What Might Interoceptive Inference Reveal About Consciousness?
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Preprint Embodied Computation Group 1 What might interoceptive inference reveal about consciousness? NIIA NIKOLOVAa,1,*,P ETER THESTRUP WAADEa,1,2,K ARL J. FRISTON3, AND MICAH ALLEN1,4,5 aEqual contribution *Corresponding author: niia@cfin.au.dk 1Center for Functionally Integrative Neuroscience, Aarhus University, Denmark 2Interacting Minds Center, Aarhus University, Denmark 3Wellcome Centre for Human Neuroimaging, UCL, United Kingdom 4Aarhus Institute of Advanced Studies, Denmark 5Cambridge Psychiatry, University of Cambridge, United Kingdom The mainstream science of consciousness offers a few predominate views of how the brain gives rise to awareness. Chief among these are the Higher Order Thought Theory, Global Neuronal Workspace The- ory, Integrated Information Theory, and hybrids thereof. In parallel, rapid development in predictive pro- cessing approaches have begun to outline concrete mechanisms by which interoceptive inference shapes selfhood, affect, and exteroceptive perception. Here, we consider these new approaches in terms of what they might offer our empirical, phenomenological, and philosophical understanding of consciousness and its neurobiological roots. INTRODUCTION thought? How might the body, or emotion, interact with these properties of consciousness? What is Consciousness? Answering these questions is no easy task. Certainly, most If you have ever been under general anaesthesia, you surely who study consciousness have heard the joke that there are as remember the experience of waking up. However, this awak- many theories of consciousness as there are consciousness theo- ening is different from the kind we do every morning, in that rists. Our goal here is not to provide a comprehensive predictive it is preceded by a complete lack of subjective experience, a processing or active inference theory of consciousness, of which dark nothingness, without even the awareness of time passing. there are already a rapidly growing number (for reviews, see [2– This transition presents a clear insight into the two extremes of 5]). Rather, we aim to illustrate how the notion of interoceptive conscious experience. inference and related concepts might inform the theoretical and While these strong contrasts delimit the borders of conscious- empirical science of consciousness, by generating alternative ness, you might also consider the phenomenological properties process theories that can then be subject to empirical evaluation. which reveal themselves upon further reflection. Foremost is the Current mainstream approaches to consciousness can be unique “mineness” of any conscious experience. In the transition largely divided into several camps, though the boundaries are from sleep to wakefulness, there seem to be distinct properties fuzzy and hybrid theories abound. Writ large, these include of ownership and agency. Whereas the infinite void of sleep the Global Neuronal Workspace Theory (GNWS), Higher-Order belongs to no one, even before opening my eyes there is a dis- Thought Theory (HOTT), and the Integrated Information The- tinct sense in which experience is happening to someone. In ory (ITT). These theories share some key properties, but also phenomenological terms, we can think about this as the mini- differ substantially in terms of the types of phenomena they mal, pre-reflexive conditions about which my experiences are seek to explain and the mechanisms they appeal to in doing uniquely my own [1]. Consciousness then is something which so. In what follows, we will discuss some of the more obvious happens to a sentient subject, which is lived through as the em- places in which predictive processing and interoceptive infer- bodied point of view of those seemingly ineffable subjective ence theories tie in with these approaches. Here, we summarize properties. key concepts from some of the leading theories of consciousness A sufficient theory of consciousness then, will deal with each and discuss how interoceptive inference might fit into them and of these properties in turn. What distinguishes conscious states inform future theoretical and empirical directions. Our main from non-conscious ones? How does selfhood and agency in- goals here are the following; first, to accurately and concisely fluence these properties? Which sorts of mechanisms give rise review several of the most popular theories of consciousness, to both the phenomenological contents of consciousness, and namely HOTT, GWS, IIT and active inference accounts. We then determines which sorts of states become accessible to conscious aim to describe the emerging concept of interoceptive inference, Preprint Embodied Computation Group 2 and finally we explore the potential of interoceptive inference to of consciousness. integrate with each of the theories, and how it might illuminate Interoception is generally used to refer to the sensation, per- future research directions. ception, and metacognition of the visceral cycles which govern an agent’s homeostasis, allostasis, and ultimately its survival What is Interoceptive Inference? [26–28]. This includes, on the ascending side, the sensory in- First, however, we must introduce the standard set pieces of formation conveying heartbeats, respiration, and the activity of predictive processing and interoceptive inference. Predictive the stomach and gut to the brain – literally, gut feelings. On processing can be described as a set of theories which aim to the descending side, interoception denotes the visceromotor sig- understand how expectations – both neural and psychological nals and allostatic reflex arcs by which agents maintain their – shape, constrain, and ultimately define the mind. These the- homeostasis in the face of environmental challenges. Interocep- ories have deep roots in cybernetics, information processing, tive processes are thus those which enable an agent to monitor and seminal prospective control models emerging from early and control the bodily states that are necessary to maintain the 1960s motor and activity theory. A key feature of predictive balance between energy expenditure and consumption. processing is the basic notion that biological information pro- We can further demarcate interoceptive processes into those cessing occurs primarily via the minimization of (information which directly subserve homeostasis, that is the maintenance of theoretic) surprise, such that the nervous system can be under- a steady state defined by specific metabolic set-points, and al- stood as a hierarchy of top-down predictions and bottom-up lostasis, the proactive control of the body – and environment – to prediction errors. Whilst most early theories extrapolated this resolve homeostatic needs before they arise [29–31]. For exam- basic scheme to explain restricted phenomena such as prospec- ple, biological necessity dictates that body temperature, blood tive motor control and the sense of agency [6–8], in recent years oxygenation, and blood glucose level are all maintained within these approaches have exploded with a myriad of conceptual, a restrictive range of values. Any sustained deviation from these computational, and empirical work. An in-depth review of the values is likely to negatively impact an organism’s survival, scope of predictive processing is beyond this current article. For whether through the direct inducement of cellular death, or by the unfamiliar reader, we here recall the basic principles, but for the slow attrition of metabolic surplus through starvation. If a more thorough treatment numerous recent reviews exist, both oxygen is too low, or temperature too high, the brain can directly of the general computational and theoretical principles [9–13], engage adaptive physiological reflexes, maintaining homeosta- and their relationship with notions of embodiment and selfhood sis by increasing respiratory frequency or decreasing systolic [14–16]. blood pressure. In summary, these approaches surmise that the brain, much These simple sensory-motor reflex arcs, illustrated in Figure like a Russian Matryoshka or nesting doll, comprises an inter- 1, can be readily understood by appeal to predictive mecha- locking hierarchical web, with each unit or level of this web nisms not unlike that of a common household thermostat. That predicting the output of the lower level. At the outermost layer is to say, a low-level spinal, thalamic, or brainstem circuit is of this hierarchical ‘brain web’ one finds the sensory epithelium generally sufficient to encode the set-point as a prior expecta- and motor apparatus of the agent – that is, the means by which tion on the heart-rate, respiratory frequency, or blood pressure. the agent takes in information about the world external to itself, As in afferent control theory, this problem reduces to one of in- and acts upon those sensory inputs to alter the world. As one creasing or decreasing the descending visceromotor predictions moves from these outermost layers, venturing deeper into the to minimize any sensory prediction error that occurs: c.f., the nervous system, neuronal populations encode or invert a model equilibrium point hypothesis in motor control [32] and related of its inputs1. This generative model comprises three key com- perceptual control theories [33]. One can thus easily envision ponents: a prediction (e.g., of a hierarchically lower expectation), simple predictive engrams, which monitor visceral inputs and a prediction error (e.g., encoding the difference between the ex- adjust bodily states as needed to maintain the overall integrity pectation and its prediction),