Faces and Hallucinations: Facial Recognition and Hallucinations as Subjects in Higher Perception
“I am having a hallucination now, I don’t need drugs for that.”
—Thomas Pynchon, writer
Macaques are good at recognizing faces and depend on facial recognition for much of their social organization. Readers of this book, unless they have a cognitive mix-up called prosopagnosia, should know how important facial recognition is in our species. There are two types of prosopagnosia, one caused by injury and the other congenital. In both forms the fusiform gyrus, a structure deep in the visual processing region of the temporal lobe, is affected, and hence this region of the brain appears to be responsible for processing visual information about faces. Indeed, macaques’ facial recognition networks can be mapped to this region, too. Although it appears that human facial recognition networks are located more toward the back of the brain (ventrally) in this area than in macaques, the way the monkey and human brains develop may produce this seemingly clear locational difference. And yet, the connectivity of facial recognition neurons shows clear differences between human and macaque. Connectivity studies in humans have indicated that there are two face-processing streams of neurons in this area of the brain that work kind of like the visual what-and-where streams discussed in Chapter 5. Like the visual what-and-where streams, for the face recognition streams one is dorsal and one is ventral, and they have only weak connectivity between the two. Macaques have the dorsal stream and even have rich interconnectivity in this stream, like humans. But the human lineage has evolved the second stream independently. These results suggest a major difference in how faces are recognized in macaques and humans. But what about chimpanzees, which are a much closer relative to humans than are macaques?
Figure 17.1. The T-shaped face in renderings of a Giuseppe Arcimboldo painting of fruit and vegetables, right side up and upside down. The T shape is easily recognizable in the upside-down orientation (right), and hence we interpret this painting as a human face. Even when the painting is right side up (left), some people detect it as a face because they recognize the upside-down T, and the information then is shunted into the face recognition visual network.
Jessica Taubert and Lisa Parr have examined how chimps respond to faces. To understand their approach, it is important to recognize that human facial recognition brain areas respond more directly to faces than to such other items as shoes or chairs. All faces have what is called a T-shaped pattern (fig. 17.1). The two eyes form the bar of the T, and the stem of the T represents the nose and mouth. Recognition of this T shape is what Taubert and Parr call first-order information about facial recognition. Recognition of the T shape is a first step that allows the information to be pushed further down the face-recognition neural pathway into what are called second-order pathways. Taubert and Parr first asked whether the chimp response to faces is based on the first-order information of the T shape or is more complicated, using what are called Mooney objects. These are images of faces or other objects that are in black and white with low contrast and little information in them with respect to typical facial features.
Taubert and Parr created Mooney objects of chimp faces, human hands, and inanimate objects such as shoes. The trick is to create a series of Mooneys with graded black and white tones of varying contrast. For humans, when contrast is optimized on a Mooney series of figures, the second-order pathway of the human face recognition system is diminished, and the only thing we use for recognition of the image is the first-order information. The second-order information is what we use to recognize individuals, so what happens in the case of a high-contrast Mooney face is that we can recognize it as a face, but we cannot recognize the individual.
Chimps can easily identify faces as faces. They can easily discriminate between human hands and shoes versus faces, too. And like humans, chimps fall back on first-order information when the contrast is ratcheted up and lack the ability to identify individuals in these cases. The results of these experiments suggest that chimps share this level of organization for facial recognition and have been part of the extra step of two visual facial recognition streams of neurons, which is a totally reasonable conclusion, considering that we shared a common ancestor with chimpanzees five to seven million years ago. What this also means is that those genus Homo species discussed previously (see Chapter 16) also probably had this more complicated visual facial recognition wiring.
Why is facial recognition so important? Many biologists argue that recognizing faces is an integral part of socialized behavior in humans and other primates. Visual recognition of faces and other objects is indeed important in an adaptive context. It is difficult to deny Dr. Pangloss a seat at the table for this one. As discussed in Chapter 10, certain brain injuries that result in interesting facial recognition phenomena, such as Capgras syndrome (“I know you look like my mom, but I am not reacting to you like you are my mom, so you must be an imposter”), and the split-brain “Mike or Me” effect are good examples of how the process works with faces. But what about other objects that mix up the sense of vision? Witness the viral image of “dog rear Jesus” that in one week’s time received nearly two hundred thousand web hits and has since become an Internet classic. Dog rear Jesus is an apparently unretouched photo of a dog’s rear end with an anus that resembles the face of a long-haired bearded man. More stunning is that the surrounding fur looks like a body in a robe with outstretched arms. It doesn’t take much for the brain (at least mine) to see the Lord and Savior in all of his humble glory.
And indeed, you would have to be a doubting Thomas, a human not familiar with Jesus, or a lying sinner to deny that the dog’s rear end resembles a ten-inch-tall replica of the Savior himself. Dog rear Jesus is not the only religious icon we see in strange and seemingly inappropriate places. For one, the Virgin Mary must have had as many fashion looks as Lady Gaga. Her likeness has appeared on everything from the walls of freeway exits to the surfaces of sandwiches. About a decade ago, a piece of a grilled cheese sandwich with her supposed image on it was auctioned off for twenty-eight thousand dollars. These sightings are not simply recent phenomena, because apparitions of the Virgin Mary have been reported ever since the Assumption—many famous and infamous images of that event, and of the Virgin, have been created by artists (including one created with elephant dung as paint). And when you throw in the toasted cheese, the water markings on walls, and assorted other apparitions, she appears in an amazing assortment of guises.
There is actually a word for this phenomenon—pareidolia—and it is a specific form of a neural process called apophenia. Apophenia is the interpretation of random data by the brain as something meaningful. Pareidolia comes from the Greek para, meaning “instead of” and eidōlon meaning “image.” In this context, it means “faulty image.” Examples of pareidolia other than imagining religious icons abound. The premise of the famous Rorschach tests is one. These tests involve the interpretation of rather randomly produced ink smears or blots. Psychologists then use the pareidolic interpretations of the ink blots for psychological interpretations. There are also auditory versions of pareidolia. Perhaps the most famous examples are “I buried Paul,” supposedly heard at the end of the Beatles’ song “Strawberry Fields,” and the purported satanic chanting in the backmasked (played backward) playing of Led Zeppelin’s “Stairway to Heaven.”
The question, then, is why do our visual and auditory senses get so twisted up that we see Jesus in a dog’s rear end, recognize the Virgin Mary on grilled cheese sandwiches, or hear satanic verses when songs are played backward? What is it about the brain that allows for such unholy profanity? Most of the answers lie in the kluginess of how the brain has evolved and how brain cells communicate with one another and with the outer world.
One last aspect of the brain that is in play when we see the Virgin Mary on a piece of toast or Jesus on a dog’s rear end is that the brain has more than likely been wired to prefer religious explanations for unusual phenomena. Most evidence for this explanation is anecdotal, but there is some experimental evidence, albeit controversial. The anecdotal evidence comes from evolutionary psychology, the branch of evolutionary biology that used to be called sociobiology, where evolutionary explanations are offered for human behaviors. The evolutionary psychology explanation for human dependence on religion, generally put, is that it offers social cohesion to populations practicing it and that this in turn is an evolutionary advantage for the population. And yes, I should be issuing a Dr. Pangloss warning here, too.
The other purported evidence that religion is perhaps hardwired is the product of some relatively wacky experiments involving the electromagnetic stimulation of specific regions of the brain. These experiments involve the so-called “god helmet,” a device developed by Michael Persinger. Stimulating the brain and then observing the resulting behaviors is not a novel approach to the study of brain function. Remember that neurosurgeon Wilder Penfield tickled various regions of the brain during his patients’ surgeries and asked them what they felt (as pointed out earlier, the surface of the brain has no pain receptors, so some brain surgery is done with the patient wide awake and conversant). These probes allowed him to map the real estate of the brain responsible for specific sensory and motor functions. The sensory and motor homunculi discussed in Chapter 3 are the results of this important work.
Using the same principle, but in a noninvasive way, Persinger outfitted a helmet with the ability to transmit electromagnetic radiation to highly specific regions of the brain of the wearer. Electromagnetic radiation apparently alters the function of the neurons in the radiated region. Persinger hoped to demonstrate the existence of a specific region of the brain responsible for ecstatic religious feelings. Some subjects report light-headedness and feelings of well-being along with a spiritual feeling when under the influence of the god helmet. Others, like the famous evolutionary biologist Richard Dawkins, report no impact at all. Although the evidence is anecdotal for a god region or a god gene, our social behavior is an oddity in the animal world. Our dependence on religion and spirituality to maintain social cohesion is more than likely the result of rapid cultural evolution. As Dawkins explains, “Religion is about turning untested belief into unshakable truth through the power of institutions and the passage of time.” But whether the visions and apparitions many report seeing when experiencing religious ecstasy are real is another story. Perhaps Dawkins’s answer to a question from a rather zealously religious attendee at one of his talks provides a clue. The question was: How can Dawkins explain the “fact” that the questioner during prayer actually sees religious icons and walks with Jesus and Mary daily? Dawkins responded that he didn’t doubt that the individual and others who do see these apparitions are “seeing” them and, more important, he didn’t doubt their sincerity. But as Dawkins added, “Sir, I believe you are hallucinating.” This brings to mind one other reference to the image of the Virgin Mary in popular culture, and that is from the famous TV series The Sopranos, when wise guy “Paulie Walnuts” Gualtieri momentarily sees the Virgin Mary near a stripper pole in the Bada Bing. His vision was not a case of pareidolia but rather a fleeting hallucination, and these are another story about messiness in our brains that now warrants consideration.
My first reaction to reading Oliver Sacks’s book Hallucinations was, “Can I get some of what he was on?” Sacks was always starkly frank about his experimentation with mind-altering drugs as a young man. In his very first experience with LSD, he comically relates that after he and a friend dropped a tab of acid they had mail ordered, they waited for it to kick in by listening to the music of Igor Stravinsky, hoping to hear something mind-bending. They quickly realized that the Stravinsky piece sounded the same as it always did and that they had short-armed their acid dose by an order of magnitude. They had taken only enough LSD to cause a cat to trip. In another drug-related story about his experiences, he injected a particularly large dose of morphine and observed the Battle of Agincourt on his dressing-gown sleeve for what he thought was a few minutes but in reality was twelve hours.
Hallucinations can be induced by drugs, as Oliver Sacks’s experiences show, but they can also be induced by brain injury, migraine, or dementia. Or they can be symptoms of psychiatric disorders. Hallucinations can present in schizophrenia disorder, a broad-spectrum psychiatric disease, and in Parkinson’s disorder and other forms of dementia. Hallucinations can affect or use all of our major senses, including the vestibular or balance system. Four of the big five senses seem to be involved in most hallucinogenic experiences of schizophrenics—vision, hearing, tactile sense, and olfaction. Auditory hallucinations appear to be most commonly experienced by people with the disorder, with visual hallucinations following next. But vision and hearing together seem also to be a rather common category of hallucination for schizophrenics. Because schizophrenia is a broad-spectrum disorder, it is difficult to pin down how the senses are affected by this general kind of psychosis.
Dementia is another group of psychiatric disorders where hallucinations occur. Two disorders—Parkinson’s and dementia with Lewy bodies—are grouped under the major category called Lewy body dementia. In the early 1900s, Frederic Lewy, a Berlin-born Jewish neurologist who worked in Alois Alzheimer’s lab in Munich before fleeing Nazi Germany to become an American citizen, discovered conspicuous anomalies in cells of the dopamine-producing area of the brain, called the substantia nigra, of patients who had died of dementia. This area of the brain is a darkened region at the tip of the pons section of the brain stem. The abnormal neural cells look very different from unaffected neural cells when stained a certain way and observed under a microscope. The abnormal cells swell and riddle the brain tissue of people with certain kinds of dementia. They appear to fill up with a protein called alpha-synuclein that tends to diminish the number of dopamine-producing neurons in the brain. People suffering from Alzheimer’s disease will also have Lewy bodies, but the major locus of pathology for Alzheimer’s patients occurs in the hippocampus. In addition, since the Lewy bodies are localized in the substantia nigra, the drastic effects of Alzheimer’s disease on the overall structure in the brain do not occur in people with Lewy body dementia, so Alzheimer’s is not considered a form of this dementia.
Whether hallucinations are present is one test of three that physicians use to diagnose Lewy body dementia. Self-reported hallucinations are one way to find out whether a person hallucinates, but another, more objective way is to exploit the pareidolia effect just discussed. In one version of the test, subjects are shown a series of blurred pictures of natural scenery for sixty seconds during which they are asked to describe what they are seeing in as much detail as they can. They are asked to point to objects in the pictures as they describe them and are not told whether they are correct while taking the test. Their answers are classified into three categories. The simplest category is the subject’s stated inability to recognize the scene or any objects in it. A second response is an accurate description of the scene and the objects in it. The third category includes any illusory or incorrectly identified objects. If a potential illusory object is identified, the individual is asked if the object is in the picture or if the object looks like what was described. Other versions of the test use the same principle of identifying illusory objects, and the degree of pareidolia scored is correlated to the number of illusory items observed by the subject. The use of pareidolia to diagnose Lewy body dementia seems to be a good way to objectively identify the disorder, and it also points to potential study of people with this disorder to pin down the neurophysiological basis of hallucinations.
So, what is the neurological basis of hallucinations? Early work on this question involved examining people who experienced hallucinations and then attempted to synthesize an overarching theory about them. The first step in getting at the source of hallucinations was to define them. In the 1930s, both hallucinations and illusions were thought to be part of the same thing—visual anomalies. Psychiatrists then decided to tease apart illusion from hallucination, and this better defined what these visual experiences consisted of. At this time, too, there were several theories about the origin of hallucinations. One suggested that they were visual anomalies caused by problems in transmitting or interpreting the signals that originated in the retina. Hence, eye injuries or diseases were the source of hallucinations. This ocular theory of hallucinations appeared reasonable because patients with eye disorders seemed to hallucinate more than individuals without eye problems, and people with eye disorders who hallucinated were cured of their hallucinations when their eye disorders were cured. But the idea that eye disorders alone caused hallucinations was rejected, and the medical state of the eye, although not excluded as part of the story, was rejected as the sole explanation.
One particular kind of hallucination that advanced thinking about the nature of these anomalous sensory experiences involved a syndrome about which Oliver Sacks wrote at length: Charles Bonnet syndrome. This syndrome affects people who have lost sight as a result of old age. These older blind people have vivid and complicated, usually pleasant, visual hallucinations, even though they have lost the sense of sight, and what’s more, they freely admit that they are hallucinating. To some physicians, Charles Bonnet syndrome was the clearest example of why the eye should be decoupled from hallucinations. But to others, the eye was kept in the picture as part of the explanation. Nonetheless, Charles Bonnet syndrome became the model system for studying the origin of hallucinations. It appears that if you can produce an explanation that also works for Charles Bonnet syndrome, you have hit the jackpot in the explaining the hallucinations sweepstakes.
Another important aspect of research on Charles Bonnet syndrome is that it has forced neurobiologists who study it and other syndromes with hallucinations to be very picky about what they are calling hallucinations. Researchers have realized, as with schizophrenia, that hallucinations fill a spectrum of phenomena. A comparison of two kinds—zoopsia and Lilliputian hallucinations—shows the potential for differences among hallucinations. Zoopsia hallucinations involve animals, and they progress in a well-defined way. Lilliputian hallucinations involve tiny people much like Sacks’s Agincourt reenactment, and they, too, have well-defined characteristics.
When different kinds of hallucinations are analyzed as separate phenomena, it becomes evident that different neural pathways or complexes of neurons cause the different kinds of hallucinations. Visual hallucinations are one of the more common and easy to follow kinds and have been the object of several fMRI studies. Other types of sensory hallucinations have also been evaluated. For example, in a study of subjects with schizophrenia, the sensory category or categories of more than five hundred hallucinatory events were recorded. Auditory hallucinations were the most common, followed by auditory and visual hallucinations (fig. 17.2).
Researchers Dominic ffytche and Paul Allen have been at the forefront of this neurovisualization work. Allen and his colleagues reviewed the large literature on hallucinations and developed a model for auditory hallucinations. The model involves the hyperactivity of the areas of the auditory cortex that process the primary information coming into the brain from the ears. It also includes the idea that altered connectivity exists between these primary auditory cortical regions and language processing in the inferior frontal cortex. The model further requires that weakened control of the entire system by other regions of the brain responsible for auditory processing should exist. While establishing the preconceived idea that the connectivity in the auditory neural system should be altered in people who hallucinate, how the altered activity happens and how it affects our sensory perception is not known.
Figure 17.2. Venn diagram showing the relative occurrence of different kinds of hallucinations and the overlap or combination of sensory kinds of hallucinations.
ffytche and his colleagues have developed a “taxonomy” of hallucination phenomena, carefully separating different kinds of hallucinations as they analyze their functional MRI data. The approach involves putting a hallucinating subject into an MRI machine and asking when hallucinations start and end. The subject is also asked to describe the hallucination so that they can categorize it. Using these approaches, ffytche and colleagues have established that brain activity associated with hallucinations is highly localized. When comparing the activation patterns of people having different kinds of hallucinations, they observe subtle differences in the neurons activated.
The visual pathways of the human brain are pretty well worked out. We know color is processed in the visual cortex, where information that is used to identify faces is processed, and even where specific parts of the face are processed. So, when the subject being examined with fMRI was having a very colorful hallucination, we know that the active region was the part of the visual cortex responsible for color interpretation. The correspondence of the regions of the visual cortex with the specific types of hallucinatory images was striking.
Other evidence for a localized nature of hallucinations in the brain comes from comparing people undergoing auditory and visual hallucinations. Functional MRI studies show clearly that these two major kinds of hallucinations activate different regions of the brain. Audio hallucinations often involve speaking, and so the relevant brain regions for speech, such as Wernicke’s and Broca’s areas, show activation during auditory speech-related phenomena.
This all makes good sense, because these brain regions control many aspects of vision, speech, and speech comprehension. So, are people who hallucinate really hearing and seeing? Their brain activation patterns suggest that they are hearing and seeing something, but is it really sight and sound? Remember mirror neurons, where specific parts of the brain that control sensory input can be activated simply by watching someone else do something? Some researchers suggest that people who hallucinate actually do feel that the sounds they “hear” are coming from the outer world or, in other words, misattribute hallucinated voices and sounds to real external stimulus. If this is the case, then people who hallucinate have tricked themselves into something akin to being able to be tickled by themselves. And indeed, Sarah-Jayne Blakemore and her colleagues have shown that normal individuals cannot tickle themselves efficiently because self-generated tactile stimulation is dampened as a result of self-awareness of where the stimulus comes from. But when people who experience auditory hallucinations are tested, they appear very capable of tickling themselves as efficiently as if someone else was tickling them. Although the exact mechanism for this tickle thyself phenomenon is unknown, it is thought that there might be a disconnect or altered connection between how normal people monitor the initiation of an act and the regions of the body that perceive the results of the action. People who regularly experience hallucinations are not good at making the connection between their action and the sensory information from that action. They are also not good at keeping time or placing actions into a temporal framework, and this contributes to the disconnect that allows them in turn to experience their hallucinations as not coming from self.
When Oliver Sacks and his friend dropped the weak dose of LSD, the chemical technically known as lysergic acid diethylamide went into the stomach, was absorbed by the digestive tract, and then passed into the blood, where the small LSD molecule was transported to the brain. This compound is structurally very similar to serotonin, a neurotransmitter in the brain, and so one of the many receptors in the brain that reacts to serotonin in particular is terribly confused by the presence of the LSD. The confusion caused by LSD’s interaction with this serotonin receptor results in altered connectivity of specific regions of the brain similar to the messed-up connectivity of people who hallucinate from brain injuries and neural disorder. But the dose Sacks took was so low that only a small proportion of the serotonin receptors were affected, and Sacks was not affected by the attempt to trip out. He did eventually get the dosage right, and when he did, the impact on his brain chemistry was very different.
It has been nearly fifty years since Oliver Sacks first tried LSD, and only now are scientists getting closer to cracking open what the brain on LSD is all about. In a novel experiment performed by Robin Carhart-Harris and his colleagues, tripping subjects were examined with three modern brain imaging technologies, including fMRI. The brain on LSD shows altered activity in expected brain regions such as the visual cortex. People who are tripping can detail the intensity of their hallucinatory experience, and the connectivity patterns before and during slight hallucinatory experiences and extreme hallucinatory experiences can be quantified. In this case, people who are tripping their brains out show expanded connectivity of their visual cortex with other regions of the brain. More important, these studies show that connections of the primary visual cortex to two areas of the brain not considered part of the visual pathway (the parahippocampus and the retrosplenial cortex) are significantly diminished in people on LSD. As the connections to these regions of the brain get weaker and weaker, subjects experience more and more dissolution of self and loss of ego. These results suggest that LSD has the same self-tickling impact on the brain as for other sources of hallucinations, by weakening the connection to the visual phenomena and the sense of where the stimulus is coming from.
It is also obvious that memories and emotions intrude on the neural processes of people who are hallucinating. There is a certain amount of overstimulation of the sensory areas of the brain responsible for auditory and visual hallucinations that initiates hallucinations, but this is augmented by unusual suggestive input from other regions of the brain that are involved in higher-level cortical processing. In one study, a person experiencing visual hallucinations was examined for unusual connectivity in the brain. The study showed hyperconnectivity between the visual cortex area and the amygdala, which is embedded in the limbic system and is heavily involved in emotional response. Although this study involved only a single individual, it is highly suggestive that hyperconnectivity might be a factor in directing or suggesting emotional content for hallucinations.
Although Oliver Sacks engaged in some extreme drug use during his life, he was always careful not to encourage it in others, and he also pointed out that his intellectual development and knowledge of the mind were very dependent on that phase of his life. He stated clearly that drugs “taught me what the mind is capable of.” Sacks was one of the most influential researchers of the past century in brain science. His treatise on hallucinations is a fascinating tour of the mind and how our senses are pirated away by hallucinations to create alternative forms of perception and in turn alternate realities. Hallucinations taught him several lessons. First, because he was an astute neurobiologist, he noted correlations of hallucinations with neural structural anomalies in people. He commented, “The phenomenology of hallucinations often points to the brain structures and mechanisms involved and can therefore, potentially, provide more direct insight into the workings of the brain.” He recognized the importance of hallucinations in how we as a species have developed socially and culturally. And he finally recognized how our perception of the world is needed for us to be conscious beings. Sacks also had an acute interest in other aspects of the brain as sources of information, leading us to a better understanding of our existence, which is how we process and mold our senses, and ultimately perceptions of the outer world, into words, language, art, and music that make us a stunningly unique organism on this planet.