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Towards a view from within: On the scientific study of and the contribution of

Renzo C. Lanfranco1,2*, Andres Canales-Johnson3,4,5, Boris Lucero5, & Valdas Noreika6,7*

1Department of , Karolinska Institutet, Stockholm, Sweden; 2Department of Psychology, University of Edinburgh, Edinburgh, United Kingdom; 3Department of Psychology, University of Cambridge, Cambridge, United Kingdom; 4Vicerrectoria de Investigación y Posgrado, Universidad Católica del Maule, Talca, Chile; 5The and Cognitive Research Center, Faculty of Health Sciences, Universidad Católica del Maule, Talca, Chile; 6Department of Biological and Experimental Psychology, School of Biological and Chemical Sciences, Queen Mary University of London, London, United Kingdom; 7Department of Psychology and Speech-Language Pathology, University of Turku, Turku, Finland.

*Corresponding authors: Dr. Renzo Lanfranco, Department of Neuroscience, Karolinska Institutet, Biomedicum, D4, Tomtebodavägen 16, 171 77, Stockholm, Sweden. Email: [email protected], and Dr. Valdas Noreika, Department of Biological and Experimental Psychology, School of Biological and Chemical Sciences, Queen Mary University of London, Mile End Road, London E1 4NS, United Kingdom. E-mail: [email protected]

Note. Sections 1-6 of this article are based on the doctoral dissertation defended by the last author at the University of Turku (Noreika, 2014).

Abstract

The contents of consciousness are complex and dynamic, presenting in most perceptual and cognitive functions. The study of consciousness and subjective has been central to philosophy for centuries. However, despite its relevance for and behaviour, the empirical study of consciousness is relatively new, embroiled by the seemingly opposing subjective and objective sources of data. Francisco Varela (1946 – 2001) pioneered the empirical study of consciousness by developing novel and rich approaches in a non- reductive and comprehensive manner. In this article, we review the main conceptual distinctions, properties, problems, and theories of consciousness, and highlight the main contributions of Varela and his associates: the development of neurophenomenology as a methodological framework that builds a bridge between subjective and objective sources of data, and the discovery of gamma-band phase synchronisation as a neural marker of perceptual awareness.

Keywords: Consciousness, Awareness, Perception, Neurophenomenology, Philosophy of , Francisco Varela

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1. Introduction using objective methods are limited by the predictability of the contents of Human individuals are unique in the consciousness, i.e. they rely on the momentary and lifelong collection of their recognition of neural activity patterns that contents of consciousness, or subjective emerge in association with the , which include – but are not standardised contents of consciousness. limited to – sensations, feelings, thoughts, For instance, in the same study mentioned and beliefs. Typically, the contents of above dream content detection relied on consciousness are complex and dynamic, the neural similarity between relatively with an extremely wide range of possible simple perceptual experiences in waking experiences that continuously adapt to and onset (Horikawa et al., 2013), internal and external stimuli as well as to which may not hold for more intense and other subjective experiences. While in unpredictable rapid eye movement (REM) standard social situations we are relatively sleep dreaming or other unresponsive successful in guessing subjective states of consciousness with complex experiences of other individuals by drawing spontaneously developing subjective inferences from their behaviour and experiences. Furthermore, - affective display (Ames, 2005), it proves to driven prediction is not explanation, while be very difficult to measure the contents of the ultimate goal of the science of consciousness with scientific methods. consciousness is the explanation of how The problem of the detection of subjective experiences arise from brain consciousness can be addressed with activity. objective methods, such as Compared to the objective methods, electroencephalography (EEG) and content analysis of subjective reports psychophysics, with subjective methods, enables a very detailed assessment of such as analysis of verbal reports and naturally and spontaneously occurring questionnaires, or with a combination of subjective experiences, including – but not both types of methods. For instance, limited to – such diverse contents of analysis of neurophysiological data can consciousness as Self and body, visual distinguish which of two competing images experiences, perception of sound, participants perceive when each of them is temporal and spatial distortions, and so on. presented to different eyes (binocular Arguably, a detailed mapping of human rivalry paradigm; Haynes & Rees, 2005), or phenomenology in different states of to evaluate if an unresponsive vegetative consciousness will eventually provide a state patient follows mental imagery- solid ground for research into the neural related instructions (Owen et al., 2006). basis of consciousness. While subjective Machine-learning-based analysis of fMRI methods alone are not able to provide data can even enable prediction above sufficient insight into the neural chance level of the visual contents of non- mechanisms of consciousness, a rapid eye movement (NREM) sleep combination of both objective and dreaming (Horikawa et al., 2013). Yet, subjective methods will probably become despite an invaluable progress, studies

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one of the most promising avenues of key used in consciousness consciousness research in the near future. research, such as awareness and access Nevertheless, it is not straightforward to consciousness, are often used in different combine subjective and objective methods, and partly controversial meanings. To and they are still being developed largely minimise conceptual confusion, these separately. terms should be carefully defined, searching for the most accurate match Francisco Varela (1946 – 2001) was a between our semantics and the natural Chilean who addressed kinds of human mind. these matters with scientific rigour while taking into account the phenomenological 2.1 Phenomenal consciousness concerns about human experience. Among his many contributions, we find When scientists and philosophers discuss neurophenomenology, a research the hard problem of consciousness approach that attempts to build a bridge (Chalmers, 1995), they primarily mean between objective and subjective phenomenal consciousness, which is the information, hence an integrative method most fundamental term in contemporary to study the hard problem of consciousness research of subjective experiences. The (see below). Additionally, Varela proposed of phenomenal consciousness neural phase synchronisation as a testable refers to the presence of a subjective mechanism of perceptual awareness. His aspect in a wide range of mental functions, contributions have influenced countless including perception, emotion, memory, consciousness scientists over the years and attention, language, decision making, and are still relevant today. motor control (Block, 1995; Revonsuo, 2006). When we say a word, touch a In this article, we review the main concepts tablecloth or remember what we have used in consciousness research, the most seen during the last trip abroad, these acts influential philosophical and are usually accompanied by internal neurobiological theories of subjective experiences, which are subjective and experience, and the contribution of private. As Nagel (1974) phrased, an Francisco Varela to the scientific study of organism is conscious if ‘there is consciousness. something it is like to be that organism’ (p. 436), that is, if it has experiences that bear distinctive subjective qualities – often 2. Defining consciousness referred to as (C. I. Lewis, 1929) – for Consciousness science is a the organism. multidisciplinary field in the intersection between philosophy, experimental 2.2 Sensory awareness psychology, neuropsychology, and Phenomenal consciousness is sometimes . Given a large equated with awareness; however, the number of competing theories and latter concept is narrower and refers to a approaches, it is natural that many of the special type of phenomenal

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consciousness: the presence of sensory 2.3 Access consciousness, reflective experiences triggered by real physical consciousness, and cognitive stimuli of which we thereby become accessibility aware. In particular, each of the classical Subjective experiences can be attended to sensory systems, i.e. vision, hearing, (accessed) and information about them olfaction, gustation, and somatosensory distributed within a broader neural network system, has not only unique receptive for further information processing, leading fields, cellular receptors, central pathways, to various cognitive and behavioural and cortical networks (Møller, 2003), but effects. This implicates that phenomenal also unique sensory qualities of consciousness can be described experience. We not only detect a leaf functionally. Functional interactions falling from a tree, but also have a between phenomenal consciousness and subjective awareness of that leaf, broader cognitive systems guiding rational awareness that does not seem necessary behaviour have been termed as access for the detection itself. Naturally, consciousness (Block, 1995). Block (1995) phenomenal consciousness within each argued for a double dissociation between sensory system is often conceptualised as phenomenal consciousness and access visual awareness (Koivisto et al., 2006), consciousness, i.e. subjective experiences auditory awareness (Gutschalk et al., might exist without being broadcasted to 2008), olfactory awareness (Li et al., 2010), executive processes, whereas functional gustatory awareness (Verhagen, 2007), or causal roles of access consciousness may somatosensory awareness (Schubert et al., be achieved without the presence of 2006). Notably, phenomenal subjective experiences. Revonsuo (1995, consciousness as a broader term also 2006) pointed out that such a definition of includes, for instance, internally access consciousness allows a subjectively generated hallucinatory experiences, or unconscious person to be called conscious, subjective experiences related to non- leading to a conceptual contradiction. sensory mental functions, such as Instead, a theoretically more coherent semantic processing. That is, awareness is approach may be a separation of two levels a type of phenomenal consciousness of consciousness: the first fundamental triggered by external physical stimuli or level would be phenomenal consciousness internal physiological processes in the and the second higher level would consist case of interoceptive awareness (Critchley of cognitive operations over selected et al., 2004), whereas phenomenal subjective experiences held in working consciousness refers to the subjective memory (Revonsuo, 2006). Farthing (1992) experience itself, regardless of what termed the second higher-order level as triggered it, external or internal stimuli, reflective consciousness, although this term thoughts, or memories. may be somewhat too narrow, as the

concept of reflective consciousness is

sometimes described in terms of abstract thinking and verbalisation of subjective

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experiences (Bartolomeo et al., 2008), consciousness, i.e. an overall pattern of whereas cognitive operations over subjective psychological functioning (Tart, phenomenal consciousness also include 1972). Alongside a theoretical distinction more basic cognitive processes that are not between the presence of specific contents necessarily verbalised, such as selective of consciousness and the presence of an attention or difference detection overall state of consciousness, two (Revonsuo, 2006). In more recent studies, independent neurophysiological research Block (2007, 2011) toned down the programmes are currently developing in arguments regarding dissociation between the empirical science of consciousness. phenomenal and access consciousness, Research on the phenomenal contents of and instead of these terms started using the consciousness focuses on the neural concepts of phenomenology and cognitive mechanisms of specific subjective accessibility, the latter of which is defined as experiences, for example, detection of the broadcasting of subjective experiences masked visual targets (Mathewson et al., within the central processing system. The 2009), whilst ignoring other concepts of phenomenology and cognitive simultaneously occurring contents of accessibility (Block, 2007) seem to be consciousness. By contrast, neuroimaging compatible with the distinction between research of the state of consciousness phenomenal and reflective consciousness typically contrasts the conscious state with (Farthing, 1992; Revonsuo, 2006). the loss or the absence of consciousness in conditions such as regaining of 2.4 Contents versus states of consciousness after its loss due to the consciousness administration of anaesthetic agents (Långsjö et al., 2012). Subjective experiences are sometimes termed as phenomenal contents of 2.5 Altered versus baseline states of consciousness, which refers to the variety consciousness of experiences that are contained or occur in phenomenal consciousness (Revonsuo, Compared to the standard waking state of 2006). Most of the phenomenal contents consciousness, which could be regarded of consciousness are also representational as a baseline state of consciousness, contents, i.e. they seem to be representing human consciousness may undergo specific aspects of the physical realm various neurocognitive alterations, such as (Chalmers, 2000). Even though not all those observed in dreaming, hypnosis, or subjective experiences have veridical meditation. Such alterations are often physical referent, for example, some referred to as altered states of bizarre dream experiences or consciousness (ASCs; Tart, 1975), and hallucinations may be unrelated to the they are typically individuated by specific actual physical world, they still typically do changes in their contents (Chalmers, appear for an experiential subject as 2000) and/or their induction techniques representing external reality. The totality (Vaitl et al., 2005). Complementing the of phenomenal contents forms the state of classical neurological approach of

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studying abnormal in order to understand qualia, but would maintain a potential to normal, ASCs can be used as important become conscious if some dream contrast conditions for studying human experiences would emerge. consciousness and the breakdown of its Nonconscious states of the brain/mind are fundamental properties (Hobson, 2001; those that have no capacity to support Revonsuo, 2006). phenomenal consciousness, such as irreversible coma (Silverman et al., 1970). 2.6 Conscious, unconscious, and By definition, there are no unconscious nonconscious processes and states contents in the nonconscious state of the brain/mind. Phenomenal contents do change rapidly, and a stimulus of which we were aware a 3. Fundamental properties of couple of seconds ago may not be a part consciousness of the current contents of consciousness. Nevertheless, some of the dissipated Given that subjective experiences contents may re-enter phenomenal accompany a very wide range of sensory, consciousness after, for instance, episodic cognitive, and behavioural functions, most memory retrieval (Düzel et al., 1997). By of which have a myriad of sub-functions, contrast, some other neural processes are phenomenal consciousness turns out to be never associated with the phenomenal a very diverse and generic brain process. contents of consciousness, for example, For instance, not only has each modality of the early latency (55 ms) of visual evoked sensory awareness exclusive experiential potential C1 (Di Russo et al., 2002) qualities, but each sensory system codes a indicates that we are not directly aware of large number of unique stimulus features neural processes underlying its that are associated with unique qualia. generation, as visual awareness-related Thus, for example, visual awareness is EEG potentials occur in the time latencies comprised of experiences of colour (Vul & above 100 ms (Koivisto & Revonsuo, MacLeod, 2006), motion (Eagleman & 2010). Neural activity patterns that are not Sejnowski, 2000), depth (Brouwer et al., associated with conscious experiences 2005), and location (Huang et al., 2007). but could, under some circumstances, While simple sensory qualities may produce phenomenal consciousness can accompany the realm of sensory be termed as unconscious contents, awareness, more complicated experiences whereas nonconscious processes are of, for instance, understanding and those deprived of capacity to reach remembering may be associated with phenomenal consciousness (Searle, complex cognitive functions, such as 1992). A similar distinction can be drawn semantic processing (Kiefer & Spitzer, between conscious, unconscious, and 2000) or autobiographic memory (Piolino nonconscious states of mind. A conscious et al., 2003). In the latter cases, subjective state would contain at least one subjective experiences do not reflect physical experience, whereas unconscious state, properties of stimuli but instead they point such as deep NREM sleep, may have no to the higher order phenomenal qualities

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such as subjective certainty (Tulving, 1985) joined into a coherent flow of a single or an awareness of semantic ambiguities unified stream of consciousness. That is, we (Zipke et al., 2009). do not have an experience of unrelated sensations that jump in time and space, When focusing on a specific type of although this may take place in certain subjective experiences in a restricted psychiatric or neurological conditions such experimental setup, phenomenal as schizophrenia (Vogeley & Kupke, 2007) consciousness seems to be a constellation or akinetopsia (Zeki, 1991), but an of a vast number of subjective experiences experience of spatially and temporally that emerge, develop, and vanish in bound qualities that form a single stream of isolation from other experiences. Thus, for consciousness. The concept of example, research on participant’s consciousness-related binding refers to the awareness of changing ambiguous Necker experienced phenomenal unity of the cubes (Intaitė et al., 2013), while being an contents of consciousness, and it should be interesting visual phenomenon in itself, demarcated from the stimulus-related seems to have no connection to other binding, which refers to the coherence of subjective experiences that may occur neural representations of external physical during the same experiment, including objects that may or may not become the feelings of hunger, boredom, or guilt after phenomenal contents of consciousness missing a stimulus, a tingling sensation in a (Revonsuo, 1999, 2006). shoulder, hearing of the background noise, or seeing objects in the peripheral visual In addition to the temporal and spatial field. However, of our own binding of phenomenal contents, they are experiences reveals that phenomenal also bound together across different consciousness, despite its richness and mental domains, including sensory, dynamics, is normally unified and coherent, executive, semantic, and motor functions. forming a consistent complex model of Such multifunctional integration of external and internal environment subjective experiences brings together (Revonsuo, 2006). different types of qualia into a coherent perception of the world, for example, James (1890) argued that there is continuity while talking with a friend, we may in the diversity of phenomenal experiences, experience visual awareness of her face, which can be conceptualised as the stream auditory awareness of verbal sounds, and of consciousness, pointing to the constantly semantic awareness of the meaning of changing, yet coherent and continuous, words, which may further surprise us or contents of phenomenal consciousness. trigger some autobiographical memories. Continuity of the stream of consciousness depends on the temporal and spatial unity 3.1 Temporal binding or binding of individual subjective experiences (Dainton, 2005; Revonsuo, Temporal binding of the phenomenal 2006). Even though each distinct contents of consciousness integrates experience may occur at different points in subjective experiences over time. In the phenomenal space and time, they are phenomenal consciousness, temporal

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binding can be studied in terms of phenomenal consciousness: the just- perception of duration and simultaneity experienced contents of consciousness (Kiverstein, 2010). Perception of duration are kept in the iconic memory, while we is typically associated with integration of experience the present contents, the same set of qualia over time, for anticipating the subsequent ones. The example, we may feel that the experience tripartite temporal structure of of a bee whose flying trajectory we just consciousness is sometimes referred to as followed lasted for a certain interval of the specious present – the temporally time, e.g. 3 seconds. Possibly, the same extended phenomenal experience of now neuronal populations representing the (Dainton, 2005; Kelly, 1882). The widest bee continued oscillating and temporal binding of phenomenal synchronizing their activity during this contents of consciousness depends on the period of time (Engel & Singer, 2001), and autobiographic memory, which integrates subjectively we experienced it as a single phenomenal experiences over many days temporally extended percept of the bee. and years, constituting the basis for self- Interestingly, it has been shown that consciousness, also called autonoetic perceptual or attentional sampling of consciousness (Piolino et al., 2003; sensory information is not completely Tulving, 1985; Wheeler et al., 1997). continuous, but instead it oscillates in the theta (4–8 Hz) or alpha (8–12 Hz) frequency 3.2 Spatial binding range (Busch et al., 2009; Mathewson et Spatial binding of the phenomenal al., 2009; Ng et al., 2012). Phenomenally, contents of consciousness refers to the we are not aware of such temporal integration of subjective experiences in snapshots underlying our perception, and space. Each stimulus-driven experience their mechanisms operate at the has a specific location in relation to other nonconscious level of processing. experiences, which is studied under the While perception of duration is often concept of location binding (Treisman, associated with awareness of a single 1996). Furthermore, experiences typically object, perception of simultaneity points have a defined location with respect to our to the integration of several different sets own body that forms the centre of of qualia over time, i.e. we may experience phenomenal space (Revonsuo, 2006). The the flying bee and the still honeybush at egocentric reference point is typically the same time. Contrary to simultaneity, located in the phenomenal head or chest perception of asynchrony or temporal and it can be used to identify the location order reveals a temporal succession of of other phenomenal contents of different phenomenal contents of consciousness (Revonsuo, 2006). consciousness. In these cases, the Phenomenal spatiality, while typically temporal binding unifies the change from studied in the visual domain (Clark, 2000), one subjective experience to another over is inherent not only for every sensory a wider interval of time. This aspect of modality but also for emotions and temporal binding likely involves feelings (Nummenmaa et al., 2014). While neurocognitive mechanisms of

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visual and auditory experiences are phenomenal contents. Furthermore, typically localised in the phenomenal awareness itself may have a crucial role in space outside our bodily space, tactile or such multisensory interactions, as in some emotional stimuli are primarily located cases only consciously perceived within the phenomenal body. Notably, information from the dominating sensory various experimental manipulations can modality is transferred to another modality reallocate experiences from the external (Palmer & Ramsey, 2012). Multisensory phenomenal space to the internal bodily interactions between different sensory space or vice versa. For example, identical modalities may also underlie generation of auditory stimuli presented binaurally spatial awareness (Clavagnier et al., 2004) through the headphones might be and bodily self-consciousness (Blanke, subjectively felt as localised inside the 2012). Another type of multifunctional head (Hartmann & Wittenberg, 1996), integration takes place in the form of whereas presentation of conflicting visual- perceptual-semantic binding, which somatosensory input in virtual reality may enables the experience of the immediate shift the self-centre outside of the physical meaningfulness of phenomenal contents of body (Lenggenhager et al., 2007). consciousness (Revonsuo, 2006). Typically, Nevertheless, spatial unity of experiences perceptual experiences are automatically is maintained even in such unexpected bound together with semantic contents, and artificial distortions, indicating the leading to the spontaneously occurring robustness of consciousness-related recognition and linguistic spatial binding. conceptualisation of these experiences.

The first-person perspective suggests that 3.3 Multifunctional integration ‘we see the very world we act in and we act In addition to the temporal and spatial in the world we see’ (Clark, 2009, p. 1460). binding, phenomenal consciousness is If so, the integration of perception and integrated across different perceptual, action along a single unified flow of body- cognitive, and behavioural functions, world interaction might be another leading to the multifunctional unity of the fundamental aspect of consciousness, experience of the self in the world. Such which has even been suggested to be the multifunctional integration takes place ontological basis of consciousness along several different axes, including (O’Regan & Noë, 2001). Indeed, embodied perception-perception, perception- vision seems to be dominating over language, and perception-action unity. For subjective experiences during wakefulness, instance, integration of phenomenal when we perceive and interact with the contents across different sensory systems world around us. However, bodily and (e.g. seeing a face and hearing its speech), motor processes do not seem to be brings together very different perceptual necessary for visual experiences to emerge, qualia under one single stream of as, for instance, people may have rather consciousness instead of forming two intense visual dreams during REM sleep, separate auditory and visual streams of when their muscular system is atonic.

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Furthermore, the neuropsychological and consistent with the absence of neuroimaging evidence suggests that phenomenal subjective experience conscious ‘vision for perception’ in the despite the presence of these processes ventral visual processing stream and non- (Chalmers, 1996; Nagel, 1974). These conscious ‘vision for action’ in the dorsal have been illustrated by several stream can be dissociated from each other famous thought-experiments (Jackson, (Goodale & Milner, 1992; Milner & 1986; Nagel, 1974). Nagel (1974) argued Goodale, 2008). Thus, perception-action that even if objective science would integration seems to be a typical, but not a acquire all physical facts about humans or fundamental property of consciousness. other mammals, we would still miss information about their subjective point of

view. For instance, even if we would know 4. The hard problem of subjectivity all neurophysiological and behavioural Given that phenomenal contents of facts about a bat, including its sensory consciousness are subjective and directly echolocation system, we would still have available only to the experiencing self, no of ‘what is it like to be a bat’, in explaining the ontology of consciousness other words, what are its subjective poses a unique problem for science: it experiences of flying in the complete violates a universal assumption that the darkness among trees. Likewise, the same phenomena studied by science should be argument can extend to other conscious equally available to all observers, and no organisms, including humans: their observer should have a privileged access subjective point of view is always left out in to a phenomenon. Even though an objective scientific description of representational contents consciousness behaviour and (Nagel, can be successfully mapped using 1974). Jackson (1986) argued that a neuroimaging techniques, specific blood- neuroscientist who is congenitally colour flow or electrophysiological activation blind but knows all objective facts about patterns do not provide access to the the psychophysics and physiology of subjective experiential qualities. colour perception would still learn Consequently, there seems to be an something new if one day her colour unbridgeable explanatory gap between vision would be cured, which seems to the objective neurophysiological data and indicate that there might be more to the subjective contents of consciousness: consciousness than physical facts about its even if we are certain that the existence of mechanisms. consciousness is dependent on the brain, Many of the consciousness-related we cannot understand how brain activities research problems, such as the ability of a cause or constitute consciousness (Levine, system to access its own internal states or 1983; McGinn, 1989). Reductive analyses the difference between wakefulness and of consciousness, i.e. suggestions that sleep, seem to be relatively easy, i.e. they consciousness is identical with some types seem to be directly susceptible to the of brain processes or functional standard methods of cognitive descriptions, always seem to be logically neuroscience (Chalmers, 1995). Even

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though some of the easy problems of mind-body problem consciousness are not yet solved, we have a clear idea of what would be their 5.1 Classical solutions to the mind- scientific explanation: discovery and body problem description of computational and/or Throughout centuries of theoretical neural mechanisms would solve each of research, controversies between dualism these problems. Contrary to this, the versus , versus realism, problem of the material basis of conscious and rationalism versus , placed experience is a problem of a different the mind and consciousness at the top of nature: it is a hard problem, which seems philosophical investigations (Crane & to resist any of the empirical methods Patterson, 2000; Heinämaa et al., 2007). available to contemporary science Dualistic approaches to the mind-body (Chalmers, 1995). We do not have any problem assume that the mind (or certain idea of how and why subjective sensations aspects of it) and the physical world are or emotions arise from a physical basis, ontologically separate and cannot be and yet they do. Even worse, we cannot reduced to each other. Proponents of even imagine how this problem could be substance dualism, most notably solved in terms of neurophysiological or Descartes (1641), suggested that neurochemical processes. consciousness and the brain are different The hard problem can be tackled by a substances, which can exist number of different philosophical theories independently of each other. Property of the mind-body relationship, and some dualists supposed the existence of one of these theories, such as dualism or substance with two fundamentally , do not seem to have the different aspects, i.e. mentality and hard problem of consciousness at all. materiality, where mental properties do Arguably, it applies only to materialistic not exist in the absence of physical theories that aim to explain subjectivity in properties (e.g. Mill, 1974). Contrary to terms of objective physical or biological dualistic positions, monism assumed the processes. Next, some of the most existence of only one independent influential classical and contemporary substance. For instance, La Mettrie (1994) metaphysical theories of the mind-body defended a materialistic position (also relationship will be presented and called physical monism), arguing that evaluated, with a special focus on the consciousness has purely physical causes biological approaches to the and there is no necessity to assume the consciousness-brain interaction. existence of a separate ‘soul- substance’.

On the opposite extreme of monistic

positions lied idealism (also called mental

monism), which states that consciousness

is the only ontologically real substance,

whereas all the other material substrates

are derivable from it (Berkeley, 1710), i.e. 5. Philosophical theories of the

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brain and other physical phenomena are observable neural states or processes. A real, but only as the subjective contents of possible answer to this argument is consciousness. Further developments of provided by eliminativism, which states classical solutions to the mind-body that subjective properties do not problem showed that there is no ‘pure physically exist. The most fundamental is dualism’ or ‘pure idealism’, but instead the existence of the brain and the whole there are many different versions of them body, while the subjective aspect of (Morton, 2010), some of which continue perception is nothing more than an being considered and developed. For epiphenomenal illusion – a instance, findings in modern physics and misrepresentation about functioning of neuroscience may inspire brain and our brains without any causal power physics-oriented refinement of property (Churchland, 1999; Dennett, 1978, 1991). dualism (Popper & Eccles, 1977) and even Yet, even if one agrees that consciousness idealism (Bolender, 2001). is an illusion, there is something left to be explained: how the brain can produce this 5.2 Contemporary theories: from subjective illusion. eliminativism to panpsychism Not all ontologies of mind that take the Contemporary ontological theories of physical world seriously seek to reduce or consciousness provide a wide range of eliminate phenomenal consciousness. For solutions of how consciousness and the instance, embodiment theories assume brain might be related, which indicates the that subjective experiences depend on lack of a single widely convincing the physical world, but processes and ontological theory of consciousness. For entities which are necessary for instance, reductionism, one of the consciousness are not limited to the brain: materialistic theories of the mind-body the contents of consciousness are relationship, suggests that each type of ontologically dependant on causal or process is identical to relations with peripheral body as well as some type of neural state or process with external physical objects (Noë & (Lewis, 1966; Smart, 1959). According to Thompson, 2004; Thompson & Varela, the type-type theory, which is a 2001). For example, Varela proposed the version of reductionism, there is no view of , in which cognition is difference between a particular neural seen as a result of the dynamic interaction level in the brain and consciousness. Yet, between an acting organism and its the identity relationship implies that environment through sensorimotor certain neural processes and interactions – a relationship of consciousness share all their properties, codetermination (Maturana & Varela, whereas conscious experiences have 1987). Unlike cognitive approaches, in subjective qualitative aspects that the which organisms are seen as passive neural mechanisms do not seem to have. receivers of information from their If so, consciousness cannot be identical or environment, the enactivist view reducible to any of the objectively conceives organisms as actors who shape

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their experience by how they act peripheral body and immediate physical (Hutchins, 1996). As argued by Thompson stimuli, panpsychism goes further and (2010), the enactivist view addresses the proposes that consciousness may be just explanatory gap in the hard problem of about everywhere. For instance, Chalmers consciousness by building a bridge (1996) argues that information between subjective experience and the implemented in any physical system, such brain. While the formulation of the hard as the brain, flowers, or microwaves, is problem often takes a dualistic form, the conscious, i.e. it is a natural law that enactivist view embraces subjective information realised physically is experience by asserting that science is phenomenally conscious (see Koch et al., also enacted and as such it arises from 2016; Tononi, 2001, 2012). Several related humankind’s interactivity with the world, proposals have been put forward by through the interaction between researchers arguing that consciousness is sensorimotor patterns of perception and a property of matter at the level of action. Crucially, enactivism conceives fundamental physical forces, such as those cognition not as the mere processing of described by quantum mechanics (Bohm, information in a computationalist sense 1990; Jibu & Yasue, 1995). However, but, rather, as an exercise of skilful know- physics- and information-oriented how in situated and embodied action. theories have difficulties in explaining why Therefore, while traditional cognitive consciousness is so tightly related to views conceive cognition as information certain processes in the brain, as processing based on a prespecified demonstrated by numerous cognitive external realm represented internally, the neuroscience studies (but see Hameroff, enactivist view conceives cognition as a 2007). relational domain enacted, i.e. cognition Functionalism suggests that the ontology would emerge from recurrent of consciousness is determined by sensorimotor patterns of perception and abstract causal interactions between action. perceptual, cognitive, and behavioural The embodiment approach seems to be processes. In fact, functionalistic theories plausible in the case of visual perception, propose that any mental state could be as one of the prerequisites of vision is defined by sensory inputs, inner external physical stimulation of retina, yet informational processes, and behavioural embodiment theories do not provide a outputs (Fodor, 1975; Wright, 1973). satisfactory explanation of how internal Descriptions of such functional subjective experiences are generated in interactions have been successfully used the absence of behavioural embodied in cognitive sciences to explain human interactions with the world, such as during rationality and decision making (Clark, mental imagery or dreaming. While the 2001), which fuelled expectations that embodiment approach extends physical consciousness could be explained foundations of consciousness from the likewise (Dennett, 1978). Importantly, the purely brain-based mechanisms to the abstract level of functional explanations

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implies that biological brains are not thought to be caused by lower-level brain necessary for the generation of processes, it also seems to be irreducible consciousness, as the same abstract to them and having its own causal efficacy functions and algorithms can be to influence cognition and behaviour implemented in different physical (Searle, 2007). Consistently with these substrates. The possibility of multiple intuitions, biological realism assumes that realisations of functional interactions phenomenal consciousness is a real seems to provide theoretical grounds for biological phenomenon that resides building artificial and within the confines of the brain and cannot consciousness (Aleksander, 2005). Yet, be reduced to the fundamental laws of while being a promising theory for physics (Revonsuo, 2006). Given that identifying functional roles of being real implies having its own causal consciousness, functionalism does not powers (J. Kim, 1992), consciousness is escape from difficulties in explaining assumed to be subordinated to causal qualitative aspects of consciousness interactions with other neural processes in (Block, 1980), as it remains unclear why the brain and, through them, with the rest some, but not all, functional networks are of the body and the physical world. conscious. Difficulties in conceptualising a Methodologically, biological realism convincing ontological theory of proposes that subjective experiences as consciousness have even led to a position biologically real phenomena should be called mysterianism, also known as strong studied by biology. In particular, the emergent : even if material basis of consciousness should be consciousness is a material phenomenon, studied within the spatial and temporal the may simply be too limited scales that are common for neurosciences. and incapable of explaining the mind- Further, biological realism assumes that body relationship, just as, for instance, we are not cognitively closed to the dog brains are incapable of understanding of consciousness, but understanding modern physics (McGinn, instead biological sciences, especially 1989, 1991). cognitive neuroscience, are (or will be) able to explain it (Revonsuo, 2006). Thus, 5.3 Biological approaches to metaphysically, biological realism consciousness represents the weak , which predicts that the The majority of the empirical researchers complete understanding of the brain will of consciousness tend to follow explain how consciousness emerges from assumptions of , brain processes (Revonsuo, 2010). which is a scientific common-sense Contrary to this, strong emergent position that consciousness is a materialism assumes that the neural basis qualitative, subjective, unified and of consciousness will remain unresolved (usually) representational high-level brain even when all facts about the human brain function (Searle, 1992, 2007, 2015). will become known to the scientific Importantly, even though consciousness is community.

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However, despite continuous While explanation in physics typically development of a biological research involves description of universal natural programme during the previous decades laws through which an explanandum, i.e. and its relative success in identifying some the target of explanation, can be reduced neural correlates of consciousness, the to physical processes at the smaller spatial hard problem of phenomenal and temporal scales, explanation in consciousness remains unsolved. Thus, biological sciences involves description of even though cognitive neuroscience and multilevel mechanisms whose causal neuropsychology already yielded a interactions are too complex to be number of fascinating discoveries and described by universal laws (Bechtel & neurocognitive theories, it remains Richardson, 1993; Craver, 2007; Craver & possible that some other approaches to Darden, 2001). Instead, biologists, consciousness than the one defended by including cognitive , biological realism might prove to be more develop constitutive, contextual, and accurate. For instance, it might turn out aetiological explanations of their that phenomenal consciousness emerges explanatory target (Revonsuo, 2006). as a product of multi-level functional Constitutive explanations reveal the lower interactions between biological entities levels of a phenomenon under and processes, and that these interactions investigation, for example, neuronal long- can be replicated in artificially designed term potentiation can be described as an systems. This would contradict the emergent outcome of the lower-level assumptions of biological naturalism and NMDA receptor activation (Craver & realism, which are regarded as an Darden, 2001). Contextual explanations alternative to functionalism (Revonsuo, point to the functional roles of 2006; Searle, 1984). Likewise, information explanandum in interaction with the integration and differentiation theory of higher levels of biological organisation. consciousness (Tononi, 2012; Tononi et Aetiological explanations describe al., 2016) may loosen its ties with biological processes that are capable of neuroscience if consciousness-generating modulating the explanandum, but cannot informational complexity would be constitute it, such as abnormal detected or designed in non-biological developmental pathways. Consciousness systems. is assumed to reside in the largely Until science and philosophy provide unknown phenomenal level of conclusive evidence and arguments, it organisation in the brain (Revonsuo, may be too early and premature to 2006), yet it is expected that descriptions commit to a single ontology of of interactions between the cognitive, consciousness, as this may hinder other phenomenal, and neural level of more accurate, yet currently neglected organisation will eventually solve the possibilities. Importantly, none of the mind-body problem (Bechtel & Mundale, discussed philosophical theories of the 1999). mind-body relationship neglects the

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importance of biological research, as even established the first psychology in substance dualism non-material entities laboratory in Leipzig in 1879. The first are thought to be able to cause changes in empirical studies of dream content were the brain (Descartes, 1641), which also carried out in the second half of the subsequently can be studied empirically. nineteenth century (for review, see Thus, successful implementation of the Noreika & Windt, 2008). For instance, methodology of biological realism may Maury (1861) investigated the influence of lead to, but currently does not require, the external stimuli on dreams, whereas acceptance of emergent materialism and Calkins (1893) proposed a statistical is compatible with metaphysical analysis of dream reports. Wundt’s indeterminacy. While it is feasible to focus student Titchener (1902) formalised on the neurobiology of consciousness, we introspection techniques and analysed do not know yet where we will end up in consciousness by systematically breaking trying to explain the hard problem of it down into elementary feelings and consciousness. Some of the currently most sensations, which led to the structuralist influential neurocognitive theories of . James (1890) took a consciousness are detailed below. different approach and instead of searching for the atoms of mind

emphasised the continuity of conscious 6. Neurocognitive theories of experiences that flow as a single stream of consciousness mental states. Despite important theoretical advances and development of 6.1 Historical sources of empirical new experimental paradigms, most of the consciousness research nineteenth century consciousness Beginnings of the modern empirical researchers relied on introspection, which research of consciousness can be traced was critically rejected by Watson (1913) back to the behavioural psychophysics and other behaviourists who argued that experiments conducted by Weber (1834) the only scientifically rigorous method to and Fechner (1860), who studied the study the human mind is a search for relationship between the physical systematic relationships between external intensity of various stimuli and the stimuli and behavioural responses. threshold of ‘just noticeable difference’ in The detailed critique of the methodology subjective sensation of these stimuli (for of introspection was soon accepted as the review, see Frith & Rees (2007). Donders general denial of the existence of (1969) developed an experimental consciousness itself. During domination of paradigm to compare simple and two- behaviourism in the first half of the choice reaction time tasks, which allowed twentieth century, the topic of differentiating mental and motor consciousness was removed from most of processes preceding motor responses. the scientifically oriented textbooks or Duration of mental events was further university programmes of psychology. investigated, although more Even though alternative approaches to the introspectively, by Wundt (1862), who

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study of mind did not completely cease, coordination, and distribution of different for example, research of principles of brain processes that otherwise would visual grouping led to the description of remain isolated, limited, and unconscious. Gestalt laws of vision (Wertheimer, 1923), Consciousness can be metaphorically they were marginalised for several depicted as a spotlight (i.e. the focus of decades until the development of attention) on a theatre stage, called global information theory (Shannon & Weaver, workspace (i.e. working memory), which is 1949) enabled the mathematical account controlled by the theatre director (i.e. of mental processes and triggered the executive Self; Baars, 2002). From a vast boost of number of the parallel and unconscious experiments (for review, see Frith & Rees information processes, consciousness 2007). Nevertheless, it took another thirty identifies the most relevant process or to forty years until quantitatively oriented representation, and distributes it widely psychology and neuroscience returned to across other cognitive functions. In the the topic of consciousness (Baars, 1988; global access networks, unconscious Crick, 1994). Notable exceptions in the resources, such as memories or neglect of subjective experiences were automatisms, may become the contents of split-brain studies in the 1960s and 1970s the conscious spotlight in the working (for review, see Gazzaniga, 2005) and memory, and subsequently may modulate empirical research of psychophysical cognitive contexts, such as expectation mechanisms and subjective contents of and intentions of Self (Baars, 2007). The dreaming, which flourished between 1953 spotlight of attention may switch from and 1993 (for review, see Foulkes, 1996). modality to modality at a rate of about 100 ms, which is considered sufficient to

produce the sense of phenomenal unity 6.2 of across different contents of consciousness consciousness (Baars, 1988). Depending on the contextual demands, the duration of The return of empirical sciences to the particular contents of consciousness may problem of consciousness was largely also be extended by re-initializing loops inspired by Baars (1988, 1997, 2002), who between unconscious resources, working developed a global workspace theory of memory and contexts, which, for instance, consciousness that seeks to explain would be needed for episodic and explicit consciousness through its functional learning or voluntary control of motor interactions with other cognitive activity. processes and functions, including attention, working memory, action Global workspace theory and models control, problem-solving, and language. were further developed by Franklin In particular, Baars (2002) proposed the (2003), who integrated it within a ‘conscious access hypothesis’, according computation model of cognition, and to which the main function of Dehaene and colleagues who consciousness is an integration, investigated neurophysiological

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mechanisms of the global distribution of and functions of consciousness. However, conscious information in the brain it does not provide a satisfactory (Dehaene & Changeux, 2011; Dehaene & explanation of the neural mechanisms of Naccache, 2001). For instance, it was subjective experience, as it assumes that demonstrated that unconsciously there is no phenomenal consciousness presented backward-masked visual words independent of or prior to access evoke localised activation of the consciousness. Phenomenal extrastriate, fusiform, and precentral consciousness as such becomes largely areas, whereas conscious presentation of eliminated from the theory. words in addition activate broad frontal and parietal networks (Dehaene & Naccache, 2001), arguably reflecting wide 6.3 Micro-consciousness versus access and broadcasting of conscious macro-consciousness information (Baars, 2007, 2017). At the While Baars (1997) and Dehaene et al. electrophysiological level of description, (2006) argued for the global workspace conscious access and global broadcasting theory of consciousness, (Zeki, 2003, seem to take place through the long- 2007) rejected the classical notion of the distance synchronisation of the beta and unity of consciousness and proposed that gamma frequencies (Dehaene & consciousness exists in the form of many Changeux, 2011; for a review, see autonomous units called ‘micro- Mashour et al., 2020). Yet, despite consciousnesses’. Neurological immense progress in the understanding observations and measurements of of functions and neural mechanisms of asynchrony of visual perception suggest conscious access, the global workspace that micro-consciousness units are theory of consciousness does not seem to distributed in both space and time (Zeki, offer a satisfactory account of the 2007; Zeki & Bartels, 1999; Zeki & Ffytche, phenomenal consciousness. In fact, 1998). For instance, lesions in the visual (Baars, 2007, 2017) argues that the typical colour area V4 produce achromatopsia, consciousness-related questions, such as but do not affect motion awareness, the status of qualia and the hard problem whereas lesions in the visual motion area of subjectivity do not apply to the global V5 produce akinetopsia, but do not workspace theory of consciousness. This is deteriorate colour awareness. simply because the global workspace Neurological cases seem to suggest that theory is a theory of conscious access, and an intact V5 is necessary and sufficient for perceptual processes outside of the the awareness of motion, even when cognitive machinery of global primary visual cortex V1 is lesioned (Zeki & broadcasting, i.e. the contents of pure Ffytche, 1998). Further, conscious phenomenal consciousness, are regarded perception, as opposed to unconscious as pre-conscious at best (Dehaene et al., information processing, may not involve 2006; Mashour et al., 2020). Such an any additional cortical region but instead approach may be successful in the it may differ by the increased activation identification of the cognitive interactions

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level of the same cortical areas, and in 6.4 Recurrent processing as the principle any anatomical region of cortex neural basis of consciousness could produce its own micro- Lamme (2006, 2020) proposed that the consciousness (Moutoussis & Zeki, 2002). generation of phenomenal consciousness Regarding temporal asynchrony of visual depends on the recurrent information micro-consciousness units, there is processing between different modules evidence showing that the earliest to across hierarchical neuronal networks. For reach the required level of activation is instance, the feedforward information micro-consciousness of location, followed sweep across regions V1, V2, V4, TE of the by micro- consciousnesses of colour, visual ventral stream is not sufficient for orientation and then of motion (Bartels & the generation of conscious perception, Zeki, 2004; Moutoussis, 2012). although it may contribute to visually Zeki (2003) distinguished three levels of guided actions. Contrary to this, recurrent consciousness: micro-consciousness as processing between V1, V2, V4, TE and subjective perception of basic between the ventral stream and fronto- phenomenal properties; macro- parietal networks will lead to reportable consciousness, i.e. the totality of micro- conscious perception. Moreover, Lamme consciousness units, as subjective (2006, 2020) argued that recurrent perception of meaningful objects; and processing within the ventral stream is unified consciousness as subjective capable of generating conscious awareness of Self. In this framework, the perception even when the ventral stream unity and binding are not treated as does not interact with the fronto-parietal fundamental properties of phenomenal accessibility networks. If so, the contents consciousness. Instead, temporary of visual awareness cannot be equated jumping activation of different areas in with the attentional focus and working cortex is assumed to be sufficient for the memory (as opposed to Baars, 2002, awareness of objects and scenes at the 2007), but instead visual awareness and macro-consciousness level of perceptual attention are doubly dissociable (Lamme, organisation. Yet, even though Zeki’s 2003, 2004). research programme shows that isolated Hypothesised independence of but conscious neuronal units may exist in phenomenal consciousness from access the cortex, the suggested account of the and reportability became one of the main disunity of consciousness is not consistent controversies in consciousness research with our phenomenology, as single (e.g. Block, 2011; Del Vecchio, 2021; objects as well as more complex sceneries Kouider et al., 2012; Overgaard & appear to us in a unified form rather than Fazekas, 2016; Tsuchiya et al., 2015). In as a stream of temporary and spatially particular, given that the presence of disintegrated features. Instead, the isolated micro-consciousness-type of findings of Zeki et al. seem to point to the processes (Zeki, 2003, 2007) cannot be lower representational or information proved directly as they are unreportable, processing levels of consciousness. there can be only indirect and thus

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questionable evidence of subjective information can be developed to detect experiences that are not available for consciousness. Tononi & Sporns (2003) conscious access. Furthermore, it remains detailed some preliminary analytic tools to unclear why recurrent processing is assess Φ – the capacity of a system to necessary for the emergence of integrate information. These tools have phenomenal consciousness. Possibly, the been updated and extended (e.g. H. Kim complexity of neuronal processing et al., 2018; Leung et al., 2021; Oizumi et required for the generation of conscious al., 2016). Effective information between experience cannot be achieved instantly any two given subsets of a system can be and requires temporally extended assessed by injecting maximum possible information processing, which may also entropy to one of the subsets and point to the neural mechanisms of measuring complexity of responses of specious present. another subset. By comparing effective connectivity between all possible subsets

of a system, one can identify if complexes 6.5 Information integration theory of of elements exist that maintain integrated consciousness information Φ that is lost if some of the elements become isolated from the Instead of selecting specific brain regions complex (Tononi, 2008). or electric frequency bands, information integration theory of consciousness, Tononi (2007) argued that information developed by Tononi (2001, 2004, 2010, integration theory is consistent with 2012), equates human conscious phenomenological observations of experience with integrated information in informativeness and unity of the brain. Each conscious experience rules consciousness, as well as psychophysical out an extraordinarily large number of studies showing that at least 100–200 ms alternative perceptual possibilities, are required for the emergence of making it highly informative (Tononi, consciousness (Bachmann, 2000), which, 2007). Further, information in conscious given the neuronal processing speed, is systems is exceedingly well integrated roughly the time required for information between the elements constituting such to be integrated in the highly connected systems, and the state of each element neuronal networks in the human brain. causally depends on the state of other Generation of consciousness may depend elements. Consequently, phenomenal on the high-level organisation of contents of a conscious state cannot be thalamocortical networks, which seem to divided into phenomenal contents of its support both functional specialisation elements, as such a disintegration of (Zeki, 1993) and functional integration information would lead to the loss of (Engel et al., 2001). By contrast, as consciousness. Given that the presence of predicted by information integration consciousness can be equated with the theory, cerebellar networks consisting of presence of integrated information, an even higher number of neurons than empirically feasible measures of such cerebral cortex but lacking associative

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connections (Bower, 2002), do not seem other. to be directly involved in the generation of Varela made two major contributions to conscious experience. Likewise, the field of consciousness research: the consciousness is absent when cortical neurophenomenological framework and networks lose effective connectivity and the study of neural phase synchronisation. presumably the capacity to integrate As described next, the former is a information during slow wave sleep or methodological programme that anaesthesia (Massimini et al., 2012). proposes an approach to study subjective However, even though information experience in a pragmatic way whereas integration measures are already used in the latter is an index of neural integration empirical studies of consciousness (e.g. of cognitive acts involved in the Casali et al., 2013; Lee et al., 2009; Leung emergence of consciousness. et al., 2021; Oizumi et al., 2016), it remains unclear how to assess the minimal degree of information integration required for 7.1 Neurophenomenology: bridging consciousness to emerge. It is also unclear the gap between subjectivity and whether any integrated information, objectivity including artificially designed systems, would be conscious. Tononi (2007) seems How can the hard problem of subjectivity to support the later conclusion, somewhat be addressed? Varela proposed a turning away from biological realism pragmatic approach called towards informational panpsychism neurophenomenology (Varela, 1996) that (Chalmers, 1995; Tononi & Koch, 2015). seeks to narrow the gap between the qualitative and quantitative aspects of

consciousness contents. To achieve this, 7. The contribution of Francisco Varela proposed that rigorous first-person Varela to the study of methods must be developed to examine consciousness qualitative experience rigorously, thus giving phenomenal data the same level of Varela was deeply concerned about the importance enjoyed by objective data in nature of consciousness; particularly, with cognitive science. The developing methods that could address neurophenomenology programme the hard problem of consciousness by entails training researchers in the skill of building a bridge between objective and phenomenological description since subjective sources of data. In addition, subjective experience is not completely Varela investigated the neural patterns private as it can be shared. In deep, Varela underlying subjective experience and sought to revolutionise how cognitive perceptual awareness; his work on this science addressed consciousness by matter led to the idea that consciousness cultivating a systematic capacity for did not happen in specific brain regions, reflexiveness and phenomenological but rather was a product of different examination (Varela & Shear, 1999). Varela neural systems communicating with each was inspired by the works of western

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phenomenologists such as Edmund what it is traditionally referred to as Husserl (1859 – 1938) and Maurice . Merleau-Ponty (1908 – 1961); he argued 3. Descriptions: invariants. The that Husserl’s phenomenological descriptive process must reduction technique could also be used to determine phenomenological develop an empirical science of invariants, i.e. controlled variations consciousness (Varela, 1997). of the subjective experience or Varela (1996) defined four intertwined “eidetic variations” as defined by moments in the neurophenomenological (Husserl, 1901). These invariants framework as part of phenomenological should be intersubjectively reduction: shareable or communicable. As explained by Varela, this is 1. Attitude: reduction. a self- comparable to what induced suspension of reference mathematicians have been doing to contents such as beliefs, for centuries, but expectations, and fast neurophenomenological elaborations, followed by a invariants refer to contents of redirection of thought towards the consciousness. process through which contents are constituted. This way, 4. Training: stability. Stabilising and neurophenomenology stresses the deepening one’s capacity for importance of tolerating the attentive bracketing and intuition suspension of conclusions that to also illuminate descriptions. This allow new aspects or insights of a can be achieved by investigating phenomenon to unfold, ideally repeated subjective experiences making this self-observing act as by the researchers themselves. discrete and automatic as possible.

In other words, to help the participant to redirect their One crucial aspect here is that a process attention towards their implicit of description must take place in order to know-how processes. define phenomenological invariants. Such an extraction of invariants supposes a 2. Intimacy: intuition. To gain work on controlled “variations” of the intimacy with the phenomenon of subjective experience, what Husserl called study so the way it is experienced “eidetic variations”, in order to specify “the can appear less encumbered and appropriate dimensions of mental states” more vividly present. This gain in (Husserl, 1901; Varela, 1996). Therefore, intimacy with the phenomenon the phenomenological description becomes the basis of the criteria of mentioned above should aim at a dynamic truth in phenomenological picture that can represent the naturalistic analysis. According to Varela, is embodied nature of experience. this intimacy with our experience

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Another important aspect of action between distant brain areas; such a neurophenomenology is its constrained process would bring unity to a conscious nature. In order to reduce the distance moment while providing it with lack of between subjective and objective stability, thus explaining or resembling its information, Varela proposed aiming at transitional nature (Rudrauf et al., 2003; finding a mutual determination between Varela, 1995). lived experience and biological Multiple studies have taken a mechanisms. By searching for a circulation neurophenomenological approach to between both while constraining each study consciousness. For example, Lutz et source of information with the other, al. (2002) trained participants to verbally neurobiological data could help describe and categorise their subjective illuminating the domain of subjective experience right before being presented experience and vice versa (Varela, 1976, with three dimensional illusions on a 1996). It was this dynamical nature of the screen. Their brain activity was recorded phenomenology that made Varela look using EEG. Then, by conversing with the into different neural dynamical processes experimenter, phenomenological clusters in his search for candidates for neural were defined as an attempt to determine mechanisms of consciousness (see invariant aspects of their subjective below). experience. Later on, EEG data were Importantly, neurophenomenology classified according to these clusters for requires subjects to act both as a subject dynamical analyses. They found patterns of a particular task but also as a subject of endogenous synchronisation in frontal who can report their own experience. electrodes before visual stimulation, Therefore, neurophenomenology which were related to the first-person requires self-awareness to provide descriptions given by the participants, accurate phenomenological descriptions. thus demonstrating the existence of a relationship between behavioural, An important task in neurophysiological, and first-person data. neurophenomenology is to distinguish In a more recent study, Martial et al. (2019) between the “content” of a moment in used a neurophenomenological consciousness or of a mental act, and the approach to study near-death “process” through which such contents experiences (NDEs). They induced NDEs appear (Varela, 1999). In Varela’s view, a by using hypnotic suggestions during moment of consciousness involves the hypnosis. Hypnotic suggestions are verbal emergence of a content in the flow of suggestions that can induce very consciousness that has uncompressible compelling changes in people’s duration. Because the constitution of a perception and cognition (Canales- conscious moment involves high temporal Johnson et al., 2012; Lanfranco et al., integration of contents in a transitory 2014, 2021; Oakley & Halligan, 2013). The manner, Varela thought that researchers recruited participants who consciousness might be the result of had NDE in the past and used hypnotic transient organising synergy of mass

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suggestions to help them re-experience yet transient – temporal integration of their NDEs while measuring their brain multiple contents between distant brain activity using EEG. By measuring EEG and regions. The brain, as a dynamical collecting phenomenological reports, the biophysical system constrained by researchers were able to isolate aspects of multiple non-stable attractors, should the EEG signal that may be related to exhibit such integrative mechanisms. phenomenological invariants in the Based on these and others, Varela hypnotically induced NDEs. proposed that transient phase-locking between brain ensembles could be the

mechanism of large-scale integration in 7.2 Neural synchronisation and the brain which, in turn, could be a perceptual awareness condition of possibility for the emergence of consciousness (Thompson & Varela, Consciousness can be seen as an 2001; Varela, 1995). Synchronisation integrative feature of cognition that between neural assemblies would only be arguably always has a unified cognitive limited by the time needed to establish content. Because consciousness is stable states between them, thus perhaps believed to involve integration among accounting for the transitoriness and different perceptual and cognitive temporal flow of experience (Uhlhaas et functions, it was proposed that a neural al., 2009; Varela, 1999). In addition, mere correlate of consciousness should entail variations in the spatial scale of the large-scale integration across the brain synchronised neural assemblies could (Engel & Singer, 2001). Based on past provide a switch between conscious and studies on non-linear dynamic systems, unconscious information processing chaos, and time-frequency analyses (Dehaene et al., 2006; Thompson & Varela began studying the brain as a Varela, 2001). This modular perspective dynamical system (Letelier, 2001); he agrees with two processing modes found proposed that neural synchronisation in small world networks (of which the brain between different neuronal assemblies seems to be a case): local modularity and could enable the dynamic integration long-range connectivity (Buzsáki, 2007; Yu necessary for such a unified perceptual et al., 2008). Thus, dynamic shifts in experience in a given cognitive instance, coupling between the same anatomical thus binding together sensory, emotional, structures in a network could support both mnemonic, and motor information local (unconscious) and global (conscious) (Thompson & Varela, 2001; Varela, 1995). processes. Varela stressed the idea of consciousness The most plausible mechanism for large- as dense moments of synthesis in the flow scale integration and therefore for the of experiences that could not be emergence of consciousness is phase temporally compressible (Engel & Singer, synchronisation across multiple frequency 2001; Thompson & Varela, 2001). This bands, according to Varela (Thompson & phenomenal integration contained in Varela, 2001; Varela et al., 2001). conscious experience could involve high –

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Neuronal assemblies can exhibit a wide technical explanation, see Cohen (2014, range of oscillations in the theta to gamma chapter 26). frequencies (6-80 Hz) as measured with Multiple studies have supported the role electroencephalography (EEG), with of neural phase synchronisation in precise phase-locking or synchrony conscious processing. More specifically, (Lachaux et al., 1999). Varela’s team that long range synchronisation in the developed a measure of synchrony called beta and gamma frequency bands may phase-locking value (PLV) to detect play a role in the emergence of the unified synchrony in a given frequency band perception of a given stimulus. For between two recording sites or example, Rodriguez et al. (1999) electrodes, irrespective of signal presented subjects with Mooney faces for amplitude: 200 ms on a screen. Mooney faces are binary images that can be easily recognisable as faces when presented 1 upright but are seen as meaningless = 𝑛𝑛 ( ( , )) shapes when presented upside down. 𝑡𝑡 𝑃𝑃𝑃𝑃𝑃𝑃 �� 𝑒𝑒𝑒𝑒𝑒𝑒 𝑗𝑗𝑗𝑗 𝑡𝑡 𝑛𝑛 � After each stimulus presentation, 𝑁𝑁 𝑛𝑛=1 participants had to press a key indicating PLV is defined at a time t as an average whether they saw a face. When value, where ( , ) is the phase participants reported seeing a face, a difference. PLV can take any value transient episode of large-scale phase 𝜃𝜃 𝑡𝑡 𝑛𝑛 between zero and 1, where 1 denotes no locking between electrodes was found phase difference between recording sites. around 250 ms after stimulus presentation See Lachaux et al. (1999) for a more (Figure 1A). This episode of phase detailed description. There are several synchronisation was found mainly in the newer phase-based connectivity gamma frequency band (30-80 Hz). measures today, such as imaginary However, no significant synchronous coherence (Nolte et al., 2004), phase- ensemble was found when participants slope index (Nolte et al., 2008), phase-lag reported not having seen a face. These index (Stam et al., 2007), and weighted findings were interpreted as evidence in phase-lag index (Vinck et al., 2011), all of favour of a relationship between which provide more reliable phase perceptual awareness and large-scale synchronisation indices. For a detailed neural synchronisation.

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Figure 1. Consciousness studies measuring phase synchronisation. (A) Main results of Rodriguez et al. (1999). By presenting Mooney faces in upright and inverted orientations, they manipulated perceptual awareness. When participants reported seeing a face (perception condition), a transient episode of large-scale phase locking between electrodes was found around 250 ms after stimulus presentation. A period of strong desynchronisation marked the transition between face perception and motor response, which was interpreted as a process of active decoupling of neural ensembles marking the transition between cognitive states. (B) Main results of Melloni et al. (2007). By presenting masked words and controlling the luminance of the masks, they manipulated the visibility of the stimuli, thereby influencing participants’ perceptual awareness. Perceived words were associated with a transient long- distance synchronisation of gamma oscillations across widely separated brain regions, suggesting that perceptual awareness is associated with an early transient global increase of phase synchronisation of oscillatory activity in the gamma frequency range. A: Copyright 1999 by Springer Nature. Reprinted and adapted with permission. B, Copyright 2007, Society for Neuroscience.

briefly presented word (33 ms) between In another study, Melloni et al. (2007) masked stimuli. Crucially, they adjusted directly compared the the strength of the masks such that in half electrophysiological signatures of of the trials, participants could not report conscious and unconscious processing by seeing the word. After a 500 ms delay, a asking participants to detect and identify a

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second word was presented. Participants specific for consciousness. When visual had to judge whether the two words were awareness and selective attention are the same or different. Researchers found dissociated, high-range phase that an early and transient burst of long- synchronisation in the gamma band distance synchronisation in the gamma correlates with attention irrespective of frequency in the visible condition but not the stimulus visibility reported by in the invisible one (Figure 1B). While the participants, whereas only mid-range amplitude and patterns of gamma phase synchronisation in the gamma band oscillations were spatially homogenous accounts for stimulus visibility (Wyart & and similar for both conditions, the Tallon-Baudry, 2008). Crucially, however, patterns of phase synchronisation phase synchronisation in gamma has been significantly differed from each other. also found during anaesthesia and NREM Interestingly, this transient period of sleep (Imas et al., 2005; Murphy et al., neural synchronisation was followed by an 2011), epileptic seizures (Pockett & increase in amplitude (P3 component), a Holmes, 2009), and unconscious emotion positive deflection in voltage that has processing (Luo et al., 2009), thus been interpreted as a correlate of indicating that phase synchronisation can information transfer into working memory occur in absence of conscious experience (Jensen & Tesche, 2002; Schack et al., (Canales et al., 2007). 2005). These findings indicate that Instead, recent studies have shown that a conscious processing of visual stimuli may neural metric specifically indexing be associated with an increase in phase distributed information sharing can synchronisation in the gamma frequency capture changes in conscious state and band that is independent of spectral conscious content (Canales-Johnson, power. Studies using binocular rivalry Billig, et al., 2020; Imperatori et al., 2019; found similar phase synchronisation King et al., 2013; Sitt et al., 2014). For effects associated with perceptual instance, information sharing has been dominance (Cosmelli et al., 2004; Fries et shown to capture network reconfiguration al., 1997), i.e. when comparing having a both in healthy (Canales-Johnson, unified and clear perceptual experience Beerendonk, et al., 2020; Imperatori et al., rather than a mixed one when presented 2019) and pathologic (King et al., 2013; with two different images to each eye. Sitt et al., 2014) states of alertness. For many years it was believed that phase Importantly, due to its sensitivity to highly synchronisation in the gamma frequency nonlinear coupling (Imperatori et al., band was necessary for consciousness, 2019), this metric has been useful for especially when it occurred between long distinguishing conscious contents during distances across the brain cortex. bistable perception in the same frequency However, these studies did not dissociate ranges in which phase-synchrony does not visual awareness from selective attention (Canales-Johnson, Billig, et al., 2020). in a rigorous manner, leaving room for the Today, gamma-band phase possibility that said findings may not be synchronisation has been disregarded as

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the specific neurophysiological on a screen. They were asked to press a mechanism of consciousness (Koch et al., key when the visual image of the face was 2016). However, the evidence still the most vivid. In the control condition, supports the claim that phase they were instructed to press as soon as synchronisation may play an important they saw the empty grey oval. Importantly, role in neuronal communication between this occipitoparietal gamma-band phase distant brain regions (Arnulfo et al., 2020; synchronisation pattern predicted Misselhorn et al., 2019), which in turn may subjective ratings of the contour definition be necessary for selective attention of the imagined faces, thus supporting our (Doesburg et al., 2008; Rohenkohl et al., interpretation that gamma-band phase 2018) and visual integration (Uhlhaas et synchronisation may be involved in the al., 2009). Recently, for instance, we found visual binding of imagined faces. that the act of imagining faces is In summary, Varela laid the groundwork to accompanied by long-range gamma- index and perhaps quantify conscious band phase synchronisation (Figure 2), processing. Despite the fact that gamma- arguably due to visual binding of facial band phase synchronisation has been features (Canales-Johnson et al., 2021). rejected as a neural marker specific to Participants had to study different perceptual awareness, Varela’s work was celebrities’ faces prior to the task. In the of prime importance in the field and imagery condition, they had to imagine inspired countless later developments. those faces inside a grey oval presented

Figure 2. Gamma-band phase synchronisation (wPLI) during visual mental imagery, reported by Canales-Johnson et al. (2021). (A) Difference in Frontoparietal phase synchronisation between frontal

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and parietal electrodes comparing imagery and control conditions based on cluster-based permutation tests. (B) Difference in Occipitoparietal phase synchronisation between occipital and parietal electrodes comparing imagery and control conditions based on cluster-based permutation tests. On the right, topographical representations of such differences between wPLI electrode pairs are shown for each condition. Grey circles represent single-participant wPLI for the clusters depicted on time-frequency charts. Red horizontal lines represent the group mean whereas the rectangle represents the standard error of the mean. Content licensed under a Creative Commons Attribution 4.0 International License. activity; but rather, it is situated more

broadly in a self-organised dynamic 8. Conclusion system coupled with its environment. Consciousness and its contents can be One of Varela’s main contributions to studied scientifically through different consciousness research was objective methods. However, its neurophenomenology, a pragmatic conceptual complexity, subjective nature, approach that attempts to build a bridge and philosophical problems make its between the realms of objective and study of great difficulty. Therefore, subjective data. Neurophenomenology different approaches have been taken to requires researchers to deal with empirically address consciousness and qualitative data (e.g. phenomenological multiple theories have been proposed. descriptions) and quantitative data (e.g. Most of these theories come from EEG signal) while giving each of them cognitive science. Even though they have equal importance, care, and rigour. By been developed and updated over the mutually constraining both sources of years, none of them have convincingly data, neurophenomenology allows circumvented, let alone solved the hard researchers to find mutual determinations problem of subjectivity, i.e. the fact that between subjective experience and subjective experiential qualities cannot be neural mechanisms, which in turn helps accessed by objective techniques. As exploring the transitions between argued above, even if objective contents of consciousness. Therefore, techniques were able to perfectly neurophenomenology addresses describe all neurophysiological and consciousness using a non-reductive behavioural aspects of a bat, we would still approach that treats phenomenology and have no idea of what it is like to be a bat. neurophysiology as equally important sources of data. Varela contributed to the study of consciousness philosophically and Varela also proposed a candidate for the empirically. His enactivist proposal is still neural correlates of consciousness: large- relevant today in the study of cognition scale gamma-phase synchronisation. He and consciousness, especially from a argued that phase synchronisation could philosophical perspective (Di Paolo et al., provide a means for different neuronal 2017). The enactivist perspective assemblies to communicate and thereby proposes that the phenomenon of enable dynamic integration for perceptual consciousness is not limited to brain awareness. A number of studies

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suggested that large-scale such claims, phase synchronisation synchronisation in the gamma frequency remains a relevant neural correlate of range might participate in the emergence cognitive integration and possibly of of conscious experience. Even though information integration. subsequent studies have cast doubt on https://doi.org/10.1016/S1364-

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10. Acknowledgements

This work was partially supported by a PhD studentship awarded by ANID/CONICYT and a postdoctoral scholarship awarded by Karolinska Institutet to Renzo Lanfranco.

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