Short Communication

Adaptive Behavior2014, Vol. 22(1) 89–95� The Author(s) 2014Reprints and permissions:sagepub.co.uk/journalsPermissions.navDOI: 10.1177/1059712313513275adb.sagepub.com

Are altered states of consciousnessdetrimental, neutral or helpful for theorigins of symbolic cognition? A responseto Hodgson and Lewis-Williams

Tom Froese1,2, Alexander Woodward3 and Takashi Ikegami3

AbstractWe respond to the commentaries by Hodgson and Lewis-Williams by clarifying the novelty of our theory. We argue thatwhenever Turing instabilities of neural activity play a role in generating visual hallucinations, they do more than shape thegeometric patterns. Their relatively autonomous self-organization is a source of intrinsic value related to their self-maintenance as a pattern of activity, and they would also thereby decouple ‘‘higher-level’’ stages of neural processing fromexternal stimulation, thus facilitating a more abstract mode of cognition. These additional features of our proposal sup-port Hodgson and Lewis-Williams in their respective theories about the very first origins of human artistic activity. Wealso 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 infacilitating the social development of more symbolic forms of life and mind.

KeywordsTuring patterns, consciousness, enactive cognitive science, symbolic cognition, origins of art, hallucination

Recap of our argument

In our article we proposed that the study of alteredstates of consciousness (ASC) provides a useful pivotpoint from which to investigate the complex relation-ships between symbolic material culture, first-personexperience, and neurobiology (Froese, Woodward, &Ikegami, 2013). In itself this is not a novel proposal;there exists already a long established holistic researchagenda (e.g., Dıaz, 2013). The hypothesis that geo-metric patterns commonly experienced during halluci-nations are shaped by the neural architecture of thevisual cortex has been around at least since the early20th century, as exemplified by Kluver’s famousresearch on the effects of mescaline. Progress in neu-roscience and complex systems theory has further sub-stantiated this hypothesis, while at the same timeexpanding it to more dynamic accounts of continuallychanging visual patterns.

We can actually see, through such hallucinations, some-thing of the dynamics of a large population of living nervecells and, in particular, the role of self-organization inallowing complex patterns of activity to emerge. Suchactivity operates at a basic cellular level, far beneath thelevel 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 ofthis literature, shortcomings still need to be addressed,especially the limited range of geometric patterns thatcan be produced by current neural network models ofthe visual system (Froese et al., 2013: 205–206).

Similarly, the hypothesis that visual hallucinationswere a source of inspiration for some prehistoric arthas been discussed for decades, especially following theseminal paper by Lewis-Williams and Dowson (1988).

1Departamento de Ciencias de la Computacion, Instituto de

Investigaciones en Matematicas Aplicadas y en Sistemas, Universidad

Nacional Autonoma de Mexico, Mexico City, Mexico2Centro de Ciencias de la Complejidad, Universidad Nacional Autonoma

de Mexico, Mexico City, Mexico3Ikegami 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 Computacion, Instituto de

Investigaciones en Matematicas Aplicadas y en Sistemas, Universidad

Nacional Autonoma de Mexico, Apdo. 20-726, 01000 Mexico D.F.,

Mexico.

Email: t.froese@gmail.com

As Hodgson (2014) emphasizes, that paper also starteda furious backlash by some critics (e.g., Helvenston &Bahn, 2003). Since we did not address this critical liter-ature in our original article, we briefly respond to it fur-ther below. However, it seems that even some of thecritics, including Hodgson, have started to accept thepossibility that ASC may have played a role in earlyprehistoric society.

The main characteristic of shamanism consists of ecstaticstates, such as in dreams or trance, and as Eliade pointsout, these constitute the originating experience (long pre-dating complex religious ideologies), which stretch far

back into human pre-History as Hodgson and Helvenston(2006) have previously proposed. [.] Thus, we argue thatthe 12000-year-old ‘shaman’ was probably a ‘spiritual hea-ler’, perhaps using trance, but in a more loosely organizedsystem of beliefs such as animism [.] Clearly, it appearsthat the shamanism of the past few hundred years devel-oped out of a corpus of preceding animistic beliefs and pri-mordial ecstatic experiences dating back many thousandsof years [.]. (Helvenston & Hodgson, 2010, pp. 75–76;footnote 6)

Similarly, Lewis-Williams and Dowson (1988) havealways accepted that recent shamanistic culturesemerged out of antecedents, which ‘‘probably had atleast some features in common with what we under-stand by shamanism’’ (p. 213), where the ‘‘overridingfeature of shamanism and the one which this paper isprincipally concerned [is] altered states of conscious-ness’’ (p. 204). Despite this explicit identification of theterm ‘‘shamanism’’ with ritualized usage of ASC (seealso the commentary by Lewis-Williams, 2014), thereensued a lot of confusion about this term, which is whyin the following we more generally refer to the use ofASC. Future archaeological work can dedicate itself toelucidating more details of these first belief systems,and whether they are more appropriately referred to asshamanistic, animistic or something different alto-gether. In other words, although some vocal skepticspersist (e.g., Bahn, 2010), there finally seems to be anopportunity to move beyond the dispute about thepotential existence of ASC in early prehistoric societiesto a debate about their potential uses.

In this regard, the contribution made by our articlewas to assess the relationship between art, ASC andneurobiology from the theoretical perspective of enac-tive cognitive science with its emphasis on biologicalself-organization and sense-making (Thompson, 2007).We argued that this new perspective helps us to addresssome of the puzzles of current research.

For example, if our visual experience is not a mentalrepresentation directly instantiated by a neural activitypattern inside of the visual system, but is rather an ela-borated outcome of an interpretative process that is par-tially shaped by that system, then the limited number ofactivity patterns produced by current neural network

models is no longer such a big problem. Visual experi-ence, even in the case of hallucinations, is constrainedby—but not identical to—neural activity (Noe, 2009).These models fail to address the biological embodimentof the agent’s own meaningful experience (a commonproblem for most, if not all, computational models,e.g., Froese & Ziemke, 2009).

Furthermore, one type of neural mechanism that isoften used to explain typical geometric patterns of hal-lucinations, namely the self-organizing neural dynamicsof Turing instabilities, is compatible with the enactivetheory that self-generating dynamics—no matterwhether they are embodied in chemical, metabolic, orneural systems—are relatively autonomous from theirenvironment and follow their own normativity (Varela,1997). We suggested that the intrinsic value of the self-organizing neural activity patterns that emerge duringASC, and which tend to be inhibited in normal con-sciousness (Butler et al., 2012), might provide a partialexplanation for why the geometric visual patterns theyhelp to generate were perceived as salient and signifi-cant by the prehistoric artists.

Response to commentaries by Hodgsonand Lewis-Williams

The two published commentaries on our article suitablyrepresent the two sides of the debate about the use ofASC in prehistory. Lewis-Williams has long been theleading proponent for the hypothesis that variousexperiences of ASC were the inspiration for much pre-historic 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 alsodeveloping an alternative neurobiological account ofgeometric art (Hodgson, 2006b) and iconic art(Hodgson & Helvenston, 2006) that specifically does notdepend on hallucinations or abnormal neural activity.

Lewis-Williams (2014) reprimands us for havingneglected the essential role of social context for explain-ing the selective biases in prehistoric art. He rightlyemphasizes that socially enacted beliefs and values influ-ence both what people experience in ASC and how theyrespond. Although we focused only on neural mechan-isms, like most neurophenomenological research despiteits holistic aims (Beaton, 2013), we recognize that lifeand mind are social through and through (Froese & DiPaolo, 2011). Indeed, more work needs to be done todetermine just how social context intertwines with brainactivity (Di Paolo & De Jaegher, 2012). We thereforehave no issue with Lewis-Williams’ proposal that thedevelopment of complex societies was initially triggeredby exploitation and manipulation of the nervous system

90 Adaptive Behavior 22(1)

(Froese, 2013), while social contestation brought aboutby the selective transmission of ritual knowledge eventu-ally ushered in more stratified societies.

Our contribution tries to explain what could havehappened during those very initial stages. For if weaccept, as Lewis-Williams does, that meaning and valueare only formed consensually, then we are faced with anew problem of origins. For example, how would agroup of early humans react to an accidentally discov-ered method of inducing geometric hallucinations?According to Lewis-Williams, this is clearly a socialand historical, rather than neurological, issue: if thegroup has no social value for these experiences, such asthe modern West, then such experiences are margina-lized and ignored. Yet Lewis-Williams seems to alsoassume that in prehistoric societies it was more likelythan not that these experiences were going to be valued.Why should this have been so? The issue is that at somepoint there must have been a time when no social pre-cedent of attaching significance to ASC yet existed.

Our article provides a response to this open questionby exploring the possibility that the significance of cer-tain experiences also depends on neurological activity,namely that the neural dynamics underlying somevisual patterns imbues those patterns with their ownsalience. In this regard, our proposal can be comparedwith Hodgson’s theories, except that he proposes thatthe normal functioning of the visual cortex is sufficientto account for this enhanced feeling. As Hodgson(2014) points out, it may be more parsimonious toargue that the nervous system resonates particularlystrongly when presented with visual patterns for whichit has been specifically optimized by evolution. Earlystages of visual processing are specifically tuned to par-allel lines and later visual stages are sensitive to thepresence of animals, so perhaps this normal neurovi-sual resonance is all that is neurologically needed toexplain prehistoric people’s bias for depicting abstractgeometric patterns and animals in their cave paintings(Hodgson, 2006a).

However, Hodgson’s idea that an accidental percep-tual experience of symmetric patterns in the world willsufficiently stimulate our visual system such that thisneurovisual resonance, by itself, will motivate the firstproduction of geometric art is not compelling. From asociological perspective, it completely neglects theexplanatory possibilities of linking these extraordinaryhuman artistic practices with extraordinary states ofmind. For example, the often obscure and rather inac-cessible locations of prehistoric paintings in deep cavessuggest that they were produced in a ritual context ofsome kind (Whitley, 2009). As Lewis-Williams has com-mented, such social factors likely played a role in muchearlier artistic practices, too. More worryingly, from abiological perspective the neural resonance theory istoo general. Abstract feature detectors of the earlystages of visual processing are not unique to human

brains, as famously exemplified by the cat’s visual cor-tex (Hubel & Wiesel, 1959). Hodgson (2006b) musttherefore appeal to a number of other extrinsic factorsto explain why earlier hominins and closely related pri-mates, such as chimpanzees, do not produce geometricart even when given the opportunity to do so.

To be fair, on the basis of extensive research in thecomparative psychology of non-representational paint-ings, Zeller (2007) concluded that both children andcaptive apes intentionally choose the colors and forms,including diagonal lines. Nevertheless, although sym-metry is hinted at in some works, it seems that none ofthe subjects had a special predilection for makingstraight, repeated lines (e.g., Figure 1). Perhaps the lackof patterns that represent the idealized forms of theearly visual system has to do with the fact that theneural activity is mediated by motoric embodiment andenvironmental situatedness.

Accordingly, if such environmentally mediated neuralresonance is not enough to motivate clear geometricpatterns, perhaps immediate neural resonance withinthe brain is more effective. This brings us back to thepotential role of ASC in the origins of geometric art.Hallucinatory visual experiences are not constrained bylimited motor capacities and environmental conditions,thereby more directly revealing the geometry of thevisual system. Neurovisual resonance is enhanced, too,in deep trance and other unusual conditions, becausethe visual pathway is ‘‘rendered hyperexcitable by a lackof normal sensory input’’ (Sacks, 2012, p. 41). It is espe-cially under these abnormally disinhibited conditionsthat neural activity in the visual system becomes self-organized into Turing patterns (Butler et al., 2012).These Turing patterns are not driven by changes in geneexpression, thus avoiding the reservations expressed by

Figure 1. Painting done by female chimpanzee Kenya of theGreat Apes Trust in Florida. Zeller (personal communication)selected this particular painting as one of the most geometricfrom her collection of 340 pictures made by chimpanzees,gorillas, and orangutans. Reproduced with kind permission fromPatti Ragan and the Center for Great Apes, Wauchula, Florida.

Froese et al. 91

Hodgson (2014). Far from being the explanatory bur-den that Hodgson assumes them to be, ASC could betaken as a manner of strengthening his own neurovisualresonance theory.

One challenge faced by the enactive theory of a bio-logically embodied mind is to explain how humans areable to transcend the concrete concerns that determinethe Umwelt of other animals (Froese, 2012). It is con-ceivable that social practices involving the induction ofASC provided the non-ordinary context through whichearly prehistoric human minds were repeatedly takenoutside of the restrictions of their basic biological sur-vival routines (Froese, 2013). It is in this respect thatHodgson has misunderstood our proposal. We do notclaim that the experience of geometric patterns duringan ASC requires abstract modes of cognition. On thecontrary, we argued that self-sustaining neuraldynamics, which constitute some geometric hallucina-tions, temporarily decouple higher-level neural activityfrom external stimuli, and proposed that this detach-ment facilitates the development of abstract modes ofcognition. In other words, social practices involvingASC can produce inspiring visual patterns and imagery,and they can also promote states of mind that canappreciate these experiences for their symbolic status.Although we have emphasized the potential effects ofchanges in neural dynamics during ASC, our accountdoes not deny the role of the personal level (phenomen-ology) nor of the social level (ritual). We agree withHodgson that an enactive account of art should con-sider how brain, body and world interact as one system.

Interestingly, Hodgson and Lewis-Williams are inagreement that the variability of the very first pieces ofsymbolic art, the abstractly engraved ochre pieces fromBlombos Cave in South Africa (Henshilwood, d’Errico,& Watts, 2009), is much more limited than we may haveimplied, but they differ regarding the reasons for thisselectivity. Whereas Hodgson favors a purely neurologi-cal bias, Lewis-Williams appeals to a purely social bias.We suggest that there may be a more productive middleway. Thus, we agree with Hodgson, contra Lewis-Williams, that the value of experiencing such geometricpatterns is at least partially based on neurobiological fac-tors, and we agree with Lewis-Williams, contra Hodgson,that social context and ASC played an essential role inthe first creation and appreciation of these patterns.

Criticisms regarding ASC in earlyprehistory

But how plausible is the appeal to ASC when explain-ing, for example, European cave art? Hodgson cites anumber of authors who have criticized the research byLewis-Williams and colleagues in this regard. Since ourproposal also depends on the plausibility of the ritua-lized enaction of ASC, and because we did not engage

with this literature before, we briefly outline ourresponse here. The skeptical arguments have beenspearheaded by Helvenston and Bahn (2003), who triedto demonstrate that ASC could not have played a rolefor prehistoric art in Europe.

Countering the universality of Kluver’s so-calledform constants, Helvenston and Bahn claim that this‘‘pattern of drug-induced vivid imagery experiences isonly produced by three substances: mescaline, psilocy-bin and LSD’’ (2004, p. 94). This is quite an extraordi-nary assertion, given that geometric patterns areexperienced during all kinds of ASC, including natu-rally occurring alterations, drug-induced alterationsand because of brain pathologies, as Sacks’ (2012)extensive review of hallucinations makes clear.

Nevertheless, Helvenston and Bahn then try to usethis assertion to refute the theory by Lewis-Williamsand colleagues by stating: ‘‘Neither mescaline nor psilo-cybin has ever been found in Europe’’ (2004, p. 94).This claim is also plainly false. The mushroom genusPsilocybe has a worldwide distribution, and over adozen hallucinogenic species have been identified inEurope (Guzman, 2005). Although Helvenston andBahn (2005) later partially realize their mistake, byadmitting to the existence of one European Psilocybespecies, they attempt to rescue their refutation by pro-posing that ‘‘it may have been imported to the OldWorld after the conquest of the Americas, [.], reach-ing Spain and Portugal around 1496 at the earliest’’ (p.31). They thereby explicitly ignore the consensusamong expert mycologists, who consider a variety ofpsilocybin-containing fungi as endemic to Europe.More importantly, some species already existed inEurope long before the arrival of the first hominins,having emerged ‘‘during the Miocene between 10 and20 million years ago’’ (Kosentka et al., 2013, p. 7).

To be sure, there is no unequivocal written record oftheir consumption in pre-modern Europe, but therecent discovery of a rock painting in Spain depictingseveral mushrooms that faithfully represent a halluci-nogenic species of Psilocybe in its ecological context(Akers, Ruiz, Piper, & Ruck, 2011), suggests a mucholder tradition of prehistoric ritual usage dating backto at least around 4000 BCE.

The critical literature is equally questionable when itcomes to ritually induced ASC without ingestion ofsubstances. For example, Helvenston and Bahn (2004)reject the possibility that deep caves, such as those inwhich prehistoric art is often found, could have servedas a suitable ‘‘hallucinogenic milieu’’ (p. 98). Theyargue that visual hallucinations are reported extremelyrarely by modern spelunkers, and that these reports arelinked to extreme exhaustion, not to the caves per se.This direct comparison between modern and prehisto-ric usage of deep caves is implausible. It also ignores along tradition of experimental psychology studying theexperiential effects of sensory deprivation. As revealed

92 Adaptive Behavior 22(1)

by a recent review (Sacks, 2012, pp. 34–44), sensorydeprivation regularly produces all kinds of visual hallu-cinations, including geometric patterns that are fol-lowed by more complex visual imagery.

Hodgson (2006a) acknowledges that controlledexperiments by Zubek and colleagues (1961) haveestablished that sensory deprivation can lead to halluci-nations of geometric shapes after a seven day isolationperiod, but for him this is ‘‘an extremely unlikely eventfor cave artists’’ (p. 29). It is unclear why a 7-day periodof isolation should be unreasonable, especially if weassume that these people were actively searching forvisions. In any case, more recent experiments in sensorydeprivation, in which participants were blindfolded butotherwise allowed to interact normally with their envi-ronment, including resting and sleeping at night, showthat visual hallucinations occur reliably and quickly:

Ten (77%) of the 13 blindfolded subjects reported visualhallucinations that varied in onset, duration, and content.Generally, the visual hallucinations began between the firstday and second day of blindfolding [.]. In six of the 10subjects who reported seeing hallucinations, the hallucina-tions were either simple (flashing lights or phosphenes) orcomplex (faces, hands, landscapes, ornate objects). In twoof these six subjects, simple visual hallucinations evolvedto more complex sensations as the blindfold period pro-gressed. (Merabet et al., 2004, p. 110)

These documented cases of progression from simple tocomplex hallucinations during days of sensory depriva-tion support the generality of Lewis-Williams andDowson’s ‘‘neuropsychological model,’’ according towhich 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 thedetails of this model, it clearly is not as implausible ascritics have claimed (e.g., Helvenston & Bahn, 2003).

Concluding remarks

In his commentary Hodgson (2014) misleadinglyconcludes that ‘‘Whether the form constants experi-enced during ASC, either induced through psychoac-tive drugs or trance states, were copied for use in artduring later periods remains an open question.’’ On thecontrary, it has long been known that the Tukano ofColombia, for example, derive their decorative patternsfrom the visual sensations seen during drug-inducedASC (Reichel-Dolmatoff, 1978). And it has beenshown that these specific motifs are diagnostic of artinspired by ASC since they do not tend to be found inother kinds of geometric art (Dronfield, 1996). Weleave the reader with a contemporary piece of art fromthe Huichol of Mexico (Figure 2), another artistic tra-dition that is influenced by the geometric motifs seen

during ASC (Schaefer, 1996). Clearly, the real openquestion is whether such indigenous cultures are thelast remnants of a much older tradition of using ASC,perhaps one dating back to the origins of the modernhuman mind. We have argued that there are good rea-sons to take this possibility seriously.

Acknowledgements

We are grateful to Anne Zeller for finding the most geometricexamples of her collection of paintings by apes and makingthem available to us.

Funding

This research received no specific grant from any fundingagency in the public, commercial, or not-for-profit sectors.

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94 Adaptive Behavior 22(1)

About the Authors

Tom Froese completed his DPhil in cognitive science from the University of Sussex in 2009. Hesubsequently held postdoctoral fellowships at the Sackler Centre for Consciousness Science andat the University of Tokyo. Since 2012 he is a postdoctoral researcher at the self-organizing sys-tems laboratory of the National Autonomous University of Mexico (UNAM). He investigatesthe relationship between life, mind and sociality using a combination of methods, including evo-lutionary robotics, complex systems theory, and phenomenology.

Alexander Woodward received his PhD in computer science from the University of Auckland,New Zealand in 2009. He is currently a postdoctoral fellow at the Ikegami laboratory of theUniversity of Tokyo (since 2010). His research into computer vision has led him to ask questionsabout the nature of visual perception in living systems. Current research focuses on computervision, neural networks and reservoir computing, subjective time in the brain, scientific comput-ing on the GPU, and a maximalist approach to artificial life.

Takashi Ikegami received his doctorate in physics from the University of Tokyo. His researchinterest is to build and study artificial life systems ranging from chemical droplets and evolution-ary robotics to Web dynamics. Some of these results have been published in Life emerges inmotion (Seido, 2007) and also The Sandwich theory of life (Kodansha, 2012). Takashi Ikegamigave 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 andBioSystems.

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