What Kind of Brain Activity is Sufficient for Consciousness?

Logan Trujillo[1]

Editorial Introduction

Symposium on The Hidden Spring: A Journey to
the Source of Consciousness

In this issue of JCS, we are pleased to present a symposium for the new book, The Hidden Spring: A Journey to the Source of Conscious­ness, by Dr Mark Solms, Director of Neuropsychology, Neuroscience Institute, University of Cape Town, South Africa. In his book, Dr Solms proposes a novel and intriguing theory of consciousness based in statistical physics and information theory as applied to a systemic view of brain function that ascribes the primary determinant of con­sciousness to neural processing in the brainstem rather than the cerebral cortex. An earlier outline of this theory has been published in JCS (Solms and Friston, 2018).

Solms’ theory directly addresses the question of how conscious experience is related to specific activity of the brain and nervous system, and thus the theory contributes to the scientific search for the neural correlates of consciousness (NCCs). A widely accepted general operationalization of an NCC defines it as ‘a minimal neural system N such that there is a mapping from states N to states of consciousness, where a given state of N is sufficient, under conditions C, for the corresponding state of consciousness’ (Chalmers, 2000, p. 31). This definition entails three criteria for an NCC. First, the neural system is minimal; that is, brain states of N do not contain subsets that are them­selves sufficient for consciousness. This criterion ensures that the brain state in question is a substrate of consciousness and not a neural prerequisite for or consequence of conscious brain activity (Hohwy and Bayne, 2015). Second, the neural system has to be sufficient for consciousness; if brain state N is present then so is consciousness. Third, the relevant conditions (internal, environmental, dynamical, etc.) for such minimal sufficiency of the neural system must be met. In addition, the general definition of an NCC can be suitably modified to pertain to background conscious states, conscious mental content, or arbitrary phenomenal properties (Chalmers, 2000).

There is still some debate over the adequacy of this definition, including what kind of sufficiency (logical, metaphysical, physical) and what range of conditions are most appropriate for an NCC (Fink, 2016; Owen and Guta, 2019), how to characterize a minimal neural system (Hohwy and Bayne, 2015), and if this definition can effectively account for the content of conscious experiences (Noë and Thompson, 2004). In addition, this definition leaves open the details about the kinds and levels of neural activity that are most relevant for an NCC (Hohwy and Bayne, 2015; Koch et al., 2016; Overgaard, Mogensen and Kirkeby-Hinrup, 2021). Nevertheless, the definition has provided a useful operational framework to guide the empirical determination of such details via the standard methods of cognitive neuroscience.

Because an NCC is conceived in terms of a correlation between neural activity and consciousness, its definition is neutral with respect to the ontological and causal basis of consciousness. Hence, technically, an NCC can be coherently interpreted in terms of any position on the metaphysics of consciousness (Hohwy and Bayne, 2015; Moody, 2014). However, for neurophysiologically-based researchers, most of whom are physicalists, it is not enough to merely correlate consciousness with a neural process; they also want to understand how consciousness is created or generated in relationship to functionally-relevant neural processing. Such an understanding will require the identification of the physical principles that distinguish conscious neural processes from those neural processes that are not conscious. Moreover, it may be the case that consciousness originates via the action of general physical principles at play within the brain rather than brain-specific principles per se. That is, consciousness is multiply realizable across different possible physical systems, of which the brain and nervous system are but one example. Hence, a final theory of consciousness requires an elucidation of the general physical causes of consciousness, which in turn may yield surprising consequences for our understanding of the NCCs.

It is just such a theory of consciousness that is presented by Solms in his book and summarized in the present précis. Solms’ theory is based on the assumption that the function of consciousness is to register internal states of an experiencing subject rather than external states of the world. Deviations of these internal states from preferred values are experienced as felt affects that constitute the core of con­sciousness itself. The function of such affects is to assist an organism in the maintenance of homeostasis, which implies a causal power for consciousness that was shaped by evolutionary selection pressure. Solms formally describes this homeostatic function in terms of the free energy framework developed by Karl Friston and others (Friston, 2010; Friston et al., 2015), which recasts the tendency of self-organizing physical systems to resist the second law of thermodyna­mics in terms of a Bayesian process of active inference. Such a system realizes active inference via minimization of free energy — an information-theoretic property of a system that indexes the difference between a system’s predictions and the sensory data it obtains from its environment (Pio-Lopez et al., 2016).

Importantly, Solms’ analysis of how a self-organized Bayesian pro­cess of active inference is anatomically- and physiologically-realized reveals a surprising claim for the NCCs. Researchers have tradition­ally assumed that the neural correlates (or causes) of consciousness, whatever they may be, are instantiated within the activity of the cerebral cortex. This assumption forms the basis for currently promi­nent neural theories of consciousness, such as global neuronal work­space theory (Mashour et al., 2020) or integrated information theory (Tononi et al., 2016). However, Solms highlights evidence indicating that consciousness can be preserved under conditions in which brain­stem activity is intact but cortical activity is impaired or absent, as in the case of locally anaesthetized patients undergoing brain surgery or hydranencephalic children, for example. These observations, in con­junction with other theoretical and neuroanatomical considerations, lead Solms to the conclusion that all conscious experience, at its core, is felt affect that originates as brain arousal processes within the brain­stem. This implies that the brainstem is the NCC (the minimal neural system sufficient for consciousness), not the cerebral cortex. How then does his theory account for the portion of cortical information processing that we are conscious of? According to Solms, such pro­cessing becomes conscious in virtue of brainstem-mediated arousal of the cortex, which extends felt affect onto perception and cognition to form more complicated forms of perceptual and cognitive conscious­ness. In other words, in contributing to the character and content of conscious experience, cortical activity is a neural prerequisite for perceptual and cognitive consciousness, but perceptual and cognitive processing readily proceed unconsciously in the absence of brainstem arousal. Hence cortical states/content are not in themselves the sub­strate of consciousness.

Note, however, that Solms’ theory also implies that brainstem arousal, or a similar functional property realized in other (possibly non-biological) self-organizing systems, is not just sufficient for con­sciousness, but is also necessary as well. That is, Solms’ theory entails that the brainstem is the physical ‘source’ of consciousness itself (at least in vertebrates). This is a counter-intuitive and controversial claim for many consciousness researchers. The goal of this symposium is to present both sides of this controversy to the readers of JCS. This symposium begins with a précis by Solms, summarizing his book, followed by commentaries from several eminent philosophers and neuroscientists with expertise in consciousness studies (Thomas Nagel, Karl Friston, Daniel Dennett, Lionel Naccache, Adam Safron). Solms then replies to each commentary in a final response.

The idea that the cortex is not the source of consciousness may be difficult for some readers to accept. It is my hope that, at the very least, readers will find this symposium thought-provoking and informative.

References

Chalmers, D.J. (2000) What is a neural correlate of consciousness?, in Metzinger, T. (ed.) Neural Correlates of Conscious Experience: Empirical and Conceptual Questions, pp. 17–39, Cambridge, MA: MIT Press.

Fink, S.B. (2016) A deeper look at the ‘neural correlate of consciousness’, Frontiers in Psychology, 7, art. 1044.

Friston, K. (2010) The free-energy principle: A unified brain theory?, Nature Reviews Neuroscience, 11, pp. 127–138.

Friston, K., Rigoli, F., Ognibene, D., Mathys, C., Fitzgerald, T. & Pezzulo, G. (2015) Active inference and epistemic value, Cognitive Neuroscience, 6, pp. 187–214.

Hohwy, J. & Bayne, T. (2015) The neural correlates of consciousness: Causes, confounds and constituents, in Miller, S.M. (ed.) The Constitution of Phenom­enal Consciousness, pp. 155–176, Amsterdam: John Benjamins.

Koch, C., Massimini, M., Boly, M. & Tononi, G. (2016) Neural correlates of consciousness: Progress and problems, Nature Reviews Neuroscience, 17, pp. 307–321.

Mashour, G.A., Roelfsem, P., Changeux, J.-P. & Dehaene, S. (2020) Conscious processing and the global neuronal workspace hypothesis, Neuron, 105, pp. 776–798.

Moody, T. (2014) Consciousness and the mind–body problem, Journal of Con­sciousness Studies, 21 (3–4), pp. 177–190.

Noë, A. & Thompson, E. (2004) Are there neural correlates of consciousness?, Journal of Consciousness      Studies, 11 (1), pp. 3–28.

Overgaard, M., Mogensen, J. & Kirkeby-Hinrup, A. (eds.) (2021) Beyond Neural Correlates of               Consciousness, New York: Routledge.

Owen, M. & Guta, M.P. (2019) Physically sufficient neural mechanisms of con­sciousness, Frontiers in Systems Neuroscience, 13, art. 24.

Pio-Lopez, L., Nizard, A., Friston, K. & Pezzulo, G. (2016) Active inference and robot control: A case study, Journal of the Royal Society Interface, 13, 20160616.

Solms, M. & Friston, K. (2018) How and why consciousness arises: Some con­siderations from physics and physiology, Journal of Consciousness Studies, 25 (5–6), pp. 202–238.

Tononi, G., Boly, M., Massimini, M. & Koch, C. (2016) Integrated information theory: From consciousness to its physical substrate, Nature Reviews Neuro­science, 17, pp. 450–461.

[1]      Department of Psychology, Texas State University, San Marcos, Texas, USA.

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