Scientific Understanding of Consciousness
Consciousness as an Emergent Property of Thalamocortical Activity

Consciousness — Experimental Markers

Citation: Gaillard R, Dehaene S, Adam C, Clémenceau S, Hasboun D, et al. (2009) Converging Intracranial Markers of Conscious Access. PLoS Biol 7(3): e1000061. doi:10.1371/journal.pbio.1000061

Converging Intracranial Markers of Conscious Access

Raphaël Gaillard^1,2,3, Stanislas Dehaene^1,4,5, Claude Adam⁶, Stéphane Clémenceau⁶, Dominique Hasboun^6,7, Michel Baulac^6,7, Laurent Cohen^1,6,7, Lionel Naccache^1,6,7*

1 INSERM, Cognitive Neuro-imaging Unit, Institut Fédératif de Recherche (IFR) 49, Gif sur Yvette, France, 2 Centre Hospitalier Sainte Anne, Service Hospitalo-Universitaire de Santé Mentale et de Thérapeutique, Paris, France, 3 Université Paris Descartes, Paris, France, 4 CEA, I2BM, NeuroSpin center, Gif sur Yvette, France, 5 Collège de France, Paris, France, 6 Assistance Publique Hôpitaux de Paris, Hôpital de la Pitié-Salpêtrière, Pôle des Maladies du Système Nerveux, Paris, France, 7 Université Pierre et Marie Curie Paris 6, Département de Physiologie, Paris, France

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We compared conscious and nonconscious processing of briefly flashed words using a visual masking procedure while recording intracranial electroencephalogram (iEEG) in ten patients. Nonconscious processing of masked words was observed in multiple cortical areas, mostly within an early time window (<300 ms), accompanied by induced gamma-band activity, but without coherent long-distance neural activity, suggesting a quickly dissipating feedforward wave. In contrast, conscious processing of unmasked words was characterized by the convergence of four distinct neurophysiological markers: sustained voltage changes, particularly in prefrontal cortex, large increases in spectral power in the gamma band, increases in long-distance phase synchrony in the beta range, and increases in long-range Granger causality. We argue that all of those measures provide distinct windows into the same distributed state of conscious processing. These results have a direct impact on current theoretical discussions concerning the neural correlates of conscious access.

What is the neural signature of the conscious perception of a visual stimulus? To address this question, we recorded neural activity directly from the brains of human subjects (who were undergoing neural surgery for medical reasons). This rare opportunity afforded greater spatial and temporal resolution than noninvasive methods used previously to probe the neural basis of consciousness. We compared neural activity concomitant with conscious and nonconscious processing of words by using a visual masking procedure that allowed us to manipulate the conscious visibility of briefly masked words. Nonconscious processing of words elicited short-lasting activity across multiple cortical areas, including parietal and visual areas. In sharp contrast, only consciously perceived words were accompanied by long-lasting effects (>200 ms) across a great variety of cortical sites, with a special involvement of the prefrontal lobes. This sustained pattern of neural activity was characterized by a specific increase of coherence between distant areas, suggesting conscious perception is broadcasted widely across the cortex.

Introduction

The neural correlates of consciousness (NCC) still remain highly controversial. The precise timing, location, and dynamics of neural events causing conscious access are not clearly and unequivocally determined. Do the NCC correspond to late or early brain events? Are they systematically associated with reentrant “top down” processing? If so, do they necessarily involve long-range coherent activity, including prefrontal cortex as an essential node, or can they be restricted to local patterns of reverberating activity? Is the concept of “integrated information” relevant, rather than the specific localization of the underlying cerebral network?

In addition to such fundamental questions, an important methodological issue also remains open. Neural data relevant to conscious access originate from a diversity of techniques including hemodynamic blood oxygen level dependent (BOLD) functional magnetic resonance imaging (fMRI) or positron emission tomography (PET) responses and electrophysiological measures using scalp and intracranial event-related potentials (iERPs), event-related spectral perturbations (ERSPs), and phase synchrony parameters. How are these distinct measures of conscious access related to each other? Do they reflect common facets of the same underlying phenomenon?

In this work, we address some of these issues using intracerebral electrophysiological recordings of neural activity in a group of implanted epileptic patients presented with visually masked and unmasked printed words. This method offers a unique opportunity to measure neural correlates of conscious access with both millisecond time resolution and centimetric spatial resolution. Its high signal-to-noise ratio allowed us to compute several neurophysiological measures from the intracerebral signal in order to unravel the relations prevailing between iERPs, ERSPs, interelectrode phase synchrony, and a recently proposed estimate of causality (Granger causality).

The Global Workspace Model of Consciousness

We adopted a theory-driven approach, trying to test experimentally a set of explicit predictions derived from the global workspace model of conscious access. This model, in part inspired from Bernard Baars' theory, proposes that at any given time, many modular cerebral networks are active in parallel and process information in an unconscious manner. Incoming visual information becomes conscious, however, if and only if the three following conditions are met: Condition 1: information must be explicitly represented by the neuronal firing of perceptual networks located in visual cortical areas coding for the specific features of the conscious percept. Condition 2: this neuronal representation must reach a minimal threshold of duration and intensity necessary for access to a second stage of processing, associated with a distributed cortical network involved in particular parietal and prefrontal cortices. Condition 3: through joint bottom-up propagation and top-down attentional amplification, the ensuing brain-scale neural assembly must “ignite” into a self-sustained reverberant state of coherent activity that involves many neurons distributed throughout the brain.

Why would this ignited state correspond to a conscious state? The key idea behind the workspace model is that because of its massive interconnectivity, the active coherent assembly of workspace neurons can distribute its contents to a great variety of other brain processors, thus making this information globally available. The global workspace model postulates that this global availability of information is what we subjectively experience as a conscious state. Neurophysiological, anatomical, and brain-imaging data strongly argue for a major role of prefrontal cortex, anterior cingulate, and the associative areas that connect to them, in creating the postulated brain-scale workspace.

Scope and Limits of Our Experimental Paradigm

In the present work, we measured the neural correlates of visually masked words and contrasted them with those of consciously visible unmasked words. On each trial, patients were randomly presented with a masked word, a visible word, or with corresponding control stimuli in which the words were replaced by blank screens. In the masked condition, words or blank screens were presented for 29 ms, preceded by a forward mask and followed by a backward mask. In the unmasked conditions, words or blank screens were made visible by simply removing the backward mask. In order to discard activations induced by the masks, we always subtracted from word-present conditions the corresponding blank condition. This subtraction allowed us to isolate the entire processing path evoked by the masked or unmasked word.

Phase Coherence

Spectral changes are complex phenomena that can be sensitive to local as well as global neuronal synchronization of thalamocortical networks. To evaluate the global workspace model's prediction that access to consciousness is associated with long-distance synchronization, we measured the phase synchrony between all electrode pairs. Phase synchrony can occur independently of changes in induced power: it solely evaluates whether oscillations are reproducibly synchronized across two distant sites in the sense that across trials, they exhibit a systematic phase relationship.

Granger Causality

A final measure of conscious processing that we evaluated is Granger causality, a mathematical tool that can estimate the causal influence that one electrode site exerts on another. Global neuronal workspace theory predicted that access to consciousness for unmasked words would be accompanied by a massive web of causal relations among distant cortical sites, not seen in the masked condition. Granger causality and phase coherence are similar in that both estimate the correlations among pairs of electrodes, but Granger causality looks for temporal contingencies inaccessible to coherence analyses. In a nutshell, the method estimates whether past samples of electrode j account for a significant amount of variance in electrode i, over and above a simpler “autoregressive” model using only past samples of electrode i. It is possible for two time series to be strongly phase coherent, yet not causally related (for instance, two sine waves with constant phase lag and independent noise). Thus, Granger causality analysis is not redundant with phase coherence analysis: finding that Granger causality increases during conscious perception, perhaps simultaneously with the beta coherence increase, would provide additional evidence in favor of a large-scale reverberating neuronal assembly linking distant sites. Furthermore, unlike phase coherence, Granger causality is a directional measure: it is possible for electrode j to causally influence i without i causally influencing j (although it is also possible for two signals to exert mutual causal influences on each other). This analysis therefore provided an opportunity to examine the top-down versus bottom-up propagation of activation during conscious and nonconscious processing.

Beta-band rather than Gamma-band Phase Synchrony.

As noted in the introduction, neuronal simulations of the global workspace architecture predicted that conscious access would correlate with increases in phase synchrony at frequencies within a large gamma band ranging from 20–100 Hz, centered around 40 Hz. Actually, such increases in synchrony appeared in the beta frequency range (13–30 Hz), where spectral power decreased, rather than in the gamma range where the largest increases in induced power (ERSP) were observed.

At the theoretical level, a systematic relation may indeed exist between the size of a neuronal assembly and the frequency at which it can sustain synchronized oscillations. Gamma oscillations in cortical areas, with periods of 10 to 30 ms, may synchronize only in the face of short conduction delays (1–3 ms) and may therefore contribute to locally coded thalamocortical representations. When the recorded neuronal groups are more distant, phase-coherent oscillations are often found in the lower-frequency beta range, probably because their slower period (30–80 ms) allows them to resist the longer conduction delays (5–15 ms) needed to bridge large cortical distances. Thus, beta-coherent oscillations may preferentially subserve long-distance synchronization and broadcasting. In the future, it will be important to incorporate this effect in the global workspace simulations, as well as to account for the observed decrease in power that accompanies the increase in beta synchrony in our data.

Toward a Neural Signature of Conscious Access

The main motivation of our study was to probe the convergence of multiple neurophysiological measures of brain activity in order to define candidate neural signatures of conscious access. Conscious word processing was associated with the following four markers: (1) sustained iERPs within a late time window (>300 ms after stimulus presentation); (2) sustained and late spectral power changes, combining a high-gamma increase, beta suppression, and alpha blockage; (3) sustained and late increases in long-range phase coherence in the beta range; and (4) sustained and late increases in long-range causal relations.

Our results suggest that in the search for neural correlates of consciousness, time-domain, frequency-domain, and causality-based electrophysiological measures should not be seen as competing possibilities. Rather, all of these measures may provide distinct glimpses into the same distributed state of long-distance reverberation. Indeed, it seems to be the convergence of these measures in a late time window, rather than the mere presence of any single one of them, that best characterizes conscious trials. For instance, masked words also elicited significant iERPs and significant increases in spectral power in the gamma band, contemporary with short-range synchronies in the beta range during the 200–300-ms window. Yet, those words were not consciously accessed, which implies that neither iERPs (even those recorded from frontal cortex), nor gamma-band activity or beta synchrony per se are unique markers of conscious experience. Our results suggest that only late sustained long-distance synchrony and late amplification (>300 ms) may be causally related to conscious-level processing.

There are yet other mathematical measures derived from nonlinear dynamics that could have been applied to our dataset, such as dimensional activation or neural complexity, although some of them remain to be made operational in a computationally tractable manner. We consider it likely that these measures would also show a pattern unique to conscious perception. The present work suggests that, rather than hoping for a putative unique marker (the neural correlate of consciousness), a more mature view of conscious processing should consider that it relates to a distributed pattern of brain activation that occurs at a specific level within a complex anatomical and functional architecture, and that it can therefore be reflected by many partially overlapping physiological measures.

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