Original Paper

Adaptive Behavior 21(3) 199–214 Ó The Author(s) 2013 Turing instabilities in biology, culture, Reprints and permissions: sagepub.co.uk/journalsPermissions.nav DOI: 10.1177/1059712313483145 and consciousness? On the enactive adb.sagepub.com origins of symbolic material culture

To m F r o e s e 1,2,3, Alexander Woodward1 and Takashi Ikegami1

Abstract It has been argued that the worldwide prevalence of certain types of geometric visual patterns found in prehistoric art can be best explained by the common experience of these patterns as geometric hallucinations during altered states of consciousness induced by shamanic ritual practices. And in turn the worldwide prevalence of these types of hallucina- tions has been explained by appealing to humanity’s shared neurobiological embodiment. Moreover, it has been proposed that neural network activity can exhibit similar types of spatiotemporal patterns, especially those caused by Turing instabilities under disinhibited, non-ordinary conditions. Altered states of consciousness thus provide a suitable pivot point from which to investigate the complex relationships between symbolic material culture, first-person experience, and neurobiology. We critique prominent theories of these relationships. Drawing inspiration from neurophenomenol- ogy, we sketch the beginnings of an alternative, enactive approach centered on the concepts of sense-making, value, and sensorimotor decoupling.

Keywords Enaction, sense-making, representation, hallucination, Turing patterns, human cognition

1 Introduction & Simon, 1976), the enactive approach instead starts with the biologically embodied mind, and must there- Forms of artistic expression, rituals, and language are fore address the ‘‘cognitive gap’’ between adaptive universal features of all known human cultures. While behavior and abstract human cognition (De Jaegher & animal behavior is mostly governed by immediate envi- Froese, 2009; Froese & Di Paolo, 2009). Thus, rather ronmental demands and the meaning of animal com- than simply assuming the notion of representation as munication is generally fixed by biological evolution, its most basic conceptual foundation for explaining the human symbolic practices and their meanings are the internal mechanisms of human cognition, it tries to historical outcome of a seemingly open-ended social understand the biological, social, and historical origins process of cultural evolution. Explaining the origin of of the phenomenon of symbolic representation as an such symbolic practices in terms of our biological aspect of our cultural environment. This approach embodiment and the social circumstances of our prehis- helps to avoid a lot of the unnecessary linguistic and toric past is one of the major outstanding challenges of theoretical confusion, which has plagued cognitive sci- science. Indeed, the origin of symbolic representation ence for many years (Harvey, 2008). And it also helps concerns the origin of the human condition as such, hence the idea of modern humans as the ‘‘symbolic 1Ikegami Laboratory, Department of General Systems Studies, Graduate species’’ (Deacon, 1997) or ‘‘Homo symbolicus’’ School of Arts and Sciences, University of Tokyo, Tokyo, Japan 2 (Henshilwood & d’Errico, 2011b). This is an issue that Instituto de Investigaciones en Matema´ticas Aplicadas y en Sistemas reaches across the great divide between the natural and (IIMAS), Universidad Nacional Auto´noma de Me´xico (UNAM), Me´xico 3Centro de Ciencias de la Complejidad (C3), Universidad Nacional social sciences, and has implications beyond the remit Auto´noma de Me´xico (UNAM), Me´xico of science itself. The enactive approach to cognitive science is in a Corresponding author: good position to advance the debate about the origins Departamento de Ciencias de la Computacio´n, Instituto de Investigaciones en Matema´ticas Aplicadas y en Sistemas (IIMAS), of the earliest symbolic practices. Whereas traditional Universidad Nacional Auto´noma de Me´xico (UNAM), Apdo. 20-726, cognitive science presupposes the existence of an inter- 01000 Mexico D.F., Mexico. nal ‘‘symbol system’’ as its basic starting point (Newell Email: [email protected] 200 Adaptive Behavior 21(3) to bring to light some unresolved foundational issues. for the cross-culturally shared value of these specific The question therefore becomes how primary adaptive kinds of geometric patterns. processes of sense-making of the here and now could We then evaluate current models of the neural basis have been transformed into secondary forms of sym- of geometric hallucinations, because basic neural pro- bolic sense-making of the absent and the imaginary cesses are prime candidates for explaining this cross- (Froese, 2012). cultural selective bias. These models typically propose Enactive accounts of this profound qualitative tran- to view the visual system as a potentially excitable sition are still in their infancy, but there is broad agree- medium whose autonomous dynamics are unleashed by ment that there is no one single biological or social disinhibiting altered states of consciousness. Essentially, explanatory factor. We are dealing with a historical it is suggested that the disinhibited visual system gener- process emerging from the interaction between biologi- ates spatiotemporal patterns of neural activity due to cal processes, social practices, and the cultural back- Turing instabilities. Researchers also generally claim ground (Froese, in press; Hutchins, 2010; McGann, that the geometric hallucinations experienced by the 2007; Stewart, 2010). The development of an account subject are mental representations of these neural pat- that theoretically bridges the cognitive gap therefore terns. However, while these neural models are capable promises to simultaneously provide an interdisciplinary of reproducing some of the geometric patterns that are bridge between the natural and social sciences. found in prehistoric art and non-ordinary visual experi- Furthermore, because the interaction between cultural ences, their range remains severely limited. In addition, processes and biological embodiment is mediated at the the models tend to trivialize the relationship between personal level through lived experience, this scientific the structure of subpersonal neural processing and the integration is not limited to objective processes, but content of personal visual experience by assuming that also includes phenomenology of the first-person per- visual experience is a representation of inverse optics spective. Cognitive science thereby becomes an applied to neural activity in region V1 of the visual ner- ‘‘anthropologically informed cultural neurophenome- vous system. nology’’ (Laughlin & Throop, 2009). The aim of this We then propose an enactive approach to resolving paper is to contribute to this enactive approach to the these issues. By drawing inspiration from the method various interplays between biology, culture, and con- of neurophenomenology, we argue that the role of self- sciousness, in particular by critically examining the role sustaining neural activity, which is closely associated of altered states of consciousness in the generation of with neural Turing instabilities, has been underappre- geometric prehistoric art. ciated. According to an enactive approach, self- sustaining neural dynamics can generate their own 1.1 Overview of the paper intrinsic value in relation to their conditions of self- maintenance, and they can also serve as a neural We first take a closer look at the one of the most promi- mechanism by which to decouple autonomous brain nent theories of the origin of prehistoric art and high- activity from the influence of environmentally mediated light its main shortcomings. The prevalence of certain sensorimotor dynamics. Both of these aspects can help geometric patterns in the symbolic material culture of to explain the aesthetic selective biases of the first art- many prehistoric cultures, starting shortly after the ists, in particular their interest in inner experience as emergence of our biological species and continuing in exemplified by abstract hallucinations and imaginary some indigenous cultures until today, is explained in phenomena, which are not directly related to the terms of the characteristic contents of biologically demands of their physical environment. We speculate determined hallucinatory experiences. However, we that the self-sustaining dynamics may account for why argue that the correlation between the first artistic these geometric hallucinations were experienced as motifs and typical hallucinatory experiences is not suffi- more significant than other phenomena, and that at the cient to serve as a full explanation. In particular, there same time their underlying neural dynamics may have is a lack of consideration of the value associated with served to mediate and facilitate a form of imaginary altered states of consciousness, both in terms of phe- sense-making that is not bound to immediate nomenology and function. What is it about these non- surroundings. ordinary visual patterns that made them more attractive for artistic expression than most others of an almost infinite set of possible patterns, both physical and ima- 2 On the origins of the symbolic mind ginary?1 Given that humans appear to be in principle capable of arbitrarily associating any kind of stimulus Starting with Darwin’s (1871) evolutionary approach to with any kind of meaning, as epitomized by language as the origins of human language in terms of natural and an open-ended symbol system, there is a need to explain sexual selection, the date for the beginning of symbolic the shared selective biases that are in evidence across thought and creative imagination has been continually prehistoric cultures. In other words, we need to account pushed back into prehistory. It was long assumed that Froese et al. 201 symbolic material culture originated during the last Ice Age in Europe. This standard view was supported by the available archaeological evidence, for instance by the famous Paleolithic cave paintings that were created by the first immigrating Homo sapiens starting from around 40,000 years ago. However, more recently the archaeological consensus has begun to be overturned by new evidence of an even older symbolic material cul- ture (Henshilwood & d’Errico, 2011a). These findings Figure 1. Illustration of a piece of red ochre with abstract were uncovered in Africa, and indicate the presence of geometric incisions that were made on one side around symbolic practices over 100,000 years ago, including 73,000 years ago. This piece was found during excavations in Blombos Cave, South Africa. This and similar pieces from the the manufacture of paint and body ornamentation. In same location are currently the oldest known human expression addition, and contrary to the idea that artistic expres- of abstract geometric patterns. Reproduced with kind sion began with primitive pictorial representations of permission from Elsevier (Henshilwood et al., 2009). the external environment, there was a tradition of engraving pieces of red ochre with a variety of abstract geometric patterns (Henshilwood, d’Errico, & Watts, 2009). An example is shown in Figure 1. Of course, it still remains to be explained why these This discovery connects well with the ethnographical particular motifs were highly regarded by the artists observation that geometric visual patterns have been and how these people became artists capable of sym- playing an important role in prehistoric cultures from bolic expression in the first place. According to Lewis- around the world (Froese, in press). Interestingly, these Williams (2002), the symbolic capacity was already pro- patterns represent only a small subset of the potentially vided by the evolution of an appropriate mutation in infinite set of possible abstract visual patterns that the brain, and the value of the particular content was could be created, and it seems that certain kinds of pat- derived from the hierarchical power structures enforced tern are particularly frequent, such as dots, circles, by shamans who had exclusive access to the visionary cross-hatchings, parallel wavy lines, and especially vari- experiences. However, this hypothesis has several short- ous kinds of spirals (Lewis-Williams & Dowson, 1988). comings. While complex social stratification and strife An important clue to the origin of this selective bias was clearly in evidence during the Neolithic period in was found by psychologists investigating the experien- Europe (Lewis-Williams & Pearce, 2005), this kind of tial effects of various kinds of alterations of conscious- social class conflict may not be generalizable to earlier ness. They discovered that the patterns of many visual periods or other parts of the world. hallucinations could be categorized into a small num- For instance, the Jomon culture of prehistoric ber of so-called ‘‘form constants’’ (Klu¨ver, 1967). In the Japan, one of the oldest pottery traditions in the world 1920s, Klu¨ver had systematically studied the effects of dating back to around 16,500 BC, was the first culture mescaline (the main psychoactive compound of the in the Japanese archipelago to produce pottery deco- peyote cactus, Lophophora williamsii) on the experience rated with abstract geometric patterns. This symbolic of its users (including on himself). He observed that the material culture flourished for well over 10,000 years, non-ordinary visual experiences were often character- producing large quantities of pieces with recognizable ized by similar kinds of abstract geometric patterns, form constants (e.g., Figure 2). However, compared to which he classified into four categories of form con- later symbolic material cultures in this region, the stants: (1) gratings, lattices,2 fretworks, filigrees, hon- Jomon period is remarkable for its long-term stability, eycombs, and checkerboards; (2) cobwebs; (3) tunnels and because of the absence of strong archaeological and funnels, alleys, cones, vessels; and (4) spirals. evidence for a complex social hierarchy, social strife, Klu¨ver’s form constants have since been found to and intergroup warfare (Habu, 2004). occur in a variety of other kinds of altered states The hypothesis that the first symbolic practices were (Bressloff, Cowan, Golubitsky, Thomas, & Wiener, an outcome of a prehistoric class struggle is lacking 2001). Intriguingly, these form constants turned out solid archaeological evidence. More importantly, even to resemble many of the abstract motifs that are often if we could find an early prehistoric society that fits associated with prehistoric art from around the Lewis-Williams’ hypothesis, the existence of a rigid world, including Paleolithic cave art in Europe. These social hierarchy and restricted accessibility of altered insights led to the provocative hypothesis that much states of consciousness by an elite class does not explain of the content of prehistoric art was inspired by pat- why such altered states were highly valued by these terns and visions seen during altered states of con- people in the first place. If the ritualized alteration of sciousness (e.g., Clottes & Lewis-Williams, 1998; consciousness and its symbolic expressions were to be a Lewis-Williams, 2002; Lewis-Williams & Dowson, tool of empowerment restricted to the elite, then the 1988; Winkelman, 2002). general population must have already valued such 202 Adaptive Behavior 21(3)

2001). Regarding visually expressive phenomena, it has been shown that the skin patterns of some animals can be generated by underlying reaction–diffusion systems (Kondo & Miura, 2010). Given the similarity between Turing patterns and some of the motifs frequently found in prehistoric art and experienced by subjects in altered states of consciousness, it makes sense to inves- tigate whether the biological mechanisms underlying the production of these visual phenomena is amenable to an analysis in terms of Turing instabilities. Indeed, this proposal is in line with Klu¨ver’s observation that ‘‘the hallucination is [.] not a static process but a dynamic process, the instability of which reflects an instability in its conditions of origin’’ (cited in Bressloff et al., 2001).

3.1 The neural Turing mechanism One of the originally proposed mechanisms for geo- metric hallucinations is that of a neural Turing mechan- ism, embodied in the Wilson–Cowan equations (H. R. Wilson & Cowan, 1973) and first mathematically ana- Figure 2. A deep pot covered with various spiral patterns; an lyzed in terms of visual hallucinations by Ermentrout early artistic example of the spiral type of Klu¨ver’s form and Cowan (1979). This is the neural context for the constants. This particular style of vessel, known as Moroiso, was made around 4000 BC by people of the Jomon culture famous Turing Instability, which describes a reaction– (Kobayashi, 2004, p. 31), a relatively peaceful and non-stratified diffusion process in which an ordered macroscopic society of prehistoric Japan (Habu, 2004). (Photo taken by Tom structure can emerge from local interactions under the Froese at the Archaeological Museum of Kokugakuin University, non-equilibrium state (Turing, 1952). Turing’s idea can Tokyo, Japan). be readily transposed to the functioning of the nervous system. For example, action potential propagation along a neuron’s axon can be directly described by non-ordinary experiences; otherwise their restriction reaction–diffusion equations, and reaction–diffusion could hardly have served as an instrument of control. In equations are analogical to the Wilson–Cowan neural addition, this hypothesis leaves any functional connec- network equations (H. R. Wilson, 1999, pp. 267–268). tion of altered states of consciousness to the origin of We can think of the reaction component as the interac- symbolic practices, including their underlying neural tions between neuronal cells, and of the diffusion com- effects, unexplored. It seems plausible that, at least under ponent as the spread of neural activity through local some circumstances, a temporary alteration of normal synaptic connections. Similarly, the local structure of sense-making can lead to heightened levels of imagina- neural interconnectivity dictates the type of emergent tion and creativity (Dobkin de Rios & Janiger, 2003). phenomena that can be produced. Neural network models of geometric hallucinations have gradually 3 Neural mechanisms incorporated these empirical insights from neural anat- omy and physiology, including the spatial arrangement Turing patterns consist of various geometric forms, of different neuronal cell types. including spots, traveling waves, grids, and spirals, The first model of geometric hallucinations to follow which emerge out of the distributed activity of non- this idea, by Ermentrout and Cowan (1979), developed linear dynamical systems with local excitatory and an isotropically connected two-layer neural network of sparse inhibitory connectivity. Some illustrative exam- excitatory and inhibitory neurons to represent the pri- ples derived from a simple Gray–Scott reaction– mary visual cortex (V1). Increasing an excitability para- diffusion system are shown in Figure 3. meter destabilized the rest state, bifurcating the system, Simple spatiotemporal pattern formation was first and led to macroscopic spatial patterns emerging due to described by Turing (1952) for the case of chemical the lateral interactions of negative feedback. Such a reaction–diffusion systems. Turing proposed that these general description of a locally connected network kinds of systems could help to explain morphogenesis, shows up the reaction–diffusion type properties of such i.e., pattern formation during biological development. systems, but they require specificity in parameters in Since then, Turing patterns have been found to be ubi- order to generate patterns. The main limitation of this quitous in a variety of biological systems (Goodwin, early work is that they do not consider the neural Froese et al. 203 architecture of V1: the arrangement of neurons in externally coupled state (Miyashita, 1995), although hypercolumns and their properties as low-level feature there is some variability in these results (Kosslyn & detectors. These are addressed in Bressloff et al.’s Thompson, 2003). Other results have pointed to the (2002) work, to be discussed later in this section. primary visual cortex interacting with the hippocampus during offline episodic memory consolidation; high- 3.2 The location of geometric hallucinations within order replay of episodic memories occurs with quite specific patterns of visual activity in V1 (Ji & Wilson, the brain 2007). Where exactly in the brain do such geometric hallucina- The visual cortex is located in the posterior region tions emanate from? Also, is it correct to say that there of the brain’s occipital lobe. V1 takes information from is a single region that constitutes the generation of a the Lateral Geniculate Nucleus (LGN), a region of the visual pattern, knowing that the brain is a highly inter- thalamus, which in turn receives information from ret- connected dynamical system? Considering that geo- inal ganglion cells that each receive information from metric hallucinations are unaffected by the physical around 5–100 photoreceptors. Anatomically, V1 is an movement of the eyes means that such phenomena array of hypercolumns involved in the low-level pro- must emanate from the endogenous activity of the cessing of visual input, with feature detectors tuned to brain. Secondly, that we ‘‘see’’ such phenomena sup- visual aspects such as color, edges, contours, motion, ports the assumption that they must be dependent on etc. (S. W. Wilson, 1983). Between regions, there is a the brain’s visual sub-system. progressive mapping to 2D cortical surfaces and all of All models of geometric hallucinations propose that the models to be discussed operate in such a dimension. such patterns emerge from V1, the ‘‘first’’ region of the After V1, higher-order processing of visual information visual cortex to receive visual input. This assumption is occurs in roughly 30 identified regions within the visual supported by fMRI scans that have shown that V1 is cortex (Miyashita, 1995). sometimes activated during mental imagery, i.e., when But it is presumptive to speak of these brain pro- one imagines something visual in either an awake or cesses happening in some sort of projective sequence. dreaming state—even when they are not in an For example, in cat brains it has been identified that

Figure 3. Examples of dynamic patterns exhibited by the Gray–Scott reaction–diffusion system under various parameters. Patterns are chosen as exemplars of various phenomena; see Pearson (1993) for a more systematic classification. (a) A spiraling pattern; (b) a chaotic pattern of travelling waves; (c) a line pattern, whereby lines grow at the ends and then bend to fill space; (d) a labyrinth pattern; (e) a hole pattern; (f) a pattern of unstable spots, whose fluctuating population is maintained by a balance between reproduction and disintegration; (g) a stable spot pattern, whereby spots reproduce to fill empty space. Reproduced with kind permission from Nathaniel Virgo (Virgo, 2011). 204 Adaptive Behavior 21(3) retinal input accounts for about 7% of synaptic con- of the original retinal frame of reference. This reason- nections to relay cells in the LGN, therefore 93% of ing has important implications for explaining geometric input is non-retinal, coming from other regions in the visual hallucinations. For example, taking a uniformly brain (Van Horn, Erisxir, & Sherman, 2000). It is certain textured ‘‘image’’ (in V1) and going from rectangular that similar physiology exists within the human visual (cortical) to polar (retinal) coordinates can generate a system and this shows that a great deal of dynamic tunnel like warping of the image. This is an effect com- feedback processes must be occurring. Accordingly, mon in many geometric hallucinations and perhaps models that do not account for this massive feedback also related to the tunnel seen in near death experiences have questionable biological plausibility. (Blackmore & Troscianko, 1989). However, the tunnel like warping effect of the inverse retinotopic mapping is not always fitting. For 3.3 The retinotopic map example, to accommodate lattice type phenomena that In general, in current models of geometric hallucina- do not have a clear center of origin or convergence, tions, an inverse retinotopic map is applied to neural Ermentrout and Cowan (1979) state that these must activity in V1 in order to virtually project back into occur at the periphery of the visual field. On the other what would have been the causally responsible retinal hand, a cobweb with a clearly defined center is said to space under normal conditions. The resulting image is appear nearer the fovea (see Figure 4 for illustrative intended to enable us to see what the subject would examples of these distinct kinds of form constants). visually experience. The retinotopic map describes how But this seems a rather odd prediction. If this model retinal input projects onto the visual cortex. This phy- is indeed biologically accurate then a large number of siological mapping has been studied extensively and, in geometric patterns that do not exhibit a tunnel-like simplified terms, is a conformal projection from retinal appearance should be constrained to only appearing at polar coordinates into cortical rectangular coordinates. the periphery of our visual experience. As far as we More space in V1 is assigned to the foveal region than know, the extant psychological literature does not make to the periphery and this is why our spatial detail is any mention of a strict division between such focal and highest at this focal point in our vision. peripheral types of hallucinatory visual patterns. Thus, The reasoning principle underlying the application although this is a prediction that still deserves to be fur- of an inverse mapping to the neural network models is ther investigated experimentally, it is more likely an that under normal awake conditions, when a subject is indication that the relationship between the retinotopic observing the external world, an undistorted view of mapping and geometric hallucinations is less direct than the world enters the retina and then, for physiological originally assumed by Ermentrout and Cowan. reasons, gets distortedly mapped to V1. However, we Another shortcoming of using inverse retinotopic never consciously experience this distorted view of V1. mapping to derive an image of the subject’s experience Therefore, it is argued, there must be some subsequent is that it lacks consideration of the temporal dimension inverting process such that, in some manner, phenom- of consciousness (Varela, 1999). Empirical research ena generated in V1 are actually experienced in terms suggests that abnormal activity in the visual system

Figure 4. Illustration of typical form constants. (a) Cobweb; (b) lattice consisting of parallelograms; and (c) lattice consisting out of hexagons. In contrast to the cobweb form, the lattice forms do not converge on a center point. Reproduced with kind permission from Springer (Ermentrout and Cowan, 1979). Froese et al. 205 only becomes consciously experienced in the form of that can emerge from a realistic non-linear model of a geometric hallucinations after more extensive recurrent cortical sheet of noisy spiking neurons. Their model processing (e.g., P. C. J. Taylor, Walsh, & Eimer, 2010), included a drug parameter and they found that under a thus again implying a more indirect mapping between normal state of activity there was incoherent low- activity in V1 and conscious visual experience. More frequency firing. As they increased the excitation of the generally, we can also take issue with the phenomenol- network, beginning from random initial conditions, ogy of mental imagery that is implied by the idea of they categorized the following emergent properties: (1) deriving the subject’s experience from a neural ‘‘image’’. stripes, (2) spirals—found to be very stable, (3) rings, Under closer phenomenological examination, the expe- and (4) collective bursts. Collectively these were termed rience of mental imagery is qualitatively different from first stage imagery, corresponding to the idea of form the experience of seeing a 2D picture (Thompson, 2007). constants. Second stage imagery, which goes beyond geometric hallucinations to include complex imagery, without any doubt involves several other areas of the 3.4 The ubiquity of spiral and wave dynamics in the brain, including memory systems (de Araujo et al., brain 2012), and was not modeled. Interestingly, once spirals exist within the modeled neural system they cannot be As stated earlier, most models assume that hallucina- extinguished, even if the drug parameter is adjusted tory phenomena are produced in V1 and then pursue a into the ranges to support categories 3 and 4. We note description of their neural underpinnings. But spiral that this kind of hysteresis can be useful during normal and wave (circular wavefront) dynamics seem to be a brain functioning. Summarily, they consider form con- ubiquitous feature of brains, not just in V1, and also of stants to be elementary excitations in the primary visual biologically realistic neural models. Huang et al. (2010) cortex and these spatiotemporal patterns involve the state that spiral waves which emanate from a central same kind of mechanism as in experimentally observed point, as an emergent property, can organize and modu- drug induced epilepsy (we will return to epilepsy late cortical population activity on the mesoscopic scale below). and may contribute to both normal cortical processing Milton, Chu, and Cowan (1993) developed similar and to pathological patterns of activity, e.g., epilepsy. work for generating spirals from a fixed excitation cen- Such wave activity is found to be robust when consid- ter that mimic cardiac arrhythmia. This also demon- ered within local excitatory interactions such as within a strates how changes in neural parameters generate quite cortical sheet (a locally connected 2D network). But the varied macroscopic phenomena despite having a consis- brain has modulatory long-range connections that can tent local connectivity. In general, however, these mod- change the properties of local sub-networks that could els do not generate all four categories of form constant. serve as regulatory protective mechanisms. And despite some authors claiming that the ‘‘perfor- For example, Rulkov, Timofeev, and Bazhenov mance of a large network does not depend on details of (2004) developed a set of computationally efficient yet the model once the neural essentials have been incorpo- highly realistic map-based neuron models to explore rated’’ (Fohlmeister et al., 1995), other models indicate large-scale cortical networks and their dynamics. In that more of the characteristic form constants could be particular, the spiking activity in different types of cor- produced if the exact structure of V1 was considered. tical pyramidal (PY) (fast spiking, regular spiking, intrinsically bursting) and interneurons (INs) was devel- oped. Experiments showed that wave properties were 3.5 Modeling geometric hallucinations as a function dictated by coupling parameters and that self-sustained dynamics were a function dependent on synaptic inter- of V1 neural architecture action between neurons, and not spontaneously firing Bressloff et al. (2001, 2002) developed a model that cells. These findings support the idea of neural architec- aimed to connect geometric visual hallucinations with ture being an important factor for the emergence of the structure of V1. It is well known that V1 consists of geometric patterns that are potentially experienced as a number of neural circuits that are involved in low- hallucinations. That spontaneous waves of activity level ‘‘image processing’’, responding preferentially to could persist within the network indefinitely is also features such as oriented edges and local contours, etc. interesting with respect to the ideas of self-sustainability Their work proposes that the specific spatial arrange- during externally decoupled mental states, maintaining ment and local coupling of these feature detectors, network wide activity to prevent neuronal atrophy from along with the neural Turing mechanism combine to disuse, or the brain’s default network—where self- generate form constants. According to their model, sustained dynamics allows the brain to be in a primed, under normal conditions the visual system is in a stable high-dimensional state. state, but the introduction of drugs destabilizes V1 and Fohlmeister, Gerstner, Ritz, and van Hemmen spontaneously generates cortical activity that reflects (1995) investigated the type of spontaneous excitations the underlying architecture of V1. The possible form 206 Adaptive Behavior 21(3) constants of this model are specific linear combinations toward one of the stable Planforms as proposed in of the eigenfunctions of the neural architecture, called Bressloff’s model. Planforms, which possess both spatial and temporal Secondly and more generally, we know that V1 and properties. Since V1 must avoid falling into these states other regions of the visual pathway show neural activity during normal visual processing, if the influences of the during imagination (Ganis, Thompson, & Kosslyn, retinal input are to have any effect in driving the sys- 2005), which shows that they can be integrated into tem, this places strong constraints on the evolution of higher-level processing in the absence of external input. the visual cortex architecture, for example in terms of Could a feedback loop between these brain areas gener- the sparsity of long-range inhibitory connectivity ate geometric hallucinations? This is much like the idea (Butler et al., 2012). of a video-feedback system, where a video camera is Bressloff et al.’s work represents perhaps the most positioned to record the same video monitor to which it complete description of a neural mechanism for gener- is connected (Crutchfield, 1984, 1988). Despite a video ating geometric hallucinations, however, it is not capa- feedback system being physically different, a conceptual ble of generating all of Klu¨ver’s form constants and analogy can be formed by making firstly a connection does not seem to account for the ubiquitous spiral wave between the neural Turing mechanism and modeling dynamics of the brain, which are realized by the neural the video-feedback as a reaction–diffusion system dynamics in a model such as Folhmeister et al.’s. To (Crutchfield, 1988), and secondly with the known abun- address this, it would be interesting to incorporate a dance of feedback pathways within the brain. The large more biologically plausible, spiking neural model. number of geometric patterns that can be produced by Secondly, the authors only considered oriented edges such physical video feedback systems, such as logarith- and local contours in their architecture; what genera- mic spirals and phyllotaxis, lends some credence to this tive power would the modeling of other feature maps, novel hypothesis. such as spatial frequency, binocular disparity, motion, However, what could constitute a neural visual feed- and color provide? back mechanism for geometric hallucinations is still Furthermore, none of the models seems to account unknown. It seems plausible that somehow the abun- for the entirety of geometric hallucinations that are dance of feedback loops could play this role, especially commonly reported in the archeological and anthropo- when considering that at some point, during an altered logical literature, for example as described by Lewis- state of mind, geometric hallucinations may be com- Williams and colleagues (Lewis-Williams & Dowson, bined, modulated by, and reinterpreted with hallucina- 1988). Future work along the lines of Bressloff et al.’s tions from memory and iconic imagery that must be model may someday show that the intrinsic properties generated elsewhere within the cerebral cortex (de of V1 are enough to describe all geometric hallucina- Araujo et al., 2012). tory phenomena, but given the large variety of pat- Another pathway that could be involved is through terns, this is unlikely. It is interesting to consider what the superior colliculus (SC)—a major region of the ver- other brain mechanisms could contribute to their for- tebrate midbrain that forms an important part of the mation, such as the large number of feedback pathways visual system, and which is considered to play a critical that exist within the visual system.3 role in the development of blind sight (Takaura, Yoshida, & Isa, 2011). The mutual interaction between the primary visual cortex and this subcortical neural 3.6 The role of neural feedback in visual processing structure, which is also involved in visual processing, could open new possibilities for explaining geometric Complex and varied experimental results on the func- hallucinations in the absence of external visual stimuli. tion of feedback pathways have been found, but it is In addition, the SC’s role in multisensory integration generally considered that higher-level cortical regions (Hall & Moschovakis, 2004) might help to explain how are involved in large-scale perceptual integration which visual hallucinations become integrated with hallucina- combine with the fine-scale resolution provided by the tions in other modalities, including synesthesia-like earlier visual regions (Sillito, Cudeiro, & Jones, 2006). effects. Feedback is involved in modulating perception; such as figure ground separation, suppressing areas of low information to generate a sparse codification of the 3.7 Beyond structural isomorphism visual signal, coordination and tuning of visual feature This overview of the putative neural mechanisms detectors, and attention (Williams et al., 2008). Back- underlying geometric hallucinations points to the key projecting pathways are therefore thought to facilitate, components being the architecture in V1 supporting a inhibit, and synchronize neural activity (Przybyszewski, neural Turing mechanism along with the retinotopic 1998). Under the influence of drugs, or in an altered mapping, the ubiquity of spiral and wave dynamics state of mind induced by other means, these pathways within the brain, and widespread and long-ranging could all be involved in moving the visual system feedback connections. But despite these insights, the Froese et al. 207 full range of reported geometric hallucinations has yet neural activity and patterns of hallucinatory experi- to be accommodated by a single mathematical neural ence, it may be more productive to consider other func- network model. The incorporation of additional phy- tionally relevant properties of such neural patterns siological detail may increase the range of geometric than their precise spatiotemporal arrangement alone. phenomena that can be modeled, especially long-range For example, all modeled neural patterns show feedback connectivity. We must consider the neural properties of robustness and self-sustainability. In the projections into and out of V1, such as its direct con- models of Ermentrout and Cowan (1979) and Bressloff nection back to the LGN, to the other 30 or so visual et al. (2001), patterns appear as the stable configura- processing regions, and the rest of the brain. tions of the system after bifurcating from a low activity Visual hallucinations can be induced in a wide num- state. The neural model of Rulkov et al. (2004) displays ber of ways, but all models make use of a single drug self-sustained wave dynamics that can spontaneously parameter that affects the entire system. Yet how does emerge from low-level random neural activity. As the experienced pattern differ depending on the route already mentioned, in the model of Fohlmeister et al. taken to such a state of mind? Dietrich (2003) proposes (1995), once spiral waves emerge they cannot be that most altered states of mind (drug induced or other- destroyed, even when increasing a drug parameter into wise) involve a transient decrease in prefrontal cortex the range where other geometric phenomena usually activity, and that the difference between types of expe- appear. This case of apparent irreversibility is probably rience arises from how the induction method affects the the strongest example of robustness and self- various prefrontal neural circuits. Connecting this func- sustainability in the surveyed models, and it is sugges- tion to models of geometric hallucinations and to the tive as a biological explanation for the fact that spirals types of patterns specific to certain altered states could are one of the most prevalent motives in prehistoric make for some interesting predictions. We can also art. wonder at what type of widespread effects the prefron- How could this property of robust self-maintenance tal cortex can have on the whole visual cortex and the relate to the hallucinatory experiences? A striking fea- rest of the brain, not just in V1. ture that differentiates geometric hallucinations from It also remains to be seen whether Turing instabil- other visual experiences is that they are generated ities in the rest of the brain, including the peripheral intrinsically when the subject has been decoupled from nervous system, play a role in generating geometric hal- its environment. The patterns form irrespective of our lucinations. Indeed, because of the generality of this lifetime learned memories. Indeed, they could be con- dynamical phenomenon, its potential role may not be sidered internally directed perceptual experiences, since limited to electrical interactions between neurons, if the proposed models hold true, they are directly either. We know that Turing patterns are crucial for a formed from the actual biological structure of the number of other biological processes, including in the visual system. We are said to have a strange subjective chemical domain (Goodwin, 2001). Therefore, more experience of looking into oneself, where the patterns realistic models of geometric hallucinations might want we see directly expose the underlying operation of our to include details of the physical and chemical pro- brains. At the same time, the robustness of the underly- cesses of the central and peripheral nervous system, ing neural patterns also reinforces this decoupling from e.g., reaction and diffusion of various neurotransmit- the environment. In the next section, we argue that ters, vitreous liquids inside the eye, oily residues on the under some conditions such a neural mechanism of surface of the cornea, etc., which could give rise to decoupling could be adaptive. Humans are adept at not Turing patterns under disinhibited conditions, and thus only understanding patterns from external sensory influence the outcome of visual processing. As a simple input, but importantly, we have a powerful faculty for proof of concept, it has been shown that the dynamics active generation—be it for purposes such as predic- of a Gray–Scott reaction–diffusion system (see patterns tion, imagination or playing. in Figure 3) can be used in order to control a mobile robot, giving rise to shape discrimination and memory (Dale & Husbands, 2010). 4 Steps toward a new approach to the But as we incorporate these additional features into origins of symbolic material culture the models, it may also turn out that the hypothesis of a strict structural isomorphism between patterns of One promising approach for systematically evaluating neural activity in V1 and geometric hallucinations will the relationship between brain functioning and human become less tenable. As a case in point, the function of experience is known as neurophenomenology, a method the inverse retinotopic map can be called into question that was proposed by Varela (1996) as part of the enac- when considering that it implies that many of the tive approach, and which has subsequently been elabo- reported geometric hallucinations have to appear extra- rated by others (e.g., Petitmengin, Navarro, & Le Van foveally. Accordingly, rather than looking for a direct Quyen, 2007; Thompson, Lutz, & Cosmelli, 2005). The one-to-one structural mapping between patterns of basic idea of neurophenomenology is to relate the 208 Adaptive Behavior 21(3) empirical data of neuroscience and verbal descriptions This consideration places a significant constraint on of first-person experience in a mutually informing and our explanation from the side of cultural practices, enriching manner. In this way both third-person and because the artists must have valued their altered visual first-person aspects of a phenomenon are taken into experiences. Some researchers have tried to address this account, but without privileging one domain over the constraint by appealing to social practices. For exam- other. While the aim is to find a formal model at which ple, Lewis-Williams (2002) argued that the value of the the dynamics of the two domains can be integrated, this experiences derives from their value as a tool to enforce does not entail a necessity of structural isomorphism. social hierarchies by restricting access to elite individu- Instead, there is a mutual braiding of structural con- als via prohibition. But this only shifts the original straints, which links the activity of the two domains problem without resolving it, because we must then into one unfolding process (Varela, 1999). explain why people would value these experiences as In addition, because perception is conceived of as a worthy of restriction to elites. relational process of sense-making that is extended over One promising alternative is to assume that when the entire brain–body–environment as a whole, the these visual patterns are seen during altered states of external–internal distinction becomes relativized (Lenay consciousness they are directly experienced as highly & Steiner, 2010). That is, the perceptual experience of charged with significance. In other words, the patterns an environment as being external is itself an outcome of are directly perceived as somehow meaningful and sense-making, and therefore becomes potentially rever- thereby offer themselves as salient motifs for use in sible and dissolvable as the conditions of sense-making rituals. This possibility seems to accord with verbal are modified under unusual conditions. In the case of reports about the range of emotional effects that can be geometric hallucinations, it could therefore be that we elicited by a variety of non-ordinary experiences (e.g., are in fact dealing with an abnormally oriented percep- Dobkin de Rios & Janiger, 2003; Huxley, 1956; tual process, where the object of perception is an aspect Shanon, 2002; Strassman, 2001). This appeal to an of the nervous system itself. This is surely a strange intrinsic value places constraints on the underlying hypothesis, but the consideration of perceptual media- neural dynamics. We therefore need to discuss how tion opens up a new perspective on the problem of the value could be realized in neurobiology, and then we mismatch between the impoverished neural patterns determine whether this neurological mechanism is com- and the rich geometric experiences. A similar mismatch patible with the neurological mechanism underlying the has been observed to hold between the impoverished experience of the most common forms of geometric retinal input and our rich visual experience of the world phenomena. (Noe¨, 2002). Accordingly, on this alternative view, the main shortcoming of the current neural network models is not an insufficiently detailed structural isomorphism, 4.2 Sketches of an enactive neurobiological account but rather a failure to take the enriching effects of of value sense-making into account.4 In the history of cognitive science, the question of value has been a profoundly puzzling one. The computa- 4.1 Neurophenomenology of value tional theory of mind holds that cognition is rule-based How might neurophenomenology address the corre- manipulation of abstract symbols, as epitomized by the spondence between spatial patterns in the cultural, digital computer program. However, this logical syntax experiential and neurobiological domains? The first leaves the concrete meaning of the symbols unac- thing to note is that the artistic patterns under consider- counted for; they are simply empty placeholders. This ation form an extremely limited set compared to the problem of meaning has resulted in major stumbling total set of all possible patterns that could have been blocks in theory of mind, as well as in the practice of created. This universal selection bias is something that AI and robotics, such as the symbol grounding prob- must be explained, but which has so far remained mys- lem and the frame problem. The enactive critique of terious. It is not sufficient to note the correlation with these theoretical and practical problems is centered on visual experiences during altered states of conscious- the grounding of value in the self-maintenance of ness. Even if we accept that internally oriented visual autonomous forms of biological organization (for a perception is possible during altered states of conscious- review, see Froese & Ziemke, 2009). ness, this does not in itself explain why those perceptual Most importantly, the enactive approach tries to experiences are more frequently expressed artistically. provide a viable alternative by defining value in opera- Why should these particular patterns be preferred over tional terms. A good starting point is the work by Di other kinds of ordinary and non-ordinary visual experi- Paolo, Rohde and De Jaegher (2010, p. 48): ‘‘We pro- ences? This selective bias must therefore be accounted pose to define value as the extent to which a situation for in terms of the value these patterns have had for the affects the viability of a self-sustaining and precarious artists who made them. network of processes that generates an identity.’’ There Froese et al. 209 are a number of entangled concepts implicated in this they are complex in many ways (Le Van Quyen, 2010; definition, which cannot be unpacked in detail here. Petitmengin et al., 2007). What is particularly remark- We briefly summarize the main ideas. To start with, able is the reported vividness or intensity of these the network’s identity is not a reified entity; it can be experiences. The content of the experiences depends on defined as operational closure, i.e., the mutual depen- the person and the precise brain region of the epileptic dence of the processes of the network on each other for discharge, but commonalities can be identified. their existence. This co-dependence provides them with Consider, for example the case of emotional experience: an internal relationship that integrates them with each other and that does not depend on a unifying distinc- Special emotional auras consist of an attack of anguish tion by an external observer. And this co-dependence and terror that suddenly takes over the consciousness with also makes the network’s identity precarious, since its such intensity that the subject has the impression she or he existence is not externally guaranteed but must be self- is losing control of the situation, which will have a terrible sustained by its own ongoing activity. In other words, end, perhaps madness or even death. In other emotional the network is only viable within certain boundary con- auras, the experience consists of a sudden state of joy with no apparent cause, and it takes over the consciousness ditions. The value of an event is therefore defined passively for a few short moments, filling it with awe and in relation to its impact on these conditions, i.e., strangeness. (Le Van Quyen, 2010, pp. 247–248) whether it contributes to the self-sustaining of the iden- tity or not. Clearly, neurophenomenology is currently not The paradigmatic example of this kind of value- advanced enough to explain the particular content of generating system is the minimal living system (Weber these experiences, but it does successfully explain why & Varela, 2002). But the same kind of organization can the experiences are characterized by such an intensely also be found in the nervous system, where we have the felt significance. Generalizing this insight to the experi- temporary emergence of cell assemblies (Varela, ences of geometric hallucinations, we can predict that Lachaux, Rodriguez, & Martinerie, 2001). The firing these, too, are felt with an increased intensity of signifi- patterns of some neurons (or of collections of neurons) cance, as long as self-sustaining processes of neural can become entrained with each other, thereby consti- activity generate them. In other words, intrinsic value is tuting a precarious, self-sustaining network of pro- built into the experience of some altered states of con- cesses, which in this case is a neurocognitive identity sciousness from the start. The ambivalence of the non- (Varela, 1997). This kind of neural pattern is therefore ordinary experiences reported by Le Van Quyen, i.e., a suitable candidate for a process of value-generation. whether they are experienced as good or bad, is not Now if we consider the models of the neural mechan- specific to altered states of consciousness induced by isms underlying some of the common geometric halluci- epilepsy, but is characteristic of altered states more gen- nations, we also find the same kind of self-sustaining erally (Huxley, 1956). Perhaps this inherent polarity of cell assembly. Moreover, it is likely that the assembly’s consciousness alteration, which Huxley famously con- robustness is enhanced considerably, because activity in trasted as scenarios of ‘‘heaven’’ and ‘‘hell’’, has to do the visual brain regions during altered states is generally with the fact that the organism is a whole meshwork of assumed to be disinhibited. In addition, under these self-sustaining processes (Varela, 1991), and the intrin- conditions the sensory input from external events no sic value of a specific self-sustaining neural process has longer has the power to modulate the cell assembly’s to be balanced against the needs of the other self- boundary conditions, thus enhancing its viability. In sustaining processes of the organism as a whole. the most extreme cases, this kind of autonomous, self- sustaining network can manifest itself in a complete loss of sensorimotor interaction. For example, it has long 4.3 Ideas for an enactive neurobiological account been known that seeing flickering light at certain fre- of imagination quencies can induce neural entrainment and geometri- cal hallucinations (for recent work in this area, see, e.g., The problem of explaining the origins of the human Billock & Tsou, 2007), but when the brain as a whole imagination is related to the transformation of basic becomes too entrained with those frequencies it can sense-making of the here and now to the enaction of cause an epileptic fit. According to the enactive account the absent and imaginary (Froese, 2012). We speculate of value, we would expect these kinds of geometric that one manner of realizing this transformation is to experiences to be experienced as significant, and the mediate the organism’s sensorimotor interactions in non-ordinary experiences encountered before or during such a way that the autonomous dynamics of the ner- epileptic fits as intensely meaningful.5 vous system temporarily become decoupled from the Verbal reports of people with epilepsy confirm this environment. Abstract forms of cognition are likely to hypothesis. Sometimes the seizures leave people uncon- be facilitated during such highly introverted states of scious, but when they do have experiences during the consciousness, which would also help to explain their prodromal phase and at the onset of the epileptic fit prehistoric origin. 210 Adaptive Behavior 21(3)

As we have already indicated, a basic dynamic the origin of abstract cognition and symbolic practices neural mechanism for realizing a temporary mode of in terms of temporary environmental decoupling of environmental decoupling can be derived from the exis- neural processing. tence of self-sustaining processes of neural activity. These neural processes might not always be easily iden- tifiable in terms of spatial patterns, especially when we 5 Conclusion are considering parts of the nervous system that do not We have criticized some of the current theories that exhibit such a regular spatial embedding as the retina 6 have been proposed to explain the origins of symbolic or V1. Nevertheless, it is helpful to think of these practices, especially as exemplified by Lewis-Williams’ neural processes in terms of an analogy with chemical account. We have argued that Lewis-Williams’ insis- reaction–diffusion systems, which are formally closely tence on social conflict and class struggle as the pri- related to the activation–inhibition models of the visual mary driving force behind changes in the first symbolic system (H. R. Wilson, 1999, pp. 267–268). Chemical practices is not compelling for a variety of reasons. reaction–diffusion systems are a well-researched area, Nevertheless, his claim that the cultivation of altered both formally and empirically, and therefore provide a states of consciousness was involved in the origins of useful source of inspiration. For example, it has been the first symbolic material cultures may still turn out to demonstrated that chemical Turing patterns, and espe- be correct, although for alternative reasons which he cially spiral patterns, are highly robust against the influ- fails to consider. ence of external perturbations such as attacks by On the basis of a review of current mathematical parasitic chemical species (Boerlijst & Hogeweg, 1991). models of neural mechanisms underlying geometric hal- Accordingly, it seems plausible that the disinhibition of lucinations, we proposed a neurophenomenological the visual cortex during altered states, perhaps via top- approach that emphasizes the enactive account of down projections from prefrontal cortex to the pathway sense-making and value. In particular, by considering from retina to V1 regions, could lead to Turing patterns some kinds of altered state of consciousness as largely of neural activity in V1 that are robust against perturba- internally mediated forms of perceptual sense-making, tions from visual sensory input, thereby effectively shut- we can better account for the richness of non-ordinary ting down external visual influence (Butler et al., 2012). experiences. Furthermore, the value generated by self- The analogy with chemical reaction–diffusion sys- sustaining cell assemblies may help to explain the tems also suggests that some of these neural Turing pat- selective bias of the first artists for the kinds of geometric terns may even exhibit their own self-individuated patterns that are typically experienced during these spatiotemporal identity, as well as the ability to engage altered states of consciousness. The enactive approach in adaptive interactions with other emergent processes also supports the idea that such altered states could have and structures. These kinds of emergent behaviors have significantly influenced the operation of the nervous sys- been demonstrated to occur in chemical reaction– tem, especially by temporarily decoupling the autono- diffusion systems, including self-moving droplets with mous activity of the brain from the usual environmental tail structures (Froese, Virgo, & Ikegami, in press). It is influences. This switch from immediate sensorimotor therefore tempting to speculate that some neural Turing sense-making, which is normally directed toward the patterns can adapt to, and perhaps even make sense of, the brain’s own activity and structures during altered external here and now, to a more internally mediated, states of consciousness. Could this help to explain the decoupled sense-making of mental and bodily structures commonly reported transition from purely geometric could thereby have facilitated the creation and diversifi- hallucinations to iconic hallucinations that appear to cation of abstract cognition and symbolic practices. exhibit their own agency (Lewis-Williams, 2002)? Future work in systems neuroscience needs to verify Notes if any of these possibilities are borne out by the empiri- 1. Some researchers prefer the hypothesis that these prehis- cal evidence. Nevertheless, an enactive approach is toric patterns are highly abstract representations of nor- compatible with current models of the neural mechan- mal perceptual experience rather than direct expressions isms underlying geometric hallucinations, and already of abnormal hallucinatory experience. For example, has more explanatory power than merely assuming a spiral patterns could be derived from ‘‘swirling water direct structural isomorphism between visual experi- flows, swirling winds, winding stems of vines and winding ence and brain activity: (1) it allows for the possibility snakes’’ (Takaki & Ueda, 2007, p. 133). However, this hypothesis presupposes a process of geometric abstrac- that the patterns of non-ordinary visual experience are tion. Moreover, other common kinds of prehistoric pat- more varied and richly detailed than the underlying terns are not so readily found in nature. Most neural patterns; (2) it can help to explain why these pat- importantly, even if all of the patterns could be terns were taken to be highly significant; and (3) it sug- abstracted from environmental phenomena, the problem gests that there may have been a functional link of explaining the cross-cultural significance of these pat- between the ritualistic alteration of consciousness and terns would remain the same. Froese et al. 211

2. Note that the engraved pattern shown in Figure 1 can be Bressloff, P. C., Cowan, J. D., Golubitsky, M., Thomas, P. J., interpreted as a lattice pattern made of triangles (i.e., one & Wiener, M. C. (2001). Geometric visual hallucinations, of Klu¨ver’s form constants). Euclidean symmetry and the functional architecture of stri- 3. In this respect it is suggestive that even the hallucinatory ate cortex. Philosophical Transactions of the Royal Society experience of small spots of light (phosphenes), induced B: Biological Sciences, 356, 299–330. by applying transcranial magnetic stimulation (TMS) Bressloff, P. C., Cowan, J. D., Golubitsky, M., Thomas, P. J., over the human visual cortex, apparently cannot be & Wiener, M. C. (2002). What geometric visual hallucina- reduced to a local neural mechanism, but arises only after tions tell us about the visual cortex. Neural Computation, more widespread recurrent processing (P. C. J. Taylor et 14, 473–491. al., 2010). A distribution across multiple neural substrates Butler, T. C., Benayoun, M., Wallace, E., von Drongelen, W., also helps to explain how such simple geometric halluci- Goldenfeld, N., & Cowan, J. D. (2012). Evolutionary con- nations can be transformed into full-blown iconic halluci- straints on visual cortex architecture from the dynamics of nations, for example under certain kinds of pathological hallucinations. Proceedings of the National Academy of conditions (J.-P. Taylor et al., 2011). Sciences of the USA, 109(2), 606–609. 4. This shift in explanatory approach helps us to resolve one Clottes, J., & Lewis-Williams, D. (1998). The shamans of pre- of the major outstanding puzzles of the current neu- history: Trance and magic in the painted caves. New York, roscience of geometric hallucinations, namely the appar- NY: Harry N. Abrams. ent mismatch between the resolution of neural Turing Crutchfield, J. P. (1984). Space-time dynamics in video feed- patterns and visually experienced patterns. However, it is back. Physica D: Nonlinear Phenomena, 10(1–2), 229–245. not a solution to the explanatory gap of the mind-body Crutchfield, J. P. (1988). Spatio-temporal complexity in non- problem as such. We thank Julien Hubert for helping us linear image processing. IEEE Transactions on Circuits and to clarify this important difference. Systems, 35(7), 770–780. 5. Strictly speaking, the enactive approach only predicts that Dale, K., & Husbands, P. (2010). The evolution of reaction– there is value for the self-sustaining neural process itself. diffusion controllers for minimally cognitive agents. Artifi- More remains to be said about how this value also cial Life, 16, 1–19. becomes significant from the perspective of the self- Darwin, C. (1871). The descent of man, and selection in relation sustaining organism as a whole. But considering that to sex. London, UK: John Murray. neural processes are constitutive of the whole organism de Araujo, D. B., Ribeiro, S., Cecchi, G. A., Carvalho, F. (Varela, 1991), it seems reasonable to assume that their M., Sanchez, T. A., Pinto, J. P., de Martinis, B. S., Crippa, values are also constitutive of the values of the whole J. A., Hallak, J. E. C., & Santos, A. C. (2012). Seeing with organism. Nevertheless, future work on an enactive the- the eyes shut: Neural basis of enhanced imagery ory of the personal self is needed in order to better con- following Ayahuasca ingestion. Human Brain Mapping, nect these distinct levels of description. Thanks to 33, 2550–2560. Nathaniel Virgo for highlighting this issue. De Jaegher, H., & Froese, T. (2009). On the role of social 6. Thanks to Chris Buckley for pressing this point during interaction in individual agency. Adaptive Behavior, 17(5), several discussions. 444–460. Deacon, T. W. (1997). The symbolic species: The co-evolution Acknowledgments of language and the brain. New York, NY: W. W. Norton We thank Chris Buckley, daboo, Julien Hubert, Guillaume & Company, Inc. Dumas, Etienne Roesch, Nathaniel Virgo and one anon- Di Paolo, E. A., Rohde, M., & De Jaegher, H. (2010). Hori- ymous reviewer for their thoughtful comments on an earlier zons for the enactive mind: Values, social interaction, and draft of this paper. Many ideas of this paper took shape dur- play. In J. Stewart, O. Gapenne & E. A. Di Paolo (Eds.), ing several seminars of the Ikegami Laboratory, and they Enaction: Toward a new paradigm for cognitive science (pp. have benefited from generous audience feedback. 33–87). Cambridge, MA: The MIT Press. Dietrich, A. (2003). Functional neuroanatomy of altered Funding states of consciousness: The transient hypofrontality hypothesis. Consciousness and Cognition, 12, 231–156. Tom Froese and Alexander Woodward were each financially Dobkin de Rios, M., & Janiger, O. (2003). LSD, Spirituality, supported by a Grant-in-Aid of the Japanese Society for the and the creative process. Rochester, VT: Park Street Press. Promotion of Science (JSPS) during the initial phase of this Ermentrout, G. B., & Cowan, J. D. (1979). A mathematical work. theory of visual hallucination patterns. Biological Cyber- netics, 34, 137–150. References Fohlmeister, C., Gerstner, W., Ritz, R., & van Hemmen, J. Billock, V. A., & Tsou, B. H. (2007). Neural interactions L. (1995). Spontaneous excitations in the visual cortex: between flicker-induced self-organized visual hallucina- Stripes, spirals, rings, and collective bursts. Neural Compu- tions and physical stimuli. Proceedings of the National tation, 7, 905–914. Academy of Sciences of the USA, 104(20), 8490–8495. Froese, T. (2012). From adaptive behavior to human Blackmore, S. J., & Troscianko, T. S. (1989). The physiology cognition: A review of Enaction. Adaptive Behavior, 20(3), of the tunnel. Journal of Near-Death Studies, 8(1), 15–28. 209–221. Boerlijst, M. C., & Hogeweg, P. (1991). Spiral wave structure Froese, T. (in press). Altered states and the prehistoric rituali- in pre-biotic evolution: Hypercycles stable against para- zation of the modern human mind. In C. Adams, A. sites. Physica D: Nonlinear Phenomena, 48, 17–28. Waldstein, B. Sessa, D. Luke & D. King (Eds.), Breaking 212 Adaptive Behavior 21(3)

convention: Essays on psychedelic consciousness. London, Laughlin, C. D., & Throop, C. J. (2009). Husserlian medita- UK: Strange Attractor Press. tions and anthropological reflections: Toward a cultural Froese, T., & Di Paolo, E. A. (2009). Sociality and the life- neurophenomenology of experience and reality. Anthropol- mind continuity thesis. Phenomenology and the Cognitive ogy of Consciousness, 20(2), 130–170. Sciences, 8(4), 439–463. Le Van Quyen, M. (2010). Neurodynamics and phenomenol- Froese, T., Virgo, N., & Ikegami, T. (in press). Motility at the ogy in mutual enlightenment: The example of the epileptic origin of life: Its characterization and a model. Artificial Life. aura. In J. Stewart, O. Gapenne & E. A. Di Paolo (Eds.), Froese, T., & Ziemke, T. (2009). Enactive artificial intelli- Enaction: Toward a new paradigm for cognitive science (pp. gence: Investigating the systemic organization of life and 245–266). Cambridge, MA: The MIT Press. mind. Artificial Intelligence, 173(3–4), 366–500. Lenay, C., & Steiner, P. (2010). Beyond the internalism/ Ganis,G.,Thompson,W.L.,&Kosslyn,S.M.(2005).Brain externalism debate: The constitution of the space of per- areas underlying visual mental imagery and visual percep- ception. Consciousness and Cognition, 19, 938–952. tion: an fMRI study. Cognitive Brain Research, 20, 226–241. Lewis-Williams, D. (2002). The mind in the cave: Conscious- Goodwin, B. (2001). How the leopard changed its spots: The ness and the origins of art. London, UK: Thames & evolution of complexity. Princeton, NJ: Princeton Univer- Hudson. sity Press. Lewis-Williams, D., & Dowson, T. A. (1988). The signs of all Habu, J. (2004). Ancient Jomon of Japan. Cambridge, UK: times: Entoptic phenomena in Upper Paleolithic art. Cur- Cambridge University Press. rent Anthropology, 29(2), 201–245. Hall, W. C., & Moschovakis, A. (Eds.). (2004). The superior Lewis-Williams, D., & Pearce, D. (2005). Inside the Neolithic colliculus: New approaches for studying sensorimotor inte- mind: Consciousness, cosmos and the realm of the gods. gration. New York, NY: CRC Press. London, UK: Thames & Hudson. Harvey, I. (2008). Misrepresentations. In S. Bullock, J. Noble, McGann, M. (2007). Enactive theorists do it on purpose: R. A. Watson & M. A. Bedau (Eds.), Artificial Life XI: Toward an enactive account of goals and goal-directedness. Proceedings of the Eleventh International Conference on the Phenomenology and the Cognitive Sciences, 6(4), 463–483. Simulation and Synthesis of Living Systems (pp. 227–233). Milton, J. G., Chu, P. H., & Cowan, J. D. (1993). Spiral Cambridge, MA: The MIT Press. waves in integrate-and-fire neural networks. In S. J. Han- Henshilwood, C. S., & d’Errico, F. (2011a). Middle Stone son, J. D. Cowan & C. L. Giles (Eds.), Advances in neural Age engravings and their significance to the debate on the information processing systems 5 (pp. 1001–1006). San emergence of symbolic material culture. In C. S. Henshil- Mateo, CA: Morgan Kaufmann Publishers. wood & F. d’Errico (Eds.), Homo symbolicus: The dawn of Miyashita, Y. (1995). How the brain creates imagery: Projection language, imagination and spirituality (pp. 75–96). Amster- to primary visual cortex. Science, 268(5218), 1719–1720. dam, Netherlands: John Benjamins Publishing Company. Newell, A., & Simon, H. A. (1976). Computer science as Henshilwood, C. S., & d’Errico, F. (Eds.). (2011b). Homo empirical enquiry: Symbols and search. Communications of symbolicus: The dawn of language, imagination and spiri- the Association for Computing Machinery, 19(3), 113–126. tuality. Amsterdam, Netherlands: John Benjamins Pub- Noe¨, A. (2002). Is the visual world a grand illusion? Journal of lishing Company. Consciousness Studies, 9(5–6), 1–12. Henshilwood, C. S., d’Errico, F., & Watts, I. (2009). Engraved Pearson, J. E. (1993). Complex patterns in a simple system. ochres from the Middle Stone Age levels at Blombos Cave, Science, 261(5118), 189–192. South Africa. Journal of Human Evolution, 57, 27–47. Petitmengin, C., Navarro, V., & Le Van Quyen, M. (2007). Huang, X., Xu, W., Liang, J., Takagaki, K., Gao, X., & Wu, Anticipating seizure: Pre-reflective experience at the center J.-y. (2010). Spiral wave dynamics in neocortex. Neuron, of neuro-phenomenology. Consciousness and Cognition, 68, 978–990. 16(3), 746–764. Hutchins, E. (2010). Enaction, imagination, and insight. In J. Przybyszewski, A. W. (1998). Vision: Does top-down process- Stewart, O. Gapenne & E. A. Di Paolo (Eds.), Enaction: ing help us to see? Current Biology, 8, R135–E139. Toward a new paradigm for cognitive science (pp. 425–450). Rulkov, N. F., Timofeev, I., & Bazhenov, M. (2004). Oscilla- Cambridge, MA: The MIT Press. tions in large-scale cortical networks: Map-based model. Huxley, A. (1956). The doors of perception and heaven and hell. Journal of Computational Neuroscience, 17, 203–223. New York, NY: Harper & Brothers. Shanon, B. (2002). The antipodes of the mind: Charting the Ji, D., & Wilson, M. A. (2007). Coordinated memory replay phenomenology of the Ayahuasca experience. Oxford, UK: in the visual cortex and hippocampus during sleep. Nature Oxford University Press. Neuroscience, 10(1), 100–107. Sillito, A. M., Cudeiro, J., & Jones, H. E. (2006). Always Klu¨ver, H. (1967). Mescal and the mechanisms of hallucination. returning: feedback and sensory processing in visual cortex Chicago, IL: The University of Chicago Press. and thalamus. Trends in Neurosciences, 29(6), 307–316. Kobayashi, T. (2004). Jomon reflections: Forager life and cul- Stewart, J. (2010). Foundational issues in enaction as a para- ture in the prehistoric Japanese archipelago. Oxford, UK: digm for cognitive science: From the origin of life to con- Oxbow Books. sciousness and writing. In J. Stewart, O. Gapenne & E. A. Kondo, S., & Miura, T. (2010). Reaction–diffusion model as Di Paolo (Eds.), Enaction: Toward a new paradigm for cog- a framework for understanding biological pattern forma- nitive science (pp. 1–31). Cambridge, MA: The MIT Press. tion. Science, 329, 1616–1620. Strassman, R. J. (2001). DMT: The spirit molecule. Rochester, Kosslyn, S. M., & Thompson, W. L. (2003). When is early VT: Park Street Press. visual cortex activated during visual mental imager? Psy- Takaki, R., & Ueda, N. (2007). Analysis of spiral curves in chological Bulletin, 129(5), 723–746. traditional cultures. Forma, 22, 133–139. Froese et al. 213

Takaura, K., Yoshida, M., & Isa, T. (2011). Neural substrate Varela, F. J. (1997). Patterns of life: Intertwining identity and of spatial memory in the superior colliculus after damage cognition. Brain and Cognition, 34(1), 72–87. to the primary visual cortex. The Journal of Neuroscience, Varela, F. J. (1999). The specious present: A neurophenome- 31(11), 4233–4241. nology of time consciousness. In J. Petitot, F. J. Varela, B. Taylor, J.-P., Firbank, M., Barnett, N., Pearce, S., Living- Pachoud & J.-M. Roy (Eds.), Naturalizing phenomenology: stone, A., Mosimann, U., Eyre, J., McKeith, I. G., & Issues in contemporary phenomenology and cognitive science O’Brien, J. T. (2011). Visual hallucinations in dementia (pp. 266–317). Stanford, CA: Stanford University Press. with Lewy bodies: Transcranial magnetic stimulation Varela, F. J., Lachaux, J.-P., Rodriguez, E., & Martinerie, J. study. The British Journal of Psychiatry, 199, 492–500. (2001). The Brainweb: Phase synchronization and large- Taylor, P. C. J., Walsh, V., & Eimer, M. (2010). The neural scale integration. Nature Reviews Neuroscience, 2, 229–239. signature of phosphene perception. Human Brain Mapping, Virgo, N. (2011). Thermodynamics and the structure of living 31, 1408–1417. systems. D.Phil. Dissertation, University of Sussex, Thompson, E. (2007). Look again: Phenomenology and men- Brighton, UK. tal imagery. Phenomenology and the Cognitive Sciences, 6, Weber, A., & Varela, F. J. (2002). Life after Kant: Natural 137–170. purposes and the autopoietic foundations of biological Thompson, E., Lutz, A., & Cosmelli, D. (2005). Neuropheno- individuality. Phenomenology and the Cognitive Sciences, menology: An introduction for neurophilosophers. In A. 1, 97–125. Brook & K. Akins (Eds.), Cognition and the brain: The phi- Williams, M. A., Baker, C. I., Op de Beeck, H. P., Shim, W. losophy and neuroscience movement (pp. 40–97). New York, M., Dang, S., Triantafyllou, C., & Kanwisher, N. (2008). NY: Cambridge University Press. Feedback of visual object information to foveal retinoto- Turing, A. M. (1952). The chemical basis of morphogenesis. pic cortex. Nature Neuroscience, 11(12), 1439–1445. Philosophical Transactions of the Royal Society B: Biologi- Wilson, H. R. (1999). Spikes, decisions and actions: The dyna- cal Sciences, 237(641), 37–42. mical foundations of neuroscience. New York, NY: Oxford Van Horn, S. C., Erisxir, A., & Sherman, S. M. (2000). Relative University Press. distribution of synapses in the A-laminae of the lateral gen- Wilson, H. R., & Cowan, J. D. (1973). A mathematical theory iculate nucleus of the cat. The Journal of Comparative Neu- of the functional dynamics of cortical and thalamic ner- rology, 416, 509–520. vous tissue. Kybernetik, 13, 55–80. Varela, F. J. (1991). Organism: A meshwork of selfless selves. Wilson, S. W. (1983). On the retino-cortical mapping. Interna- In A. I. Tauber (Ed.), Organism and the origins of self (pp. tional Journal of Man-Machine Studies, 18, 361–389. 79–107). Dordrecht, Netherlands: Kluwer Academic Winkelman, M. (2002). Shamanism and cognitive evolution. Publishers. Cambridge Archaeological Journal, 12(1), 71–101. Varela, F. J. (1996). Neurophenomenology: A methodologi- cal remedy for the hard problem. Journal of Consciousness Studies, 3(4), 330–349.

About the Authors To m F r o e s e received an MEng in computer science and cybernetics from the University of Reading, UK (2004). He then obtained a DPhil. in cognitive science from the University of Sussex, UK (2010). He was a postdoctoral research fellow at the neurodynamics and con- sciousness laboratory of the Sackler centre for consciousness science, University of Sussex, UK (2010). Froese then became a JSPS postdoctoral fellow at the Ikegami laboratory of the department of general systems studies, University of Tokyo, Japan (2010–2012). Currently, he is a postdoctoral researcher at the self-organizing systems laboratory of the Instituto de Investigaciones en Matema´ticas Aplicadas y en Sistemas, Universidad Nacional Auto´noma de Me´xico, Mexico (2012–2013). His research is focused on developing enactive approaches to understanding the biology, phenomenology, and dynamics of life, mind, and sociality.

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 labora- tory 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. 214 Adaptive Behavior 21(3)

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 con- ference in Winchester, UK. He is also a member of the editorial boards of Artificial Life, Adaptive Behavior and BioSystems.