Who’s in Charge?

Chapter Two
The Parallel and Distributed Brain

DO YOU REMEMBER THE TELLING SCENE IN THE MOVIE MEN in Black, when a corpse is undergoing an autopsy? The face popped open only to reveal the underlying brain machinery, and right there was an extraterrestrial-looking homunculus pulling levers to make it all work. It was the “I,” the “self,” the phenomenal center and take-charge thing we all think we have. Hollywood captured it perfectly, and we all believe in it even though we may understand that that is not at all how it works. Instead, we understand that we are stuck with these automatic brains, these vastly parallel and distributed systems that don’t seem to have a boss, much like the Internet does not have a boss. So much of us comes from the factory all wired up and ready to go. Think about the wallaby, for example. The last ninety-five hundred years have been Easy Street for the Tamar wallabies that live on Kangaroo Island off the coast of Australia. They have lived there without a single predator to worry them all those years. They have never even seen one. So why then, when presented with stuffed models of predatory animals such as a cat, fox, or the now-extinct animal that had been their historical predator, do they stop foraging and become vigilant, but they don’t when presented with a model of a nonpredatory animal? From their own experience, they shouldn’t even know that there are such things as animals they should be wary of.

Like the wallaby we have thousands, if not millions, of wired-in predilections for various actions and choices. I don’t know about wallaby minds, but we humans think we are making all our decisions to act consciously and willfully. We all feel we are wonderfully unified, coherent mental machines and that our underlying brain structure must somehow reflect this overpowering sense we all possess. It doesn’t. Again, no central command center keeps all other brain systems hopping to the instructions of a five-star general. The brain has millions of local processors making important decisions. It is a highly specialized system with critical networks distributed throughout the 1,300 grams of tissue. There is no one boss in the brain. You are certainly not the boss of the brain. Have you ever succeeded in telling your brain to shut up already and go to sleep?

It has taken hundreds of years to accumulate the knowledge we currently have about the organization of the human brain. It has been a rocky road as well. While the story unfolded, however, a persistent uneasiness remained about the knowledge. How can stuff be localized in the brain in so many ways and still seemingly function as an integrated whole? The story begins a long time ago.

Localized Brain Functions?

The first hints came from anatomy, and the modern understanding of human brain anatomy stemmed from studies done by the English physician Thomas Willis, he of the circle of Willis^* fame, in the seventeenth century. He was the first to describe the longitudinal fibers of the corpus callosum and several other structures. A little over a hundred years later, in 1796, Franz Joseph Gall, an Austrian physician, came up with the idea that different parts of the brain produced different mental functions which resulted in a person’s talents, traits, and dispositions. He even suggested that morality and intelligence were innate. Although these were good ideas, they were based on a faulty premise that was not grounded in good science. His premise was that the brain was composed of different organs, and that each was responsible for a mental process that resulted in a specific trait or faculty. If a particular faculty were more highly developed, its corresponding organ would enlarge and could be felt by pressing on the surface of the skull. From this idea he suggested that one could then examine the skull and diagnose that individual’s particular abilities and character. This became known as phrenology.

Gall had another good idea: He moved to Paris. As the story goes, however, he displeased Napoleon Bonaparte by not attributing to his skull certain noble characteristics that the future emperor was sure he possessed. Obviously Gall was no politician. When he applied to the Academy of Science of Paris, Napoleon ordered the academy to get some scientific evidence for his conjectures, so the academy asked the physiologist Marie-Jean-Pierre Flourens to see if he could come up with any concrete findings that would back up this theory.

At that time there were three methods of inquiry that Flourens could tackle: (1) surgically destroying specific parts of animal brains and observing the results; (2) stimulating parts of animal brains with electrical pulses and seeing what happened; (3) or studying neurological patients clinically and performing autopsies on them after their deaths. Flourens became quite taken with the notion that specific locations in the brain performed specific processes (cerebral localization), and went with option one to investigate this idea. Studying rabbit and pigeon brains, he became the first to show that yes, certain parts of the brain were responsible for certain functions: When he removed the cerebral hemispheres, that was the end of perception, motor ability, and judgment; without the cerebellum the animals became uncoordinated and lost their equilibrium; and when he cut out the brain stem—well, you know what happened—they died. He could not, however, find any areas for advanced abilities like memory or cognition, just as psychologist Karl Lashley, who we read about in the last chapter, would later observe studying rat brains. He concluded that these functions were more diffusely scattered throughout the brain. Examining skulls to determine character and intelligence did not stand up to the rigors of science, and slid into the hands of charlatans. Unfortunately, Gall’s good idea, that there was localization of cerebral function, got tossed out with the bad. His other good idea, moving to Paris, has been well accepted.

Not too many years later, however, evidence relevant to Gall’s idea started trickling in from clinical studies. In 1836 another Frenchman, Marc Dax, a neurologist in Montpellier, sent a report to the Academy of Sciences about three patients, noting the coincidence that each had speech disturbances and similar left-hemisphere lesions found at autopsy. A report from the provinces, however, didn’t get much air time in Paris. It wasn’t until nearly thirty years later that anyone took much notice of this observation that speech could be disrupted by a lesion to one hemisphere only. This happened in 1861, when a well-known Parisian physician, Paul Broca, published his autopsy on a patient who had been nicknamed Tan. Tan had developed aphasia and was so named because tan was the only word he could utter. Broca found that Tan had a syphilitic lesion in his left hemisphere, in the inferior frontal lobe. He went on to study several more patients with aphasia, all with lesions in the same area. This region, later called the speech center, is also known as Broca’s area. Meanwhile, German physician Carl Wernicke was finding patients with lesions in an area of their temporal lobe, who could hear words and sounds just fine, but could not understand them. The hunt for sites in the brain for specific abilities was off to the races.

Hughlings Jackson, a British neurologist, confirmed Broca’s findings, but he is a part of this story in his own right. His wife suffered generalized seizures, which he was able to observe very closely. He noticed that they always started in a specific part of her body and progressed systematically in a pattern that did not vary. This suggested to Jackson that specific areas of the brain controlled the motor movements of different parts of the body and gave rise to his theory that motor activity originated from and was localized in the cerebral cortex. He also wielded an ophthalmoscope that had been invented a few years earlier by Hermann von Helmholtz, the German physician and physicist. This instrument allows physicians to peer into the nether reaches behind the eye. Jackson thought it important for neurologists to study the eye, and why this is so will become apparent as we travel further on. From these early clinical observations that were followed up with autopsy findings, it was looking more and more as if Gall had been on the right track about cerebral localization of functions.

The Great World of the Unconscious

Localization was not the only idea about cerebral functioning that had been simmering. Fictional writing, from Shakespeare’s Othello to Jane Austen’s Emma, was implying that much was going on in the nonconscious brain department. While Sigmund Freud tends to get the credit for the buried iceberg of nonconscious processes, he was not the originator of the idea, but the trumpet. Many, notably the philosopher Arthur Schopenhauer, from whom many of Freud’s ideas sprung, preceded him in emphasizing the importance of the unconscious and as did later, the English Victorian version of a Renaissance man, Francis Galton. Galton wore many hats. He was an anthropologist, tropical explorer (Southwest Africa), geographer, sociologist, geneticist, statistician, inventor, meteorologist, and was also considered the father of psychometry, which is the development of both instruments and techniques for measuring intelligence, knowledge, personality traits, and so forth. In the journal Brain,^** he painted a picture of the mind as if it were a house set upon a “complex system of drains and gas- and water-pipes . . . which are usually hidden out of sight, and of whose existence, so long as they acted well, we had never troubled ourselves.” In the conclusion to this paper he wrote: “Perhaps the strongest of the impressions left by these experiments regards the multifariousness of the work done by the mind in a state of half-unconsciousness, and the valid reason they afford for believing in the existence of still deeper strata of mental operations, sunk wholly below the level of consciousness, which may account for such mental phenomena as cannot otherwise be explained.”¹ Galton, unlike Freud, was interested in basing his theories on concrete findings and statistical methods. He added to the researchers’ armamentarium the statistical concepts of correlation, standard deviations, and regression to the mean, and was also the first to use surveys and questionnaires. Galton was also interested in heredity (no wonder—his cousin was Charles Darwin). Galton was the first to use the term nature versus nurture and to do studies on twins to tease out the varying influences.^†

So emerging into the twentieth century, the ideas of localized brain functions and nonconscious processes were being batted around, but as we saw in the last chapter, these ideas suffered a detour early in the twentieth century with the wide acceptance of behaviorism and the equipotential brain theory. The theory of an equipotential brain, however, had always faced a serious challenge from clinical medicine. This began with Dax’s observation of the correlation of a lesion in a specific part of the brain with a specific result in a variety of people. The equipotential brain theory never could explain this or many of the other seemingly mysterious cases from neurology. Once scientists understood, however, that the brain has distributed and specialized networks, some of these clinical mysteries could be solved. Even before the advent of modern brain imaging and EEG techniques, studying the deficits of patients with lesions allowed a type of reverse engineering and provided insights into how the brain enables cognitive states.

Help from Patients

Neuroscientists owe much to the many clinical patients who have generously participated in our research. Studying clinical patients with X-rays and early scanning devices began to reveal that all sorts of unusual behaviors were caused by lesions in specific locations. For instance, a lesion in one specific area of the parietal lobe can produce the odd syndrome of reduplicative paramnesia, a delusional belief that a place has been duplicated or exists in more than one spot at the same time, or has been moved to a different location. I had a patient who, although she was being examined in my office at New York Hospital, claimed we were in her home in Freeport, Maine. I started with the question “So, where are you?” She replied, “I am in Freeport, Maine. I know you don’t believe it. Dr. Posner told me this morning when he came to see me that I was in Memorial Sloan-Kettering Hospital and that when the residents come on rounds to say that to them. Well, that is fine, but I know I am in my house on Main Street in Freeport, Maine!” I asked, “Well, if you are in Freeport and in your house, how come there are elevators outside the door here?” She calmly responded, “Doctor, do you know how much it cost me to have those put in?”

As we proceed toward the front of the brain, a lesion in the lateral frontal lobes produces deficits in sequencing behavior, leaving one unable to plan or multitask. Orbital frontal lesions, located right above the eye sockets, may interrupt the emotional pathways that give feedback to monitor cognitive states and may be associated with a loss of the ability to judge right and wrong. There can be a decreased ability to inhibit behavior, leading to more impulsive, obsessive-compulsive, aggressive, and/or violent actions and higher-order cognitive dysfunctions. And in the left temporal lobe, a lesion in Wernicke’s area produces Wernicke’s aphasia, where the affected person may have no comprehension of either written or spoken language, and although he or she may speak fluently with a natural language rhythm, it’s gibberish. So from clinical medicine, we can see that specific parts of the brain are involved with particular aspects of cognitive activity.

Functional Modules

Indeed, today it seems that localized brain function is very much more specific than even Gall may have considered. Some patients have lesions in the temporal lobe that leave them very poor at recognizing animals but not man-made artifacts and vice versa.² A lesion in one spot leaves you unable to tell a Jack Russell from a badger (not that there is much difference), and with damage in another spot, the toaster is unrecognizable. There are even people with certain brain lesions who specifically cannot recognize fruit. Harvard researchers Alfonso Caramazza and Jennifer Shelton claim that the brain has specific knowledge systems (modules) for animate and inanimate categories that have distinct neural mechanisms. These domain-specific knowledge systems aren’t actually the knowledge itself, but systems that make you pay attention to particular aspects of situations, and by doing so, increase your survival chances. For example, there may be quite specific detectors for certain classes of predatory animals such as snakes and big cats.³ A stable set of visual clues may be encoded in the brain that make you pay attention to certain aspects of biological motion, such as slithering in the case of snakes or sharp teeth, forward-facing eyes, body size, and shape in the case of big cats, which are used as input to identify them.⁴ You don’t have innate knowledge that a tiger is a tiger, but you may have innate knowledge that when you see a large animal with forward-facing eyes and sharp teeth that stalks, it is a predator and you automatically become wary; similarly, you automatically get a little shot of adrenaline and veer away from the slithering movement in the grass.

This domain specificity for predators is not limited to humans, of course. Richard Cross and colleagues at the University of California–Davis studied some squirrels that had been raised in isolation and had never seen a snake in their lives. When exposed to snakes for the first time they avoided them, but did not avoid other novel objects: The squirrels had an innate wariness of snakes. In fact these researchers have been able to document that it takes ten thousand years of snake-free living for this snake template to disappear in populations.⁵ And this explains our Kangaroo Island wallabies. They were reacting to some visual cue that the stuffed predators exhibited, not to any behavior or odor. Thus, highly specific modules exist, in this case for identification, that do not require prior experience or social context to work. These mechanisms are innate and hard-wired; some of these we share with other animals; some animals have mechanisms that we don’t have; and some are uniquely human.

Splitting the Brain

Starting in 1961, there was a new opportunity to study the brain at work, with patients who had had their cerebral hemispheres divided, the so-called split-brain patients. In the late 1950s, Roger Sperry’s lab at Caltech was studying the effects of dividing the corpus callosum (CC) in monkeys and cats,⁶ and was developing new methods to test for these effects. They had found that if they taught one hemisphere a task in animals with an intact CC, the skill would transfer to the other hemisphere, but that if the CC were divided, it did not. The divided brains had divided perception and learning. Big effects were being found, and the question presented itself, could similar effects be found in the human? There was a great deal of skepticism, for a few reasons. Although many neurological cases reported in the late nineteenth century described specific impairments with focal lesions in the CC, these findings were the victims of Lashley’s equipotential cerebral cortex theory and had been ignored, swept under the carpet, and literally forgotten about for many years. More seeming evidence for the skeptics was that children who were born without a CC showed no ill effects.^†† The final big reason was that in a series of twenty-six patients who each had had their corpus callosum cut (known as a commissurotomy) to treat intractable epilepsy at the University of Rochester in the 1940s, no neurological or psychological consequences had been observed by a gifted young neurologist, Andrew Akelaitis, who had tested them.⁷ The patients all felt just fine after their surgery and they themselves noticed no differences. Karl Lashley had seized on these findings to push his idea of mass action and equipotentiality of the cerebral cortex; discrete circuits of the brain were not important, he claimed—only cortical mass. He suggested that the function of the corpus callosum was simply to hold the hemispheres together.

In the summer between my junior and senior year at Dartmouth College, I landed in Roger Sperry’s lab at Caltech as an undergraduate summer fellow because I was interested in the nerve regeneration studies I wrote about in the last chapter. The lab, however, was now focused on the corpus callosum, so I spent the summer trying to anesthetize the half brain of a rabbit and decided basic research was the life for me. I was captivated by the question of what was happening to humans after callosal surgery. Because the lab was finding dramatically altered brain function in the cats, monkeys, and chimps with callosal sections, I was convinced there had to be some effect on humans. During my senior year, I came up with the plan of retesting Akelaitis’s Rochester patients during my spring break and designed a different method of testing them. Armed with my first grant of $200 from the Hitchcock Foundation at Dartmouth Medical School to cover a rental car and hotel room, I drove to Rochester. My rental car was full of borrowed taschistoscopes (pre–computer age devices that display images on a screen for a specific amount of time) from the Dartmouth psychology department for the testing that had been set up. While I was waiting to begin, however, the testing was canceled, and I was left empty-handed and disappointed. However, my curiosity was unabated; I was determined to return to the vibrant atmosphere of Caltech for graduate school, which came about the following summer.

To begin my graduate studies, a new opportunity presented itself. Dr. Joseph Bogen, a neurosurgery resident at the White Memorial Hospital in Los Angeles, and his attending physician, Philip Vogel, had a patient whom Bogen, after critically reviewing the medical literature, thought would benefit from a split-brain procedure; the patient agreed. For the previous ten years, this patient, a robust and charming man, WJ, had been suffering two grand mal seizures a week, each of which took him a day to recover from. Obviously this had an enormous impact on his life, and he was ready to risk the surgery. Already armed with the testing procedures that I had designed at Dartmouth, I was assigned to test WJ, both before and after his surgery.⁸ His surgery was a great success, and he was electrified by the facts that he felt no different and his grand mal seizures were completely resolved. I was electrified, too, by what I discovered about WJ’s brain function and have been fascinated with the results from this patient and those who followed ever since.

The surgical procedure to cut the CC was performed after all other treatments for intractable epilepsy had been tried. William Van Wagenen, a Rochester, New York, neurosurgeon, performed the procedure for the first time in 1940, following the observation that one of his patients with severe seizures got relief after developing a tumor in his corpus callosum.⁹ It was thought that if the connection between the two sides of the brain were cut, then the electrical impulses causing the seizures wouldn’t spread from one side of the brain to the other, and a generalized convulsion would be prevented. Splitting the brain in half, however, is a big deal. The great fear was what the side effects of the surgery might be. Would it create a split personality with two brains in one head? In fact the treatment was very successful. Patients’ seizure activity decreased on average 60–70 percent, some were totally free of seizures altogether, and they all felt just fine: no split personality, no split consciousness.¹⁰ Most seemed completely unaware of any changes in their mental processes. They appeared completely normal. This was great, but puzzling nonetheless.

The procedure for fully dividing the hemispheres includes cutting the two fiber pathways that connect the hemispheres: the anterior commissure and the corpus callosum. Not all the connectivity between the two hemispheres is severed, however. Both hemispheres are still connected to a common brain stem, which supports similar arousal levels, so conveniently, both sides sleep and wake at the same time.¹¹ The subcortical pathways remain intact and both sides receive much of the same sensory information from the body’s nerves relating to the five senses and proprioceptive information from the sensory nerves in the muscle, joints, and tendons about the body’s position in space. At the time, we didn’t know that both hemispheres can initiate eye movements and that there also appears to be only one integrated spatial attention system, a set of processes that allows the selection of some stimuli over others, which continues to be unifocal after the brain has been split. Thus, attention cannot be distributed to two spatially disparate locations:¹² unfortunately, contrary to what most modern drivers are quite sure they are capable of, the right brain can’t watch the traffic while the left brain is reading text messaging. We have since also learned that emotional stimuli presented to one hemisphere will still affect the judgment of the other hemisphere. We did know initially, as we learned earlier from the studies of Dax and Broca, that our language areas are located in the left hemisphere (exceptions are in a few left-handed people).

When WJ was tested before his surgery, he could name objects presented to either visual field or objects placed in either of his hands. He could understand any command and carry it out with either hand, that is to say, he was normal. When he returned for testing after surgery, WJ felt just fine, and like the patients from Rochester, noticed no changes, except that he was no longer having seizures. I had devised a testing procedure, which, unlike the one used by Akelaitis, took advantage of the anatomy of the human visual system. In humans, the optic nerves from each eye meet at what is called the optic chasm. Here, each nerve splits in half, and the medial half (the inside track) of each crosses the optic chasm into the opposite side of the brain and the lateral half (that on the outside) stays on the same side. The parts of both eyes that attend to the right visual field send information to the left hemisphere and information from the left visual field goes to and is processed by the right hemisphere. In the animal experiments, this information did not cross over from one disconnected hemisphere to the other. Only the right side of the brain had access to information from the left visual field and vice versa. Because the visual system is set up in this manner, I could feed information to one half of the animals’ brains only.

The day arrived for WJ’s first test after his surgery. What would we find? Things, at first, progressed as expected. We expected that because his speech center was located in his left hemisphere, he would be able to name objects seen by his left hemisphere. Accordingly, he could easily name objects presented to his left hemisphere. Thus, when we flashed a picture of a spoon in the right visual field and then asked, “Did you see anything?” He quickly replied, “A spoon.” Then came the initial critical test: What would happen when these objects were presented to his right hemisphere from the left visual field? Akelaitis’s work had suggested that the corpus callosum played no essential role in the interhemispheric integration of information. Thus it could be predicted that WJ would be able to describe the object normally. The animal studies being done at Cal Tech, however, suggested otherwise, and that was where I was putting my money. We flashed a picture to his left hemisphere and I asked, “Did you see anything?”

If you are not engaged in scientific research, you may better understand the electricity of the moment if you think of a roulette wheel spinning around with a couple years’ wages riding on red. You would be hoping that the ball would land on red, anticipation mounting as the wheel begins to slow, with your livelihood and hours of work invested in the outcome. I was hoping that my experimental design would reveal something as of yet unknown, and my anticipation grew as the time approached to flash a picture to the right hemisphere. What would happen? Adrenaline was pumping through my body, my heart was bouncing around like a football at Dartmouth when Bob Blackman was the coach. While the findings are old hat now and fodder for cocktail party discussions, there is no describing my amazement when WJ said, “No, I didn’t see anything.” Not only could he no longer verbally describe, using his left hemisphere, an object presented to his freshly disconnected right hemisphere, but he did not know that it was there at all. The experiment that I had designed as an undergraduate and was able to do as a graduate student had revealed a startling discovery! Christopher Columbus could not have felt any more excited on spotting land than I felt at that moment.

Initially, it seemed, he was blind to stimuli presented to his left visual field. On further investigation, however, this was not the case. I had another trick up my sleeve to ferret out whether the right hemisphere was receiving any visual information. While both hemispheres can guide the facial and upper arm proximal muscles, the separate hemispheres have control over the hand’s distal muscles. Thus, the left hemisphere controls the right hand and the right hemisphere controls the left hand.¹³ If the hands are kept out of sight, then the left brain has no idea what the left hand is up to, and vice versa. I devised an experiment in which WJ could respond using a Morse code key with his left hand (controlled by his right hemisphere) before giving a verbal response (controlled by his left hemisphere). I flashed a light to his right hemisphere; he responded by pressing the key with his left hand when it flashed, but stated that he saw nothing! His right hemisphere was not blind to the stimuli, it saw the flash just fine and could report it using the Morse code key. The only reason for WJ denying the light flash had to be that there was a total disruption of the transfer of information between the two hemispheres!

It turned out that any visual, tactile, proprioceptive, auditory, or olfactory information that was presented to one hemisphere was processed in that half of the brain alone, without any awareness on the part of the other half. The left half did not know what the right half was processing, and vice versa. I found that a split-brain patient’s left hemisphere and language center has no access to the information that is being fed to the right brain. We were being presented a completely new opportunity: to study the presence of an ability in one hemisphere separated from the other hemisphere, not a deficit caused by a lesion.

In later experiments with other patients, we put assorted objects within reach of the left hand but blocked from view. A picture of one of the objects was flashed to the right hemisphere, and the left hand felt among the objects and was able to select the one that had been pictured. When asked, however, “Did you see anything?” or “What is in your left hand?” the patient denied seeing the picture and could not describe what was in his left hand. In another scenario we flashed the picture of a bicycle to the right hemisphere and asked the patient if he had seen anything. Once again he replied in the negative, but his left hand drew a picture of a bike.

It soon became apparent that the right hemisphere was superior at visual spatial skills. While the left hand, under right-hemisphere control, could easily put together a series of colored blocks to match a pattern in a picture flashed to the right hemisphere, the right hand, when the picture was flashed to the left hemisphere, took forever to solve the puzzle. In fact, one patient had to sit on his left hand to prevent it from coming up and trying to solve the problem. The left hand could copy and draw three-dimensional pictures, but the right hand, that one that so easily can write a letter, could not draw a cube. The right hemisphere turned out to be specialized for such tasks as recognizing upright faces, focusing attention, and making perceptual distinctions. The left hemisphere was the intellectual. It specialized in language, speech, and intelligent behavior. After commissurotomy, the verbal IQ of a patient is unchanged,¹⁴ as is his problem-solving capacity. There may be some deficits in free-recall capacity and in other performance measures, but isolating essentially half of the cortex from the dominant left hemisphere caused no major change in cognitive functions. The left remains unchanged from its preoperative capacity, yet the largely disconnected, same-size right hemisphere is seriously impoverished in cognitive tasks. It was becoming apparent that the right hemisphere had its own rich mental life, quite different from that of the left.

We already knew from the study of neurological patients that the brain had two completely different neuronal pathways for generating spontaneous facial expressions and voluntary ones. Only the dominant left hemisphere could generate voluntary facial expressions.¹⁵ In patients who have a particular lesion in their right hemisphere that disrupts communication between the hemispheres, only the right side of the face responds when asked to smile, and the left side remains immobile.^‡ If the same patient is told a joke and spontaneously smiles, however, his facial muscles respond normally bilaterally, because a different pathway is used that doesn’t require communication between the hemispheres. The exact opposite is true with Parkinson patients who have damage in their extrapyramidal systems, the part of the motor system that is involved with the coordination of movements. They are unable to have spontaneous expressions, but can voluntarily control their facial muscles. In our split-brain experiments, we figured that if we gave a command to the left hemisphere of a patient, then the right side of the face should respond first, and this is exactly what happened. When the left hemisphere of a split-brain patient sees the command to smile or frown, the right side of the face responds about 180 milliseconds before the left side responds; the time lag is due to the right hemisphere’s having to get the somatic feedback through subcortical pathways.

All of these findings led to a picture of many specializations distributed around the brain. But another conclusion seemed to follow our studies: With the observation that each hemisphere could possess information outside the realm of awareness of the other half-brain, it suggested that the surgery had induced a state of double consciousness.

Double Consciousness?

Not everyone was excited by these findings. While riding up in the elevator at Rockefeller University, George Miller introduced me to the great American psychologist William Estes and said, “You know Mike, he is the guy that discovered the split-brain phenomenon in humans?” and Estes responded, “Great, now we have two systems we don’t understand!” It appeared that split-brain surgery produced two separate conscious hemispheres and, at the time, we thought there were two conscious systems: mind left and mind right.

In 1968 Roger Sperry wrote: “One of the more general and also more interesting and striking features of this syndrome may be summarized as an apparent doubling in most of the realms of conscious awareness. Instead of the normally unified single stream of consciousness, these patients behave in many ways as if they have two independent streams of conscious awareness, one in each hemisphere, each of which is cut off from and out of contact with the mental experiences of the other. In other words, each hemisphere seems to have its own separate and private sensations; its own perceptions; its own concepts; and its own impulses to act, with related volitional, cognitive, and learning experiences.”¹⁶

Four years later I went overboard and added even more to this: “Over the past ten years we have collected evidence that, following midline section of the cerebrum, common normal conscious unity is disrupted, leaving the split-brain patient with two minds (at least), mind left and mind right. They coexist as two completely conscious entities, in the same manner as conjoined twins are two completely separate persons.”¹⁷

This posed the problem of whether each consciousness had its own protagonist: Were there then two selves? Were there also two free wills? Why aren’t the two halves of the brain conflicting over which half is in charge? Is one half in charge? Were the two selves of the brain trapped in a body that could only be at one place at one time? Which half decided where the body would be? WHY WHY WHY was there this apparent feeling of unity? Was consciousness and the sense of self actually located in one half of the brain?

What Is Consciousness?

It was turning into a theoretical nightmare! And not only that, we were batting around the term consciousness and didn’t really even know what it meant. No one had bothered to look it up. Years later, I decided to, and this is what I found in the 1989 International Dictionary of Psychology. The definition, written by psychologist Stuart Sutherland, was entertaining, if not edifying:

CONSCIOUSNESS: The having of perceptions, thoughts, and feelings: awareness. The term is impossible to define except in terms that are unintelligible without a grasp of what consciousness means. Consciousness is a fascinating but elusive phenomenon; it is impossible to specify what it is, what it does, or why it evolved. Nothing worth reading has been written about it.¹⁸

That last bit was a relief to know, because more than eighteen thousand articles had been written about it the last time I did a Medline search, and Sutherland just told me not to bother reading them. You know you are treading on thin ice dealing with a topic when professionals are nervous about discussing it, and everybody else seems to think they understand it or has an opinion about it—something like explaining sex to your kids. At least if you are a physicist, the guy on the street isn’t acting like he has string theory wired. The trouble with consciousness is that it has a mystique about it; we somehow want to treat it differently than, say, something like memory or instinct, which are also rather nebulous. We have not yet seen a physical instance in the brain of either of those but we have been able to slowly chip away at them, so I see no problem in tackling consciousness without having an exact definition. Neuroscientists are not alone with such problems. Researchers at the Santa Fe Institute recently told me that their current concept of the gene bears a weak resemblance to the original conception.

So while during the 1970s we were stuck with the idea that the split-brain patient was left with two conscious systems, Sir John Eccles and Donald MacKay were having none of it. Eccles, in his Gifford lectures in 1979 argued that the right hemisphere had a limited kind of self-consciousness, but not enough to bestow personhood, which resided in the left hemisphere. Donald MacKay was not satisfied with the idea, either, and commented in his Gifford lecture, “But I would say that the idea that you can create two individuals merely by splitting the organizing system at the level of the corpus callosum which links the cerebral hemispheres is unwarranted by any of the evidence so far. . . . It is also in a very important sense implausible.”¹⁹

Well, science marches on, and we have left the idea of dichotomous mental systems in the dust, although, annoyingly, it still looms large in the popular press. With more patients to test, different testing methods, fancier equipment and brain scanners, much more data, the benefit of our own cerebral flexibility, and more smart people asking questions and designing experiments, we have moved toward the idea of a plethora of systems, some within a hemisphere and some distributed across hemispheres. We no longer think of the brain as being organized into two conscious systems at all but into multiple dynamic mental systems.

Dichotomous Brain Theory Bites the Dust

The theory began to crack apart when we started to test the cognitive abilities of the right hemisphere and realized that the two hemispheres are not coequal. We had come to know the left hemisphere to be this whiz kid who could talk and understand language, while the right didn’t talk and had a very limited understanding of language. So we began to give simple, first-grade-type conceptual tests to the right hemisphere using pictures and simple words it could understand. For example, when we flashed the word pan to the right hemisphere, the left hand would point to a pan. Next, we flashed the word water, and the left hand pointed to water. So far, so good: the right hemisphere could read the words and relate the words to the pictures. When we flashed the two together, however, the left hand could not put them together into the concept of water in a pan, and pointed to the empty pan picture. This water/pan task was quickly solved by the left hemisphere. It turns out that the right hemisphere is poor at making inferences. We tried presenting a problem only using pictures, such as flashing a picture of a match to the right hemisphere, followed by a picture of a woodpile, and then asking it to pick out one of six pictures that reflected the causal relationship. It could not pick out the picture of the burning woodpile. Even when using more visual-spatial stimuli, such as when we presented a form in the shape of a U and then asked which of a series of shapes would turn the U into a square, the right hemisphere was dismal at solving the puzzle. The left hemisphere, however, easily solved this problem. This difference was still present when some of our patients actually began to speak out of their right hemispheres and develop quite an extensive vocabulary: The right hemisphere still was unable to draw inferences.

This led us to the obvious conclusion that the conscious experience of the two hemispheres was very different. Among other things, one lived in a world where it could draw inferences, and the other did not. The right hemisphere lives a literal life. When asked to decide whether various items appeared in a series of items previously shown to it, the right hemisphere is able to correctly identify items it saw previously and to reject new items. “Yes, there was the plastic spoon, the pencil, the eraser, and the apple.” The left hemisphere, however, tends to falsely recognize new items when they are similar to previously presented items, presumably because they fit into the schema it has constructed.²⁰ “Yep, they are all there: the spoon [but we substituted a silver one for a plastic one], the pencil [although this one is mechanical and the other was not], the eraser [though it is gray and not pink], and the apple.” As a consequence of not being able to draw inferences, the right hemisphere is limited by what it can have feelings about. A box of candy presented to the right hemisphere is a box of candy. The left hemisphere can infer all sorts of things from this gift.

If we had had Marcellus^§ around in our lab, perhaps he would have said, “There is something rotten in the state of dichotomous brain theory!” and we would have been forced to agree. Our findings gradually indicated to us that both halves of the brain had specializations, but each half of the brain was not equally conscious, that is, it was not conscious of the same things, and not equally capable of performing tasks. This was rotten enough for dichotomous brain theory, but absolutely stinking for the existing concepts about the unity of consciousness. Back to the drawing board with the question, Where is this conscious experience coming from? Does the information get processed and then channeled through one kind of conscious activation center that makes subjective experiences aware to you and me, or is it organized differently? The scales were tipping toward a different type of organization; a modular organization with multiple subsystems. We began to doubt that a single mechanism existed that enables conscious experience, but rather were heading toward the idea that conscious experience is the feeling engendered by multiple modules, each of which has specialized capacities. Since we were finding specialized capacities in all different regions of the brain and since we had seen that conscious experience was closely associated with the part of the cortex involved with a capacity, we came to understand that consciousness is distributed everywhere across the brain. Such an idea was directly contrary to that of John Eccles, who had championed the left hemisphere as the site of consciousness.

The essential observation that allows me to make this point is this: Right after split-brain surgery, when you ask a patient, “How are you?” The answer is “Fine.” Then you ask,” Do you notice anything different?” and the reply is “No.” How could this be? You must remember that as the patient is looking at you, he cannot describe anything in the left part of his visual field. The left hemisphere, which is telling you that all is fine, cannot see half of what is in front of him and is not concerned about it. To compensate for this when not under testing conditions, split-brain patients will unconsciously move their heads to input visual information to both hemispheres. If you woke up from most other types of surgery and couldn’t see anything in your left visual field, you would certainly be complaining about it, “Ahh, doc, I can’t see anything on the left—what’s up with that?” These patients never comment on this. Even after years of frequent testing, when asked if they know why they are being tested, they have no sense that they are special, no sense that anything is different about them or their brain. Their left brain does not miss their right brain or any of its functions. This has led us to realize that in order to be conscious about a particular part of space, the part of the cortex that processes that part of space is involved. If it is not functioning, then that part of space no longer exists for that brain or that person. If you are talking out of your left hemisphere, and I am asking you about your awareness of things in the left visual field, that processing is over in the disconnected right hemisphere and that hemisphere is conscious about it, but your left hemisphere is not. That area simply does not exist for the left hemisphere. It doesn’t miss what it doesn’t have processing for, just like you don’t miss some random person that you have never heard of.

This started us thinking that maybe consciousness is really a local phenomenon, and it is due to local processes associated with a particular sensory moment in left space or right space. This idea has allowed us to explain some of the previously inexplicable behaviors encountered in neurological patients.

Why do some people, who suddenly become blind in a large portion of their visual field complain about—are conscious of—it (“Hey, I can’t see anything on my left side, what’s going on?”) and others don’t say a word about—aren’t conscious of—their sudden visual loss? The complainer’s lesion is somewhere along his optic nerve, which carries information about vision to the visual cortex, the part of the brain that processes this information. If no information is coming in to a portion of his visual cortex, he is left with a blind spot and complains. The noncomplainer, however, has a lesion in the visual associative cortex (the part of the cortex associated with advanced stages of visual information processing that produces the visual experience) itself and not the optic nerve. The lesion also produces the very same blind spot, but the patient does not usually complain. Just like our split-brain patient does not complain. Why not? The visual cortex is the part of the brain that represents, or assembles the pictures from, the visual world. Each part of the visual field has a corresponding area in the visual cortex. So, for instance, there is an area that ordinarily asks, “What is going on to the left of visual center?” With a lesion on the optic nerve, this brain area is functioning; when it cannot get any information from the nerve, it puts up a squawk—“something is wrong, I am not getting any input!” When that very area of the associative visual cortex has a lesion, however, the patient’s brain no longer has an area responsible for processing what is going on in that part of the visual field; for that patient that part of the visual field ceases to exist consciously; there is no squawk at all. The patient with the central lesion does not have a complaint, because the part of the brain that might complain has been incapacitated, and no other part takes over. The logical conclusion to these observations is that phenomenal consciousness, that feeling you have about being conscious of some perception, is generated by local processes that are uniquely involved with a specific activity.

I am suggesting that the brain has all kinds of local consciousness systems, a constellation of them, which are enabling consciousness. Although the feelings of consciousness appear to be unified to you, they are given form by these vastly separate systems. Whichever notion you happened to be conscious of at a particular moment is the one that comes bubbling up, the one that becomes dominant. It’s a dog-eat-dog world going on in your brain with different systems competing to make it to the surface to win the prize of conscious recognition.

For instance, a few years after her surgery, one of our split-brain patients developed the ability to speak simple words out of her right hemisphere. This presents an interesting scenario, because it becomes a bit of a challenge to know which hemisphere is talking when she is speaking. In one interview she described her experience of looking at pictures of objects that were being flashed up on a screen in her different visual fields, “On this side [pointing to a picture on the left of the screen, flashed to her right hemisphere] I see the picture, I see everything more clearly; on my right side I feel more confident, in a way, with my answer.” From previous testing, we knew that the right hemisphere was better at all kinds of perceptual judgments, so we knew that the statement about seeing more clearly was coming from her right hemisphere; and her confident speech center in her left hemisphere made the other. She put these two stories together, one from each hemisphere, but to the listener, it sounds like a completely unified statement coming from one unified system. We know intellectually, however, that it is information coming from two separate systems being woven together by our minds listening to her.

How Does It Work?

How did we become so decentralized and end up with all these multiple systems? The answer harks back to what we touched upon in the last chapter in discussing the changes in connectivity patterns in big brains. With larger brains, more neurons, and increasing network size, proportional connectivity decreases. The number of neurons that each neuron is connected to remains about the same: The neuron does not connect up with more neurons as the total number rises for a few practical and neuroeconomical reasons. One is that if each neuron were connected to every other one, our brains would be gigantic. In fact two computational neuroscientists, Mark Nelson and James Bower, figured out that if our brains were fully connected and were the shape of a sphere, they would have to be 20 kilometers in diameter!²¹ Talk about having a big head. The metabolic costs would also be too great, with our brains constantly yelling “Feed me!” Currently our brains expend about 20 percent of the energy our bodies consume.²² Imagine how much energy it would take to run a brain that was 20 kilometers across! (At least it would solve the obesity problem.) With long axons connecting neurons in distant parts of the brain, the processing speed would slow down, making synchronizing activity difficult. It would also require increased dendrite size in order to increase the number of synapses, and this would alter the electrical properties of the neuron, because the branching of the dendrites influences how it integrates electrical input from other neurons. No, our neurons could not feasibly all connect to each other; another solution was employed by our evolving brain.

Neurobiologist Georg Striedter, taking into account what is currently known about comparative neuroanatomy and connectivity in mammals, suggests that certain neuronal wiring “laws” apply to the evolutionary development of the large human brain.²³

• Decreased connectivity with increasing network size: By maintaining absolute connectivity, not proportional connectivity, large brains actually became more sparsely interconnected, but they had two tricks up their sleeve:

• Minimizing connection lengths: They maintained local connectivity using the shortest of connections.²⁴ Thus, less room was taken up with axons traveling back and forth, less energy was required to maintain the lines, and signaling was faster because it traveled over short distances. This set the stage for local networks to divide up and specialize, forming multiple clusters of processing modules. With all this separate processing, however, different parts of the brain must still exchange information and therefore, . . .

• Not all connections are minimized, but some very long connections between distant sites are retained. Primate brains have developed a “small-world architecture”: many short, fast, local connections (a high degree of local connectivity), with a few long-distance ones to communicate their processing (a small number of steps to connect any two).²⁵ This design allows both a high degree of efficient local processing (modularity), and at the same time, quick communication to the global network. It is common to many complex systems, including human social relations.²⁶

Our decentralization was the outcome of having a large brain and the neuroeconomies which allowed it to function: less dense connections forced the brain to specialize, create local circuits, and automate. The end result is thousands of modules, each doing their own thing.

Our conscious awareness is the mere tip of the iceberg of nonconscious processing. Below our level of awareness is the very busy nonconscious brain hard at work. Not hard for us to imagine are the housekeeping jobs the brain constantly juggles to keep homeostatic mechanisms up and running, such as our heart beating, our lungs breathing, and our temperature just right. Less easy to imagine, but being discovered left and right over the past fifty years, are the myriads of nonconscious processes smoothly putt-putting along. Think about it. To begin with there are all the automatic visual and other sensory processing we have talked about. In addition, our minds are always being unconsciously biased by positive and negative priming processes, and influenced by category identification processes. In our social world, coalitionary bonding processes, cheater detection processes, and even moral judgment processes (to name only a few) are cranking away below our conscious mechanisms. With increasingly sophisticated testing methods, the number and diversity of identified processes is only going to multiply.

Our Brain’s Job Description

What we always must keep in mind is that our brains, hence all these processes, have been sculpted by evolution to enable us to make better decisions that increase our reproductive success. Our brain’s job description is to get its genes into the next generation. Years of split-brain research have made clear to us that the brain is not an all-purpose computing device, but a device made up of an enormous number of serially wired specialty circuits, all running in parallel and distributed across the brain to make those better decisions.²⁷ This network allows all sorts of simultaneous nonconscious processing to go on²⁸ and is what enables you to do things such as drive a car. You are simultaneously keeping in mind your route, judging distances between your car and those around you, your speed, when to brake, when to speed up, when to clutch and shift gears, remembering and following the traffic laws, and singing along with Bob Dylan on the radio, all at the same time. Pretty impressive!

Germane to our current discussion, however, is that while hierarchical processing takes place within the modules, it is looking like there is no hierarchy among the modules.^¶ All these modules are not reporting to a department head, it is a free-for-all, self-organizing system. This is not the network that Gifford lecturer and neuroscientist Donald MacKay envisioned. He thought that conscious agency was the outcome of a central supervisory activity: “Conscious experience does not have its origin in any one of the participating brain nuclei, but in the positive feedback chain-mesh that is set up when the evaluative system becomes it own evaluator.”

Who or What Is in Charge?

Yet we are still confronted with the question of why do we feel so unified and in control? We don’t feel like there is a pack of snarling dogs in our brains. And why, for those who suffer from schizophrenia, does it feel as if someone else is in control of their actions or thoughts? Your friends at the cocktail party with no knowledge of psychology or neuroscience are fascinated or disbelieving if told about these nonconscious processes, only because they aren’t apparent to the individual’s personal experience. It’s all very counterintuitive to us humans, with our strong sense of being unified into one self and feeling in control of our actions. Even among ourselves, we neuroscientists are having a hard time dispelling the idea of a homunculus, some central processor, calling the shots in our brains, such as Donald MacKay’s proposal that we had a supervisory system overseeing our intentions and behavior that made adjustments to our environment. We may not actually say the “H” word, but use euphemisms such as “executive function” or “top-down processing.” How can a system work without a head honcho and why does it feel like there is one? The answer to the first question may be that our brain functions as a complex system.

Complex Systems

A complex system is composed of many different systems that interact and produce emergent properties that are greater than the sum of their parts and cannot be reduced to the properties of the constituent parts. The classic example that is easily understandable is traffic. If you look at car parts, you won’t be able to predict a traffic pattern. You cannot predict it by looking at the next higher state of organization, the car, either. It is from the interaction of all the cars, their drivers, society and its laws, weather, roads, random animals, time, space, and who knows what else that traffic emerges.

In the past, it was thought that the reason such systems were complex was that not enough was known about them and that once all the variables were identified and understood, they would be completely predictable. Such a view is fully deterministic. Over the years, however, experimental data and theories are questioning such a conclusion. In fact, it is becoming accepted that complexity itself is rooted in the laws of physics, and we will discuss this further in chapter four. The study of complex systems is in itself complex and interdisciplinary, including not just physicists and mathematicians, but economists, molecular biologists up to population biologists, computer scientists, socialists, psychologists, and engineers.

Examples of complex systems are popping up all over the place: weather and climate in general, the spread of infectious disease, ecosystems, the Internet, and the human brain. Ironically for psychology in its quest to fully understand behavior, the signature phenomenon of a complex system “is the multiplicity of possible outcomes, endowing it with the capacity to choose, to explore and to adapt.”²⁹ The implications of the idea that the human brain is a complex system has repercussions for discussions about free will, neuroscience and the law, and determinism, some of which we will discuss in later chapters.

Relevant to our current question about feeling unified and in control is an important point that Northwestern University’s physicist Luis Amaral and chemical engineer Julio Ottino make: “The common characteristic of all complex systems is that they display organization without any external organizing principle being applied.”³⁰ That means no head honcho, no homunculus.

All you have to think about is the Google ad auction to realize you can have a system that looks like someone is in charge, but no one is. It is run on algorithms. The ad auction has three selfish parties to please, the advertiser who wants to sell a product, thus needs a relevant ad; the user who wants relevant ads so he doesn’t waste time; and Google, which wants satisfied advertisers and users to return for more business. Every time a user makes a query on Google, Google runs an auction for clicks. Advertisers have to pay only when they get a click. How this works is the advertisers provide a list of keywords, ads, and bids for how much they will pay when a person clicks their ad; however, the advertiser does not pay what he bids, he pays the bid of the advertiser that is below him in rank; that way he pays the minimum amount that is necessary to maintain ranking position. The Google user enters a search query, and Google compiles a list of ads whose keywords match the query. Google wants to be sure that the ads shown to users have a high quality. Quality is judged on three components. The most important is the click-through rate. Thus every time that a user clicks an ad, he votes on it. The second component is relevancy. Google looks to see how well the key words and context of an ad match up to the search query. It only uses relevant ads, saving shoppers from irrelevant ads by preventing ads from paying their way on to a search unrelated to their product. The third component is the advertiser’s landing page quality, which should be relevant, easily navigable, and transparent. Ad rank is determined by the bid multiplied by the page quality. The beauty of the design is that the selfish motives of each party are harnessed and, voilà! As Google’s chief economist points out, the most productive interaction results.³¹ The system, while appearing to be run by a single controller, runs without one, by an algorithm.

Why do we feel so unified? We have discovered something in the left brain, another module that takes all the input into the brain and builds the narrative. We call this the interpreter module, and that is the topic of the next chapter.

^* The vascular structure at the base of the brain.

^** Cofounded by Hughlings Jackson.

^† Galton, a man of many firsts, also devised the classification system used to identify fingerprints and figured out the probabilities that two people would share the same fingerprint.

^†† Later it was concluded that they had developed compensatory pathways.

^‡ The left hemisphere predominantly controls the facial muscles on the right, and right hemisphere controls those on the left.

^§ Thanks to William Shakespeare.

^¶ Except in the sensory system. See: Bassett, D. S., Bullmore, E., Verchinski, B. A., Mattay, V. S., Weinberger, D. R., Meyer-Lindenberg, A. (2008). Hierarchical organization of human cortical networks in health and schizophrenia. Journal of Neuroscience, 28(37), 9239–9248.