The River of Consciousness

by Oliver Sacks

  The calcium ion channels that plants rely on do not support rapid or repetitive signaling between cells; once a plant action potential is generated, it cannot be repeated at a fast enough rate to allow, for example, the speed with which a worm “dashes…into its burrow.” Speed requires ions and ion channels that can open and close in a matter of milliseconds, allowing hundreds of action potentials to be generated in a second. The magic ions, here, are sodium and potassium ions, which enabled the development of rapidly reacting muscle cells, nerve cells, and neuromodulation at synapses. These made possible organisms that could learn, profit by experience, judge, act, and finally think.

  This new form of life—animal life—emerging perhaps 600 million years ago, conferred great advantages and transformed populations rapidly. In the so-called Cambrian explosion (datable with remarkable precision to 542 million years ago), a dozen or more new phyla, each with very different body plans, arose within the space of a million years or less—a geological eyeblink. The once peaceful pre-Cambrian seas were transformed into a jungle of hunters and hunted, newly mobile. And while some animals (like sponges) lost their nerve cells and regressed to a vegetative life, others, especially predators, evolved increasingly sophisticated sense organs, memories, and minds.

  It is fascinating to think of Darwin, Romanes, and other biologists of their time searching for “mind,” “mental processes,” “intelligence,” even “consciousness” in primitive animals like jellyfish, and even in protozoa. A few decades afterwards, radical behaviorism would come to dominate the scene, denying reality to what was not objectively demonstrable, denying in particular any inner processes between stimulus and response, deeming these irrelevant or at least beyond the reach of scientific study.

  Such a restriction or reduction indeed facilitated studies of stimulation and response, both with and without “conditioning,” and it was Pavlov’s famous studies of dogs that formalized—as “sensitization” and “habituation”—what Darwin had observed in his worms.*2

  As Konrad Lorenz wrote in The Foundations of Ethology, “An earthworm [that] has just avoided being eaten by a blackbird…is indeed well-advised to respond with a considerably lowered threshold to similar stimuli, because it is almost certain that the bird will still be nearby for the next few seconds.” This lowering of threshold, or sensitization, is an elementary form of learning, even though it is nonassociative and relatively short-lived. Correspondingly, a diminution of response, or habituation, occurs when there is a repeated but insignificant stimulus—something to be ignored.

  It was shown within a few years of Darwin’s death that even single-cell organisms like protozoa could exhibit a range of adaptive responses. In particular, Herbert Spencer Jennings showed that the tiny, stalked, trumpet-shaped unicellular organism Stentor employs a repertoire of at least five different responses to being touched, before finally detaching itself to find a new site if these basic responses are ineffective. But if it is touched again, it will skip the intermediate steps and immediately take off for another site. It has become sensitized to noxious stimuli, or, to use more familiar terms, it “remembers” its unpleasant experience and has learned from it (though the memory lasts only a few minutes). If, conversely, Stentor is exposed to a series of very gentle touches, it soon ceases to respond to these at all—it has habituated.

  Jennings described his work with sensitization and habituation in organisms like Paramecium and Stentor in his 1906 book Behavior of the Lower Organisms. Although he was careful to avoid any subjective, mentalistic language in his description of protozoan behaviors, he did include an astonishing chapter at the end of his book on the relation of observable behavior to “mind.”

  He felt that we humans are reluctant to attribute any qualities of mind to protozoa because they are so small:

  The writer is thoroughly convinced, after long study of the behavior of this organism, that if Amoeba were a large animal, so as to come within the everyday experience of human beings, its behavior would at once call forth the attribution to it of states of pleasure and pain, of hunger, desire, and the like, on precisely the same basis as we attribute these things to the dog.

  Jennings’s vision of a highly sensitive, dog-size Amoeba is almost cartoonishly the opposite of Descartes’s notion of dogs as so devoid of feelings that one could vivisect them without compunction, taking their cries as purely “reflex” reactions of a quasi-mechanical kind.

  Sensitization and habituation are crucial for the survival of all living organisms. These elementary forms of learning are short-lived—a few minutes at most—in protozoa and plants; longer-lived forms require a nervous system.

  While behavioral studies flourished, there was almost no attention paid to the cellular basis of behavior—the exact role of nerve cells and their synapses. Investigations in mammals—involving, for example, the hippocampal or memory systems in rats—presented almost insuperable technical difficulties, due to the tiny size and extreme density of neurons (there were difficulties, moreover, even if one could record electrical activity from a single cell, in keeping it alive and fully functioning for the duration of protracted experiments).

  Faced with such difficulties in his anatomical studies in the early twentieth century, Ramón y Cajal—the first and greatest microanatomist of the nervous system—had turned to study simpler systems: those of young or fetal animals, and those of invertebrates (insects, crustaceans, cephalopods, and others). For similar reasons, Eric Kandel, when he embarked in the 1960s on a study of the cellular basis of memory and learning, sought an animal with a simpler and more accessible nervous system. He settled on the giant sea snail Aplysia, which has 20,000 or so neurons, distributed in ten or so ganglia of about 2,000 neurons apiece. It also has particularly large neurons—some even visible to the naked eye—connected with one another in fixed anatomical circuits.

  That Aplysia might be considered too low a form of life for studies of memory did not discountenance Kandel, despite some skepticism from his colleagues—any more than it had discountenanced Darwin when he spoke of the “mental qualities” of earthworms. “I was beginning to think like a biologist,” Kandel writes, recalling his decision to work with Aplysia. “I appreciated that all animals have some form of mental life that reflects the architecture of their nervous system.”

  As Darwin had looked at an escape reflex in worms and how it might be facilitated or inhibited in different circumstances, Kandel looked at a protective reflex in Aplysia, the withdrawal of its exposed gill to safety, and the modulation of this response. Recording from (and sometimes stimulating) the nerve cells and synapses in the abdominal ganglion that governed these responses, he was able to show that relatively short-term memory and learning, as involved in habituation and sensitization, depended on functional changes in synapses—but longer-term memory, which might last several months, went with structural changes in the synapses. (In neither case was there any change in the actual circuits.)

  As new technologies and concepts emerged in the 1970s, Kandel and his colleagues were able to complement these electrophysiological studies of memory and learning with chemical ones: “We wanted to penetrate the molecular biology of a mental process, to know exactly what molecules are responsible for short-term memory.” This entailed, in particular, studies of the ion channels and neurotransmitters involved in synaptic functions—monumental work that earned Kandel a Nobel Prize.

  Where Aplysia has only 20,000 neurons distributed in ganglia throughout its body, an insect may have up to a million nerve cells and despite its tiny size may be capable of extraordinary cognitive feats. Thus bees are expert in recognizing different colors, smells, and geometrical shapes presented in a laboratory setting, as well as systematic transformations of these. And of course, they show superb expertise in the wild or in our gardens, where they not only recognize the patterns and smells and colors of flowers but can remember their locations and communicate these to their fellow bees.

  It has even been shown, in a
highly social species of paper wasp, that individuals can learn and recognize the faces of other wasps. Such face learning has hitherto been described only in mammals; it is fascinating that a cognitive power so specific can be present in insects as well.

  We often think of insects as tiny automata—robots with everything built in and programmed. But it is increasingly evident that insects can remember, learn, think, and communicate in quite rich and unexpected ways. Much of this, doubtless, is built in, but much, too, seems to depend on individual experience.

  Whatever the case with insects, there is an altogether different situation with those geniuses among invertebrates, the cephalopods, consisting of octopuses, cuttlefish, and squid. Here, as a start, the nervous system is much larger—an octopus may have half a billion nerve cells distributed between its brain and its “arms” (a mouse, by comparison, has only 75 to 100 million). There is a remarkable degree of organization in the octopus brain, with dozens of functionally distinct lobes in the brain and similarities to the learning and memory systems of mammals.

  Not only are cephalopods easily trained to discriminate test shapes and objects, but some can learn by observation, a power otherwise confined to certain birds and mammals. They have remarkable powers of camouflage and can signal complex emotions and intentions by changing their skin colors, patterns, and textures.

  Darwin noted in The Voyage of the Beagle how an octopus in a tidal pool seemed to interact with him, by turns watchful, curious, and even playful. Octopuses can be domesticated to some extent, and their keepers often empathize with them, feeling some sense of mental and emotional proximity. Whether one can use the c word—“consciousness”—in regard to cephalopods can be argued all ways. But if one allows that a dog may have consciousness of a significant and individual sort, one has to allow it for an octopus, too.

  Nature has employed at least two very different ways of making a brain—indeed, there are almost as many ways as there are phyla in the animal kingdom. Mind, to varying degrees, has arisen or is embodied in all of these, despite the profound biological gulf that separates them from one another, and us from them.

  * * *

  *1 In 1852, Hermann von Helmholtz was able to measure the speed of nerve conduction at eighty feet per second. If we speed up a time-lapse film of plant movement by a thousandfold, plant behaviors start to look animal-like and may even appear “intentional.”

  *2 Pavlov used dogs in his famous experiments on conditioned reflexes, and the conditioning stimulus was usually a bell, which the dogs learned to associate with food. But on one occasion, in 1924, there was a huge flood in the laboratory that nearly drowned the dogs. After this, many of the dogs were sensitized, even terrified, by the sight of water for the rest of their lives. Extreme or long-lasting sensitization underlies PTSD, in dogs as in humans.

  The Other Road: Freud as Neurologist

  It is making severe demands on the unity of the personality to try and make me identify myself with the author of the paper on the spinal ganglia of the petromyzon. Nevertheless I must be he, and I think I was happier about that discovery than about others since.

  —SIGMUND FREUD TO KARL ABRAHAM,

  SEPTEMBER 21, 1924

  Everyone knows Freud as the father of psychoanalysis, but relatively few know about the twenty years (from 1876 to 1896) when he was primarily a neurologist and anatomist; Freud himself rarely referred to them in later life. Yet his neurological life was the precursor to his psychoanalytic one, and perhaps an essential key to it.

  Freud’s early and enduring passion for Darwin (along with Goethe’s “Ode to Nature”), he tells us in his autobiography, made him decide to study medicine; in his first year at university, he was attending courses on “Biology and Darwinism,” as well as lectures by the physiologist Ernst Brücke. Two years later, eager to do some hands-on research, Freud asked Brücke for a position in his laboratory. Though, as Freud was later to write, he already felt that the human brain and mind might be the ultimate subject of his explorations, he was intensely curious about the early forms and origins of the nervous systems and wished to get a sense of their evolution first.

  Brücke suggested that Freud look at the nervous system of a very primitive fish—Petromyzon, the lamprey—and in particular at the curious “Reissner” cells clustered about the spinal cord. These cells had attracted attention since Brücke’s own student days forty years before, but their nature and function had never been understood. The young Freud was able to detect the precursors of these cells in the singular larval form of the lamprey, and to show they were homologous with the posterior spinal ganglia cells of higher fish—a significant discovery. (This larva of the Petromyzon is so different from the mature form that it was long considered to be a separate genus, Ammocoetes.) He then turned to studying an invertebrate nervous system, that of the crayfish. At that time the nerve “elements” of invertebrate nervous systems were considered radically different from those of vertebrate ones, but Freud was able to show that they were, in fact, morphologically identical—it was not the cellular elements that differed between primitive and advanced animals but their organization. Thus there emerged, even in Freud’s earliest researches, a sense of a Darwinian evolution whereby, using the most conservative means (that is, the same basic anatomical cellular elements), more and more complex nervous systems could be built.*1

  It was natural that in the early 1880s—he now had his medical degree—Freud should move on to clinical neurology, but it was equally crucial to him that he continue his anatomical work, too, looking at human nervous systems, and he did this in the laboratory of the neuroanatomist and psychiatrist Theodor Meynert.*2 For Meynert (as for Paul Emil Flechsig and other neuroanatomists at the time) such a conjunction did not seem at all strange. There was assumed to be a simple, almost mechanical relation of mind and brain, both in health and in disease; thus Meynert’s 1884 magnum opus, entitled Psychiatry, bore the subtitle A Clinical Treatise on Diseases of the Fore-brain.

  Although phrenology itself had fallen into disrepute, the localizationist impulse had been given new life in 1861, when the French neurologist Paul Broca was able to demonstrate that a highly specific loss of function—of expressive language, a so-called expressive aphasia—followed damage to a particular part of the brain on the left side. Other correlations were quick in coming, and by the mid-1880s something akin to the phrenological dream seemed to be approaching realization, with “centers” being described for expressive language, receptive language, color perception, writing, and many other specific capabilities. Meynert reveled in this localizationist atmosphere—indeed he himself, after showing that the auditory nerves projected to a specific area of the cerebral cortex (the Klangfeld, or sound field), postulated that damage to this was present in all cases of sensory aphasia.

  But Freud was disquieted at this theory of localization and, at a deeper level, profoundly dissatisfied, too, for he was coming to feel that all localizationism had a mechanical quality, treating the brain and nervous system as a sort of ingenious but idiotic machine, with a one-to-one correlation between elementary components and functions, denying it organization or evolution or history.

  During this period (from 1882 to 1885), he spent time on the wards of the Vienna General Hospital, where he honed his skills as a clinical observer and neurologist. His heightened narrative powers, his sense of the importance of a detailed case history, are evident in the clinicopathological papers he wrote at the time: of a boy who died from a cerebral hemorrhage associated with scurvy, an eighteen-year-old baker’s apprentice with acute multiple neuritis, and a thirty-six-year-old man with a rare spinal condition—syringomyelia—who had lost the sense of pain and temperature but not the sense of touch (a dissociation caused by very circumscribed destruction within the spinal cord).

  In 1886, after spending four months with the great neurologist Jean-Martin Charcot in Paris, Freud returned to Vienna to set up his own neurological practice. It is not entirely easy to reconstruct�
��from Freud’s letters or from the vast numbers of studies and biographies of him—exactly what “neurological life” consisted of for him. He saw patients in his consulting room at 19 Berggasse, presumably a mix of patients, as might come to any neurologist then or now: some with everyday neurological disorders such as strokes, tremors, neuropathies, seizures, or migraines; and others with functional disorders such as hysterias, obsessive-compulsive conditions, or neuroses of various sorts.

  He also worked at the Institute for Children’s Diseases, where he held a neurological clinic several times a week. (His clinical experience here led to the books for which he became best known to his contemporaries—his three monographs on the infantile cerebral paralyses of children. These were greatly respected among the neurologists of his time and are still, on occasion, referred to even now.)

  As he continued with his neurological practice, Freud’s curiosity, his imagination, his theorizing powers, were on the rise, demanding more complex intellectual tasks and challenges. His earlier neurological investigations, during his years at the Vienna General Hospital, had been of a fairly conventional type, but now, as he pondered the much more complex question of the aphasias, he became convinced that a different view of the brain was needed. A more dynamic vision of the brain was taking hold of him.

  It would be of great interest to know exactly how and when Freud discovered the work of the English neurologist Hughlings Jackson, who, very quietly, stubbornly, persistently, was developing an evolutionary view of the nervous system, unmoved by the localizationist frenzy all around him. Jackson, twenty years Freud’s senior, had been moved to an evolutionary view of nature with the publication of Darwin’s Origin of Species and by Herbert Spencer’s evolutionary philosophy. In the early 1870s, Jackson proposed a hierarchic view of the nervous system, picturing how it might have evolved from the most primitive reflex levels, up through a series of higher and higher levels, to those of consciousness and voluntary action. In disease, Jackson conceived, this sequence was reversed, so that a dis-evolution or dissolution or regression occurred, and with this a “release” of primitive functions normally held in check by higher ones.