Brain, Vol. 124, No. 7, 1263-1289,
July 2001
© 2001 Oxford University Press
Invited review |
Consciousness
Department of Clinical Neurosciences, Western General Hospital, Edinburgh, UK
Correspondence to:
A. Zeman, Department of Clinical Neurosciences, Western General Hospital, Edinburgh EH4 2XU, UK E-mail: az{at}skull.dcn.ed.ac.uk
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Abstract |
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Consciousness is topical, for reasons including its renewed respectability among psychologists, rapid progress in the neuroscience of perception, memory and action, advances in artificial intelligence and dissatisfaction with the dualistic separation of mind and body. Consciousness is an ambiguous term. It can refer to (i) the waking state; (ii) experience; and (iii) the possession of any mental state. Self-consciousness is equally ambiguous, with senses including (i) proneness to embarrassment in social settings; (ii) the ability to detect our own sensations and recall our recent actions; (iii) self-recognition; (iv) the awareness of awareness; and (v) self-knowledge in the broadest sense. The understanding of states of consciousness has been transformed by the delineation of their electrical correlates, of structures in brainstem and diencephalon which regulate the sleep–wake cycle, and of these structures' cellular physiology and regional pharmacology. Clinical studies have defined pathologies of wakefulness: coma, the persistent vegetative state, the `locked-in' syndrome, akinetic mutism and brain death. Interest in the neural basis of perceptual awareness has focused on vision. Increasingly detailed neuronal correlates of real and illusory visual experience are being defined. Experiments exploiting circumstances in which visual experience changes while external stimulation is held constant are tightening the experimental link between consciousness and its neural correlates. Work on unconscious neural processes provides a complementary approach. `Unperceived' stimuli have detectable effects on neural events and subsequent action in a range of circumstances: blindsight provides the classical example. Other areas of cognitive neuroscience also promise experimental insights into consciousness, in particular the distinctions between implicit and explicit memory and deliberate and automatic action. Overarching scientific theories of consciousness include neurobiological accounts which specify anatomical or physiological mechanisms for awareness, theories focusing on the role played by conscious processes in information processing and theories envisaging the functions of consciousness in a social context. Whether scientific observation and theory will yield a complete account of consciousness remains a live issue. Physicalism, functionalism, property dualism and dual aspect theories attempt to do justice to three central, but controversial, intuitions about experience: that it is a robust phenomenon which calls for explanation, that it is intimately related to the activity of the brain and that it has an important influence on behaviour.
consciousness; awareness; perception; neuropsychology; neuroscience
ARAS = ascending reticular activating system; NCC = neural correlate of consciousness; REM = rapid eye movement; SWS = slow wave sleep
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Introduction |
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TopAbstractIntroductionI. IntroductionII. Concepts of consciousnessIII. The science of...IV. The science of...V. Theories of consciousnessVI. The philosophy of...VII. ConclusionAcknowledgementsReferences |
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Contents
Summary
I Introduction 1264
II Concepts of consciousness 1265
(a) The etymology of `consciousness' and `conscience' 1265
(b) The meanings of `consciousness' 1265
(i) Consciousness as the waking state 1265
(ii) Consciousness as experience 1266
(iii) Consciousness as mind 1266
(c) The meanings of `self-consciousness' 1266
(i) Self-consciousness as proneness to embarrassment 1266
(ii) Self-consciousness as self-detection 1266
(iii) Self-consciousness as self-recognition 1266
(iv) Self-consciousness as awareness of awareness 1266
(v) Self-consciousness as self-knowledge 1266
III The science of wakefulness 1267
(a) The electricity of the brain 1267
(b) The control of conscious states 1268
(i) Anatomy 1268
(ii) Physiology 1269
(iii) Pharmacology 1270
(c) Pathologies of wakefulness 1271
IV The science of awareness 1272
(a) Exquisite correlations 1273
(b) Implicit perception 1275
(c) Insights from the study of memory and action 1277
V Theories of consciousness 1278
(a) Neurobiological theories 1278
(b) Information processing theories 1280
(c) Social theories 1281
VI The philosophy of consciousness 1282
(a) Three intuitions about consciousness 1282
(b) Identity theory 1282
(c) Functionalism 1283
(d) Dualism 1283
VII Conclusion 1284
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I. Introduction |
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The past decade has seen a rising tide of interest in consciousness, accompanied by a surge of publications, new journals and scientific meetings (Dennett, 1991
; McGinn, 1991; Edelman, 1992; Flanagan, 1992; Milner and Rugg, 1992; Searle, 1992; Crick, 1994; Penrose, 1994; Metzinger, 1995; Chalmers, 1996; Velmans 1996; Weiskrantz, 1997; Hurley, 1998; Jasper et al., 1998; Rose, 1998; Velmans, 2000). The `problem of consciousness' has been identified as an outstanding intellectual challenge across disciplines ranging from basic neuroscience through psychology to philosophy, although opinions vary widely on the chances of achieving a solution. The subject is unusual in drawing together scholars from both sides of the gulfs which separate the sciences and the arts, the study of the body and the study of the mind. Several factors help to explain the current fascination with consciousness. The techniques of physiological psychology, human neuropsychology and, recently, functional imaging are revealing exquisitely detailed correlations between neural processes and features of conscious experience. The recognition of unconscious or `implicit' capacities which can exert an influence on behaviour, such as blindsight, has opened up the way to distinguishing the neural substrates of conscious and unconscious activity in the brain. Advances in computational science and artificial intelligence hold out the prospect of engineering conscious systems. More generally, there is a deep dissatisfaction with the Cartesian separation of body and mind, and a desire to find a place for subjective experience in the scientist's world picture.
This is a timely moment to review progress in the field. As at least part of the problem of consciousness flows from the ambiguities of the term, I shall briefly consider its various senses, and its relationship to `self-consciousness', in Section II, flagging up some philosophical problems for later discussion. Sections III and IV provide a necessarily selective review of empirical research bearing on mechanisms of arousal, visual awareness, memory and volitional, or conscious, action. Section V examines a number of overarching theories of consciousness. Section VI reflects on the philosophical `problem of consciousness' in the light of the empirical advances and recent contributions to the philosophical debate.
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II. Concepts of consciousness |
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(a) The etymology of `consciousness' and `conscience'
The word `consciousness' has its Latin root in conscio, formed by the coalescence of cum, meaning `with', and scio, meaning `know'. In its original Latin sense, to be conscious of something was to share knowledge of it, with someone else, or with oneself. The knowledge in question was often of something secret or shameful, the source of a bad conscientia, a bad conscience. A `weakened' sense of conscientia coexisted in Latin with the stronger sense which implies shared knowledge: in this weak sense conscientia was, simply, knowledge. All three senses (knowledge shared with another, knowledge shared with oneself and, simply, knowledge) entered the English language with `conscience', the first equivalent of conscientia. The words `conscious' and `consciousness' first appear early in the 17th century, rapidly followed by `self-conscious' and `self-consciousness' (Lewis, 1960
).
(b) The meanings of `consciousness'
The Oxford English Dictionary distinguishes 12 senses of `conscious' and eight of `consciousness'. For our purposes it is helpful to distinguish three principal meanings (Zeman et al., 1997).
(i) Consciousness as the waking state
In everyday neurological practice consciousness is generally equated with the waking state, and the abilities to perceive, interact and communicate with the environment and with others in the integrated manner which wakefulness normally implies. Consciousness in this sense is a matter of degree: a range of conscious states extends from waking through sleep into coma. These states can be defined objectively, using behavioural criteria like those supplied by the Glasgow Coma Scale (Teasdale and Jennett, 1974). Thus we speak of consciousness dwindling, waning, lapsing and recovering; it may be lost, depressed and regained. To be conscious in this sense is to be awake, aroused, alert or vigilant.
(ii) Consciousness as experience
Consciousness in its first sense is the behavioural expression of our normal waking state.1 But when we are conscious in this first sense we are always conscious of something. In its second sense consciousness is the content of experience from moment to moment: what it feels like to be a certain person, now, in a sense in which we suppose there is nothing it feels like to be a stone or lost in dreamless sleep (Nagel, 1979). This second sense of consciousness is more inward than the first. It highlights the qualitative, subjective dimension of experience. Philosophers sometimes use the technical (and controversial) term `qualia' to refer to the subjective texture of experience which is the essence of this second sense of consciousness (Dennett, 1988; Chalmers, 1996).
Several authors have followed William James in seeking to characterize the general properties of consciousness which call for scientific explanation (James, 1890; Shallice, 1988; Searle, 1992; Crick, 1994; Chalmers, 1996; Greenfield, 1998; Tononi and Edelman, 1998a). There is a broad consensus that, in addition to its qualitative character, the following features are central: consciousness is personal, involving a conscious subject with a necessarily limited point of view; its contents are stable for short periods, lasting from hundreds of milliseconds to a few seconds, but characteristically vary over longer intervals; its contents are unified at any one time; they are continuous over time, in the sense that memory normally allows us to connect consciousness of the present with consciousness of the past; consciousness is selective, with a foreground and background, and a limited capacity at a given moment; over time, however, it ranges over innumerable contents, with potential contributions from each of the senses, and from all the major psychological processes, including thought, emotion, memory, imagination, language and action planning. Most states of consciousness are `intentional', in the philosophical sense that they are directed at the world, consciousness of this or that, and these states, in turn, are `aspectual': conditioned by the perspective which our conscious viewpoint affords (Searle, 1992). Finally, most commentators emphasize the centrality of consciousness to human values: the prolongation of human life, where one can be certain that consciousness has been lost forever, is generally regarded as a wasted effort.
Although we all tend to consider ourselves expert witnesses on the nature of our experiences, the thought that we may be misled by introspection, and that our experience is not as we usually take it to be, underlies several lines of recent work. For example, research on our sensitivity to change in our visual surroundings suggests that the focus of our visual attention is much narrower than we normally suppose (O'Regan, 2000; O'Regan and Noe, 2001); work requiring subjects to give instantaneous reports of their current experience, at the moment a random buzzer sounds, reveals a surprising preponderance of reports of `inner thought' (Hurlburt, 2000); approaches inspired both by the phenomeno-logical tradition in continental philosophy2, and by the practice of meditation, emphasize the potential value of disciplined observation of awareness in supplying first-person data for the scientific study of consciousness (Varela and Shear, 1999). These lines of research take the qualitative character of consciousness seriously while recognizing that our ordinary assumptions about it may be mistaken. This attentive but critical scrutiny of the `view from within' (Varela and Shear, 1999) is a promising development.
(iii) Consciousness as mind
Echoing the weakened Latin sense of conscientia, any mental state with a propositional content can be said to be conscious—anything that we believe, hope, fear, intend, expect, desire, etc. Thus we might accurately say that `the prime minister is conscious of the funding crisis in the health service' at a time when his thoughts are quite otherwise occupied. Most of the recent interest in consciousness has centred on its first and second senses, rather than this third sense in which consciousness is synonymous with mind.
It may be helpful to give one example of the use of `conscious' in each of these three main senses: (i) after a lucid interval, the injured soldier lapsed into unconsciousness; (ii) I became conscious of a feeling of dread, and an overpowering smell of burning rubber; (iii) I am conscious that I may be straining your patience.
(c) The meanings of `self-consciousness'
`Self-consciousness' is also a multi-faceted concept.
(i) Self-consciousness as proneness to embarrassment
The idiomatic sense of self-consciousness implies awkwardness in the company of others. Interestingly, we are self-conscious in this sense when we are excessively aware of others' awareness of ourselves. This humdrum usage thus turns out to be rather sophisticated, hinting at a link between consciousness of self and consciousness of others which is a focus of current research in developmental psychology (Baron-Cohen, 1995; Frith and Frith, 1999).
(ii) Self-consciousness as self-detection
We might speak of an organism as self-conscious if it can respond to stimuli which impinge upon it directly, or modify its behaviour in ways which imply an awareness of its own actions. Thus your awareness of an insect walking across your hand involves self-consciousness in this rather minimal sense. Rats, who can be trained to respond to a signal in a way that depends on what they were doing last, may be conscious of their own actions in a similar sense (Beninger et al., 1974). But this variety of self-consciousness amounts to little more than perceptual awareness, directed towards events brought about by, or ones which impinge directly upon, the creature in question.
(iii) Self-consciousness as self-recognition
Chimpanzees and orang-utans, but not monkeys, in common with children over ~18 months of age can recognize themselves in mirrors (Gallop, 1970). This ability implies the possession of a rudimentary concept of self. The flowering of the `idea of me' in the human child over subsequent months is attested by the mastery of the first person pronoun and a growing interest in self-adornment (Parker et al., 1995). But physical and verbal self-recognition falls short of the most distinctively human species of self-consciousness, which allows us to reflect upon the mental lives of others and ourselves.
(iv) Self-consciousness as awareness of awareness
We constantly attribute mental states in the everyday explanation and prediction of behaviour: talk of states of perception, desire and belief, for example, peppers our conversation. These have recently been described as evidence for an implicit `theory of mind' (Frith and Frith, 1999). Thus by the age of 5 most children have discovered that they and others are fallible subjects of experience, who glimpse the world from eccentric points of view and are prey to deception and misapprehension. An influential account of autism suggests that the core impairment in this condition stems from the failure to acquire such a `theory of mind' (Baron-Cohen, 1995). This sense of self-consciousness echoes the idiomatic use of the term, and although we tend to regard self-consciousness in its colloquial sense as a social disadvantage, we would not really want to be without it: only a nuance separates the valuable ability to inform ourselves about the impression we are making on others from the awkward encumbrance of `self-consciousness'.
(v) Self-consciousness as self-knowledge
Like consciousness, self-consciousness has an extended final sense. It can refer to our knowledge of the broad social and cultural background which shapes us: thus my `idea of me' takes in not just a body and a mind but membership of a cultural and linguistic community, a profession, a family group. In this extended sense our self-consciousness evolves throughout our lives, as it has done through the course of history. It finds its richest expression in self-portraiture and autobiography, activities of which most human children, but no other animals, are enthusiastic practitioners from an early age.
How do consciousness and self-consciousness in their various senses interrelate? Superficially they appear to be independent. There is no compelling reason to regard self-consciousness in any of the important senses we have distinguished (iii–v) as an absolute prerequisite for the three varieties of consciousness which we have teased apart. But we need to beware of prejudging difficult issues with premature definition. There are at least two connections in which my definitions may prove misleading. I will highlight these here, and return to the difficulties they point towards later.
First, I have taken the existence of `qualia', the supposed subjective qualities of experience, on trust, but in the philosophical literature their existence is highly contentious (Dennett, 1988; O'Regan and Noe, 2001). Reductive analyses of consciousness hold out the hope that experience, in all its subjective richness, can be exhaustively described in the objective terms of function and physiology (Dennett, 1991). If it can, the characterization of consciousness which I have offered in its second sense, as the inescapably subjective contents of awareness, may lure us into the pursuit of an illusion. Reductionists seek to dispel this illusion, and in so doing to cure us of the misunderstandings which, allegedly, give rise to the `problem of consciousness'. I shall examine the merits of these views in Section VI.
Secondly, although I have argued that consciousness is independent of self-consciousness, possible interconnections between them compose a recurring theme in the literature, echoing consciousness' connotation of knowledge shared. The idea is in play, for example, in Mead's description of consciousness as `self-address using significant symbols' (Natsoulas, 1983), in Rosenthal's conception of consciousness as involving `the thought that one is in [a certain] mental state' (Rosenthal, 1986) and in Nicholas Humphrey's suggestion that consciousness evolved to provide Machiavellian insight into the minds of others by way of awareness of one's own mental states (Humphrey, 1978). Most, but probably not all, of these links between consciousness and self-consciousness, imply a social origin for consciousness. We will take this issue up again in Section V.
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III. The science of wakefulness |
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A full biological account of consciousness would specify its mechanisms, functions, phylogeny and ontogeny. I will concentrate on its mechanisms in the following two sections, reviewing first our knowledge of the neural basis of sleep and wakefulness (Section III), and then our understanding of the neural processes which underly the contents of awareness, particularly visual awareness ( Section IV).
Two interlacing strands of enquiry have informed the study of wakefulness over the past century: the investigation of the electrical correlates of states of consciousness, and the discovery that critical structures in the brainstem, thalamus and basal forebrain regulate conscious states.
(a) The electricity of the brain
Sensory evoked potentials were recorded from the brains of experimental animals by physiologists in Britain and continental Europe during the 19th century (Brazier, 1961). Several of these scientists also noted the occurrence of spontaneous electrical activity over the cortex of unstimulated animals, but it was not until 1929 that Hans Berger, a psychiatrist working in Jena, published his landmark observations `On the Electroencephalogram of Man' (Berger, 1929) (Fig. 1). Although Berger's foremost achievement was to demonstrate that spontaneous activity could be recorded from the human brain with extracranial electrodes, his underlying purpose was to elucidate the physical basis of consciousness. His first paper closed with a series of questions which were to launch a fertile, continuing programme of research: how is the EEG affected by sensory stimulation, by sleep, by drugs which alter mental state and by intellectual activity?
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Berger distinguished two contrasting rhythms of wakefulness: `alpha' at 8–13 Hz which characterizes the `passive EEG', typically recorded from occipital electrodes in a waking subject with eyes closed; and `beta' rhythm, occurring at frequencies >13 Hz, the `active EEG' which accompanies mental exertion. It was soon appreciated that slower rhythms (`theta' waves, at 4–7 Hz, and `delta' at <3.5 Hz) at higher amplitudes characterize states of reduced arousal in adults. Their cyclical involvement in sleep became apparent in the 1950s, particularly from the work of Kleitman and his collaborators (Fig. 2
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) rhythm (8–13 Hz); theta (
) rhythm (4–7 Hz) and delta (
) rhythm (<4 Hz). The theta trace was obtained from a sleep encephalogram; the delta trace from a wakeful, but confused, patient with an encephalopathy. In each case the dotted line bisects a 2 s sample.In 1955 Aserinsky and Kleitman reported the repeated occurrence of periods of `rapid eye movement sleep' in the course of the night; sleepers woken during these periods were likely to report concurrent dreams (Aserinsky and Kleitman, 1955
). Two years later Dement and Kleitman demonstrated the cyclical structure of sleep on the basis of observations of eye movements, body movements and EEG appearances in normal sleepers (Dement and Kleitman, 1957). This work helped to define the distinction between `slow wave sleep' (SWS), associated with a high proportion of delta activity in the EEG, and `rapid eye movement' (REM) or `paradoxical' sleep, during which the features of the EEG resemble those in the waking state, although subjects are paradoxically difficult to arouse. Predictable cycles of descent into SWS, followed by ascent into REM sleep, recur four or five times each night, with decreasing proportions of SWS and increasing proportions of REM sleep as the night proceeds (Chokroverty, 1999).
These behavioural and electrical observations have helped to define three principle states of consciousness in health: wakefulness, REM sleep and SWS. This view has historical precedent: the Upanishads, dating from around 2000 BC, define the same three basic states (Jones, 1998). While SWS has sometimes been characterized as a state of electrical synchronization in contrast to the `desynchronized' EEG of wakefulness and REM sleep, interest has been aroused recently by the possibility that activity synchronized across the brain in the gamma frequency range, at 35–45 Hz, may be a signature of the waking state and REM sleep (Llinas and Ribary, 1993; John, 2000) (Fig. 3). If so, such activity might provide an explanation for the unity of the contents of awareness. We shall return to this topic.
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More generally, Berger's discovery and its subsequent developments suggest a tendency to widespread synchronization of brain activity, whose functional significance has not yet been fully unravelled. The existence of mechanisms for synchronization helps to explain why epilepsy—resulting from the pathological synchronization of cerebral activity—should be such a common disorder of consciousness. In its applications to the topics which Berger thought promising at the end of his first paper, the EEG has proved hugely fruitful: sensory evoked potentials, the growing variety of cognitive potentials and the Bereitschaftpotential (a `readiness potential' which can be recorded over motor areas up to 1 s before the execution of a movement) have demonstrated that sensation, attention, intellectual activity and the planning of movement all have distinctive electrical correlates at the surface of the skull (Kutas and Dale, 1997
).
(b) The control of conscious states
(i) Anatomy
Clinico-pathological studies made at the time of the epidemic of encephalitis lethargica which occurred during and after the First World War suggested to the Viennese pathologist Constantin Von Economo that structures in the upper brainstem and posterior hypothalamus mediate arousal (Von Economo, 1931). Frederic Bremer later confirmed this suggestion experimentally by showing that transection of the cat's brain at the cervicomedullary junction had no effect on arousal, or on the sleep–wake cycle, while transection through the midbrain brought about a state resembling deep sleep (Bremer, 1929).
Bremer hypothesized that this impairment of arousal resulted from interruption of ascending sensory pathways in the midbrain. His student Giuseppe Moruzzi, working with Horace Magoun, later showed that the critical areas were not, in fact, in the sensory pathways but rather in the reticular core of the upper brainstem and, probably, their thalamic targets (Moruzzi and Magoun, 1949). Moreover, electrical stimulation of this region in a drowsy animal `activated' the EEG. These observations gave birth to the concept of the `ascending reticular activating system' (ARAS) (Fig. 4). While the central insight of this concept, that structures in the brainstem regulate our states of consciousness, still holds true, a much more complex picture has emerged since the pioneering work of Moruzzi and Magoun. The ARAS is no longer regarded as a monolithic unit, nor as a system restricted to the classically defined `reticular' nuclei of the brainstem; indeed, activating structures are not confined to the brainstem at all, and their influence descends to the spinal cord as well as ascending to the cerebral hemispheres.
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Rather than revealing any single `place where consciousness dwells', the exploration of these structures is identifying a series of somewhat specialized nodes in a complex network controlling aspects of arousal (Fig. 5
). It would be surprising if functions as fundamental as the maintenance of wakefulness or the control of the sleep–wake cycle depended exclusively and unalterably on any single region of the brain (Steriade, 1999). Experimental work in animals suggests that the following structures play key roles in the maintenance and modulation of wakefulness: cholinergic nuclei in the upper brainstem and basal forebrain; noradrenergic nuclei, in particular the locus coeruleus; a histaminergic projection from the posterior hypothalamus; and probably dopaminergic and serotonergic pathways arising from the brainstem (McCarley, 1999) (Fig. 6). Much, but not all, of the influence exerted by these pathways is mediated by the thalamus, which can be regarded as the apex of the ARAS, as well as a critical synaptic relay for most sensory and many intracerebral pathways (Jones, 1998) (Fig. 7). The function of these activating structures is not, of course, confined to the maintenance of wakefulness: they are of profound importance to a wide range of interrelated functions including mood, motivation, attention, learning, memory and movement (Robbins and Everitt, 1993; Marrocco et al., 1994).
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Some specific contributions made by these and other structures to the regulation of conscious states have been defined. For example, the suprachiasmatic nucleus of the hypothalamus has emerged as the timekeeper of consciousness (Kilduff and Kushida, 1999
). It normally entrains the sleep–wake cycle to the alternation of night and day under the influence of the direct retinohypothalamic projection. Transection experiments by Jouvet and subsequent work have established the key importance of cholinergic nuclei at the pontomesencephalic junction, the laterodorsal tegmental and pedunculopontine nuclei, in orchestrating the phenomena of REM sleep, i.e. activation of the EEG, pontogeniculo-occipital waves, rapid eye movements and muscle atonia (McCarley, 1999). The location of structures crucial for the induction of SWS remains uncertain (McCarley, 1999). A reduction of activity in the cholinergic, noradrenergic and histaminergic nuclei which maintain wakefulness is clearly relevant (Zoltoski et al., 1999); candidates for a critical role in sleep induction include the anterior hypothalamus (Sherin et al., 1996) and basal forebrain (McCarley, 1999).
Recent functional imaging studies of regional brain activity in the three major behavioural states in man have corroborated and extended the conclusions drawn from animal experiment and clinical observations. Global cerebral glucose metabolism falls in SWS by ~20%, rising back to, or even above, waking levels in REM (Heiss et al., 1985; Buchsbaum et al., 1989). During SWS regional blood flow declines, in proportion to the amount of slow wave activity on EEG, in the rostral brainstem, thalamus, prefrontal and cingulate cortex (Hofle et al., 1997; Macquet et al., 1997). In REM sleep regional blood flow increases in the rostral brainstem, thalamus and limbic regions, in keeping with the electrical and subjective features of dreaming sleep, but declines in prefrontal and posterior cingulate cortex, and in some regions of parietal cortex (Macquet et al., 1996). Variations in the level of arousal during wakefulness also appear to correlate with levels of activity in the structures of midbrain and thalamus which regulate conscious states: Kinomura and colleagues reported activation of the midbrain tegmentum and intralaminar nuclei of the thalamus by the transition from a resting state to the performance of visual and somatosensory reaction time tasks (Kinomura et al., 1996); Paus and colleagues have described a decrease in midbrain and thalamic activation during a tedious 1 h auditory detection task, associated with declining performance and increasing slow wave activity on EEG (Paus et al., 1997). Finally, there is evidence that the loss of consciousness induced by some anaesthetics is associated with selective depression of thalamic function, linking the mechanisms of anaesthesia and sleep (Fiset et al., 1999; Alkire, 2000).
(ii) Physiology
It should, in principle, be possible to explain the behavioural and electrical features of the three major states of consciousness in terms of the characteristics of relevant neuronal types and the networks in which they are organized. Substantial progress has been made in this direction. This is well illustrated by way of the contrast between neuronal activity during sleep and during wakefulness within the thalamus.
In the waking state thalamocortical neurones are tonically depolarized by cholinergic, noradrenergic and histaminergic inputs from the brainstem and hypothalamus, which block a hyperpolarizing potassium conductance (Steriade et al., 1990, 1993; McCarley, 1999; Steriade, 1999). This induces a `spike mode' of response in thalamocortical cells, permitting faithful onward transmission of afferent signals to the thalamus. The reduction of the depolarizing input in SWS induces a contrasting `burst mode' of response, dependent upon a low threshold calcium conductance, which predisposes these cells to patterns of repetitive discharge while hyperpolarized (Fig. 8). The simultaneous disinhibition of the reticular nucleus of the thalamus in early sleep, following reduction of inhibitory cholinergic input from the brainstem, allows it to exert a synchronized GABAergic inhibition of thalamocortical cells, which ultimately gives rise to the `spindles' abounding in stage 2 sleep. Further hyperpolarization of thalamocortical cells, as sleep deepens, allows them to participate in slow wave oscillations to which the individual and network properties of thalamocortical cells, corticothalamic cells and neurones of the reticular nucleus all contribute. Reduction of direct non-specific excitatory inputs to the cortex, as well as effects occurring primarily at the level of the thalamus, is conducive to the generation of these rhythms. Thus the distinction at an electrophysiological level between spike and burst modes of response in thalamocortical neurones corresponds with the behavioural distinction between the responsiveness of the waking state and the inaccessibility of sleep, and mirrors the global shift between the waking and the sleeping EEG.
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(iii) Pharmacology
As we have seen, the pharmacological dissection of the `reticular activating system' has revealed the presence of several chemically distinct but interactive subsystems: cholinergic, noradrenergic, dopaminergic, serotonergic and histaminergic (Robbins and Everitt, 1993; Marrocco et al., 1994
). The actions of each of these transmitters are complex, depending upon the site of release and the nature of the receptor targeted. Nonetheless it is at least clear that the firing of cells in cholinergic and noradrenergic brainstem nuclei is `state dependent' and correlates with wakefulness (McCarley, 1999).
Evidence that REM sleep is dependent upon activity in cholinergic nuclei, while noradrenergic and serotonergic nuclei are least active in this phase of sleep has given rise to a `reciprocal interaction' model of sleep architecture. This proposes that the regular alternation of SWS and REM sleep over the course of the night is regulated by the waxing and waning of mutually inhibitory activity in these nuclei. The pharmacological basis of `sleep debt', i.e. the increasing pressure to sleep as the period of wakefulness extends, remains a confusing area. A number of potential `hypnotoxins', i.e. sleep-promoting substances, usually accumulating during wakefulness, have been identified (Zoltoski et al., 1999). Recent evidence suggests that a particularly important role may be played by elevation of extracellular adenosine concentrations during wakefulness, with resulting inhibition of activating cholinergic nuclei in the upper brainstem and basal forebrain (McCarley, 1999).
Future work on the pharmacology of wakefulness is likely to demonstrate distinctive roles for the neurotransmitters of the `activating system' in modulating different aspects of arousal. `Wakefulness', after all, is shorthand for a set of associated neural, behavioural and psychological functions which are, to some extent, independently controlled. This is evident from a range of pathological states in which the usual associations between these states break down. Thus, for example, a sleepwalker is capable of coordinated movement, may be able to avoid obstacles and accede to gentle urging to return to bed, but will later have no recall of the episode; motor control, perception and memory have lost their usual relationship (Mahowald and Schenck, 1992). In work exploring the idea that the neurotransmitters linked with arousal make distinctive contributions, Robbins and Everitt have found, using a consistent set of behavioural tests, that selective damage to the noradrenergic system impairs selective attention, damage to the cholinergic system impairs baseline accuracy, damage to the dopaminergic system lengthens response latency and probability of response, and damage to the serotonergic system leads to impulsive responding (Robbins and Everitt, 1995).
(c) Pathologies of wakefulness
The key roles of the brainstem and thalamus in the maintenance of wakefulness help to explain the pathologies of arousal which follow structural brain damage.
Coma is a state of continuous `eyes-closed' unconsciousness, in the absence of a sleep–wake cycle (Plum and Posner, 1982; Plum, 1991; Schiff and Plum, 2000). It varies in degree from mild to profound unresponsiveness, and is associated with a comparably variable reduction in cerebral metabolism. It results from diffuse hemispheric or focal brainstem/thalamic injury and is usually a transitional state, en route to full recovery, brainstem death or a state of chronically impaired awareness with recovery of the sleep–wake cycle. The risk of confusing the `locked-in state' with coma is now well recognized. In this syndrome, which follows brainstem lesions abolishing the descending control of voluntary movement, patients are only able to communicate using movements of the eyes or eyelids.
Brainstem death (Pallis and Harley, 1996) implies the irreversible loss of all brainstem functions. In the United Kingdom it renders legal the removal of organs for transplantation, provided that appropriate consent has been obtained. It is generally followed by cardiac death, within hours to weeks, although there are reported exceptions to this rule (Shewmon, 1998).
The vegetative state, described by Jennett and Plum in 1972 (Jennett and Plum, 1972; Multi-Society Task Force on PVS, 1994; Zeman et al., 1997), is in a sense the converse of brainstem death: in this condition, characterized by `wakefulness without awareness', patients regain their sleep–wake cycle, and may be aroused by painful or salient stimuli, but show no unambiguous signs of conscious perception or deliberate action, including communicative acts. Recovery from a vegetative state often occurs: younger age and a traumatic, rather than hypoxic–ischaemic, causation improve the outlook. After 1 month the state is often termed `persistent', and in patients in whom recovery appears highly unlikely it may be deemed `permanent', although permanence cannot be predicted with certainty. The underlying pathology usually involves (i) diffuse cortical injury, typically cortical laminar necrosis; (ii) diffuse white matter injury, typically diffuse axonal injury or leucoencephalopathy; or (iii) thalamic necrosis. `Minimally responsive states' are sometimes distinguished from the vegetative state; these involve some consistent or inconsistent evidence of intelligent awareness in the presence of profound continuing physical and cognitive impairment. Akinetic mutism is a related state of profound apathy with evidence of preserved awareness, characterized by attentive visual pursuit and an unfulfilled `promise of speech'. It is often associated with damage to the medial frontal lobes.
The distinctions between coma, brainstem death and the vegetative state are useful and moderately robust in clinical practice. But they are not immune to practical or theoretical criticism. At a practical level, there are apparent examples of long survival in `brain dead' patients (Shewmon, 1998), and evidence that the vegetative state is often misdiagnosed in patients who are, in fact, aware of their surroundings (Childs et al., 1993; Andrews et al., 1996). At a theoretical level, it is conceivable that brainstem death may become a treatable disorder as neural prostheses are developed, and it is open to question whether patients in vegetative states are wholly unaware. These clinical concepts are still in evolution.
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IV. The science of awareness |
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TopAbstractIntroductionI. IntroductionII. Concepts of consciousnessIII. The science of...IV. The science of...V. Theories of consciousnessVI. The philosophy of...VII. ConclusionAcknowledgementsReferences |
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If the study of healthy and disordered states of consciousness has clarified the neural basis of arousal, the study of vision has provided the outstanding source of evidence on the mechanisms underlying the contents of consciousness. Research in animals and man is defining increasingly fine-grained correlations between cerebral activity and visual experience, including experiences which occur, like visual hallucinations, or change, like ambiguous figures, without any corresponding changes in external stimuli. A second, complementary, approach has been opened up by the distinction between `explicit' neural processes which directly give rise to conscious awareness, e.g. conscious vision, and `implicit' processes, e.g. blindsight, which allow visuomotor performance in the absence of awareness. Subtracting the processes required for implicit perception from those involved in explicit perception should, in principle, help to delineate the key neural substrates of awareness. Work on learning has developed a parallel distinction between declarative and procedural memory. A third approach, linked to the last, looks toward action: changes in cerebral activity, as consciously directed action becomes automatized or otherwise divorced from conscious control, may illuminate the neurology of consciousness. I shall outline these approaches in turn.
(a) Exquisite correlations
Although it is not usually framed in these terms, one of the main goals of visual physiology is to account for the contents of visual consciousness. A series of discoveries in the course of this century have revolutionized our picture of the cerebral events which underlie conscious vision. Key findings include the definition of the retinotopic map in striate cortex (Holmes and Lister, 1916); the discovery of its orientation-specific columns by Hubel and Wiesel (Hubel and Wiesel, 1977); the realization that 30–40 functionally and anatomically visual areas surround area V1 (Cowey, 1994); the evidence that parallel, though interconnected, streams of visual information flow through these areas, subserving the perception of form, colour, depth and motion (Livingstone and Hubel, 1988); and the broad distinction between an occipitotemporal stream concerned with object identification and an occipitoparietal stream concerned with visually-guided action (Milner and Goodale, 1995).
A few examples will illustrate the grain of the correlations which have emerged between visual experience and regional activity in the visual system. Comparison of regional brain activation by coloured and by moving grey-tone visual stimuli indicates that the former strongly activate an area in the fusiform gyrus, possibly the human homologue of area V4, which has been shown in monkeys to contain a high proportion of colour selective neurones (Zeki, 1993). By contrast, moving achromatic stimuli selectively excite a more lateral region, at the occipitotemporal junction, termed `human V5' by Zeki and colleagues. The anatomical distinction between these regions helps to explain the existence of selective deficits of colour and movement perception in man occurring after focal cortical lesions, respectively cerebral achromatopsia and akinetopsia (Zeki, 1990, 1991). Zeki has extended these findings by showing that a figure which gives rise to a compelling illusion of movement also selectively activates human V5 (Zeki et al., 1993). There is some evidence that activity in area V5, in the absence of striate cortex, may be sufficient to generate the conscious experience of visual movement (Barbur et al., 1993), although this has recently been challenged (Cowey and Walsh, 2000). As visual information travels further down the stream of visual areas, retinotopic mapping tends to become less precise and the stimulus requirements of the local neurones become more complex. These downstream areas, demonstrated by functional MRI, are illustrated by the `fusiform face area' (Kanwisher et al., 1997), an area in the human fusiform gyrus selectively responsive to faces, and the `parahippocampal place area' (Epstein and Kanwisher, 1998), a region responsive to the visual appearance of locations.
Inferences about the generation of visual awareness, drawn from work of this kind, are open to the potential objection that, although these areas are activated by appropriate stimuli, they may not mediate the conscious experience of vision. Correlation does not imply cause, and, after all, much of the work on cortical visual responses in animals has been performed under anaesthesia. It is open to question, for example, whether area 17, primary visual cortex, directly contributes to visual awareness (Crick and Koch, 1995; Rees et al., 2000). This objection can be met, at least in part, by the use of paradigms in which visual awareness changes while external stimulation is held constant. Change in neuronal activity, detected under these circumstances, is more likely, although not guaranteed, to be linked specifically to changes in awareness. Work on visual imagery, hallucinations, attentional shifts and binocular rivalry has exploited this strategy.
We can summon up visual images `in the mind's eye' and interrogate them much as we do a real visual scene (Kosslyn and Shin, 1994). Shepard, Kosslyn and colleagues have shown that, in many respects, mental images are processed in similar ways to percepts of items in the real world (Shepard, 1978; Kosslyn and Shin, 1994). For example, decision tasks involving a minor mental rotation of complex shape are performed more quickly than tasks involving more extensive rotation, and the time required to search an imagined map is proportional to the distance travelled in the mind's eye. Recent reports, using functional imaging, indicate that these similarities in processing extend to similarities in the brain regions activated by real and imagined objects: for example, imagining a small object activates the representation of central vision in striate cortex, while imagining a large object activates more peripheral parts of the cortical map (Kosslyn et al., 1995); mental rotation tasks engage areas involved in tracking moving objects and encoding spatial relations (Cohen et al., 1996); imagining faces and places respectively excite the fusiform face area and hippocampal place area mentioned earlier (Kanwisher, 2000). This line of research suggests that the neural correlates of mental imagery overlap substantially with the correlates of perception.
Like mental images, visual hallucinations are visual percepts which occur in the absence of a corresponding external stimulus, but, unlike images, hallucinations are perceived as if they originated in the external world. A wide range of pathologies is associated with complex visual hallucinations, including partial epilepsy, structural disorders of the central visual pathways, disorders of the brainstem causing peduncular hallucinosis, narcolepsy, drug-induced hallucinosis, psychotic disorders and peripheral visual disorders giving rise to the Charles Bonnet syndrome (Manford and Andermann, 1998). A recent functional imaging study of this last condition found that hallucinations of faces, colours, textures and objects were associated with activity in the ventral occipital lobe (ffytche et al., 1998). Comparable results have been reported recently in the auditory domain (Griffiths, 2000). The blood flow changes detected by functional imaging, which usually follow the onset of the responsible stimulus by an appreciable delay, occurred in these patients several seconds before the onset of the hallucinations, suggesting that the neural activity responsible for a hallucination must evolve to a certain state before it gives rise to a conscious percept.
States of imagery and hallucination are rather special cases of perception. The very best opportunities to isolate the neural correlates of ordinary visual perception may come instead from studies of attentional shifts and `multistable' visual percepts.
Attention is the sentry at the gate of consciousness: `My experience is what I agree to attend to' (James, 1890).3 The essence of attention is `selection': whether we are displaying `preparatory attention' as we await an anticipated event, switching our attention between the senses or between the targets presented to a single sense, or sustaining our attention to a task, we are excluding a range of rival stimuli from the focus of our interest. Changes in the neural representation of items as they move in and out of the focus of attention should shed light on the neural accompaniments of consciousness. These changes have been termed the neural `expression' of attention (LaBerge, 1995).
Single cell recording from monkeys trained to shift visual attention without altering their gaze indicates that firing rates are increased in cells responding to attended stimuli, and reduced in cells responding to unattended stimuli in extrastriate visual areas, for example, areas V4 and V5 (Moran and Desimone, 1985; Treue and Maunsell, 1996). Recent functional imaging studies suggest that the neural expression of attention in man also involves focal enhancement and inhibition of neural activity; for example, switches of attention between faces and places presented simultaneously are associated with detectable modulations of activity in the fusiform and parahippocampal regions mentioned above (Kanwisher, 2000).
Multistable or ambiguous visual stimuli, like the Necker cube, which appears to reverse in depth during protracted viewing, are open to alternative visual readings. If incompatible stimuli are presented to the two eyes, they also tend to generate a `multistable' percept, as most viewers experience an alternation between the two images rather than a fusion. This paradigm has been applied both to animals and man to study the neural correlates of the alternating percept. Logothetis, working with monkeys, has reported that while many neurones in visual areas respond to the stimuli throughout their presentation, regardless of the current conscious percept, a subset of extrastriate neurones recorded in V4 and V5 raise or lower their firing rate markedly as the stimulus to which they respond gains or loses perceptual dominance (Logothetis and Schall, 1989; Leopold and Logothetis, 1996). Work by Engel and colleagues suggests that cells responding to the currently perceived member of a pair of rivalrous stimuli synchronize their discharges during the period of perceptual dominance to a greater degree than during periods of suppression (Engel et al., 2000).
Further down the processing stream, in experiments with human subjects, the modulation of neuronal activity in the fusiform face area and parahippocampal place area, as simultaneously presented faces and places alternate in awareness, is of similar size to the modulation seen when faces and places are alternately presented (Kanwisher, 1998). Thus, by this stage of processing in the human brain, activity correlates with the contents of awareness rather than with the raw features of the impinging stimuli. Using magnetoencephalography, Tononi and colleagues have reported that as conscious perception shifts between two gratings of different orientations, one horizontal, the other vertical, flickering at different frequencies, so the power of electromagnetic activity at the corresponding frequency waxes and wanes by 30–60% over wide regions of cortex (Tononi and Edelman, 1998b). Lumer and colleagues have found that right frontoparietal activation is associated with the transition between multistable percepts, suggesting that the neural control of these transitions, as opposed to the neural expression of the resulting percepts, may share common ground with the direction of spatial attention (Lumer et al., 1998).
These experiments, investigating imagery, hallucinations, attentional shifts and ambiguous percepts, are beginning to capture the neural correlates of visual experience. The precise definition of the `neural correlate of consciousness' in man (Koch, 1998) remains a goal for the future, and will probably require more sophisticated methods than those we currently have at our disposal, allowing the detailed measurement of disparate neuronal activity over short time scales in the human brain. Nevertheless the work we have just reviewed is helping to justify the neuroscientist's long-held article of faith: that every distinction drawn in experience and behaviour will be reflected by distinctions between patterns of neuronal activity.
(b) Implicit perception
The correlation of aspects of conscious vision with details of neural activity has been complemented by another approach, which aims to highlight the neurology of consciousness by contrasting it with the neural basis of unconscious processes. This offers an alternative solution to the problem mooted in the last section, that the correlation of neural events with conscious processes does not prove a causal relationship. `Subtraction' of the neural processes associated with unconscious processing from those correlated with consciousness should help to define the fundamental neural substrate of awareness. This is, so to speak, an attempt to conquer consciousness by stealth.
Two lines of research can be distinguished. The first studies the neural effects of sensory stimulation which may have no discernible effect whatever on behaviour; the second, more provocative, project is to explore the neural consequences of events which `might influence our experience, thought and action even though they themselves have not been consciously perceived' (Kihlstrom et al., 1992).
Some conceptual difficulties and terminological distinctions deserve a mention before reviewing examples of these two lines of research. The major conceptual problem for students of `unconscious' or `implicit' psychological processes is how to determine the presence or absence of consciousness. Much of the neuropsychological work in this area relies on verbal report (Barbur et al., 1993) or the use of a `commentary key' (Weiskrantz, 1997) to indicate the degree of awareness. But verbal reports and presses on commentary keys may not provide exhaustive measures of the information available to consciousness. Indeed, there are no conclusive reasons for thinking that consciousness should always be reportable, even in principle (Zeman, 2000). On the other hand, if any successful discrimination is taken to provide evidence of conscious perception, the possibility of unconscious perception is ruled out by definition (Kihlstrom et al., 1992). The lack of any `exhaustive measure that exclusively indexes relevant conscious perceptual experiences' is therefore a significant problem, though not necessarily an insuperable one (Merikle and Reingold, 1992). Psychologists have suggested a number of sophisticated solutions to the dilemma (Jacoby et al., 1992; Merikle and Reingold, 1992).
The following terminological distinctions are helpful. Implicit—or unconscious or subliminal—perception generally refers to perception occurring in the absence of any conscious experience of the information perceived. In this respect it is distinct from `residual experience', a term describing the rudimentary conscious experience which sometimes survives the substantial loss of a sense: for example, residual but clearly conscious experience of visual movement sometimes survives the substantial loss of sight caused by injuries to striate cortex (Weiskrantz, 1980; Barbur et al., 1993). Whether or not some examples of vaguely sensory `knowledge' surviving such damage represent residual experience has given rise to debate (Zeki and ffytche, 1998). A second useful distinction is between explicit and implicit processes and direct and indirect tasks (Weiskrantz, 1997). Explicit processes are those which yield overt knowledge of the material on which a given act or judgement is based; for example, if I can straightforwardly see the target at which I take my aim, the visual process is explicit and, if I can later recall the event, my process of recollection is as well. Direct tasks, by contrast, are those which involve instructions referring directly to the dimension of interest to the experimenter: a direct test of memory might ask for the contents of a word list; an indirect test might examine whether prior exposure to the words increased the ease with which they are identified on a very brief presentation. But a direct task may tap an implicit process—if, for example, we are asked to guess at the location of a visual stimulus which we have not consciously perceived—and an indirect task may tap an explicit process, if I recognize the items from the word list on their brief presentation.
Turning to the first line of research on implicit perception, the idea that stimuli impinging on the nervous system may have neural effects in the absence of any discernible effect on `experience, thought and action' is familiar. It is no surprise, for example, that some reflex responses, like the pupillary light reflex, can be elicited from the visual system in the absence of visual experience. Penetrating deeper into brain, cortical evoked potentials can be recorded from patients under anaesthesia (Jones, 1994; Schwender et al., 1994), as they can from anaesthetized experimental animals; low concentration odours evoke activity in olfactory regions at levels which do not permit even accurate guesses about their presence (Sobel et al., 1999); brief masked presentations of fearful faces activate the amygdala in the absence of acknowledged awareness (Morris et al., 1998; Whalen et al., 1998); some patients with prosopagnosia who a