Review
The ‘correlates’ in neural correlates of consciousness

https://doi.org/10.1016/j.neubiorev.2011.05.012Get rights and content

Abstract

In the search for neural correlates of consciousness (NCC), the concept of ‘consciousness’ remains problematic. We suggest that not only the ‘consciousness’ in neural correlates of consciousness is a confused term, but ‘correlates’ is as well. When brain events are found to covary with conscious experience, these brain events can be the neural substrates of the experience, as is often (implicitly) suggested, but they can also be neural prerequisites or neural consequences of the experience. We here disentangle these different sorts of brain processes conceptually. But we also propose a concrete multi-pronged research program that may, in near-future consciousness research, distinguish these brain processes empirically.

Highlights

► The search for neural correlates of consciousness presses on. ► While ‘consciousness’ is difficult to define, we suggest that ‘correlates’ is confused as well. ► These neural correlates of consciousness may be disentangled conceptually and empirically. ► We conceptually subdivide ‘correlates’ into ‘prerequisites’, ‘consequences’, and ‘substrates’. ► We outline a concrete multi-pronged research program for near-future awareness research.

Introduction

The cognitive neuroscience of consciousness is blossoming. Age-old questions about where our experiences come from, centuries-old questions about what distinguishes conscious from unconscious processing, or recent questions about which exact brain regions are involved in these conscious or unconscious processes, today we can address all these questions. The search for ‘Neural Correlates of Consciousness’ (NCC: Koch, 2004) has given rise to many theoretical proposals and debate (e.g. Cleeremans, 2006, Noë and Thompson, 2004) and has taken flight especially since science has been able to look directly into brains to both see and manipulate what happens there. Using a variety of experimental paradigms, conscious experience can be manipulated independently of stimulus parameters. This is important, because changes in our conscious experience are generally confounded by changes in external input. To isolate changes in conscious experience for study, these changes must be separated from changes in stimulation conditions.

One example is the multistable paradigm, in which a constant stimulus gives rise to alternating conscious experiences over time (e.g. Blake, 2001, Fox, 1991, Howard and Rogers, 1995, Kim and Blake, 2005, Kleinschmidt et al., 1998, Levelt, 1965, Wheatstone, 1838). While a participant engages in multistable perception, brain imaging methods such as functional magnetic resonance imaging (fMRI) and electroencephalography (EEG) can be used to look at activity throughout the brain, to evaluate in which areas the activity covaries with conscious experience. Whereas the sequence of conditions in an fMRI experiment (the protocol) is usually defined by experimenters beforehand, in these kinds of studies the protocol is defined by the subject. He or she generally uses button presses to indicate which conscious percept is currently experienced. This subjective report then defines the timing and duration of conditions that are later contrasted in statistical analyses. In a set of binocular rivalry experiments, one form of multistable paradigm, one eye was continually presented with one image (e.g. a grating, or house), and the other eye with a second image (e.g. a face). The conscious experience alternated between the two images despite constant visual input, and the subjects indicated with button presses when, for example, a face or house was perceived. Activity related to these switches (Lumer et al., 1998, Lumer and Rees, 1999) or activity in house- and face-specific regions (Tong et al., 1998) were then evaluated to see which regions modulated their activation in response to subjective experience changes, rather than objective visual input. We will discuss the results of these experiments below, but it should be clear that brain areas thus revealed were related to consciousness. Since their activity correlated to conscious experience, such areas are commonly referred to as NCCs.

These studies were as important as they were interesting, since they offered early insights into brain mechanisms to do with consciousness-related processes. But in this writing, we would like to draw attention to a largely neglected conceptual problem within the cognitive neuroscience of consciousness. To look ahead, the problem is that several sorts of brain processes can correlate to consciousness and are therefore often lumped together. However, these processes can have rather different roles or meanings. In other words, there is not one consciousness-related process, there are probably several. And these consciousness-related processes are generally all grouped together under the banner of ‘NCC’. We suggest that this is no longer appropriate, or necessary. But before we can outline this issue in more detail, we will first need to make clear what we mean exactly by ‘consciousness’—so that it is unambiguous what we are discussing the correlates of. This is the ‘consciousness’ in neural correlates of consciousness. Then, we will outline the various types of brain processes that will correlate to consciousness. These are the ‘correlates’ in neural correlates of consciousness. It may come as a surprise that there is not one brain ‘correlate’ of a conscious experience, but we suggest there are actually three. We will distinguish them conceptually, but also proceed to suggest a program that may in future studies distinguish them empirically.

Section snippets

The ‘consciousness’ in neural correlates of consciousness

There are many classifications that can be made when it comes to ‘types’, ‘kinds’, or ‘definitions’ of consciousness. Consciousness remains, after all, one of the most ill-defined concepts in science and philosophy. In our view, one can distinguish between self-awareness, higher-order awareness, medical awareness, and consciousness as experience. Self-awareness, or self-consciousness, refers to all the aspects of our mind that create our perception of being some ‘one’ in a world consisting of

The ‘correlates’ in neural correlates of consciousness

We have now distinguished different ‘types’, or ‘kinds’, or ‘definitions’ of ‘consciousness’. We also constrained our discussion to the type of consciousness that is ‘experience’, or ‘qualia’, also referred to as the ‘contents of consciousness’. To make such clear distinctions and demarcations constitutes one step forward. However, even within the NCC program as restricted to experiences, a conceptual entanglement remains. This is illustrated by the schematic in Fig. 1. Say, a human subject is

How to untangle the entanglement: empirically distinguishing the correlates

The question is: if neural prerequisites (preconditions) and consequences always co-occur with the neural substrate of a ‘quale’ (experience, content of consciousness), how can we ever separate the substrates from the non-substrates? We here propose five general approaches for a near-future cognitive neuroscience of consciousness, which we will apply to the frontoparietal cortex as a candidate for NCC.

Conclusion

New methods and analysis tools, and a comprehensive search of the literature combined, should make it possible for future cognitive neuroscience to begin a separation of neural prerequisites, neural consequences, and neural substrates of conscious experience. At the very least an awareness of these conceptual distinctions would be valuable for both fledgling and established consciousness researchers. At any rate, we suggest that it will not suffice to simply identify neural correlates of

Acknowledgements

T.A.G. and A.T.S. are supported by NWO, Dutch Organization for Scientific Research, grant numbers 021-002-087 and 452-06-003, respectively.

Funding: The research leading to these results has also received funding from the European Research Council under the European Union's Seventh Framework Programme (FP7/2007-2013) /ERC Grant agreement n̊ [263472]).

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