Dehaene & Nacchache - Towards a cognitive neuroscience of consciousness

Towards a cognitive neuroscience of consciousness: basic evidence and a workspace framework Stanislas Dehaene*, Lionel Naccache Unite INSERM 334, Service Hospitalier FreÂdeÂric Joliot, CEA/DRM/DSV, 4, Place du GeÂneÂral Leclerc, 91401 Orsay Cedex, France Received 8 February 2000; accepted 27 September 2000 Abstract This introductory chapter attempts to clarify the philosophical, empirical, and theoretical bases on which a cognitive neuroscience approach to consciousness can be founded. We isolate three major empirical observations that any theory of consciousness should incorpo- rate, namely (1) a considerable amount of processing is possible without consciousness, (2) attention is a prerequisite of consciousness, and (3) consciousness is required for some speci®c cognitive tasks, including those that require durable information maintenance, novel combinations of operations, or the spontaneous generation of intentional behavior. We then propose a theoretical framework that synthesizes those facts: the hypothesis of a global neuronal workspace. This framework postulates that, at any given time, many modular cerebral networks are active in parallel and process information in an unconscious manner. An information becomes conscious, however, if the neural population that represents it is mobi- lized by top-down attentional ampli®cation into a brain-scale state of coherent activity that involves many neurons distributed throughout the brain. The long-distance connectivity of these `workspace neurons' can, when they are active for a minimal duration, make the information available to a variety of processes including perceptual categorization, long- term memorization, evaluation, and intentional action. We postulate that this global avail- ability of information through the workspace is what we subjectively experience as a conscious state. A complete theory of consciousness should explain why some cognitive and cerebral representations can be permanently or temporarily inaccessible to consciousness, what is the range of possible conscious contents, how they map onto speci®c cerebral circuits, and whether a generic neuronal mechanism underlies all of them. We confront the workspace model with those issues and identify novel experimental predictions. Neurophysiological, anatomical, and brain-imaging data strongly argue for a major role of prefrontal cortex, S. Dehaene, L. Naccache / Cognition 79 (2001) 1±37 1 Cognition 79 (2001) 1±37 www.elsevier.com/locate/cognit 0010-0277/01/$ - see front matter q 2001 Elsevier Science B.V. All rights reserved. PII: S0010-0277(00)00123-2 COGN I T I O N * Corresponding author. Tel.: 133-1-69-86-78-73; fax: 133-1-69-86-78-16. E-mail address: dehaene@shfj.cea.fr (S. Dehaene). anterior cingulate, and the areas that connect to them, in creating the postulated brain-scale workspace. q 2001 Elsevier Science B.V. All rights reserved. Keywords: Consciousness; Awareness; Attention; Priming 1. Introduction The goal of this volume is to provide readers with a perspective on the latest contributions of cognitive psychology, neuropsychology, and brain imaging to our understanding of consciousness. For a long time, the word `consciousness' was used only reluctantly by most psychologists and neuroscientists. This reluctance is now largely overturned, and consciousness has become an exciting and quickly moving ®eld of research. Thanks largely to advances in neuropsychology and brain imaging, but also to a new reading of the psychological and neuropsychological research of the last decades in domains such as attention, working memory, novelty detection, or the body schema, a new comprehension of the neural underpinnings of conscious- ness is emerging. In parallel, a variety of models, pitched at various levels in neural and/or cognitive science, are now available for some of its key elements. Within this fresh perspective, ®rmly grounded in empirical research, the problem of consciousness no longer seems intractable. Yet no convincing synthesis of the recent literature is available to date. Nor do we know yet whether the elements of a solution that we currently have will suf®ce to solve the problem, or whether key ingredients are still missing. By grouping some of the most innovative approaches together in a single volume, this special issue aims at providing the readers with a new opportunity to see for themselves whether a synthesis is now possible. In this introduction, we set the grounds for subsequent papers by ®rst clarifying what we think should be the aim of a cognitive neuroscience approach to conscious- ness. We isolate three major ®ndings that are explored in greater detail in several chapters of this volume. Finally, we propose a synthesis that integrates them into what we view as a promising theoretical framework: the hypothesis of a global neuronal workspace. With this framework in mind, we look back at some of the remaining empirical and conceptual dif®culties of consciousness research, and examine whether a clari®cation is in sight. 2. Nature of the problem and range of possible solutions Let us begin by clarifying the nature of the problem that a cognitive neuroscience of consciousness should address. In our opinion, this problem, though empirically challenging, is conceptually simple. Human subjects routinely refer to a variety of conscious states. In various daily life and psychophysical testing situations, they use phrases such as `I was not conscious of X', `I suddenly realized that Y', or `I knew S. Dehaene, L. Naccache / Cognition 79 (2001) 1±372 that Z, therefore I decided to do X'. In other words, they use a vocabulary of psychological attitudes such as believing, pretending, knowing, etc., that all involve to various extents the concept of `being conscious'. In any given situation, such conscious phenomenological reports can be very consistent both within and across subjects. The task of cognitive neuroscience is to identify which mental representa- tions and, ultimately, which brain states are associated with such reports. Within a materialistic framework, each instance of mental activity is also a physical brain state.1 The cognitive neuroscience of consciousness aims at determining whether there is a systematic form of information processing and a reproducible class of neuronal activation patterns that systematically distinguish mental states that subjects label as `conscious' from other states.2 From this perspective, the problem of the cognitive neuroscience of conscious- ness does not seem to pose any greater conceptual dif®culty than identifying the cognitive and cerebral architectures for, say, motor action (identifying what cate- gories of neural and/or information-processing states are systematically associated with moving a limb). What is speci®c to consciousness, however, is that the object of our study is an introspective phenomenon, not an objectively measurable response. Thus, the scienti®c body of consciousness calls for a speci®c attitude which departs from the `objectivist' or `behaviorist' perspective often adopted in behavioral and neural experimentation. In order to cross-correlate subjective reports of conscious- ness with neuronal or information-processing states, the ®rst crucial step is to take seriously introspective phenomenological reports. Subjective reports are the key phenomena that a cognitive neuroscience of consciousness purport to study. As such, they constitute primary data that need to be measured and recorded along with other psychophysiological observations (Dennett, 1992; Weiskrantz, 1997; see also Merikle, Smilek, & Eastwood, this volume). The idea that introspective reports must be considered as serious data in search of a model does not imply that introspection is a privileged mode of access to the inner workings of the mind. Introspection can be wrong, as is clearly demonstrated, for instance, in split-brain subjects whose left-hemispheric verbal `interpreter' invents a plausible but clearly false explanation for the behavior caused by their right hemi- sphere (Gazzaniga, LeDoux, & Wilson, 1977). We need to ®nd a scienti®c explana- tion for subjective reports, but we must not assume that they always constitute accurate descriptions of reality. This distinction is clearest in the case of hallucina- tions. If someone claims to have visual hallucinations of ¯oating faces, or `out-of- body' experiences, for instance, it would be wrong to take these reports as unequi- S. Dehaene, L. Naccache / Cognition 79 (2001) 1±37 3 1 We use the word `state' in the present context to mean any con®guration of neural activity, whether stable (a ®xed point) or dynamic (a trajectory in neural space). It is an open question as to whether neural states require stability over a minimal duration to become conscious, although the workspace model would predict that some degree of stable ampli®cation over a period of at least about 100 ms is required. 2 One should also bear in mind the possibility that what naive subjects call `consciousness' will ultimately be parceled into distinct theoretical constructs, each with its own neural substrate, just like the naive concept of `warmth' was ultimately split into two distinct physical parameters, temperature and heat. vocal evidence for parapsychology, but it would be equally wrong to dismiss them as unveri®able subjective phenomena. The correct approach is to try to explain how such conscious states can arise, for instance by appealing to an inappropriate activa- tion of face processing or vestibular neural circuits, as can indeed be observed by brain-imaging methods during hallucinations (Ffytche et al., 1998; Silbersweig et al., 1995). The emphasis on subjective reports as data does not mean that the resulting body of knowledge will be inherently subjective and therefore non-scienti®c. As noted by Searle (1998), a body of knowledge is scienti®c (`epistemically objective') inas- much as it can be veri®ed independently of the attitudes or preferences of the experimenters, but there is nothing in this de®nition that prevents a genuinely scienti®c approach of domains that are inherently subjective because they exist only in the experience of the subject (`ontologically subjective' phenomena). ªThe requirement that science be objective does not prevent us from getting an epistemically objective science of a domain that is ontologically subjective.º (Searle, 1998, p. 1937). One major hurdle in realizing this program, however, is that ªwe are still in the grip of a residual dualismº (Searle, 1998, p. 1939). Many scientists and philosophers still adhere to an essentialist view of consciousness, according to which conscious states are ineffable experiences of a distinct nature that may never be amenable to a physical explanation. Such a view, which amounts to a Cartesian dualism of substance, has led some to search for the bases of consciousness in a different form of physics (Penrose, 1990). Others make the radical claim that two human brains can be identical, atom for atom, and yet one can be conscious while the other is a mere `zombie' without consciousness (Chalmers, 1996). Contrary to those extreme statements, contributors to the present volume share the belief that the tools of cognitive psychology and neuroscience may suf®ce to analyze consciousness. This need not imply a return to an extreme form of direct psycho- neural reductionism. Rather, research on the cognitive neuroscience of conscious- ness should clearly take into account the many levels of organization at which the nervous system can be studied, from molecules to synapses, neurons, local circuits, large scale networks, and the hierarchy of mental representations that they support (Changeux & Dehaene, 1989). In our opinion, it would be inappropriate, and a form of `category error', to attempt to reduce consciousness to a low level of neural organization, such as the ®ring of neurons in thalamocortical circuits or the proper- ties of NMDA receptors, without specifying in functional terms the consequences of this neural organization at the cognitive level. While characterization of such neural bases will clearly be indispensable to our understanding of consciousness, it cannot suf®ce. A full theory will require many more `bridging laws' to explain how these neural events organize into larger-scale active circuits, how those circuits them- selves support speci®c representations and forms of information processing, and how these processes are ultimately associated with conscious reports. Hence, this entire volume privileges cognitive neuroscienti®c approaches to consciousness that seem capable of addressing both the cognitive architecture of mental representations and their neural implementation. S. Dehaene, L. Naccache / Cognition 79 (2001) 1±374 3. Three fundamental empirical ®ndings on consciousness In this section, we begin by providing a short review of empirical observations that we consider as particularly relevant to the cognitive neuroscience of conscious- ness. We focus on three ®ndings: the depth of unconscious processing; the attention- dependence of conscious perception; and the necessity of consciousness for some integrative mental operations. 3.1. Cognitive processing is possible without consciousness Our ®rst general observation is that a considerable amount of processing can occur without consciousness. Such unconscious processing is open to scienti®c investigation using behavioral, neuropsychological and brain-imaging methods. By increasing the range of cognitive processes that do not require consciousness, studies of unconscious processing contribute to narrowing down the cognitive bases of consciousness. The current evidence indicates that many perceptual, motor, semantic, emotional and context-dependent processes can occur unconsciously. A ®rst line of evidence comes from studies of brain-lesioned patients. PoÈppel, Held, and Frost (1973) demonstrated that four patients with a partial blindness due to a lesion in visual cortical areas (hemianopsic scotoma) remained able to detect visual stimuli presented in their blind ®eld. Although the patients claimed that they could not see the stimuli, indicating a lack of phenomenal consciousness, they nevertheless performed above chance when directing a visual saccade to them. This `blindsight' phenomenon was subsequently replicated and extended in numerous studies (Weiskrantz, 1997). Importantly, some patients performed at the same level as control subjects, for instance in motor pointing tasks. Thus, uncon- scious processing is not limited to situations in which information is degraded or partially available. Rather, an entire stream of processing may unfold outside of consciousness. Dissociations between accurate performance and lack of consciousness were subsequently identi®ed in many categories of neuropsychological impairments such as visual agnosia, prosopagnosia, achromatopsia, callosal disconnection, apha- sia, alexia, amnesia, and hemineglect (for reviews, see KoÈhler & Moscovitch, 1997; Schacter, Buckner, & Koutstaal, 1998; see also Driver & Vuilleumier, this volume). The current evidence suggests that, in many of these cases, unconscious processing is possible at a perceptual, but also a semantic level. For instance, Renault, Signoret, Debruille, Breton, and Bolgert (1989) recorded event-related potentials to familiar and unknown faces in a prosopagnosic patient. Although the patient denied any recognition of the familiar faces, an electrical waveform indexing perceptual proces- sing, the P300, was signi®cantly shorter and more intense for the familiar faces. Similar results were obtained by recording the electrodermal response, an index of vegetative processing of emotional stimuli, in prosopagnosic patients (Bauer, 1984; Tranel & Damasio, 1985). Even clearer evidence for semantic-level processing comes from studies of picture±word priming in neglect patients (McGlinchey- Berroth, Milberg, Verfaellie, Alexander, & Kilduff, 1993). When two images are S. Dehaene, L. Naccache / Cognition 79 (2001) 1±37 5 presented simultaneously in the left and right visual ®elds, neglect patients deny seeing the one on the left, and indeed cannot report it beyond chance level. Never- theless, when having to perform a lexical decision task on a subsequent foveal word, which can be related or unrelated to the previous image, they show the same amount of semantic priming from both hemi®elds, indicating that even the unreportable left- side image was processed to a semantic level. Similar priming studies indicate that a considerable amount of unconscious processing also occurs in normal subjects. Even a very brief visual stimulus can be perceived consciously when presented in isolation. However, the same brief stimulus can fail to reach consciousness when it is surrounded in time by other stimuli that serve as masks. This lack of consciousness can be assessed objectively using signal detection theory (for discussion, see Holender, 1986; Merikle, 1992; see also Merikle et al.).3 Crucially, the masked stimulus can still have a measurable in¯uence on the processing of subsequent stimuli, a phenomenon known as masked priming. There are now multiple demonstrations of perceptual, semantic, and motor processing of masked stimuli. For instance, in various tasks, processing of a conscious target stimulus can be facilitated by the prior masked presentation of the same stimulus (repetition priming; e.g. Bar & Biederman, 1999). Furthermore, masked priming also occurs when the relation between prime and target is a purely semantic one, such as between two related words (Dehaene, Naccache et al., 1998; Klinger & Greenwald, 1995; Marcel, 1983; see also Merikle et al.). We studied semantic priming with numerical stimuli (Dehaene, Naccache et al., 1998; Koechlin, Naccache, Block, & Dehaene, 1999). When subjects had to decide whether target numbers were larger or smaller than ®ve, the prior presentation of another masked number accelerated the response in direct proportion to its amount of similarity with the target, as measured by numerical distance (Koechlin et al., 1999). Furthermore, the same number-comparison experiment also provided evidence that processing of the prime occurs even beyond this semantic stage to reach motor preparation systems (Dehaene, Naccache et al., 1998). When the instruction speci®ed that targets larger than ®ve should be responded to with the right hand, for instance, primes that were larger than ®ve facilitated a right-hand response, and measures of brain activation demonstrated a signi®cant covert activation of motor cortex prior to the main overt response (see also Eimer & Schlaghecken, 1998; Neumann & Klotz, 1994). Thus, an entire stream of perceptual, semantic and motor processes, speci®ed by giving arbitrary verbal instructions to a normal subject, can occur outside of consciousness. The number priming experiment also illustrates that it is now feasible to visualize S. Dehaene, L. Naccache / Cognition 79 (2001) 1±376 3 Unfortunately, signal detection theory provides an imperfect criterion for consciousness. If subjects exhibit a d 0 measure that does not differ signi®cantly from zero in a forced-choice stimulus detection or discrimination task, one may conclude that no information about the stimulus was available for conscious processing. Conversely, however, a non-zero d 0 measure need not imply consciousness, but may result from both conscious and unconscious in¯uences. Experimental paradigms that partially go beyond this limitation have been proposed (e.g. Jacoby, 1991; Klinger & Greenwald, 1995). We concur with Merikle et al. (this vo