When shall we three meet again . . . ?


THE BRAIN of a fish isn’t much. A fish has a notochord or spinal cord, which it shares with even humbler invertebrates. A primitive fish also has a little swelling at the front end of the spinal cord, which is its brain. In higher fish the swelling is further developed but still weighs no more than a gram or two. That swelling corresponds in higher animals to the hindbrain or brainstem and the midbrain.


The brain of modern fish are chiefly midbrain, with a tiny forebrain; in modern amphibians and reptiles, it is the other way around (see figure on page 55). And yet fossil endocasts of the earliest known vertebrates show that the principal divisions of the modern brain (hind-brain, midbrain and forebrain, for example) were already established.


Five hundred million years ago, swimming in the primeval seas, there were fishy creatures called ostracoderms and placoderms, whose brains had recognizably the same major divisions as ours. But the relative size and importance of these components, and even their early functions, were certainly very different from today. One of the most engaging views of the subsequent evolution of the brain is a story of the successive accretion and specialization of three further layers surmounting the spinal cord, hindbrain and midbrain. After each evolutionary step, the older portions of the brain still exist and must still be accommodated. But a new layer with new functions has been added.

The principal contemporary exponent of this view is Paul MacLean, chief of the Laboratory of Brain Evolution and Behavior of the National Institute of Mental Health. One hallmark of MacLean’s work is that it encompasses many different animals, ranging from lizards to squirrel monkeys.

Another is that he and his colleagues have studied carefully the social and other behavior of these animals to improve their prospects of discovering what part of the brain controls what sort of behavior.

Squirrel monkeys with “gothic” facial markings have a kind of ritual or display which they perform when greeting one another. The males bare their teeth, rattle the bars of their cage, utter a high-pitched squeak, which is possibly terrifying to squirrel monkeys, and lift their legs to exhibit an erect penis. While such behavior would border on impoliteness at many contemporary human social gatherings, it is a fairly elaborate act and serves to maintain dominance hierarchies in squirrel-monkey communities.

MacLean has found that a lesion in one small part of a squirrel monkey’s brain will prevent this display while leaving a wide range of other behavior intact, including sexual and combative behavior. The part that is involved is in the oldest part of the forebrain, a part that humans as well as other primates share with out mammalian and reptilian ancestors. In non-primate mammals and in reptiles, comparable ritualized behavior seems to be controlled in the same part of the brain, and lesions in this reptilian component can impair other automatic types of behavior besides ritual-for example, walking or running.

The connection between sexual display and position in a dominance hierarchy can be found frequently among the primates. Among Japanese macaques, social class is maintained and reinforced by daily mounting: males of lower caste adopt the characteristic submissive sexual posture of the female in oestrus and are briefly and ceremonially mounted by higher-caste males. These mountings are both common and perfunctory. They seem to have little sexual content but rather serve as easily understood symbols of who is who in a complex society.

In one study of the behavior of the squirrel monkey, Caspar, the dominant animal in the colony and by far the most active displayer, was never seen to copulate, although he accounted for two-thirds of the genital display in the colony - most of it directed toward other adult males. The fact that Caspar was highly motivated to establish dominance but insignificantly motivated toward sex suggests that while these two functions may involve identical organ systems, they are quite separate. The scientists studying this colony concluded:

“Genital display is therefore considered the most effective social signal with respect to group hierarchy. It is ritualized and seems to acquire the meaning, ‘I am the master.’ It is most probably derived from sexual activity, but it is used for social communication and separated from reproductive activity. In other words, genital display is a ritual derived from sexual behavior but serving social and not reproductive purposes.”

In a television interview in 1976, a professional football player was asked by the talk-show host if it was embarrassing for football players to be together in the locker room with no clothes on. His immediate response:

“We strut! No embarrassment at all. It’s as if we’re saying to each other, ‘Let’s see what you got, man!’ - except for a few, like the specialty team members and the water boy.”

The behavioral as well as neuroanatomical connections between sex, aggression and dominance are borne out in a variety of studies. The mating rituals of great cats and many other animals are barely distinguishable, in their early stages, from fighting. It is a commonplace that domestic cats sometimes purr loudly and perversely while their claws are slowly raking over upholstery or lightly clad human skin. The use of sex to establish and maintain dominance is sometimes evident in human heterosexual and homosexual practices (although it is not, of course, the only element in such practices), as well as in many “obscene” utterances.


Consider the peculiar circumstance that the most common two-word verbal aggression in English, and in many other languages, refers to an act of surpassing physical pleasure; the English form probably comes from a Germanic and Middle Dutch verb fok-ken, meaning “to strike.” This otherwise puzzling usage can be understood as a verbal equivalent of macaque symbolic language, with the initial word “I” unstated but understood by both parties. It and many similar expressions seem to be human ceremonial mountings. As we will see, such behavior probably extends much farther back than the monkeys, back through hundreds of millions of years of geological time.

From experiments such as those with squirrel monkeys, MacLean has developed a captivating model of brain structure and evolution that he calls the triune brain. “We are obliged,” he says, “to look at ourselves and the world through the eyes of three quite different mentalities,” two of which lack the power of speech. The human brain, MacLean holds,

“amounts to three interconnected biological computers,” each with “its own special intelligence, its own subjectivity, its own sense of time and space, its own memory, motor, and other functions.”

Each brain corresponds to a separate major evolutionary step. The three brains are said to be distinguished neuroanatomically and functionally, and contain strikingly different distributions of the neurochemicals dopamine and cholinesterase.

At the most ancient part of the human brain lies the spinal cord; the medulla and pons, which comprise the hindbrain; and the midbrain. This combination of spinal cord, hindbrain and midbrain MacLean calls the neural chassis. It contains the basic neural machinery for reproduction and self-preservation, including regulation of the heart, blood circulation and respiration. In a fish or an amphibian it is almost all the brain there is. But a reptile or higher animal deprived of its forebrain is, according to MacLean, “as motionless and aimless as an idling vehicle without a driver.”

Indeed, grand mal epilepsy can, I think, be described as a disease in which the cognitive drivers are. all turned off because of a kind of electrical storm in the brain, and the victim is left momentarily with nothing operative but his neural chassis. This is a profound impairment, temporarily regressing the victim back several hundreds of millions of years. The ancient Greeks, whose name for the disease we still use, recognized its profound character and called it the disease inflicted by the gods.

MacLean has distinguished three sorts of drivers of the neural chassis. The most ancient of them surrounds the midbrain (and is made up mostly of what neuroanatomists call the olfactostriatum, the corpus striatum, and the globus pallidus). We share it with the other mammals and the reptiles. It probably evolved several hundred million years ago. MacLean calls it the reptilian or R-complex. Surrounding the R-complex is the limbic system, so called because it borders on the underlying brain. (Our arms and legs are called limbs because they are peripheral to the rest of the body.)


We share the limbic system with the other mammals but not, in its full elaboration, with the reptiles. It probably evolved more than one hundred and fifty million years ago. Finally, surmounting the rest of the brain, and clearly the most recent evolutionary accretion, is the neocortex. Like the higher mammals and the other primates, humans have a relatively massive neocortex. It becomes progressively more developed in the more advanced mammals. The most elaborately developed neocortex is ours (and the dolphins’ and whales’). It probably evolved several tens of millions of years ago, but its development accelerated greatly a few million years ago when humans emerged.


A schematic representation of this picture of the human brain is shown opposite, and a comparison of the limbic system with the neocortex in three contemporary mammals is shown above. The concept of the triune brain is in remarkable accord with the conclusions, drawn independently from studies of brain-body mass ratios in the previous chapter, that the emergence of mammals and of primates (especially humans) was accompanied by major bursts in brain evolution.

It is very difficult to evolve by altering the deep fabric of life; any change there is likely to be lethal. But fundamental change can be accomplished by the addition of new systems on top of old ones. This is reminiscent of a doctrine which was called recapitulation by Ernst Haeckel, a nineteenth-century German anatomist, and which has gone through various cycles of scholarly acceptance and rejection. Haeckel held that in its embryological development, an animal tends to repeat or recapitulate the sequence that its ancestors followed during their evolution. And indeed in human intrauterine development we run through stages very much like fish, reptiles and nonprimate mammals before we become recognizably human.

The fish stage even has gill slits, which are absolutely useless for the embryo who is nourished via the umbilical cord, but a necessity for human embryology: since gills were vital to our ancestors, we run through a gill stage in becoming human. The brain of a human fetus also develops from the inside out, and, roughly speaking, runs through the sequence: neural chassis, R-complex, limbic system and neocortex.

The reason for recapitulation may be understood as follows:

Natural selection operates only on individuals, not on species and not very much on eggs or fetuses. Thus the latest evolutionary change appears postpartum. The fetus may have characteristics, like the gill slits in mammals, that are entirely maladaptive after birth, but as long as they cause no serious problems for the fetus and are lost before birth, they can be retained. Our gill slits are vestiges not of ancient fish but of ancient fish embryos.


Many new organ systems develop not by the addition and preservation but by the modification of older systems, as, for example, the modification of fins to legs, and legs to flippers or wings; or feet to hands to feet; or sebaceous glands to mammary glands; or gill arches to ear bones; or shark scales to shark teeth. Thus evolution by addition and the functional preservation of the preexisting structure must occur for one of two reasons-either the old function is required as well as the new one, or there is no way of bypassing the old system that is consistent with survival.

There are many other examples in nature of this sort of evolutionary development. To take an almost random case, consider why plants are green. Green-plant photosynthesis utilizes light in the red and the violet parts of the solar spectrum to break down water, build up carbohydrates and do other planty things. But the sun gives off more light in the yellow and the green part of the spectrum than in the red or violet.


Plants with chlorophyll as their only photosynthetic pigment are rejecting light where it is most plentiful. Many plants seem belatedly to have “noticed” this and have made appropriate adaptations. Other pigments, which reflect red light and absorb yellow and green light, such as carotenoids and phycobilins, have evolved. Well and good. But have those plants with new photo-synthetic pigments abandoned chlorophyll? They have not.


The figure on page 61 shows the photosynthetic factory of a red alga. The striations contain the chlorophyll, and the little spheres nestling against these striations contain the phycobilins, which make a red alga red. Conservatively, these plants pass along the energy they acquire from green and yellow sunlight to the chlorophyll pigment that, even though it has not absorbed the light, is still instrumental in bridging the gap between light and chemistry in all plant photosynthesis.


Nature could not rip out the chlorophyll and replace it with better pigments; the chlorophyll is woven too deeply into the fabric of life. Plants with accessory pigments are surely different. They are more efficient. But there, still working, although with diminished responsibilities, at the core of the photosynthetic process is chlorophyll.


The evolution of the brain has, I think, proceeded analogously. The deep and ancient parts are functioning still.


If the preceding view is correct, we should expect the R-complex in the human brain to be in some sense performing dinosaur functions still; and the limbic cortex to be thinking the thoughts of pumas and ground sloths. Without a doubt, each new step in brain evolution is accompanied by changes in the physiology of the preexisting components of the brain. The evolution of the R-complex must have seen changes in the midbrain, and so on. What is more, we know that the control of many functions is shared in different components of the brain. But at the same time it would be astonishing if the brain components beneath the neocortex were not to a significant extent still performing as they did in our remote ancestors.

MacLean has shown that the R-complex plays an important role in aggressive behavior, territoriality, ritual and the establishment of social hierarchies. Despite occasional welcome exceptions, this seems to me to characterize a great deal of modern human bureaucratic and political behavior. I do not mean that the neocortex is not functioning at all in an American political convention or a meeting of the Supreme Soviet; after all, a great deal of the communication at such rituals is verbal and therefore neocortical. But it is striking how much of our actual behavior -as distinguished from what we say and think about it- can be described in reptilian terms. We speak commonly of a “cold-blooded” killer. Machiavelli’s advice to his Prince was “knowingly to adopt the beast.”

In an interesting partial anticipation of these ideas, the American philosopher Susanne Langer wrote:

“Human life is shot through and through with ritual, as it is also with animalian practices. It is an intricate fabric of reason and rite, of knowledge and religion, prose and poetry, fact and dream....  Ritual, like art, is essentially the active termination of a symbolic transformation of experience. It is born in the cortex, not in the ‘old brain’; but it is born of an elementary need of that organ, once the organ has grown to human estate.”

Except for the fact that the R-complex is in the “old brain,” this seems to be right on target.

I want to be very clear about the social implications of the contention that reptilian brains influence human actions. If bureaucratic behavior is controlled at its core by the R-complex, does this mean there is no hope for the human future? In human beings, the neo-cortex represents about 85 percent of the brain, which is surely some index of its importance compared to the brainstem, R-complex and limbic system. Neuro-anatomy, political history, and introspection all offer evidence that human beings are quite capable of resisting the urge to surrender to every impulse of the reptilian brain.

There is no way, for example, in which the Bill of Rights of the U.S. Constitution could have been recorded, much less conceived, by the R-complex. It is precisely our plasticity, our long childhood, that prevents a slavish adherence to genetically preprogrammed behavior in human beings more than in any other species. But if the triune brain is an accurate model of how human beings function, it does no good whatever to ignore the reptilian component of human nature, particularly our ritualistic and hierarchical behavior.


On the contrary, the model may help us to understand what human beings are about.


(I wonder, for example, whether the ritual aspects of many psychotic illnesses-e. g., hebephrenic schizophrenia-could be the result of hyperactivity of some center in the R-complex, or of a failure of some neocortical site whose function is to repress or override the R-complex. I also wonder whether the frequent ritualistic behavior in young children is a consequence of the still-incomplete development of their neocortices.)

In a curiously apt passage, G. K. Chesterton wrote:

“You can free things from alien or accidental laws, but not from the laws of their own nature. . . . Do not go about . . . encouraging triangles to break out of the prison of their three sides. If a triangle breaks out of its three sides, its life comes to a lamentable end.”

But not all triangles are equilateral. Some substantial adjustment of the relative role of each component of the triune brain is well within our powers.


The limbic system appears to generate strong or particularly vivid emotions. This immediately suggests an additional perspective on the reptilian mind: it is not characterized by powerful passions and wrenching contradictions but rather by a dutiful and stolid acquiescence to whatever behavior its genes and brains dictate.

Electrical discharges in the limbic system sometimes result in symptoms similar to those of psychoses or those produced by psychedelic or hallucinogenic drugs. In fact, the sites of action of many psychotropic drugs are in the limbic system. Perhaps it controls exhilaration and awe and a variety of subtle emotions that we sometimes think of as uniquely human.

The “master gland,” the pituitary, which influences other glands and dominates the human endocrine system, is an intimate part of the limbic region. The mood-altering qualities of endocrine imbalances give us an important hint about the connection of the limbic system with states of mind. There is a small almond-shaped inclusion in the limbic system called the amygdala which is deeply involved in both aggression and fear.

Electrical stimulation of the amygdala in placid domestic animals can rouse them to almost unbelievable states of fear or frenzy. In one case, a house cat cowered in terror when presented with a small white mouse. On the other hand, naturally ferocious animals, such as the lynx, become docile and tolerate being petted and handled when their amygdalas are extirpated. Malfunctions in the limbic system can produce rage, fear or sentimentality that have no apparent cause.


Natural hyperstimulation may produce the same results: those suffering from such a malady find their feelings inexplicable and inappropriate; they may be considered mad.

At least some of the emotion-determining role of such limbic endocrine systems as the pituitary amygdala, and hypothalamus is provided by small hormonal proteins which they exude, and which affect other areas of the brain. Perhaps the best-known is the pituitary protein, ACTH (adrenocorticotropic hormone), which can affect such diverse mental functions as visual retention, anxiety and attention span.


Some small hypothalamic proteins have been identified tentatively in the third ventricle of the brain, which connects the hypothalamus with the thalamus, a region also within the limbic system. The stunning pictures on page 65, taken with an electron microscope, show two close-ups of action in the third ventricle. The diagram on page 73 may help clarify some of the brain anatomy just described.

There are reasons to think that the beginnings of altruistic behavior are in the limbic system. Indeed, with rare exceptions (chiefly the social insects), mammals and birds are the only organisms to devote substantial attention to the care of their young-an evolutionary development that, through the long period of plasticity which it permits, takes advantage of the large information-processing capability of the mammalian and primate brains. Love seems to be an invention of the mammals.*

* This rule on the relative parental concern of mammals and reptiles is, however, by no means without exceptions. Nile crocodile mothers carefully put their fresh hatchlings in their mouths and carry them to the comparative safety of the river waters; while Serengeti male lions will, upon newly dominating a pride, destroy all the resident cubs. But on the whole, mammals show a strikingly greater degree of parental care than do reptiles. The distinction may have been even more striking one hundred million years ago.

Much in animal behavior substantiates the notion that strong emotions evolved chiefly in mammals and to a lesser extent in birds. The attachment of domestic animals to humans is, I think, beyond question. The apparently sorrowful behavior of many mammalian mothers when their young are removed is well-known. One wonders just how far such emotions go. Do horses on occasion have glimmerings of patriotic fervor? Do dogs feel for humans something akin to religious ecstasy? What other strong or subtle emotions are felt by animals that do not communicate with us?

The oldest part of the limbic system is the olfactory cortex, which is related to smell, the haunting emotional quality of which is familiar to most humans. A major component of our ability to remember and recall is localized in the hippocampus, a structure within the limbic system. The connection is clearly shown by the profound memory impairment that results from lesions of the hippocampus. In one famous case, H. M., a patient with a long history of seizures and convulsions, was subjected to a bilateral extirpation of the entire region about the hippocampus in a successful attempt to reduce their frequency and severity. He immediately became amnesic. He retained good perceptual skills, was able to learn new motor skills and experienced some perceptual learning but essentially forgot everything more than a few hours old.


His own comment was “Every day is alone in itself-whatever enjoyment I’ve had and whatever sorrow I’ve had.” He described his life as a continuous extension of the feeling of disorientation many of us have upon awakening from a dream, when we have great difficulty remembering what has just happened. Remarkably enough, despite this severe impairment, his IQ improved after his hippocampectomy. He apparently could detect smells but had difficulty identifying by name the source of the smell. He also exhibited an apparent total disinterest in sexual activity.

In another case, a young American airman was injured in a mock duel with another serviceman, when a miniature fencing foil was plunged into his right nostril, puncturing a small part of the limbic system immediately above. This resulted in a severe impairment of memory, similar to but not so severe as H. M.’s; a wide range of his perceptual and intellectual abilities was unaffected. His memory impairment was particularly noticeable with verbal material. In addition, the accident seems to have rendered him both impotent and unresponsive to pain. He once walked barefoot on the sun-heated metal deck of a cruise ship, without realizing that his feet were being badly burned until his fellow passengers complained of the uncomfortable odor of charring flesh. On his own, he was aware of neither the pain nor the smell.

From such cases, it seems apparent that so complex a mammalian activity as sex is controlled simultaneously by all three components of the triune brain - the R-complex, the limbic system and the neocortex. (We have already mentioned the involvement of the R-complex and the limbic system in sexual activity. Evidence for involvement of the neocortex can be easily obtained by introspection.)

One segment of the old limbic system is devoted to oral and gustatory functions; another, to sexual functions. The connection of sex with smell is very ancient, and is highly developed in insects-a circumstance that offers insight into both the importance and the disadvantages of reliance on smell in our remote ancestors.

I once witnessed an experiment in which the head of a green bottle fly was connected by a very thin wire to an oscilloscope that displayed, in a kind of graph, any electrical impulses produced by the fly’s olfactory system. (The fly’s head had only recently been severed from its body-in order to gain access to the olfactory apparatus-and was still in many respects functional.*)


* The heads and bodies of anthropods can briefly function without each other very nicely. A female praying mantis will often respond to earnest courting by decapitating her suitor. While this would be viewed as unsociable among humans, it is not so among insects: extirpation of the brain removes sexual inhibitions and encourages what is left of the male to mate. Afterwards, the female completes her celebratory repast, dining, of course, alone. Perhaps this represents a cautionary lesson against excessive sexual repression. Such olfactory specialization is quite common in insects. The male silkworm moth is able to detect the female’s sex attractant molecule if only about forty molecules per second reach its feathery antennae. A single female silkworm moth need release only a hundredth of a microgram of sex attractant per second to attract every male silkworm in a volume of about a cubic mile. That is why there are silkworms.


The experimenters wafted a wide variety of odors in front of it, including obnoxious and irritating gases such as ammonia, with no discernible effects. The line traced out on the oscilloscope screen was absolutely flat and horizontal. Then a tiny quantity of the sex attractant released by the female of the species was waved before the severed head, and an enormous vertical spike obligingly appeared on the oscilloscope screen. The bottle fly could smell almost nothing except the female sex attractant. But that molecule he could smell exceedingly well.

Perhaps the most curious exploitation of the reliance on smell to find a mate and continue the species is found in a South African beetle, which burrows into the ground during the winter. In the spring, as the ground thaws, the beetles emerge, but the male beetles groggily disinter themselves a few weeks before the females do. In this same region of South Africa, a species of orchid has evolved which gives off an aroma identical to the sex attractant of the female beetle. In fact, orchid and beetle evolution have produced essentially the same molecule.


The male beetles turn out to be exceedingly nearsighted; and the orchids have evolved a configuration of their petals that, to a myopic beetle, resembles the female in a receptive sexual posture. The male beetles enjoy several weeks of orgiastic ecstasy among the orchids, and when eventually the females emerge from the ground, we can imagine a great deal of wounded pride and righteous indignation. Meanwhile the orchids have been successfully cross-pollinated by the amorous male beetles, who, now properly abashed, do their best to continue the beetle species; and both organisms survive. (Incidentally, it is in the interest of the orchids not to be too consummately attractive; if the beetles fail to reproduce themselves, the orchids are in trouble.)


We thus discover one limitation to purely olfactory sexual stimuli. Another is that since every female beetle produces the same sex attractant, it is not easy for a male beetle to fall in love with the lady insect of his heart’s desire. While male insects may display themselves to attract a female, or-as with stag beetles-engage in mandible-to-mandible combat with the female as the prize, the central role of the female sex attractant in mating seems to reduce the extent of sexual selection among the insects.

Other methods of finding a mate have been developed in reptiles, birds and mammals. But the connection of sex with smell is still apparent neuro-anatomically in higher animals as well as anecdotally in human experience. I sometimes wonder if deodorants, particularly “feminine” deodorants, are an attempt to disguise sexual stimuli and keep our minds on something else.



Even in fish, lesions of the forebrain destroy the traits of initiative and caution. In higher animals these traits, much elaborated, seem localized in the neo-cortex, the site of many of the characteristic human cognitive functions. It is frequently discussed in terms of four major regions or lobes: the frontal, parietal, temporal and occipital lobes. Early neurophysiologists held that the neocortex was primarily connected only to other places in the neocortex, but it is now Known that there are many neural connections with the sub-cortical brain. It is, however, by no means clear that the neocortical subdivisions are actually functional units.


Each certainly has many quite different functions, and some functions may be shared among or between lobes. Among other functions, the frontal lobes seem to be connected with deliberation and the regulation of action; the parietal lobes, with spatial perception and the exchange of information between the brain and the rest of the body; the temporal lobes, with a variety of complex perceptual tasks; and the occipital lobes, with vision, the dominant sense in humans and other primates.

For many decades the prevailing view of neurophysiologists was that the frontal lobes, behind the forehead, are the sites of anticipation and planning for the future, both characteristically human functions. But more recent work has shown that the situation is not so simple. A large number of cases of frontal lesions-largely suffered in warfare and as gunshot wounds-have been investigated by the American neurophysiologist Hans-Lukas Teuber of the Massachusetts Institute of Technology.


He found that many frontal-lobe lesions have almost no obvious effects on behavior; however, in severe pathology of the frontal lobes,

“the patient is not altogether devoid of capacity to anticipate a course of events, but cannot picture himself in relation to those events as a potential agent.”

Teuber emphasized the fact that the frontal lobe may be involved in motor as well as cognitive anticipation, particularly in estimating what the effect of voluntary movements will be. The frontal lobes also seem to be implicated in the connection between vision and erect bipedal posture.

Thus the frontal lobes may be involved with peculiarly human functions in two different ways. If they control anticipation of the future, they must also be the sites of concern, the locales of worry. This is why transection of the frontal lobes reduces anxiety. But prefrontal lobotomy must also greatly reduce the patient’s capacity to be human. The price we pay for anticipation of the future is anxiety about it. Foretelling disaster is probably not much fun; Pollyanna was much happier than Cassandra.


But the Cassandric components of our nature are necessary for survival. The doctrines for regulating the future that they produced are the origins of ethics, magic, science and legal codes. The benefit of foreseeing catastrophe is the ability to take steps to avoid it, sacrificing short-term for long-term benefits. A society that is, as a result of such foresight, materially secure generates the leisure time necessary for social and technological innovation.

The other suspected function of the frontal lobes is to make possible mankind’s bipedal posture. Our upright stance may not have been possible before the development of the frontal lobes. As we shall see later in more detail, standing on our own two feet freed our hands for manipulation, which then led to a major accretion of human cultural and physiological traits. In a very real sense, civilization may be a product of the frontal lobes.

Visual information from the eyes arrives in the human brain chiefly in the occipital lobe, in the back of the head; auditory impressions, in the upper part of the temporal lobe, beneath the temple. There is fragmentary evidence that these components of the neo-cortex are substantially less well developed in blind deaf-mutes. Lesions in the occipital lobe-as produced by gunshot wounds, for example - frequently induce an impairment in the field of vision. The victim may be in all other respects normal but able to see only with peripheral vision, perceiving a solid, dark blot looming in front of him at the center of the normal field of view.


In other cases, more bizarre perceptions follow, including geometrically regular, cursive floating impairments in the visual field, and “visual fits” in which (for example) objects on the floor to the patient’s lower right are momentarily perceived as floating in the air to his upper left and rotated 180 degrees through space. It may even be possible to map which parts of the occipital lobes are responsible for which visual functions by systematically calculating the impairments of vision from various occipital lesions. Permanent impairments of vision are much less likely to occur in the very young, whose brains seem able to repair themselves or transfer functions to neighboring regions very well.

The ability to connect auditory with visual stimuli is also localized in the temporal lobe. Lesions in the temporal lobe can result in a form of aphasia, the inability to recognize spoken words. It is remarkable and significant that brain-damaged patients can be completely competent in spoken language and entirely incompetent in written language, or vice versa. They may be able to write but unable to read; able to read numbers but not letters; able to name objects but not colors. There is in the neocortex a striking separation of function, which is contrary to such common-sense notions as that reading and writing, or recognizing words and numbers, are very similar activities.


There are also as yet unconfirmed reports of brain damage that results only in the inability to understand the passive voice or prepositional phrases or possessive constructions. (Perhaps the locale of the subjunctive mood will one day be found. Will Latins turn out to be extravagantly endowed and English-speaking peoples significantly short-changed in this minor piece of brain anatomy?) Various abstractions, including the “parts of speech” in grammar, seem, astonishingly, to be wired into specific regions of the brain.

In one case, a temporal-lobe lesion resulted in a surprising impairment in the patient’s perception of faces, even the faces of his immediate family. Presented with the face on this page, he described it as “possibly” being an apple. Asked to justify this interpretation, he identified the mouth as a cut in the apple, the nose as the stem of the apple folded back on its surface, and the eyes as two worm holes. The same patient was perfectly able to recognize sketches of houses and other inanimate objects. A wide range of experiments shows that lesions in the right temporal lobe produce amnesia for certain types of nonverbal material, while lesions in the left temporal lobe produce a characteristic loss of memory for language.

Our ability to read and make maps, to orient ourselves spatially in three dimensions and to use the appropriate symbols-all of which are probably involved in the development if not the use of language -are severely impaired by lesions in the parietal lobes, near the top of the head. One soldier who suffered a massive wartime penetration of the parietal lobe was for a full year unable to orient his feet into his slippers, much less find his bed in the hospital ward. He nevertheless eventually experienced an almost complete recovery.

A lesion of the angular gyrus of the neocortex, in the parietal lobe, results in alexia, the inability to recognize the printed word. The parietal lobe appears to be involved in all human symbolic language and, of all the brain lesions, a lesion in the parietal lobe causes the greatest decline in intelligence as measured by activities in everyday life.

Chief among the neocortical abstractions are the human symbolic languages, particularly reading and writing and mathematics. These seem to require cooperative activities of the temporal, parietal and frontal lobes, and perhaps the occipital as well. Not all symbolic languages are neocortical however; bees- without a hint of a neocortex- have an elaborate dance language, first elucidated by the Austrian entomologist Karl von Frisch, by which they communicate information on the distance and direction of available food. It is an exaggerated gestural language, imitative of the motions bees in fact perform when finding food-as if we were to make a few steps towards the refrigerator, point and rub our bellies, with our tongues lolling out all the while.


But the vocabularies of such languages are extremely limited, perhaps only a few dozen words. The kind of learning that human youngsters experience during their long childhood seems almost exclusively a neocortical function.

While most olfactory processing is in the limbic system, some occurs in the neocortex. The same division of function seems to apply to memory. A principal part of the limbic system, other than the olfactory cortex, is, as we have mentioned, the hippocampal cortex. When the olfactory cortex is excised, animals can still smell, although with a much lower efficiency. This is another demonstration of the redundancy of brain function.


There is some evidence that, in contemporary humans, the short-term memory of smell resides in the hippocampus. The original function of the hippocampus may have been exclusively the short-term memory of smell, useful in, for example, tracking prey or finding the opposite sex. But a bilateral hippocampal lesion in humans results, as in the case of H. M., in a profound impairment of all varieties of short-term memory. Patients with such lesions literally cannot remember from one moment to the next. Clearly, both hippocampus and frontal lobes are involved in human short-term memory.

One of the many interesting implications of this is that short-term and long-term memory reside mostly in different parts of the brain. Classical conditioning- the ability of Pavlov’s dogs to salivate when the bells rang-seems to be located in the limbic system. This is long-term memory, but of a very restricted kind. The sophisticated sort of human long-term memory is situated in the neocortex, which is consistent with the human ability to think ahead.


As we grow old, we sometimes forget what has just been said to us while retaining vivid and accurate recollections of events in our childhood. In such cases, little seems to be wrong with either our short-term or our long-term memories; the problem is the connection between the two-we have great difficulty in accessing new material into the long-term memory. Penfield believed that this lost accessing ability arises from an inadequate blood supply to the hippocampus in old age-because of arteriosclerosis or other physical disabilities. Thus elderly people-and ones not so elderly-may have serious impairments in accessing short-term memory while being otherwise perfectly alert and intellectually keen.*


* Indeed, there is a range of medical evidence on the connection between blood supply and intellectual abilities. It has long been known that patients deprived of oxygen for some minutes can experience permanent and serious mental impairment. Operations to remove material from clogged carotid arteries in an effort to prevent stroke yield unexpected benefits. According to one study, six weeks after such operations, the patients showed an average increase in IQ of eighteen points, a substantial improvement. And there has been some speculation that immersion in hyperbaric oxygen-that is, oxygen under high pressure-can raise the intelligence of infants.


This phenomenon also shows a clear-cut distinction between short-term and long-term memory, consistent with their localization in different parts of the brain. Waitresses in short-order restaurants can remember an impressive amount of information, which they accurately transmit to the kitchen. But an hour later, the information has vanished utterly. It was put into the short-term memory only, and no effort was made to access it into the long-term memory.

The mechanics of recall can be complex. A common experience is that we know something is in our long-term memory - a word, a name, a face, an experience - but find ourselves unable to call it up. No matter how hard we try, the memory resists retrieval. But if we think sideways at it, recalling some slightly related or peripheral item, it often follows unbidden. (Human vision is also a little like this. When we look directly at a faint object-a star, say-we are using the fovea, the part of the retina with the greatest acuity and the greatest density of cells called cones.

But when we avert our vision slightly-when, in a manner of speaking, we look sideways at the object-we bring into play the cells called rods, which are sensitive to feeble illumination and so able to perceive the faint star.) It would be interesting to know why thinking sideways improves memory retrieval; it may be merely associating to the memory trace by a different neural pathway. But it does not suggest particularly efficient brain engineering.

We have all had the experience of awakening with a particularly vivid, chilling, insightful or otherwise memorable dream clearly in mind; saying to ourselves, “I’ll certainly remember this dream in the morning”; and the next day having not the foggiest notion about the content of the dream or, at best, a vague trace of an emotion tone. On the other hand, if I am sufficiently exercised about the dream to awaken my wife in the middle of the night and tell her about it, I have no difficulty remembering its contents unaided in the morning.


Likewise, if I take the trouble of writing the dream down, when I awaken the next morning I can remember the dream perfectly well without referring to my notes. The same thing is true of, for example, remembering a telephone number. If I am told a number and merely think about it, I am likely to forget it or transpose some of the digits. If I repeat the numbers out loud or write them down, I can remember them quite well. This surely means that there is a part of our brain which remembers sounds and images, but not thoughts.


I wonder if that sort of memory arose before we had very many thoughts-when it was important to remember the hiss of an attacking reptile or the shadow of a plummeting hawk, but not our own occasional philosophical reflections.


Despite the intriguing localization of function in the triune brain model, it is, I stress again, an oversimplification to insist upon perfect separation of function. Human ritual and emotional behavior are certainly influenced strongly by neocortical abstract reasoning; analytical demonstrations of the validity of purely religious beliefs have been proffered, and there are philosophical justifications for hierarchical behavior, such as Thomas Hobbes’ “demonstration” of the divine right of kings. Likewise, animals that are not human - and in fact even some animals that are not primates - seem to show glimmerings of analytical abilities. I certainly have such an impression about dolphins, as I described in my book The Cosmic Connection.

Nevertheless, while bearing these caveats in mind, it seems a useful first approximation to consider the ritualistic and hierarchical aspects of our lives to be influenced strongly by the R-complex and shared with our reptilian forebears; the altruistic, emotional and religious aspects of our lives to be localized to a significant extent in the limbic system and shared with our nonprimate mammalian forebears (and perhaps the birds); and reason to be a function of the neo-cortex, shared to some extent with the higher primates and such cetaceans as dolphins and whales.


While ritual, emotion and reasoning are all significant aspects of human nature, the most nearly unique human characteristic is the ability to associate abstractly and to reason. Curiosity and the urge to solve problems are the emotional hallmarks of our species; and the most characteristically human activities are mathematics, science, technology, music and the arts - a somewhat broader range of subjects than is usually included under the “humanities.” Indeed, in its common usage this very word seems to reflect a peculiar narrowness of vision about what is human. Mathematics is as much a “humanity” as poetry. Whales and elephants may be as “humane” as humans.

The triune-brain model derives from studies of comparative neuroanatomy and behavior. But honest introspection is not unknown in the human species, and if the triune-brain model is correct, we would expect some hint of it in the history of human self-knowledge. The most widely known hypothesis that is at least reminiscent of the triune brain is Sigmund Freud’s division of the human psyche into id, ego and superego. The aggressive and sexual aspects of the R-complex correspond satisfyingly to the Freudian description of the id (Latin for “it”-i.e., the beast-like aspect of our natures); but, so far as I know, Freud did not in his description of the id lay great stress on the ritual or social-hierarchy aspects of the R-complex.


He did describe emotions as an ego function-in particular the “oceanic experience,” which is the Freudian equivalent of the religious epiphany. However, the superego is not depicted primarily as the site of abstract reasoning but rather as the internalizer of societal and parental strictures, which in the triune brain we might suspect to be more a function of the R-complex. Thus I would have to describe the psychoanalytic tripartite mind as only weakly in accord with the triune-brain model.

Perhaps a better metaphor is Freud’s division of the mind into the conscious; the preconscious, which is latent but capable of being tapped; and the unconscious, which is repressed or otherwise unavailable. It was the tension that exists among the components of the psyche that Freud had in mind when he said of man that “his capacity for neurosis would merely be the obverse of his capacity for cultural development.” He called the unconscious functions “primary processes.”

A superior agreement is found in the metaphor for the human psyche in the Platonic dialogue Phaedrus. Socrates likens the human soul to a chariot drawn by two horses-one black, one white-pulling in different directions and weakly controlled by a charioteer. The metaphor of the chariot itself is remarkably similar to MacLean’s neural chassis; the two horses, to the R-complex and the limbic cortex; and the charioteer barely in control of the careening chariot and horses, to the neocortex.

In yet another metaphor, Freud described the ego as the rider of an unruly horse. Both the Freudian and the Platonic metaphors emphasize the considerable independence of and tension among the constituent parts of the psyche, a point that characterizes the human condition and to which we will return. Because of the neuroanatomical connections between the three components, the triune brain must itself, like the Phaedrus chariot, be a metaphor; but it may prove to be a metaphor of great utility and depth.


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