Are altered states of consciousness detrimental, neutral or helpful for the origins of symbolic cognition? A response to Hodgson and Lewis-Williams

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1 Short Communication Are altered states of consciousness detrimental, neutral or helpful for the origins of symbolic cognition? A response to Hodgson and Lewis-Williams Adaptive Behavior 2014, Vol. 22(1) Ó The Author(s) 2014 Reprints and permissions: sagepub.co.uk/journalspermissions.nav DOI: / adb.sagepub.com Tom Froese 1,2, Alexander Woodward 3 and Takashi Ikegami 3 Abstract We respond to the commentaries by Hodgson and Lewis-Williams by clarifying the novelty of our theory. We argue that whenever Turing instabilities of neural activity play a role in generating visual hallucinations, they do more than shape the geometric patterns. Their relatively autonomous self-organization is a source of intrinsic value related to their selfmaintenance as a pattern of activity, and they would also thereby decouple higher-level stages of neural processing from external stimulation, thus facilitating a more abstract mode of cognition. These additional features of our proposal support Hodgson and Lewis-Williams in their respective theories about the very first origins of human artistic activity. We also evaluate the critical literature regarding the possibility of ritualized enaction of altered states of consciousness (ASC) in early prehistory. We conclude that ASC were indeed possible, and suggest that they were likely involved in facilitating the social development of more symbolic forms of life and mind. Keywords Turing patterns, consciousness, enactive cognitive science, symbolic cognition, origins of art, hallucination Recap of our argument In our article we proposed that the study of altered states of consciousness (ASC) provides a useful pivot point from which to investigate the complex relationships between symbolic material culture, first-person experience, and neurobiology (Froese, Woodward, & Ikegami, 2013). In itself this is not a novel proposal; there exists already a long established holistic research agenda (e.g., Díaz, 2013). The hypothesis that geometric patterns commonly experienced during hallucinations are shaped by the neural architecture of the visual cortex has been around at least since the early 20th century, as exemplified by Klüver s famous research on the effects of mescaline. Progress in neuroscience and complex systems theory has further substantiated this hypothesis, while at the same time expanding it to more dynamic accounts of continually changing visual patterns. We can actually see, through such hallucinations, something of the dynamics of a large population of living nerve cells and, in particular, the role of self-organization in allowing complex patterns of activity to emerge. Such activity operates at a basic cellular level, far beneath the level of personal experience. The hallucinatory forms are, in this way, physiological universals of human experience. (Sacks, 2012, p. 131) Nevertheless, as we concluded from our review of this literature, shortcomings still need to be addressed, especially the limited range of geometric patterns that can be produced by current neural network models of the visual system (Froese et al., 2013: ). Similarly, the hypothesis that visual hallucinations were a source of inspiration for some prehistoric art has been discussed for decades, especially following the seminal paper by Lewis-Williams and Dowson (1988). 1 Departamento de Ciencias de la Computación, Instituto de Investigaciones en Matemáticas Aplicadas y en Sistemas, Universidad Nacional Autónoma de México, México City, México 2 Centro de Ciencias de la Complejidad, Universidad Nacional Autónoma de México, México City, México 3 Ikegami Laboratory, Department of General Systems Studies, Graduate School of Arts and Sciences, University of Tokyo, Tokyo, Japan Corresponding author: Tom Froese, Departamento de Ciencias de la Computación, Instituto de Investigaciones en Matemáticas Aplicadas y en Sistemas, Universidad Nacional Autónoma de México, Apdo , Mexico D.F., Mexico. t.froese@gmail.com

2 90 Adaptive Behavior 22(1) As Hodgson (2014) emphasizes, that paper also started a furious backlash by some critics (e.g., Helvenston & Bahn, 2003). Since we did not address this critical literature in our original article, we briefly respond to it further below. However, it seems that even some of the critics, including Hodgson, have started to accept the possibility that ASC may have played a role in early prehistoric society. The main characteristic of shamanism consists of ecstatic states, such as in dreams or trance, and as Eliade points out, these constitute the originating experience (long predating complex religious ideologies), which stretch far back into human pre-history as Hodgson and Helvenston (2006) have previously proposed. [.] Thus, we argue that the year-old shaman was probably a spiritual healer, perhaps using trance, but in a more loosely organized system of beliefs such as animism [.] Clearly, it appears that the shamanism of the past few hundred years developed out of a corpus of preceding animistic beliefs and primordial ecstatic experiences dating back many thousands of years [.]. (Helvenston & Hodgson, 2010, pp ; footnote 6) Similarly, Lewis-Williams and Dowson (1988) have always accepted that recent shamanistic cultures emerged out of antecedents, which probably had at least some features in common with what we understand by shamanism (p. 213), where the overriding feature of shamanism and the one which this paper is principally concerned [is] altered states of consciousness (p. 204). Despite this explicit identification of the term shamanism with ritualized usage of ASC (see also the commentary by Lewis-Williams, 2014), there ensued a lot of confusion about this term, which is why in the following we more generally refer to the use of ASC. Future archaeological work can dedicate itself to elucidating more details of these first belief systems, and whether they are more appropriately referred to as shamanistic, animistic or something different altogether. In other words, although some vocal skeptics persist (e.g., Bahn, 2010), there finally seems to be an opportunity to move beyond the dispute about the potential existence of ASC in early prehistoric societies to a debate about their potential uses. In this regard, the contribution made by our article was to assess the relationship between art, ASC and neurobiology from the theoretical perspective of enactive cognitive science with its emphasis on biological self-organization and sense-making (Thompson, 2007). We argued that this new perspective helps us to address some of the puzzles of current research. For example, if our visual experience is not a mental representation directly instantiated by a neural activity pattern inside of the visual system, but is rather an elaborated outcome of an interpretative process that is partially shaped by that system, then the limited number of activity patterns produced by current neural network models is no longer such a big problem. Visual experience, even in the case of hallucinations, is constrained by but not identical to neural activity (Noe, 2009). These models fail to address the biological embodiment of the agent s own meaningful experience (a common problem for most, if not all, computational models, e.g., Froese & Ziemke, 2009). Furthermore, one type of neural mechanism that is often used to explain typical geometric patterns of hallucinations, namely the self-organizing neural dynamics of Turing instabilities, is compatible with the enactive theory that self-generating dynamics no matter whether they are embodied in chemical, metabolic, or neural systems are relatively autonomous from their environment and follow their own normativity (Varela, 1997). We suggested that the intrinsic value of the selforganizing neural activity patterns that emerge during ASC, and which tend to be inhibited in normal consciousness (Butler et al., 2012), might provide a partial explanation for why the geometric visual patterns they help to generate were perceived as salient and significant by the prehistoric artists. Response to commentaries by Hodgson and Lewis-Williams The two published commentaries on our article suitably represent the two sides of the debate about the use of ASC in prehistory. Lewis-Williams has long been the leading proponent for the hypothesis that various experiences of ASC were the inspiration for much prehistoric art, including in the European Paleolithic (Clottes & Lewis-Williams, 1998; Lewis-Williams, 2002), the European Neolithic (Lewis-Williams & Pearce, 2005), and for the San rock art of South Africa (Lewis- Williams & Challis, 2011). Conversely, Hodgson (2006a) has been an active critic of this hypothesis, while also developing an alternative neurobiological account of geometric art (Hodgson, 2006b) and iconic art (Hodgson & Helvenston, 2006) that specifically does not depend on hallucinations or abnormal neural activity. Lewis-Williams (2014) reprimands us for having neglected the essential role of social context for explaining the selective biases in prehistoric art. He rightly emphasizes that socially enacted beliefs and values influence both what people experience in ASC and how they respond. Although we focused only on neural mechanisms, like most neurophenomenological research despite its holistic aims (Beaton, 2013), we recognize that life and mind are social through and through (Froese & Di Paolo, 2011). Indeed, more work needs to be done to determine just how social context intertwines with brain activity (Di Paolo & De Jaegher, 2012). We therefore have no issue with Lewis-Williams proposal that the development of complex societies was initially triggered by exploitation and manipulation of the nervous system

3 Froese et al. 91 (Froese, 2013), while social contestation brought about by the selective transmission of ritual knowledge eventually ushered in more stratified societies. Our contribution tries to explain what could have happened during those very initial stages. For if we accept, as Lewis-Williams does, that meaning and value are only formed consensually, then we are faced with a new problem of origins. For example, how would a group of early humans react to an accidentally discovered method of inducing geometric hallucinations? According to Lewis-Williams, this is clearly a social and historical, rather than neurological, issue: if the group has no social value for these experiences, such as the modern West, then such experiences are marginalized and ignored. Yet Lewis-Williams seems to also assume that in prehistoric societies it was more likely than not that these experiences were going to be valued. Why should this have been so? The issue is that at some point there must have been a time when no social precedent of attaching significance to ASC yet existed. Our article provides a response to this open question by exploring the possibility that the significance of certain experiences also depends on neurological activity, namely that the neural dynamics underlying some visual patterns imbues those patterns with their own salience. In this regard, our proposal can be compared with Hodgson s theories, except that he proposes that the normal functioning of the visual cortex is sufficient to account for this enhanced feeling. As Hodgson (2014) points out, it may be more parsimonious to argue that the nervous system resonates particularly strongly when presented with visual patterns for which it has been specifically optimized by evolution. Early stages of visual processing are specifically tuned to parallel lines and later visual stages are sensitive to the presence of animals, so perhaps this normal neurovisual resonance is all that is neurologically needed to explain prehistoric people s bias for depicting abstract geometric patterns and animals in their cave paintings (Hodgson, 2006a). However, Hodgson s idea that an accidental perceptual experience of symmetric patterns in the world will sufficiently stimulate our visual system such that this neurovisual resonance, by itself, will motivate the first production of geometric art is not compelling. From a sociological perspective, it completely neglects the explanatory possibilities of linking these extraordinary human artistic practices with extraordinary states of mind. For example, the often obscure and rather inaccessible locations of prehistoric paintings in deep caves suggest that they were produced in a ritual context of some kind (Whitley, 2009). As Lewis-Williams has commented, such social factors likely played a role in much earlier artistic practices, too. More worryingly, from a biological perspective the neural resonance theory is too general. Abstract feature detectors of the early stages of visual processing are not unique to human Figure 1. Painting done by female chimpanzee Kenya of the Great Apes Trust in Florida. Zeller (personal communication) selected this particular painting as one of the most geometric from her collection of 340 pictures made by chimpanzees, gorillas, and orangutans. Reproduced with kind permission from Patti Ragan and the Center for Great Apes, Wauchula, Florida. brains, as famously exemplified by the cat s visual cortex (Hubel & Wiesel, 1959). Hodgson (2006b) must therefore appeal to a number of other extrinsic factors to explain why earlier hominins and closely related primates, such as chimpanzees, do not produce geometric art even when given the opportunity to do so. To be fair, on the basis of extensive research in the comparative psychology of non-representational paintings, Zeller (2007) concluded that both children and captive apes intentionally choose the colors and forms, including diagonal lines. Nevertheless, although symmetry is hinted at in some works, it seems that none of the subjects had a special predilection for making straight, repeated lines (e.g., Figure 1). Perhaps the lack of patterns that represent the idealized forms of the early visual system has to do with the fact that the neural activity is mediated by motoric embodiment and environmental situatedness. Accordingly, if such environmentally mediated neural resonance is not enough to motivate clear geometric patterns, perhaps immediate neural resonance within the brain is more effective. This brings us back to the potential role of ASC in the origins of geometric art. Hallucinatory visual experiences are not constrained by limited motor capacities and environmental conditions, thereby more directly revealing the geometry of the visual system. Neurovisual resonance is enhanced, too, in deep trance and other unusual conditions, because the visual pathway is rendered hyperexcitable by a lack of normal sensory input (Sacks, 2012, p. 41). It is especially under these abnormally disinhibited conditions that neural activity in the visual system becomes selforganized into Turing patterns (Butler et al., 2012). These Turing patterns are not driven by changes in gene expression, thus avoiding the reservations expressed by

4 92 Adaptive Behavior 22(1) Hodgson (2014). Far from being the explanatory burden that Hodgson assumes them to be, ASC could be taken as a manner of strengthening his own neurovisual resonance theory. One challenge faced by the enactive theory of a biologically embodied mind is to explain how humans are able to transcend the concrete concerns that determine the Umwelt of other animals (Froese, 2012). It is conceivable that social practices involving the induction of ASC provided the non-ordinary context through which early prehistoric human minds were repeatedly taken outside of the restrictions of their basic biological survival routines (Froese, 2013). It is in this respect that Hodgson has misunderstood our proposal. We do not claim that the experience of geometric patterns during an ASC requires abstract modes of cognition. On the contrary, we argued that self-sustaining neural dynamics, which constitute some geometric hallucinations, temporarily decouple higher-level neural activity from external stimuli, and proposed that this detachment facilitates the development of abstract modes of cognition. In other words, social practices involving ASC can produce inspiring visual patterns and imagery, and they can also promote states of mind that can appreciate these experiences for their symbolic status. Although we have emphasized the potential effects of changes in neural dynamics during ASC, our account does not deny the role of the personal level (phenomenology) nor of the social level (ritual). We agree with Hodgson that an enactive account of art should consider how brain, body and world interact as one system. Interestingly, Hodgson and Lewis-Williams are in agreement that the variability of the very first pieces of symbolic art, the abstractly engraved ochre pieces from Blombos Cave in South Africa (Henshilwood, d Errico, & Watts, 2009), is much more limited than we may have implied, but they differ regarding the reasons for this selectivity. Whereas Hodgson favors a purely neurological bias, Lewis-Williams appeals to a purely social bias. We suggest that there may be a more productive middle way. Thus, we agree with Hodgson, contra Lewis- Williams, that the value of experiencing such geometric patterns is at least partially based on neurobiological factors, and we agree with Lewis-Williams, contra Hodgson, that social context and ASC played an essential role in the first creation and appreciation of these patterns. Criticisms regarding ASC in early prehistory But how plausible is the appeal to ASC when explaining, for example, European cave art? Hodgson cites a number of authors who have criticized the research by Lewis-Williams and colleagues in this regard. Since our proposal also depends on the plausibility of the ritualized enaction of ASC, and because we did not engage with this literature before, we briefly outline our response here. The skeptical arguments have been spearheaded by Helvenston and Bahn (2003), who tried to demonstrate that ASC could not have played a role for prehistoric art in Europe. Countering the universality of Klüver s so-called form constants, Helvenston and Bahn claim that this pattern of drug-induced vivid imagery experiences is only produced by three substances: mescaline, psilocybin and LSD (2004, p. 94). This is quite an extraordinary assertion, given that geometric patterns are experienced during all kinds of ASC, including naturally occurring alterations, drug-induced alterations and because of brain pathologies, as Sacks (2012) extensive review of hallucinations makes clear. Nevertheless, Helvenston and Bahn then try to use this assertion to refute the theory by Lewis-Williams and colleagues by stating: Neither mescaline nor psilocybin has ever been found in Europe (2004, p. 94). This claim is also plainly false. The mushroom genus Psilocybe has a worldwide distribution, and over a dozen hallucinogenic species have been identified in Europe (Guzma n, 2005). Although Helvenston and Bahn (2005) later partially realize their mistake, by admitting to the existence of one European Psilocybe species, they attempt to rescue their refutation by proposing that it may have been imported to the Old World after the conquest of the Americas, [.], reaching Spain and Portugal around 1496 at the earliest (p. 31). They thereby explicitly ignore the consensus among expert mycologists, who consider a variety of psilocybin-containing fungi as endemic to Europe. More importantly, some species already existed in Europe long before the arrival of the first hominins, having emerged during the Miocene between 10 and 20 million years ago (Kosentka et al., 2013, p. 7). To be sure, there is no unequivocal written record of their consumption in pre-modern Europe, but the recent discovery of a rock painting in Spain depicting several mushrooms that faithfully represent a hallucinogenic species of Psilocybe in its ecological context (Akers, Ruiz, Piper, & Ruck, 2011), suggests a much older tradition of prehistoric ritual usage dating back to at least around 4000 BCE. The critical literature is equally questionable when it comes to ritually induced ASC without ingestion of substances. For example, Helvenston and Bahn (2004) reject the possibility that deep caves, such as those in which prehistoric art is often found, could have served as a suitable hallucinogenic milieu (p. 98). They argue that visual hallucinations are reported extremely rarely by modern spelunkers, and that these reports are linked to extreme exhaustion, not to the caves per se. This direct comparison between modern and prehistoric usage of deep caves is implausible. It also ignores a long tradition of experimental psychology studying the experiential effects of sensory deprivation. As revealed

5 Froese et al. 93 by a recent review (Sacks, 2012, pp ), sensory deprivation regularly produces all kinds of visual hallucinations, including geometric patterns that are followed by more complex visual imagery. Hodgson (2006a) acknowledges that controlled experiments by Zubek and colleagues (1961) have established that sensory deprivation can lead to hallucinations of geometric shapes after a seven day isolation period, but for him this is an extremely unlikely event for cave artists (p. 29). It is unclear why a 7-day period of isolation should be unreasonable, especially if we assume that these people were actively searching for visions. In any case, more recent experiments in sensory deprivation, in which participants were blindfolded but otherwise allowed to interact normally with their environment, including resting and sleeping at night, show that visual hallucinations occur reliably and quickly: Ten (77%) of the 13 blindfolded subjects reported visual hallucinations that varied in onset, duration, and content. Generally, the visual hallucinations began between the first day and second day of blindfolding [.]. In six of the 10 subjects who reported seeing hallucinations, the hallucinations were either simple (flashing lights or phosphenes) or complex (faces, hands, landscapes, ornate objects). In two of these six subjects, simple visual hallucinations evolved to more complex sensations as the blindfold period progressed. (Merabet et al., 2004, p. 110) These documented cases of progression from simple to complex hallucinations during days of sensory deprivation support the generality of Lewis-Williams and Dowson s neuropsychological model, according to which deepening ASC often pass through three stages: from geometric patterns (Stage 1), to iconic forms (Stage 2), to complex scenes and self-transformations (Stage 3). Although we do not fully agree with the details of this model, it clearly is not as implausible as critics have claimed (e.g., Helvenston & Bahn, 2003). Figure 2. A yarn painting made by a Huichol shaman. Two sacred plants with psychoactive properties are depicted, left the arbol del viento (Solandra spp.) and in the center the peyote cactus (Lophophora williamsii). The shaman on the right is shown with a deer tail, the deer being culturally identified with peyote. Notice the inclusion of several phosphene blobs in the painting. Photo courtesy of Iliana Mendoza Villafuerte. during ASC (Schaefer, 1996). Clearly, the real open question is whether such indigenous cultures are the last remnants of a much older tradition of using ASC, perhaps one dating back to the origins of the modern human mind. We have argued that there are good reasons to take this possibility seriously. Acknowledgements We are grateful to Anne Zeller for finding the most geometric examples of her collection of paintings by apes and making them available to us. Concluding remarks In his commentary Hodgson (2014) misleadingly concludes that Whether the form constants experienced during ASC, either induced through psychoactive drugs or trance states, were copied for use in art during later periods remains an open question. On the contrary, it has long been known that the Tukano of Colombia, for example, derive their decorative patterns from the visual sensations seen during drug-induced ASC (Reichel-Dolmatoff, 1978). And it has been shown that these specific motifs are diagnostic of art inspired by ASC since they do not tend to be found in other kinds of geometric art (Dronfield, 1996). We leave the reader with a contemporary piece of art from the Huichol of Mexico (Figure 2), another artistic tradition that is influenced by the geometric motifs seen Funding This research received no specific grant from any funding agency in the public, commercial, or not-for-profit sectors. References Akers, B. P., Ruiz, J. F., Piper, A., & Ruck, C. A. P. (2011). A prehistoric mural in Spain depicting neurotropic Psilocybe mushrooms. Economic Botany, 20(10), 1 8. Bahn, P. G. (2010). Prehistoric rock art: Polemics and progress. New York, NY: Cambridge University Press. Beaton, M. (2013). Phenomenology and embodied action. Constructivist Foundations, 8(3), Butler, T. C., Benayoun, M., Wallace, E., von Drongelen, W., Goldenfeld, N., & Cowan, J. D. (2012). Evolutionary constraints on visual cortex architecture from the dynamics of hallucinations. Proceedings of the National Academy of Sciences of the USA, 109(2),

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7 Froese et al. 95 About the Authors Tom Froese completed his DPhil in cognitive science from the University of Sussex in He subsequently held postdoctoral fellowships at the Sackler Centre for Consciousness Science and at the University of Tokyo. Since 2012 he is a postdoctoral researcher at the self-organizing systems laboratory of the National Autonomous University of Mexico (UNAM). He investigates the relationship between life, mind and sociality using a combination of methods, including evolutionary robotics, complex systems theory, and phenomenology. Alexander Woodward received his PhD in computer science from the University of Auckland, New Zealand in He is currently a postdoctoral fellow at the Ikegami laboratory of the University of Tokyo (since 2010). His research into computer vision has led him to ask questions about the nature of visual perception in living systems. Current research focuses on computer vision, neural networks and reservoir computing, subjective time in the brain, scientific computing on the GPU, and a maximalist approach to artificial life. Takashi Ikegami received his doctorate in physics from the University of Tokyo. His research interest is to build and study artificial life systems ranging from chemical droplets and evolutionary robotics to Web dynamics. Some of these results have been published in Life emerges in motion (Seido, 2007) and also The Sandwich theory of life (Kodansha, 2012). Takashi Ikegami gave the keynote address at the 20th anniversary of the Artificial Life conference in Winchester, UK. He is also a member of the editorial boards of Artificial Life, Adaptive Behavior and BioSystems.