Neural correlates of consciousness: progress and problems

Journal name:
Nature Reviews Neuroscience
Volume:
17,
Pages:
307–321
Year published:
DOI:
doi:10.1038/nrn.2016.22
Published online
Corrected online

Abstract

There have been a number of advances in the search for the neural correlates of consciousness — the minimum neural mechanisms sufficient for any one specific conscious percept. In this Review, we describe recent findings showing that the anatomical neural correlates of consciousness are primarily localized to a posterior cortical hot zone that includes sensory areas, rather than to a fronto-parietal network involved in task monitoring and reporting. We also discuss some candidate neurophysiological markers of consciousness that have proved illusory, and measures of differentiation and integration of neural activity that offer more promising quantitative indices of consciousness.

At a glance

Figures

  1. Identifying the neural correlates of consciousness.
    Figure 1: Identifying the neural correlates of consciousness.

    This schematic diagram illustrates the absolute levels of brain activity across different conditions designed to identify the neural correlates of consciousness (NCC). a | Haemodynamic activity in a report-based paradigm in which the experience of seeing a face or other stimulus manipulations such as backward masking is contrasted with not seeing it as a result of image noise142. The participant presses a button to report seeing (yes) or not seeing (no) the face. This isolates the brain regions involved in conscious face recognition, a content-specific NCC, but also the regions involved in the maintenance of the face in working memory and access to the concept 'face' for decision making. Note that the background conditions for consciousness, such as an active reticular activating system, are eliminated by this contrast. b | Haemodynamic activity in a no-report, seen/not seen paradigm, similar to part a, in which the participants do not report on their percept during the trial. Instead, either retrospective reports or physiological indicators, such as eye movements or pupil dilation, are used to avoid confounds related to the act of reporting34, 36. This allows the content-specific NCC to be isolated. The union of all such content-specific NCC constitutes the full NCC. c | In a between-states paradigm, the haemodynamic activity associated with the experience of seeing anything (here the experience of seeing pure black) while awake is contrasted with the activity associated with the condition of no experience that would occur during dreamless sleep37. This analysis identifies brain regions involved in having any conscious experience, but also regions that mediate being awake rather than being asleep. d | In a within-state, no-task paradigm, participants are awakened at random during sleep (stage N2) and are asked whether, before they were awakened, they were dreaming and, if so, about what. This paradigm identifies brain activity associated with having dream experiences up to 20 s before awakening44 — a candidate for the full NCC of dreaming consciousness — and avoids confounds associated with task execution and state change. NREM, non-rapid eye movement.

  2. Identifying content-specific and full neural correlates of consciousness.
    Figure 2: Identifying content-specific and full neural correlates of consciousness.

    a | Findings from a functional MRI (fMRI) experiment searching for content-specific neural correlates of consciousness (NCC). This experiment contrasts activity during the presentation of visual words with activity when the same words are masked and therefore invisible. This task involves an explicit report via button-press. Such studies have suggested that activity in the fronto-parietal networks and extrastriate occipital regions142 constitute the NCC. b | Similar fronto-parietal activity patterns are found during a binocular rivalry paradigm in which volunteers actively report their percept (task). However, when the volunteers experience rivalry without explicitly reporting perceptual alternations (no task), neural activity in the frontal areas is absent, whereas activation of the occipital and parietal regions remains36. c | Findings from an electrocorticogram (ECoG) study using a visual one-back paradigm in patients with epilepsy implanted with subdural electrode arrays. Participants press a button when two consecutive pictures are identical (the target trial). The colours indicate how strongly neural activity is modulated by the motor task (red represents low modulation and yellow represents high modulation) across all significantly responsive electrodes (either during non-target or target trials). Occipito-temporal visual cortical regions (shown to the right of the dashed white line) respond rapidly to the seen stimulus irrespective of the type of task (red), whereas the frontal regions are modulated by the type of task (yellow)117. d | Findings from a positron emission tomography (PET) study using a between-states paradigm that contrasts brain activity during deep non-rapid eye movement (NREM) sleep with wakefulness indicate that there are decreased levels of absolute cerebral blood flow in both parietal and frontal cortices during sleep. This suggested that activity in a fronto-parietal network may be essential for consciousness110. e | Voxel-by-voxel maps of the mean percentage change in fMRI signals during absence seizures: fronto-parietal activity increases during the loss of consciousness (warm colours) and decreases during the subsequent recovery of consciousness (cool colours)112. Part a is adapted with permission from Ref. 142, Elsevier. Part b is adapted from Ref. 36, republished with permission of Society for Neuroscience, from Binocular rivalry: frontal activity relates to introspection and action but not to perception, Frässle, S., Sommer, J., Jansen, A., Naber, M. & Einhäuser, W., 34, 5, 2014; permission conveyed through Copyright Clearance Center, Inc. Part c is adapted with permission from Ref. 117, Elsevier. Part d is adapted from Ref. 110, republished with permission of Society for Neuroscience, from Activity of midbrain reticular formation and neocortex during the progression of human non-rapid eye movement sleep, Kajimura, N., Uchiyama, M., Takayama, Y., Uchida, S., Uema, T., Kato, M., Sekimoto, M., Watanabe, T., Nakajima, T., Horikoshi, S., Ogawa, K., Nishikawa, M., Hiroki, M., Kudo, Y., Matsuda, H., Okawa, M. & Takahashi, K., 19, 22, 1999; permission conveyed through Copyright Clearance Center, Inc. Part e is adapted from Ref. 112, republished with permission of Society for Neuroscience, from Dynamic time course of typical childhood absence seizures: EEG, behavior, and functional magnetic resonance imaging, Bai, X., Vestal, M., Berman, R., Negishi, M., Spann, M., Vega, C., Desalvo, M., Novotny, E. J., Constable, R. T. & Blumenfeld, H., 30, 17, 2010; permission conveyed through Copyright Clearance Center, Inc.

  3. Candidate neurophysiological markers of consciousness.
    Figure 3: Candidate neurophysiological markers of consciousness.

    a | Gamma synchrony has been proposed as a correlate of consciousness. Cross-correlograms computed from the firing responses of two units recorded 7 mm apart in the visual cortex of cats reveal a strong gamma band synchronization when a moving bar stimulates the receptive fields of the two neurons162. b | In the high-level visual cortex in humans, however, the intracranial gamma band responses increase when a degraded stimulus is made visible by increasing sensory evidence, but not when visibility is increased to the same extent by previous exposure33. c | Visible grating stimuli elicit robust gamma oscillations (30–80 Hz) in the human visual cortex, whereas equally visible noise patterns or natural images do not, indicating that gamma activity is not necessary for visual conciousness175. d | The late positive component of the event-related potential (known as the P3b) was also proposed as a signature of consciousness. In attentional blink paradigms, the P3b is a robust correlate of stimulus visibility178. e | When visual awareness and task relevance are manipulated independently, however, the P3b is absent for task-irrelevant stimuli regardless of whether the participants are aware of them or not34. f | Stimuli that are not consciously detected can trigger a significant P3b component180. g | A shift in electroencephalography (EEG) activity from low to high frequencies has been proposed as a correlate of consciousness. Electrical stimulation of the midbrain reticular formation (MRF) elicits EEG activation and behavioural awakening in a cat; EEG slow waves are replaced by low-voltage fast activity and by a steady membrane potential in the cortex247, 248. h | High-amplitude bilateral slow waves have been observed in awake, conscious patients in some cases of non-convulsive status epilepticus199. Part a is from Ref. 162, Nature Publishing Group. Part b is adapted from Ref. 33, Society for Neuroscience, from Local category-specific gamma band responses in the visual cortex do not reflect conscious perception, Aru, J., Axmacher, N., Do Lam, A. T., Fell, J., Elger, C. E., Singer, W. & Melloni, L., 32, 43, 2012; permission conveyed through Copyright Clearance Center, Inc. Part c is adapted from Ref. 175, Hermes, D., Miller, K. J., Wandell, B. A. & Winawer, J. Stimulus dependence of gamma oscillations in human visual cortex. Cereb. Cortex, 2015, 25, 9, 29512959, by permission of Oxford University Press. Part d is from Ref. 178, Nature Publishing Group. Part e is adapted from Ref. 34. Part f is adapted with permission from Ref. 180, Elsevier. Part g is adapted with permission from Ref. 248, American Association for the Advancement of Science. Part h is adapted with permission from Ref. 199, John Wiley &Sons.

  4. Neural differentiation and integration as neural correlates of consciousness.
    Figure 4: Neural differentiation and integration as neural correlates of consciousness.

    a | Schematic diagram showing two idealized time series of spontaneous brain activity (electroencephalography (EEG)) and the corresponding maps of cortical connectivity. Integration, as measured by indices of functional connectivity, tends to be high when time series are highly correlated (top panel) and low when time series are not highly correlated (bottom panel). b | The same two time series are shown together with the corresponding maps of spatiotemporal variability in brain activity. Differentiation, here reflected in the difference between subsequent maps of cortical activity, tends to be high (top panel) when the time series are not highly correlated (maximum for random time series) and low when they are highly correlated (bottom panel). c | The perturbational complexity index (PCI) simultaneously quantifies integration and differentiation. Calculating the PCI involves perturbing the brain with transcranial magnetic stimulation (TMS), recording the results of EEG to detect the pattern of causal cortical interactions engaged by the TMS perturbation (integration) and compressing this pattern to calculate its spatiotemporal variability with algorithmic complexity measures (differentiation). Responses that are both integrated and differentiated are less compressible, resulting in high PCI values. By contrast, local (low integration) or stereotypical (low differentiation) EEG responses to TMS can be effectively compressed, yielding low PCI values. As shown in the right-hand panel (real data), jointly measuring integration and differentiation with PCI establishes a common measurement scale that is valid across many different conditions along the unconsciousness–consciousness spectrum and is reliable at the level of single paticipants219, 220, including: those who are awake and able to report immediately that they are conscious (red circles); participants in rapid eye movement (REM) sleep and under ketamine anaesthesia who are unresponsive, but able to report retrospectively that they were conscious (green circles); participants in non-REM (NREM) sleep or general anaesthesia (midazolam, propofol and xenon) who provide no conscious report on awakening (dark blue circles); vegetative state/unresponsive wakefulness syndrome (VS/UWS) patients (light blue circles); and responsive brain-injured patients who are in a minimally conscious state (MCS), emerged from the MCS (EMCS) or in a locked-in syndrome (LIS) (light red circles). Part c is adapted with permission from Ref. 219, American Association for the Advancement of Science.

Change history

Corrected online 06 May 2016
The traces in panel e of Figure 3 were incorrectly colour coded. The colour coding has been corrected in the online version of the article.

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Affiliations

  1. Allen Institute for Brain Science, Seattle, Washington 98109 USA.

    • Christof Koch
  2. Department of Biomedical and Clinical Sciences 'Luigi Sacco', University of Milan, Milan, Italy.

    • Marcello Massimini
  3. Instituto Di Ricovero e Cura a Carattere Scientifico, Fondazione Don Carlo Gnocchi, Milan, Italy.

    • Marcello Massimini
  4. Department of Neurology, University of Wisconsin, Madison, Wisconsin 53719, USA.

    • Melanie Boly
  5. Department of Psychiatry, University of Wisconsin, Madison, Wisconsin 53719, USA.

    • Melanie Boly &
    • Giulio Tononi

Competing interests statement

The authors declare no competing interests.

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Author details

  • Christof Koch

    Christof Koch is the President and Chief Scientific Officer of the Allen Institute for Brain Science in Seattle, Washington, USA. He was trained as a physicist. On a quest to understand the physical roots of consciousness before his brain stops functioning, he published his first paper on the neural correlates of consciousness with Francis Crick a quarter of a century ago.

  • Marcello Massimini

    Marcello Massimini is Associate Professor of Neurophysiology at the University of Milan, Italy. He was trained as a medical doctor and devotes his research to understanding the neuronal mechanisms of loss and recovery of consciousness in sleep and anaesthesia, and in brain-injured patients.

  • Melanie Boly

    Melanie Boly is a neurologist and neuroscientist at the University of Wisconsin, Madison, USA. She uses neuroimaging and theoretical approaches to understand the neural substrate of experience and its alterations in sleep, anaesthesia and disorders of consciousness.

  • Giulio Tononi

    Giulio Tononi is a neuroscientist and psychiatrist at the Department of Psychiatry at the University of Wisconsin, Madison, USA, where he works on the nature of consciousness and the functions of sleep.

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    Consciousness and other cognitive functions

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