Tuesday, July 01, 2003

A Neurologist Confronts Ultimate Questions

Consciousness: A User’s Guide

By: Frederick E. Lepore M.D.


On the short list of Big Questions is the nature and origin of consciousness. The human record suggests that for as long as we have been lifting our gaze to the immensity of the cosmos in search of the origins of the universe, we have been turning it inward, as well, to that defining quality of humanity— consciousness. The point at which consciousness emerged during evolution remains unknown, but its mixture with abstract thought and language distinguishes human consciousness from that of animals. As Thomas Carlyle observed, “To Newton and to Newton’s dog Diamond, what a different pair of universes; while the painting on the optical retina of both was, most likely, the same!”

In Consciousness: A User’s Guide, Scottish neurologist Adam Zeman confronts the question of consciousness (calling it “the mind-body problem in disguise”) with clarity, honesty, and insight. At the outset, he confesses himself unable to provide “a new solution to the riddle,” but he atones with a vivid and informative snapshot of the state of the art of consciousness studies at the dawn of the 21st century.

Like Caesar’s Gaul, the terrain of consciousness studies can be divided into three parts: artificial intelligence, philosophy, and neuroscience (including neuropsychology). Frequently, the savants in one area are not well apprised of developments in the others. Francis Crick and Christof Koch once asserted that Daniel Dennett, a highly regarded neurophilosopher and author of Consciousness Explained, had declared that neurons “are not my department.” Zeman avoids this unfortunate by-product of specialization, lucidly examining all three approaches to consciousness from the uncommon vantage point of an academic neurologist involved in the daily care of patients. I count myself fortunate to ply the same trade, and I have observed that neurologic practitioners are frequently drawn, like moths to a flame, to seek more profound understanding of disorders of consciousness that confront them on ward rounds and during office hours.

Clinical neurology, as defined in F.M.R. Walshe’s classic introductory textbook, Diseases of the Nervous System, “is largely a study in the applied anatomy and physiology of the nervous system,” and Zeman never strays far from his own neurologic credo: “that events in the brain do in fact provide the physical basis of consciousness.” At our present, relatively rudimentary level of knowledge, equating mind with brain is not easy. In a recent New Yorker profile, linguistic philosopher Noam Chomsky declared that “there’s no proof that there is any neurological basis even for computations as basic as addition.” Rather than embracing a mystical scheme of Cartesian dualism, Chomsky may simply be acknowledging the daunting gaps in our knowledge of the nervous system. Indeed, it is not surprising that much of the nervous system remains terra incognita. Neurology, after all, is a relatively young science. A Nobel Prize for discovery of its fundamental building block, the neuron, was awarded less than a century ago. Confronting the complexity of the nervous system, even a conceptual tool as powerful as genetics has major limitations: The roughly 30,000 protein-coding genes of the human genome cannot reasonably be expected to provide a complete “wiring diagram” for a thousand trillion synapses. 

Zeman heralds this new age of respectability with an even-handed synthesis that firmly establishes consciousness as a legitimate subject for the scientific method and engages the reader in the pursuit of the Holy Grail of the neural correlate of consciousness.

The vacuum created by our incomplete knowledge of the nervous system was filled by religious beliefs and mystical notions that, until recently, placed the study of consciousness outside the boundaries of proper scientific inquiry. Beginning in the 1990s, however, books by Crick (The Astonishing Hypothesis), Antonio Damasio (The Feeling of What Happens), Gerald Edelman (Bright Air, Brilliant Fire), and others transformed consciousness research from vaguely disreputable science to a blood sport for retired Nobelists and academic neurologists funded by the National Institutes of Health. Zeman heralds this new age of respectability with an evenhanded synthesis that firmly establishes consciousness as a legitimate subject for the scientific method and engages the reader in the pursuit of the Holy Grail of the neural correlate of consciousness.


Consciousness: A User’s Guide begins by asking what we mean when we say someone is “conscious” and then identifies four overlapping elements. The most basic operation is wakefulness, and certainly the “switch” for consciousness is turned on when we awaken and is turned off when we fall asleep. Being awake is necessary but not sufficient for consciousness. Consider severely brain-injured patients in a persistent vegetative state who are awake but not aware or, in irreverent neurologic parlance, “the lights are on but nobody’s home.” The second aspect of consciousness encompasses “the perceptual experience the waking state permits.” The knowledge derived from perceptual experience is the third facet of consciousness and constitutes “all that we can know, think, mean, intend, all that we can hope, wish, remember or believe.” It is “simply the realm of the mind.” Finally, Zeman distinguishes between consciousness of external ideas and objects and the special case of consciousness of oneself. Entailed in self-consciousness is the capacity to be “aware of awareness” that emerges at around five years of age in healthy children.

Having established these working definitions of consciousness, Zeman maps the physical constraints on “such stuff as dreams are made of ”—neuroanatomy. Our lesson begins with the architecture of a single cell and ends with Donald Hebb’s theory of the mechanism of modifying connections between nerve cells, a theory encapsulated in the neurophysiologist’s adage, “cells that fire together, wire together.” In between, the reader glimpses the welter of information that engulfs a first-year medical student as Zeman adroitly traces the characteristic course of “information flowing through the brain” from primary sensory cortices (for example, the visual cortex), to areas where inputs from senses like vision and hearing are combined, and to evolutionarily ancient limbic regions where emotion and remembrance are integrated with sensory information. The oncoming cognitive (or precognitive) procession is diverted to subcortical structures (thalamus, cerebellum, and basal ganglia) that further modify the neural signals that will eventually “influence the frontal lobes, where actions are prepared, released, and monitored.”

In his guide to the crosstalk of the billions of neurons that populate a lobe of the brain, Zeman juxtaposes an account of the individual neuron’s facts of life, ranging from the surging voltage of the all-or-none action potential to the synaptic cleft between neurons, to the neurotransmitters that must traverse that gap. Functional implications of the staggering complexity of the human nervous system notwithstanding, Zeman cautions us that “perceptual consciousness is not an inevitable accompaniment of the operation of large neuronal networks.” 

Before perceptual consciousness can occur, a waking state must be attained, and the regular reemergence of this state when the bedside alarm clock buzzes is a daily neurophysiological marvel.

Before perceptual consciousness can occur, a waking state must be attained, and the regular reemergence of this state when the bedside alarm clock buzzes is a daily neurophysiological marvel. Investigators in the early decades of the 20th century discovered that states of arousal “are mirrored by the electrical activity of the brain” and are “profoundly affected by an ‘activating system’ located in or close to the brain-stem.” In 1924, Hans Berger made the initial crude measurements of the brain’s electrical activity in a teenager with a large, surgically created cranial defect. Although electrical stimulation of nerves had been performed by Luigi Galvani as early as the 18th century, Berger was the first to record the brain’s electrical activity or electroencephalogram (EEG). His primitive string galvanometer tracings of faint cortical currents would in time lead to tantalizing but inconsistent glimpses of a relationship between mental states and the brain’s electrical activity.

The nascent field of clinical neurophysiology would uncover a hitherto unsuspected four-stage “architecture of sleep” in which the 8 to 13 cycles-per-second alpha rhythms of relaxed wakefulness is gradually supplanted by the delta rhythms (4 cycles/ second or less) of stage 4 sleep. Despite their outwardly tranquil appearance, sleepers repeatedly ascend and descend a neurophysiological mountain range of varying cerebral voltage patterns throughout the night. At times, an active EEG belies profound muscular relaxation when the patient enters the stage of rapid eye movement (so-called because of associated darting eye motion) sleep. The anatomical underpinnings of sleep began to reveal themselves in the pandemic of encephalitis lethargica that appeared in the winter of 1916-1917. As described by Oliver Sacks in Awakenings, “a third of those affected died in the acute stages of the sleeping-sickness, in states of coma so deep as to preclude arousal, or in states of sleeplessness so intense as to preclude sedation.” When his patients succumbed to this strange illness, the Viennese neurologist and psychiatrist, Constantin von Economo, found upper brainstem damage on postmortem examination and made “a rough correlation between sites of damage in the brainstem and their effects on awareness.” By 1949, Giuseppe Moruzzi and Horace Magoun had identified the interconnecting cells of the reticular formation in the upper brainstem as essential for arousal.

With this brief grounding in the neurophysiology and neuroanatomy of arousal, the reader comes face to face with the disorders of consciousness encountered on a neurologist’s daily rounds. 


With this brief grounding in the neurophysiology and neuroanatomy of arousal, the reader comes face to face with the disorders of consciousness encountered on a neurologist’s daily rounds. These encounters range from the commonplace faint, which heralds the brain’s loss of blood supply, to the anesthetic-induced states that usually abolish consciousness (and pain), possibly by a reversible disruption of the neuron’s membrane. Through the study of these diseases and drug effects, we arrive at the gateway to consciousness; with Zeman’s discourse on the visual system, we pass through that gate and begin to learn how the contents of consciousness are acquired.

If you doubt that visual anatomy is visual (and maybe cognitive) destiny, consider Jerome Lettvin’s description of the “no-frills” frog retina that serves admirably as a detector of moving insects but will allow the frog to starve to death if surrounded by food that is not moving.

Much of our contemporary conception of the brain’s organization stems from discoveries such as the receptive fields of visual neurons; the existence of individual cortical modules for visual capacities such as color, form, and motion; and the “what” (ventral pathway) and “where” (dorsal pathway) streams of visual processing. We are just beginning to learn how this elaborate neural circuitry governs the contents of consciousness. If you doubt that visual anatomy is visual (and maybe cognitive) destiny, consider Jerome Lettvin’s description of the “no-frills” frog retina that serves admirably as a detector of moving insects but will allow the frog to starve to death if surrounded by food that is not moving.

By describing disorders of visual perception that 19th century German clinicians termed seelenblindheit, or “mind-blindness,” Zeman begins to tease apart the intertwined strands of vision and visual consciousness. The potential separability of these two capacities is readily observable in a patient with damage to the occipitotemporal pathways, who is unable to visually identify a common object despite adequate eyesight. This condition is associative visual agnosia in which, to paraphrase the neuropsychologist Hans Teuber, a normal visual percept is stripped of its meaning. By way of contrast, a “blindsight” patient with surgically excised primary visual cortex can see nothing in a portion of his visual field and yet when urged to identify an “X” or “O” presented to the region of absent vision, he will guess the correct letter at a level better than chance. The clinical antipodes of an agnosic patient—who sees but cannot recognize objects—and the blindsight patient—who recognizes letters without consciously seeing them—underscore that vision is not a homogeneous process and that “only some of the activity within the visual brain gives rise to visual awareness.”


The discussion of both normal and disordered acquisition of the contents of visual consciousness leads Zeman inexorably back to the central problem of the relationship of cerebral activity and consciousness. True to the intellectual bloodlines of clinical neurology, Zeman declares that the “theories which depict experience and its neural basis as inseparable aspects of a single process may hold out the greatest promise.” Brain-mind equivalence is the Zeitgeist of contemporary neuroscience, and Zeman, like most neurologists, leans away from the dualism of Descartes, who famously posited, in the words of the neurophilosopher Patricia Churchland, that the essential self “is a nonphysical, conscious thing.” Churchland rejects the Cartesian approach for three reasons: conscious thoughts such as “I exist” are activities of the physical brain, self-regulation such as inhibiting sexual proclivities may be non-conscious, and Hume in the 18th century denied introspective experience of the “self” as distinct from the body.

Zeman broaches artificial consciousness, acknowledging the dilemma of our carbon-based neuronal assemblages contemplating their impending replacement by silicon chips.

Will the “greatest promise” of the theory of brain-mind equivalence be realized? Not unexpectedly, Zeman cannot provide unequivocal assurance that this is the royal road to solving a problem that marks out “the limits of human understanding.” He does provide a panoramic view, based on more than 15 “philosophical accounts of the relationship between experience and brain events,” ranging from Cartesian dualism to physicalism unifying mind and matter, and from John Searle’s “simple solution” of consciousness as an “emergent property” of a sufficiently complex biological system to Colin McGinn’s dark vision of consciousness as forever beyond the grasp of human intelligence.

Along the way, Zeman broaches artificial consciousness, acknowledging the dilemma of our carbon-based neuronal assemblages contemplating their impending replacement by silicon chips. It is possible that we will finally arrive at the point of transition whereby computers cease to be exclusively machines that implement algorithms and become, according to artificial intelligence innovator Ray Kurzweil, “spiritual machines” that are worthy objects of Alan Turing’s incisive question, “Can machines think?” Zeman finds “no wholly compelling argument against the possibility of artificial consciousness.” But if such consciousness can be created, its scientific verification will pose a formidable problem, and over the past half century no replacement has been forthcoming for Turing’s test in which the interrogator compared the written responses of a machine and a person. If machine and human responses were indistinguishable, Turing averred the presence of a “thinking machine,” and he predicted that by the end of the 20th century “one will be able to speak of machines thinking without expecting to be contradicted.” Turing’s methodology may be suspect, however; neurophilosopher Searle contends that a successful Turing test may only affirm the ingenious but sterile syntax of machine logic and not the content of conscious minds, which are “semantical” in attaching meaning to the symbols of formal logic.

An alternative to Turing’s test would be to judge the potential for consciousness by the similitude of the computer’s wiring diagram with the brain’s neural circuitry. This similitude presupposes a better knowledge of neuroanatomy and neurophysiology than is now available. A schematic diagram of brain circuitry is the stock-in-trade of neurologists who must localize a brain lesion before they can treat it, however, and Zeman does not stint in sketching the currently hazy outlines of the circuitry of consciousness. Most theories of the neural correlate of consciousness assume a “loosely linked but temporarily coherent network of neurons” and an interaction of cerebral cortex, thalamus, and other subcortical structures. The interaction of these disparate structures may be made possible by synchronous neuronal firing.

In time, the vague outlines of one of the schemas of consciousness that Zeman reviews may come into sharp and detailed focus, but having read Consciousness: A User’s Guide, we are still left with the hard question: “But why are we conscious?” True, normal human life without consciousness is inconceivable, and the notion of zombies having “absolutely no awareness whatsoever” is easily dismissed, but this brings us no closer to the “why” of consciousness. Striking an eloquent and essential equipoise between science and philosophy, Zeman suggests that the function of consciousness is to assure flexibility of response when routine stereotypical solutions fail. Fair enough, but the enigma of consciousness remains, as Zeman concludes, “akin to our difficulty in explaining existence itself.”  


From Consciousness: A User’s Guide, by Adam Zeman. © 2002 by Adam Zeman. Reprinted with permission of Yale University Press.

Coma is usually a staging post en route to some other destination. This may be a full recovery. A patient etched on my memory, because I discovered his plight was the result of low blood glucose 20 minutes later than I would have wished, was none the worse for his experience. The other outcomes of coma are less happy; two of these have occasioned plenty of controversy in recent years.

Coma due to extensive damage to the hemispheres or to the thalamus, with relative preservation of the brainstem, sometimes gives way to a state which superficially resembles ordinary consciousness. Sleep alternates with waking, presumably because the structures which regulate sleep and waking in the brain-stem are intact. While awake, the sufferer’s eye are open. Smiles may pass across his face; he may shed tears or moan. There is no doubt in such a case that wakefulness is present; but what of awareness?

This condition, the persistent vegetative state, is sometimes described as a condition of “wakeful unconsciousness” or “wakefulness without awareness.” Despite the recovery of the sleep-wake cycle, sufferers appear to be unaware of their surroundings and their bodies, make no purposeful response to stimulation, and neither understand nor produce speech.

It is impossible to be absolutely sure that another human being, especially one who appears to be awake, is utterly unaware. Indeed, a recent report from a center which specializes in the care of such cases claims that the vegetative state is diagnosed in error about half the time. Nevertheless, there is general agreement that this state—of wakefulness without awareness—sometimes genuinely occurs. Confidence in the diagnosis grows when brain scans show damage in all the brain areas which are thought to supply the content of consciousness, or when studies of the brain’s energy consumption show that it has fallen profoundly. In the persistent vegetative state it may drop to around one-third of its normal value, well below the levels recorded in sleep or even in general anaesthesia.

Studies of large groups of patients in this state indicate that after a certain duration— from six months to one year, varying with the cause—the persistent vegetative state is very likely to be permanent. Many believe that further medical support is then inappropriate, a view upheld by British courts.

In the vegetative state the brainstem survives while the hemispheres perish. In the state of “brain death” the hemispheres may be perfectly healthy, but the brainstem has succumbed. We diagnose this unhappy outcome of coma when brainstem functions are all unequivocally absent; these range from the control of breathing to the reflex movement of the eyes. Remediable causes of this state of affairs—such as an overdose of certain drugs— must have been excluded before brain death is diagnosed. The implications of this diagnosis are of course profound. Once it has been made, assuming the family gives consent, it is regarded as legitimate—in the United Kingdom—to remove a patient’s organs for transplantation.

It may seem curious that the brainstem is the crux of life; the hemispheres, surely, are the key to our humanity and intellect. So they may be, but intellect ain’t everything. We can survive the loss of our hemispheres, albeit much diminished, but even if life is given its best chance by artificial ventilation the loss of the brainstem appears to lead inexorably to death. A recent study from Taiwan followed 73 patients who satisfied criteria for brainstem death; the heart stopped beating in all 73 within seven days despite full-scale life support.

One last condition which can mimic coma deserves a mention here. Partial damage to the brainstem occasionally spares the activating system, while disabling the fibre tracts and nuclei which enable us to move our face and limbs. In these circumstances awareness may survive while almost all means of expressing it are lost, an unhappy state of affairs known as the “locked-in syndrome.” Sufferers from this disorder usually retain the ability to make voluntary up and down movements of their eyes, and can use these to communicate. This was the fate of Jean-Dominique Bauby, the author of the bestseller The Diving-Bell and the Butterfly. It is difficult to rule out the disturbing possibility that individuals like Bauby are not the only sufferers from the syndrome—but rather the only ones we can readily recognize.  

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Scientific Advisory Board
Joseph T. Coyle, M.D., Harvard Medical School
Kay Redfield Jamison, Ph.D., The Johns Hopkins University School of Medicine
Pierre J. Magistretti, M.D., Ph.D., University of Lausanne Medical School and Hospital
Robert Malenka, M.D., Ph.D., Stanford University School of Medicine
Bruce S. McEwen, Ph.D., The Rockefeller University
Donald Price, M.D., The Johns Hopkins University School of Medicine

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