint.”
Several mentioned spontaneous changes in their hallucinations; for one subject, a butterfly became a sunset, which changed to an otter and, finally, a flower. None of the subjects had any voluntary control over their hallucinations, which seemed to have “a mind” or “a will” of their own.
No hallucinations were experienced when subjects were engaged in challenging sensory activity of another mode, such as listening to television or music, talking, or even attempting to learn Braille. (The study was concerned not only with hallucinations but with the power of blindfolding to improve and heighten tactile skills and the ability to conceive of space and the world around one in nonvisual terms.)
Merabet et al. felt that the hallucinations reported by their subjects were entirely comparable with those experienced by patients with Charles Bonnet syndrome, and their results suggested to them that visual deprivation alone could be a sufficient cause for CBS.2
But what exactly is going on in the brains of such experimental subjects—or in the brains of pilots who crash in cloudless blue skies, or truckers who see phantoms on an empty road, or prisoners watching their enforced “cinema” in darkness?
With the advent of functional brain imaging in the 1990s it became possible to visualize, at least in gross terms, how the brain might respond to sensory deprivation—and, if one was lucky (hallucinations are notoriously fickle, and the inside of an fMRI machine is not an ideal place for delicate sensory experiences), one might even catch the neural correlates of a fugitive hallucination. One such study, by Babak Boroojerdi and his colleagues, showed an increase in the excitability of the visual cortex when subjects were visually deprived, a change that occurred within minutes. Another group of researchers, in the neuroscience lab led by Wolf Singer, studied a single subject, a visual artist with excellent powers of visual imagery (an article on this by Sireteanu et al. was published in 2008). The subject was blindfolded for twenty-two days and spent several sessions in an fMRI machine, where she was able to indicate the exact times her hallucinations appeared and disappeared. The fMRI showed activations in her visual system, both in the occipital cortex and in the inferotemporal cortex, in precise coincidence with her hallucinations. (When, by contrast, she was asked to recall or imagine the hallucinations using her powers of visual imagery, there was, additionally, a good deal of activation in the executive areas of the brain, in the prefrontal cortex—areas that had been relatively inactive when she was merely hallucinating.) This made it clear that, at a physiological level, visual imagery differs radically from visual hallucination. Unlike the top-down process of voluntary visual imagery, hallucination is the result of a direct, bottom-up activation of regions in the ventral visual pathway, regions rendered hyperexcitable by a lack of normal sensory input.
The deafferentation tanks used in the 1960s produced not only visual deprivation but every other sort of deprivation: of hearing, touch, proprioception, movement, and vestibular sensation, as well as, to varying degrees, deprivation of sleep and social contact—any of which may in themselves lead to hallucinations.
Hallucinations engendered by immobility, whether from motor system disease or external constraints, were frequently seen when polio was rampant. The worst afflicted, unable even to breathe by themselves, lay motionless in coffinlike “iron lungs” and would often hallucinate, as Herbert Leiderman and his colleagues described in a 1958 article. The immobility produced by other paralyzing diseases—or even splints and casts for broken bones—may likewise provoke hallucinations. Most commonly these are corporeal hallucinations, in which limbs may seem to be absent, distorted, misaligned, or multiplied; but voices, visual hallucinations, and even full-blown psychoses have been reported, too. I saw this especially with my postencephalitic patients, many of whom were, in effect, enclosed in immoveable parkinsonism and catatonia.
Sleep deprivation beyond a few days leads to hallucination, and so may dream deprivation, even with otherwise normal sleep. When this is combined with exhaustion or extreme physical stress, it can be an even more potent source of hallucinations. Ray P., a triathlete, described one example:
Once, I was competing in the Ironman Triathlon in Hawaii. I was not having a good race, I was overheated and dehydrated—miserable. Three miles into the marathon portion of the race, I saw my wife and my mom standing on the side of the road. I ran over to them to say I would be late to the finish line, but when I reached them and began telling my tale of woe, two complete strangers who did not even remotely resemble my wife and mother looked back at me.
The Hawaiian Ironman Triathlon, with its extreme temperatures and long hours of monotony under grueling conditions, can provide an athlete with a fertile venue for hallucination, much the same as the vision quest rites of passage of Native Americans. I have seen Madame Pele, the Hawaiian Volcano and Fire Goddess, at least once out there in the lava fields.
Michael Shermer has spent much of his life debunking the paranormal; he is a historian of science and the director of the Skeptics Society. In his book The Believing Brain, he provides other examples of hallucinations in marathon athletes, like those of the mushers competing in the Iditarod dogsled race:
Mushers go for 9–14 days on minimum sleep, are alone except for their dogs, rarely see other competitors, and hallucinate horses, trains, UFOs, invisible airplanes, orchestras, strange animals, voices without people, and occasionally phantom people on the side of the trail or imaginary friends.… A musher named Joe Garnie became convinced that a man was riding in his sled bag, so he politely asked the man to leave, but when he didn’t move Garnie tapped him on the shoulder and insisted he depart his sled, and when the stranger refused Garnie swatted him.
Shermer, an endurance athlete himself, had an uncanny experience while competing in a grueling bike marathon, which he later described in his Scientific American column:
In the wee hours of the morning of August 8, 1983, while I was traveling along a lonely rural highway approaching Haigler, Neb., a large craft with bright lights overtook me and forced me to the side of the road. Alien beings exited the craft and abducted me for 90 minutes, after which time I found myself back on the road with no memory of what transpired inside the ship.… My abduction experience was triggered by sleep deprivation and physical exhaustion. I had just ridden a bicycle 83 straight hours and 1,259 miles in the opening days of the … transcontinental Race Across America. I was sleepily weaving down the road when my support motor home flashed its high beams and pulled alongside, and my crew entreated me to take a sleep break. At that moment a distant memory of the 1960s television series “The Invaders” was inculcated into my waking dream. In the series, alien beings were taking over the earth by replicating actual people but, inexplicably, retained a stiff little finger. Suddenly the members of my support crew were transmogrified into aliens. I sta
red intensely at their fingers and grilled them on both technical and personal matters.
After a nap, Shermer recognized this as a hallucination, but at the time it seemed completely real.
1. While the romantic use of sensory deprivation, as that of vision-producing drugs, has diminished since the 1960s, its political use is still horrifyingly common in the treatment of prisoners. In a 1984 paper on “hostage hallucinations,” Ronald K. Siegel pointed out that such hallucinations can be magnified sometimes to madness, especially when combined with social isolation, sleep deprivation, hunger, thirst, torture, or the threat of death.
2. There may be severe visual impairment or complete blindness without a hint of CBS, and this might seem to imply that visual deprivation alone is not a sufficient cause for it. But we are still ignorant as to why some people with visual problems get CBS and others do not.
3
A Few Nanograms of Wine: Hallucinatory Smells
The ability to imagine smells, in normal circumstances, is not that common—most people cannot imagine smells with any vividness, even though they may be very good at imagining sights or sounds. It is an uncommon gift, as Gordon C. wrote to me in 2011:
Smelling objects that are not visible seems to have been a part of my life for as long as I can remember.… If, for instance, I think for a few minutes about my long dead grandmother, I can almost immediately recall with near perfect sensory awareness the powder that she always used. If I’m writing to someone about lilacs, or any specific flowering plant, my olfactory senses produce that fragrance. This is not to say that merely writing the word “roses” produces the scent; I have to recall a specific instance connected with a rose, or whatever, in order to produce the effect. I always considered this ability to be quite natural, and it wasn’t until adolescence that I discovered that it was not normal for everyone. Now I consider it a wonderful gift of my specific brain.
Most of us, in contrast, have difficulty summoning smells to mind, even with strong suggestion. And it may be oddly difficult to know whether a smell is real or not. Once I revisited the house where I grew up and where my family lived for sixty years. The house had been sold to the British Association of Psychotherapists in 1990, and what used to be our dining room had been turned into an office. When I entered this room on a visit in 1995, I immediately and strongly smelled the kosher red wine which used to be kept in a wooden sideboard next to the dining table and drunk with Kiddush on the Sabbath. Was I just imagining the smell, assisted by these once intensely familiar, beloved surroundings and nearly sixty years of memory and association? Or could a few nanograms of wine have survived all of the repainting and renovation? Smells can be oddly persistent, and I am not sure whether my experience should be called a heightened perception, a hallucination, a memory, or some combination of all these.
My father had an acute sense of smell as a young man, and like all doctors of his generation, he depended on it when seeing patients. He could detect the smell of diabetic urine or of a putrid lung abscess as soon as he entered a patient’s house. A series of sinus infections in middle age blunted his sense of smell, and he could no longer rely on his nose as a diagnostic tool. But he was fortunate that he did not lose his sense of smell entirely, for total loss of the sense of smell—anosmia, which affects perhaps as many as 5 percent of people—causes many problems. People with anosmia cannot smell gas, smoke, or rancid food; they may be beset by social anxiety, not knowing whether they themselves smell of something rank. They cannot enjoy the good smells of the world, either, and they cannot enjoy many of the subtler flavors of food (for most of these depend equally on smell).1
I wrote about one anosmic patient in The Man Who Mistook His Wife for a Hat. He had suddenly lost all sense of smell, as the result of a head injury. (The long olfactory tracts are easily sheared as they cross the base of the skull, so loss of smell can be caused by a relatively mild head injury.) This man had never given much conscious thought to the sense of smell, but once he lost it, he found his life radically poorer. He missed the smell of people, of books, of the city, of springtime. He hoped against hope that the lost sense would return. And, indeed, it seemed to come back some months later when, to his surprise and delight, he smelled his morning coffee as it was brewing. Tentatively, he tried his pipe, abandoned for many months, and caught a whiff of his favorite aromatic tobacco. He returned, excitedly, to his neurologist, but after careful testing, he was told that there was not a trace of recovery. Clearly, though, he was having an olfactory experience of some sort, and I could only think that his power to imagine smells, at least in situations charged with memories and associations, had been enhanced by his anosmia, perhaps as the power to visualize may be enhanced in some who have lost their sight.
The heightened sensitivity of sensory systems when they have lost their normal input of sight, smell, or sound is not an unmixed blessing, for it may lead to hallucinations of sight, smell, or sound—phantopsia, phantosmia, or phantacusis, to use the old but useful terms. And just as 10 to 20 percent of those who lose their sight get Charles Bonnet syndrome, a similar percentage of those who lose their sense of smell experience the olfactory equivalent. In some cases these phantom smells follow sinus infections or head injuries, but occasionally they are associated with migraine, epilepsy, parkinsonism, PTSD, or other conditions.2
In CBS, if there is some remaining vision, there may also be perceptual distortions of all sorts. Similarly, those who have lost much but not all of their sense of smell tend to suffer from distortions of smell, often of an unpleasant sort (a condition called parosmia or dysosmia).
Mary B., a Canadian woman, acquired dysosmia two months after an operation performed under general anesthesia. Eight years later, she sent me a detailed account of her experiences, entitled “A Phantom in My Brain.” She wrote:
It happened fast. In September 1999 I felt great. I’d had a hysterectomy in the summer, but I was already back to daily Pilates and ballet classes, feeling fit and full of vigour. Four months later I was still fit and vigorous, but I was locked in an invisible prison by a disorder no one could see, that no one seemed to know anything about, that I couldn’t even find a name for.
The changes were gradual at first. In September tomatoes and oranges started tasting metallic and a bit rotten, and cottage cheese tasted like sour milk. I tried different brands; they were all bad.
During October, lettuce began to smell and taste of turpentine, and spinach, apples, carrots and cauliflower tasted slightly rotten. Fish and meat, especially chicken, smelt as if they’d been rotting for a week. My partner couldn’t detect the off tastes at all. Was I developing some sort of food allergy?…
Soon the exhaust fans of restaurant kitchens started smelling weirdly unpleasant. Bread tasted rancid; chocolate, like machine oil. The only meat or fish I could eat was smoked salmon. I started having it three times a week. In early December we ate out with friends. I had to choose carefully, but I enjoyed the meal, except that the mineral water smelt like bleach. But the others were drinking it happily, and I decided that my glass hadn’t been rinsed properly. Smells and tastes got dramatically worse in the next week. Traffic smelt so bad that I had to force myself to go out; I made long detours to go to my Pilates and ballet classes by pedestrian-only routes. Wine smelt revolting; so did anybody who was wearing scent. The smell of Ian’s morning coffee had been getting worse, but between one day and the next it turned into a lurid, intolerable stench that permeated the house and lingered for hours. He started having coffee at work.
Ms. B. kept careful notes, hoping to find, if not an explanation, at least some pattern to the distortions, but she could find none. “There was no rhyme or reason to it,” she wrote. “How could lemons taste okay but not oranges; garlic, but not onions?”
With complete anosmia, rather than exaggerations or distortions of perceived smells, there can only be hallucinations of smell. These too can be very various, and sometimes difficult to define or describe. This was brought ou
t by Heather A.:
The hallucinations generally cannot be described by one smell descriptor (except one night I smelled dill pickles for most of an evening). I can kind of describe them as an amalgam of other smells (metallic-y roll-on deodorant; dense acrid-sweet cake; melted plastic in a three-day-old garbage pile). I have been able to have fun with it in this way, make an art of naming/describing them. In the beginning, I would go through phases where I would access one at a time for a couple of weeks, multiple times a day. After a few months, the family of smells I had gone through had diversified, and now I can reference several different ones in a day. Sometimes a new one will pop up and I may not smell it again. The experience of them varies. Sometimes they will come up strong, like something stuck right under my nose, and dissipate quickly; sometimes one will be subtle and linger, at times barely noticeable.
Some people hallucinate a particular smell, which may be influenced by context or suggestion. Laura H., who lost most of her sense of smell after a craniotomy, wrote to me that she would occasionally have a brief burst of smells that were plausible, though not always entirely accurate from what she remembered sensing before her loss. Sometimes they were not really there at all:
Our kitchen was being revamped, and the electrics blew one evening. My husband assured me that all was safe but I was very worried about a possible electrical fire that might start.… I woke up in the middle of the night and had to get up to check the kitchen because I thought I could smell electrical burning.… I checked everywhere I could see in the kitchen, hall, cupboards, but could see nothing burning.… I then started to think the smell could be coming from behind a wall or somewhere I couldn’t see.
