Original Paper

Turing instabilities in biology, culture,

and consciousness? On the enactive
origins of symbolic material culture

Adaptive Behavior
21(3) 199214
The Author(s) 2013
Reprints and permissions:
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DOI: 10.1177/1059712313483145
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Tom Froese1,2,3, 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 hallucinations has been explained by appealing to humanitys 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 neurophenomenology, 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
Forms of artistic expression, rituals, and language are
universal features of all known human cultures. While
animal behavior is mostly governed by immediate environmental demands and the meaning of animal communication is generally fixed by biological evolution,
human symbolic practices and their meanings are the
historical outcome of a seemingly open-ended social
process of cultural evolution. Explaining the origin of
such symbolic practices in terms of our biological
embodiment and the social circumstances of our prehistoric past is one of the major outstanding challenges of
science. Indeed, the origin of symbolic representation
concerns the origin of the human condition as such,
hence the idea of modern humans as the symbolic
species (Deacon, 1997) or Homo symbolicus
(Henshilwood & dErrico, 2011b). This is an issue that
reaches across the great divide between the natural and
social sciences, and has implications beyond the remit
of science itself.
The enactive approach to cognitive science is in a
good position to advance the debate about the origins
of the earliest symbolic practices. Whereas traditional
cognitive science presupposes the existence of an internal symbol system as its basic starting point (Newell

& Simon, 1976), the enactive approach instead starts

with the biologically embodied mind, and must therefore address the cognitive gap between adaptive
behavior and abstract human cognition (De Jaegher &
Froese, 2009; Froese & Di Paolo, 2009). Thus, rather
than simply assuming the notion of representation as
its most basic conceptual foundation for explaining the
internal mechanisms of human cognition, it tries to
understand the biological, social, and historical origins
of the phenomenon of symbolic representation as an
aspect of our cultural environment. This approach
helps to avoid a lot of the unnecessary linguistic and
theoretical confusion, which has plagued cognitive science for many years (Harvey, 2008). And it also helps
1

Ikegami Laboratory, Department of General Systems Studies, Graduate

School of Arts and Sciences, University of Tokyo, Tokyo, Japan
2
Instituto de Investigaciones en Matematicas Aplicadas y en Sistemas
(IIMAS), Universidad Nacional Autonoma de Mexico (UNAM), Mexico
3
Centro de Ciencias de la Complejidad (C3), Universidad Nacional
Autonoma de Mexico (UNAM), Mexico
Corresponding author:
Departamento de Ciencias de la Computacion, Instituto de
Investigaciones en Matematicas Aplicadas y en Sistemas (IIMAS),
Universidad Nacional Autonoma de Mexico (UNAM), Apdo. 20-726,
01000 Mexico D.F., Mexico.
Email: t.froese@gmail.com

200
to bring to light some unresolved foundational issues.
The question therefore becomes how primary adaptive
processes of sense-making of the here and now could
have been transformed into secondary forms of symbolic sense-making of the absent and the imaginary
(Froese, 2012).
Enactive accounts of this profound qualitative transition are still in their infancy, but there is broad agreement that there is no one single biological or social
explanatory factor. We are dealing with a historical
process emerging from the interaction between biological processes, social practices, and the cultural background (Froese, in press; Hutchins, 2010; McGann,
2007; Stewart, 2010). The development of an account
that theoretically bridges the cognitive gap therefore
promises to simultaneously provide an interdisciplinary
bridge between the natural and social sciences.
Furthermore, because the interaction between cultural
processes and biological embodiment is mediated at the
personal level through lived experience, this scientific
integration is not limited to objective processes, but
also includes phenomenology of the first-person perspective. Cognitive science thereby becomes an
anthropologically informed cultural neurophenomenology (Laughlin & Throop, 2009). The aim of this
paper is to contribute to this enactive approach to the
various interplays between biology, culture, and consciousness, in particular by critically examining the role
of altered states of consciousness in the generation of
geometric prehistoric art.

1.1 Overview of the paper

We first take a closer look at the one of the most prominent theories of the origin of prehistoric art and highlight its main shortcomings. The prevalence of certain
geometric patterns in the symbolic material culture of
many prehistoric cultures, starting shortly after the
emergence of our biological species and continuing in
some indigenous cultures until today, is explained in
terms of the characteristic contents of biologically
determined hallucinatory experiences. However, we
argue that the correlation between the first artistic
motifs and typical hallucinatory experiences is not sufficient to serve as a full explanation. In particular, there
is a lack of consideration of the value associated with
altered states of consciousness, both in terms of phenomenology and function. What is it about these nonordinary visual patterns that made them more attractive
for artistic expression than most others of an almost
infinite set of possible patterns, both physical and imaginary?1 Given that humans appear to be in principle
capable of arbitrarily associating any kind of stimulus
with any kind of meaning, as epitomized by language as
an open-ended symbol system, there is a need to explain
the shared selective biases that are in evidence across
prehistoric cultures. In other words, we need to account

Adaptive Behavior 21(3)

for the cross-culturally shared value of these specific
kinds of geometric patterns.
We then evaluate current models of the neural basis
of geometric hallucinations, because basic neural processes are prime candidates for explaining this crosscultural selective bias. These models typically propose
to view the visual system as a potentially excitable
medium whose autonomous dynamics are unleashed by
disinhibiting altered states of consciousness. Essentially,
it is suggested that the disinhibited visual system generates spatiotemporal patterns of neural activity due to
Turing instabilities. Researchers also generally claim
that the geometric hallucinations experienced by the
subject are mental representations of these neural patterns. However, while these neural models are capable
of reproducing some of the geometric patterns that are
found in prehistoric art and non-ordinary visual experiences, their range remains severely limited. In addition,
the models tend to trivialize the relationship between
the structure of subpersonal neural processing and the
content of personal visual experience by assuming that
visual experience is a representation of inverse optics
applied to neural activity in region V1 of the visual nervous system.
We then propose an enactive approach to resolving
these issues. By drawing inspiration from the method
of neurophenomenology, we argue that the role of selfsustaining neural activity, which is closely associated
with neural Turing instabilities, has been underappreciated. According to an enactive approach, selfsustaining neural dynamics can generate their own
intrinsic value in relation to their conditions of selfmaintenance, and they can also serve as a neural
mechanism by which to decouple autonomous brain
activity from the influence of environmentally mediated
sensorimotor dynamics. Both of these aspects can help
to explain the aesthetic selective biases of the first artists, in particular their interest in inner experience as
exemplified by abstract hallucinations and imaginary
phenomena, which are not directly related to the
demands of their physical environment. We speculate
that the self-sustaining dynamics may account for why
these geometric hallucinations were experienced as
more significant than other phenomena, and that at the
same time their underlying neural dynamics may have
served to mediate and facilitate a form of imaginary
sense-making that is not bound to immediate
surroundings.

2 On the origins of the symbolic mind

Starting with Darwins (1871) evolutionary approach to
the origins of human language in terms of natural and
sexual selection, the date for the beginning of symbolic
thought and creative imagination has been continually
pushed back into prehistory. It was long assumed that

Froese et al.
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 culture (Henshilwood & dErrico, 2011a). These findings
were uncovered in Africa, and indicate the presence of
symbolic practices over 100,000 years ago, including
the manufacture of paint and body ornamentation. In
addition, and contrary to the idea that artistic expression began with primitive pictorial representations of
the external environment, there was a tradition of
engraving pieces of red ochre with a variety of abstract
geometric patterns (Henshilwood, dErrico, & Watts,
2009). An example is shown in Figure 1.
This discovery connects well with the ethnographical
observation that geometric visual patterns have been
playing an important role in prehistoric cultures from
around the world (Froese, in press). Interestingly, these
patterns represent only a small subset of the potentially
infinite set of possible abstract visual patterns that
could be created, and it seems that certain kinds of pattern are particularly frequent, such as dots, circles,
cross-hatchings, parallel wavy lines, and especially various kinds of spirals (Lewis-Williams & Dowson, 1988).
An important clue to the origin of this selective bias
was found by psychologists investigating the experiential effects of various kinds of alterations of consciousness. They discovered that the patterns of many visual
hallucinations could be categorized into a small number of so-called form constants (Kluver, 1967). In the
1920s, Kluver had systematically studied the effects of
mescaline (the main psychoactive compound of the
peyote cactus, Lophophora williamsii) on the experience
of its users (including on himself). He observed that the
non-ordinary visual experiences were often characterized by similar kinds of abstract geometric patterns,
which he classified into four categories of form constants: (1) gratings, lattices,2 fretworks, filigrees, honeycombs, and checkerboards; (2) cobwebs; (3) tunnels
and funnels, alleys, cones, vessels; and (4) spirals.
Kluvers form constants have since been found to
occur in a variety of other kinds of altered states
(Bressloff, Cowan, Golubitsky, Thomas, & Wiener,
2001). Intriguingly, these form constants turned out
to resemble many of the abstract motifs that are often
associated with prehistoric art from around the
world, including Paleolithic cave art in Europe. These
insights led to the provocative hypothesis that much
of the content of prehistoric art was inspired by patterns and visions seen during altered states of consciousness (e.g., Clottes & Lewis-Williams, 1998;
Lewis-Williams, 2002; Lewis-Williams & Dowson,
1988; Winkelman, 2002).

201

Figure 1. Illustration of a piece of red ochre with abstract

geometric incisions that were made on one side around
73,000 years ago. This piece was found during excavations in
Blombos Cave, South Africa. This and similar pieces from the
same location are currently the oldest known human expression
of abstract geometric patterns. Reproduced with kind
permission from Elsevier (Henshilwood et al., 2009).

Of course, it still remains to be explained why these

particular motifs were highly regarded by the artists
and how these people became artists capable of symbolic expression in the first place. According to LewisWilliams (2002), the symbolic capacity was already provided by the evolution of an appropriate mutation in
the brain, and the value of the particular content was
derived from the hierarchical power structures enforced
by shamans who had exclusive access to the visionary
experiences. However, this hypothesis has several shortcomings. While complex social stratification and strife
was clearly in evidence during the Neolithic period in
Europe (Lewis-Williams & Pearce, 2005), this kind of
social class conflict may not be generalizable to earlier
periods or other parts of the world.
For instance, the Jomon culture of prehistoric
Japan, one of the oldest pottery traditions in the world
dating back to around 16,500 BC, was the first culture
in the Japanese archipelago to produce pottery decorated with abstract geometric patterns. This symbolic
material culture flourished for well over 10,000 years,
producing large quantities of pieces with recognizable
form constants (e.g., Figure 2). However, compared to
later symbolic material cultures in this region, the
Jomon period is remarkable for its long-term stability,
and because of the absence of strong archaeological
evidence for a complex social hierarchy, social strife,
and intergroup warfare (Habu, 2004).
The hypothesis that the first symbolic practices were
an outcome of a prehistoric class struggle is lacking
solid archaeological evidence. More importantly, even
if we could find an early prehistoric society that fits
Lewis-Williams hypothesis, the existence of a rigid
social hierarchy and restricted accessibility of altered
states of consciousness by an elite class does not explain
why such altered states were highly valued by these
people in the first place. If the ritualized alteration of
consciousness and its symbolic expressions were to be a
tool of empowerment restricted to the elite, then the
general population must have already valued such

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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 reactiondiffusion 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 investigate 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 Kluvers 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

Figure 2. A deep pot covered with various spiral patterns; an

early artistic example of the spiral type of Kluvers form
constants. This particular style of vessel, known as Moroiso, was
made around 4000 BC by people of the Jomon culture
(Kobayashi, 2004, p. 31), a relatively peaceful and non-stratified
society of prehistoric Japan (Habu, 2004). (Photo taken by Tom
Froese at the Archaeological Museum of Kokugakuin University,
Tokyo, Japan).

non-ordinary experiences; otherwise their restriction

could hardly have served as an instrument of control. In
addition, this hypothesis leaves any functional connection of altered states of consciousness to the origin of
symbolic practices, including their underlying neural
effects, unexplored. It seems plausible that, at least under
some circumstances, a temporary alteration of normal
sense-making can lead to heightened levels of imagination and creativity (Dobkin de Rios & Janiger, 2003).

3 Neural mechanisms
Turing patterns consist of various geometric forms,
including spots, traveling waves, grids, and spirals,
which emerge out of the distributed activity of nonlinear dynamical systems with local excitatory and
sparse inhibitory connectivity. Some illustrative examples derived from a simple GrayScott reaction
diffusion system are shown in Figure 3.
Simple spatiotemporal pattern formation was first
described by Turing (1952) for the case of chemical
reactiondiffusion systems. Turing proposed that these
kinds of systems could help to explain morphogenesis,
i.e., pattern formation during biological development.
Since then, Turing patterns have been found to be ubiquitous in a variety of biological systems (Goodwin,

One of the originally proposed mechanisms for geometric hallucinations is that of a neural Turing mechanism, embodied in the WilsonCowan equations (H. R.
Wilson & Cowan, 1973) and first mathematically analyzed in terms of visual hallucinations by Ermentrout
and Cowan (1979). This is the neural context for the
famous Turing Instability, which describes a reaction
diffusion process in which an ordered macroscopic
structure can emerge from local interactions under the
non-equilibrium state (Turing, 1952). Turings idea can
be readily transposed to the functioning of the nervous
system. For example, action potential propagation
along a neurons axon can be directly described by
reactiondiffusion equations, and reactiondiffusion
equations are analogical to the WilsonCowan neural
network equations (H. R. Wilson, 1999, pp. 267268).
We can think of the reaction component as the interactions between neuronal cells, and of the diffusion component as the spread of neural activity through local
synaptic connections. Similarly, the local structure of
neural interconnectivity dictates the type of emergent
phenomena that can be produced. Neural network
models of geometric hallucinations have gradually
incorporated these empirical insights from neural anatomy and physiology, including the spatial arrangement
of different neuronal cell types.
The first model of geometric hallucinations to follow
this idea, by Ermentrout and Cowan (1979), developed
an isotropically connected two-layer neural network of
excitatory and inhibitory neurons to represent the primary visual cortex (V1). Increasing an excitability parameter destabilized the rest state, bifurcating the system,
and led to macroscopic spatial patterns emerging due to
the lateral interactions of negative feedback. Such a
general description of a locally connected network
shows up the reactiondiffusion type properties of such
systems, but they require specificity in parameters in
order to generate patterns. The main limitation of this
early work is that they do not consider the neural

Froese et al.
architecture of V1: the arrangement of neurons in
hypercolumns and their properties as low-level feature
detectors. These are addressed in Bressloff et al.s
(2002) work, to be discussed later in this section.

3.2 The location of geometric hallucinations within

the brain
Where exactly in the brain do such geometric hallucinations emanate from? Also, is it correct to say that there
is a single region that constitutes the generation of a
visual pattern, knowing that the brain is a highly interconnected dynamical system? Considering that geometric hallucinations are unaffected by the physical
movement of the eyes means that such phenomena
must emanate from the endogenous activity of the
brain. Secondly, that we see such phenomena supports the assumption that they must be dependent on
the brains visual sub-system.
All models of geometric hallucinations propose that
such patterns emerge from V1, the first region of the
visual cortex to receive visual input. This assumption is
supported by fMRI scans that have shown that V1 is
sometimes activated during mental imagery, i.e., when
one imagines something visual in either an awake or
dreaming stateeven when they are not in an

203
externally coupled state (Miyashita, 1995), although
there is some variability in these results (Kosslyn &
Thompson, 2003). Other results have pointed to the
primary visual cortex interacting with the hippocampus
during offline episodic memory consolidation; highorder replay of episodic memories occurs with quite
specific patterns of visual activity in V1 (Ji & Wilson,
2007).
The visual cortex is located in the posterior region
of the brains occipital lobe. V1 takes information from
the Lateral Geniculate Nucleus (LGN), a region of the
thalamus, which in turn receives information from retinal ganglion cells that each receive information from
around 5100 photoreceptors. Anatomically, V1 is an
array of hypercolumns involved in the low-level processing of visual input, with feature detectors tuned to
visual aspects such as color, edges, contours, motion,
etc. (S. W. Wilson, 1983). Between regions, there is a
progressive mapping to 2D cortical surfaces and all of
the models to be discussed operate in such a dimension.
After V1, higher-order processing of visual information
occurs in roughly 30 identified regions within the visual
cortex (Miyashita, 1995).
But it is presumptive to speak of these brain processes happening in some sort of projective sequence.
For example, in cat brains it has been identified that

Figure 3. Examples of dynamic patterns exhibited by the GrayScott reactiondiffusion 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
retinal input accounts for about 7% of synaptic connections to relay cells in the LGN, therefore 93% of
input is non-retinal, coming from other regions in the
brain (Van Horn, Erisxir, & Sherman, 2000). It is certain
that similar physiology exists within the human visual
system and this shows that a great deal of dynamic
feedback processes must be occurring. Accordingly,
models that do not account for this massive feedback
have questionable biological plausibility.

3.3 The retinotopic map

In general, in current models of geometric hallucinations, an inverse retinotopic map is applied to neural
activity in V1 in order to virtually project back into
what would have been the causally responsible retinal
space under normal conditions. The resulting image is
intended to enable us to see what the subject would
visually experience. The retinotopic map describes how
retinal input projects onto the visual cortex. This physiological mapping has been studied extensively and, in
simplified terms, is a conformal projection from retinal
polar coordinates into cortical rectangular coordinates.
More space in V1 is assigned to the foveal region than
to the periphery and this is why our spatial detail is
highest at this focal point in our vision.
The reasoning principle underlying the application
of an inverse mapping to the neural network models is
that under normal awake conditions, when a subject is
observing the external world, an undistorted view of
the world enters the retina and then, for physiological
reasons, gets distortedly mapped to V1. However, we
never consciously experience this distorted view of V1.
Therefore, it is argued, there must be some subsequent
inverting process such that, in some manner, phenomena generated in V1 are actually experienced in terms

Adaptive Behavior 21(3)

of the original retinal frame of reference. This reasoning has important implications for explaining geometric
visual hallucinations. For example, taking a uniformly
textured image (in V1) and going from rectangular
(cortical) to polar (retinal) coordinates can generate a
tunnel like warping of the image. This is an effect common in many geometric hallucinations and perhaps
also related to the tunnel seen in near death experiences
(Blackmore & Troscianko, 1989).
However, the tunnel like warping effect of the
inverse retinotopic mapping is not always fitting. For
example, to accommodate lattice type phenomena that
do not have a clear center of origin or convergence,
Ermentrout and Cowan (1979) state that these must
occur at the periphery of the visual field. On the other
hand, a cobweb with a clearly defined center is said to
appear nearer the fovea (see Figure 4 for illustrative
examples of these distinct kinds of form constants).
But this seems a rather odd prediction. If this model
is indeed biologically accurate then a large number of
geometric patterns that do not exhibit a tunnel-like
appearance should be constrained to only appearing at
the periphery of our visual experience. As far as we
know, the extant psychological literature does not make
any mention of a strict division between such focal and
peripheral types of hallucinatory visual patterns. Thus,
although this is a prediction that still deserves to be further investigated experimentally, it is more likely an
indication that the relationship between the retinotopic
mapping and geometric hallucinations is less direct than
originally assumed by Ermentrout and Cowan.
Another shortcoming of using inverse retinotopic
mapping to derive an image of the subjects experience
is that it lacks consideration of the temporal dimension
of consciousness (Varela, 1999). Empirical research
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.
only becomes consciously experienced in the form of
geometric hallucinations after more extensive recurrent
processing (e.g., P. C. J. Taylor, Walsh, & Eimer, 2010),
thus again implying a more indirect mapping between
activity in V1 and conscious visual experience. More
generally, we can also take issue with the phenomenology of mental imagery that is implied by the idea of
deriving the subjects experience from a neural image.
Under closer phenomenological examination, the experience of mental imagery is qualitatively different from
the experience of seeing a 2D picture (Thompson, 2007).

3.4 The ubiquity of spiral and wave dynamics in the

brain
As stated earlier, most models assume that hallucinatory phenomena are produced in V1 and then pursue a
description of their neural underpinnings. But spiral
and wave (circular wavefront) dynamics seem to be a
ubiquitous feature of brains, not just in V1, and also of
biologically realistic neural models. Huang et al. (2010)
state that spiral waves which emanate from a central
point, as an emergent property, can organize and modulate cortical population activity on the mesoscopic scale
and may contribute to both normal cortical processing
and to pathological patterns of activity, e.g., epilepsy.
Such wave activity is found to be robust when considered within local excitatory interactions such as within a
cortical sheet (a locally connected 2D network). But the
brain has modulatory long-range connections that can
change the properties of local sub-networks that could
serve as regulatory protective mechanisms.
For example, Rulkov, Timofeev, and Bazhenov
(2004) developed a set of computationally efficient yet
highly realistic map-based neuron models to explore
large-scale cortical networks and their dynamics. In
particular, the spiking activity in different types of cortical pyramidal (PY) (fast spiking, regular spiking,
intrinsically bursting) and interneurons (INs) was developed. Experiments showed that wave properties were
dictated by coupling parameters and that self-sustained
dynamics were a function dependent on synaptic interaction between neurons, and not spontaneously firing
cells. These findings support the idea of neural architecture being an important factor for the emergence of
geometric patterns that are potentially experienced as
hallucinations. That spontaneous waves of activity
could persist within the network indefinitely is also
interesting with respect to the ideas of self-sustainability
during externally decoupled mental states, maintaining
network wide activity to prevent neuronal atrophy from
disuse, or the brains default networkwhere selfsustained dynamics allows the brain to be in a primed,
high-dimensional state.
Fohlmeister, Gerstner, Ritz, and van Hemmen
(1995) investigated the type of spontaneous excitations

205
that can emerge from a realistic non-linear model of a
cortical sheet of noisy spiking neurons. Their model
included a drug parameter and they found that under a
normal state of activity there was incoherent lowfrequency firing. As they increased the excitation of the
network, beginning from random initial conditions,
they categorized the following emergent properties: (1)
stripes, (2) spiralsfound to be very stable, (3) rings,
and (4) collective bursts. Collectively these were termed
first stage imagery, corresponding to the idea of form
constants. Second stage imagery, which goes beyond
geometric hallucinations to include complex imagery,
without any doubt involves several other areas of the
brain, including memory systems (de Araujo et al.,
2012), and was not modeled. Interestingly, once spirals
exist within the modeled neural system they cannot be
extinguished, even if the drug parameter is adjusted
into the ranges to support categories 3 and 4. We note
that this kind of hysteresis can be useful during normal
brain functioning. Summarily, they consider form constants to be elementary excitations in the primary visual
cortex and these spatiotemporal patterns involve the
same kind of mechanism as in experimentally observed
drug induced epilepsy (we will return to epilepsy
below).
Milton, Chu, and Cowan (1993) developed similar
work for generating spirals from a fixed excitation center that mimic cardiac arrhythmia. This also demonstrates how changes in neural parameters generate quite
varied macroscopic phenomena despite having a consistent local connectivity. In general, however, these models do not generate all four categories of form constant.
And despite some authors claiming that the performance of a large network does not depend on details of
the model once the neural essentials have been incorporated (Fohlmeister et al., 1995), other models indicate
that more of the characteristic form constants could be
produced if the exact structure of V1 was considered.

3.5 Modeling geometric hallucinations as a function

of V1 neural architecture
Bressloff et al. (2001, 2002) developed a model that
aimed to connect geometric visual hallucinations with
the structure of V1. It is well known that V1 consists of
a number of neural circuits that are involved in lowlevel image processing, responding preferentially to
features such as oriented edges and local contours, etc.
Their work proposes that the specific spatial arrangement and local coupling of these feature detectors,
along with the neural Turing mechanism combine to
generate form constants. According to their model,
under normal conditions the visual system is in a stable
state, but the introduction of drugs destabilizes V1 and
spontaneously generates cortical activity that reflects
the underlying architecture of V1. The possible form

206
constants of this model are specific linear combinations
of the eigenfunctions of the neural architecture, called
Planforms, which possess both spatial and temporal
properties. Since V1 must avoid falling into these states
during normal visual processing, if the influences of the
retinal input are to have any effect in driving the system, this places strong constraints on the evolution of
the visual cortex architecture, for example in terms of
the sparsity of long-range inhibitory connectivity
(Butler et al., 2012).
Bressloff et al.s work represents perhaps the most
complete description of a neural mechanism for generating geometric hallucinations, however, it is not capable of generating all of Kluvers form constants and
does not seem to account for the ubiquitous spiral wave
dynamics of the brain, which are realized by the neural
dynamics in a model such as Folhmeister et al.s. To
address this, it would be interesting to incorporate a
more biologically plausible, spiking neural model.
Secondly, the authors only considered oriented edges
and local contours in their architecture; what generative power would the modeling of other feature maps,
such as spatial frequency, binocular disparity, motion,
and color provide?
Furthermore, none of the models seems to account
for the entirety of geometric hallucinations that are
commonly reported in the archeological and anthropological literature, for example as described by LewisWilliams and colleagues (Lewis-Williams & Dowson,
1988). Future work along the lines of Bressloff et al.s
model may someday show that the intrinsic properties
of V1 are enough to describe all geometric hallucinatory phenomena, but given the large variety of patterns, this is unlikely. It is interesting to consider what
other brain mechanisms could contribute to their formation, such as the large number of feedback pathways
that exist within the visual system.3

3.6 The role of neural feedback in visual processing

Complex and varied experimental results on the function of feedback pathways have been found, but it is
generally considered that higher-level cortical regions
are involved in large-scale perceptual integration which
combine with the fine-scale resolution provided by the
earlier visual regions (Sillito, Cudeiro, & Jones, 2006).
Feedback is involved in modulating perception; such as
figure ground separation, suppressing areas of low
information to generate a sparse codification of the
visual signal, coordination and tuning of visual feature
detectors, and attention (Williams et al., 2008). Backprojecting pathways are therefore thought to facilitate,
inhibit, and synchronize neural activity (Przybyszewski,
1998). Under the influence of drugs, or in an altered
state of mind induced by other means, these pathways
could all be involved in moving the visual system

Adaptive Behavior 21(3)

toward one of the stable Planforms as proposed in
Bressloffs model.
Secondly and more generally, we know that V1 and
other regions of the visual pathway show neural activity
during imagination (Ganis, Thompson, & Kosslyn,
2005), which shows that they can be integrated into
higher-level processing in the absence of external input.
Could a feedback loop between these brain areas generate geometric hallucinations? This is much like the idea
of a video-feedback system, where a video camera is
positioned to record the same video monitor to which it
is connected (Crutchfield, 1984, 1988). Despite a video
feedback system being physically different, a conceptual
analogy can be formed by making firstly a connection
between the neural Turing mechanism and modeling
the video-feedback as a reactiondiffusion system
(Crutchfield, 1988), and secondly with the known abundance of feedback pathways within the brain. The large
number of geometric patterns that can be produced by
such physical video feedback systems, such as logarithmic spirals and phyllotaxis, lends some credence to this
novel hypothesis.
However, what could constitute a neural visual feedback mechanism for geometric hallucinations is still
unknown. It seems plausible that somehow the abundance of feedback loops could play this role, especially
when considering that at some point, during an altered
state of mind, geometric hallucinations may be combined, modulated by, and reinterpreted with hallucinations from memory and iconic imagery that must be
generated elsewhere within the cerebral cortex (de
Araujo et al., 2012).
Another pathway that could be involved is through
the superior colliculus (SC)a major region of the vertebrate midbrain that forms an important part of the
visual system, and which is considered to play a critical
role in the development of blind sight (Takaura,
Yoshida, & Isa, 2011). The mutual interaction between
the primary visual cortex and this subcortical neural
structure, which is also involved in visual processing,
could open new possibilities for explaining geometric
hallucinations in the absence of external visual stimuli.
In addition, the SCs role in multisensory integration
(Hall & Moschovakis, 2004) might help to explain how
visual hallucinations become integrated with hallucinations in other modalities, including synesthesia-like
effects.

3.7 Beyond structural isomorphism

This overview of the putative neural mechanisms
underlying geometric hallucinations points to the key
components being the architecture in V1 supporting a
neural Turing mechanism along with the retinotopic
mapping, the ubiquity of spiral and wave dynamics
within the brain, and widespread and long-ranging
feedback connections. But despite these insights, the

Froese et al.
full range of reported geometric hallucinations has yet
to be accommodated by a single mathematical neural
network model. The incorporation of additional physiological detail may increase the range of geometric
phenomena that can be modeled, especially long-range
feedback connectivity. We must consider the neural
projections into and out of V1, such as its direct connection back to the LGN, to the other 30 or so visual
processing regions, and the rest of the brain.
Visual hallucinations can be induced in a wide number of ways, but all models make use of a single drug
parameter that affects the entire system. Yet how does
the experienced pattern differ depending on the route
taken to such a state of mind? Dietrich (2003) proposes
that most altered states of mind (drug induced or otherwise) involve a transient decrease in prefrontal cortex
activity, and that the difference between types of experience arises from how the induction method affects the
various prefrontal neural circuits. Connecting this function to models of geometric hallucinations and to the
types of patterns specific to certain altered states could
make for some interesting predictions. We can also
wonder at what type of widespread effects the prefrontal cortex can have on the whole visual cortex and the
rest of the brain, not just in V1.
It also remains to be seen whether Turing instabilities in the rest of the brain, including the peripheral
nervous system, play a role in generating geometric hallucinations. Indeed, because of the generality of this
dynamical phenomenon, its potential role may not be
limited to electrical interactions between neurons,
either. We know that Turing patterns are crucial for a
number of other biological processes, including in the
chemical domain (Goodwin, 2001). Therefore, more
realistic models of geometric hallucinations might want
to include details of the physical and chemical processes of the central and peripheral nervous system,
e.g., reaction and diffusion of various neurotransmitters, vitreous liquids inside the eye, oily residues on the
surface of the cornea, etc., which could give rise to
Turing patterns under disinhibited conditions, and thus
influence the outcome of visual processing. As a simple
proof of concept, it has been shown that the dynamics
of a GrayScott reactiondiffusion system (see patterns
in Figure 3) can be used in order to control a mobile
robot, giving rise to shape discrimination and memory
(Dale & Husbands, 2010).
But as we incorporate these additional features into
the models, it may also turn out that the hypothesis of
a strict structural isomorphism between patterns of
neural activity in V1 and geometric hallucinations will
become less tenable. As a case in point, the function of
the inverse retinotopic map can be called into question
when considering that it implies that many of the
reported geometric hallucinations have to appear extrafoveally. Accordingly, rather than looking for a direct
one-to-one structural mapping between patterns of

207
neural activity and patterns of hallucinatory experience, it may be more productive to consider other functionally relevant properties of such neural patterns
than their precise spatiotemporal arrangement alone.
For example, all modeled neural patterns show
properties of robustness and self-sustainability. In the
models of Ermentrout and Cowan (1979) and Bressloff
et al. (2001), patterns appear as the stable configurations of the system after bifurcating from a low activity
state. The neural model of Rulkov et al. (2004) displays
self-sustained wave dynamics that can spontaneously
emerge from low-level random neural activity. As
already mentioned, in the model of Fohlmeister et al.
(1995), once spiral waves emerge they cannot be
destroyed, even when increasing a drug parameter into
the range where other geometric phenomena usually
appear. This case of apparent irreversibility is probably
the strongest example of robustness and selfsustainability in the surveyed models, and it is suggestive as a biological explanation for the fact that spirals
are one of the most prevalent motives in prehistoric
art.
How could this property of robust self-maintenance
relate to the hallucinatory experiences? A striking feature that differentiates geometric hallucinations from
other visual experiences is that they are generated
intrinsically when the subject has been decoupled from
its environment. The patterns form irrespective of our
lifetime learned memories. Indeed, they could be considered internally directed perceptual experiences, since
if the proposed models hold true, they are directly
formed from the actual biological structure of the
visual system. We are said to have a strange subjective
experience of looking into oneself, where the patterns
we see directly expose the underlying operation of our
brains. At the same time, the robustness of the underlying neural patterns also reinforces this decoupling from
the environment. In the next section, we argue that
under some conditions such a neural mechanism of
decoupling could be adaptive. Humans are adept at not
only understanding patterns from external sensory
input, but importantly, we have a powerful faculty for
active generationbe it for purposes such as prediction, imagination or playing.

4 Steps toward a new approach to the

origins of symbolic material culture
One promising approach for systematically evaluating
the relationship between brain functioning and human
experience is known as neurophenomenology, a method
that was proposed by Varela (1996) as part of the enactive approach, and which has subsequently been elaborated by others (e.g., Petitmengin, Navarro, & Le Van
Quyen, 2007; Thompson, Lutz, & Cosmelli, 2005). The
basic idea of neurophenomenology is to relate the

208
empirical data of neuroscience and verbal descriptions
of first-person experience in a mutually informing and
enriching manner. In this way both third-person and
first-person aspects of a phenomenon are taken into
account, but without privileging one domain over the
other. While the aim is to find a formal model at which
the dynamics of the two domains can be integrated, this
does not entail a necessity of structural isomorphism.
Instead, there is a mutual braiding of structural constraints, which links the activity of the two domains
into one unfolding process (Varela, 1999).
In addition, because perception is conceived of as a
relational process of sense-making that is extended over
the entire brainbodyenvironment as a whole, the
externalinternal distinction becomes relativized (Lenay
& Steiner, 2010). That is, the perceptual experience of
an environment as being external is itself an outcome of
sense-making, and therefore becomes potentially reversible and dissolvable as the conditions of sense-making
are modified under unusual conditions. In the case of
geometric hallucinations, it could therefore be that we
are in fact dealing with an abnormally oriented perceptual process, where the object of perception is an aspect
of the nervous system itself. This is surely a strange
hypothesis, but the consideration of perceptual mediation opens up a new perspective on the problem of the
mismatch between the impoverished neural patterns
and the rich geometric experiences. A similar mismatch
has been observed to hold between the impoverished
retinal input and our rich visual experience of the world
(Noe, 2002). Accordingly, on this alternative view, the
main shortcoming of the current neural network models
is not an insufficiently detailed structural isomorphism,
but rather a failure to take the enriching effects of
sense-making into account.4

4.1 Neurophenomenology of value

How might neurophenomenology address the correspondence between spatial patterns in the cultural,
experiential and neurobiological domains? The first
thing to note is that the artistic patterns under consideration form an extremely limited set compared to the
total set of all possible patterns that could have been
created. This universal selection bias is something that
must be explained, but which has so far remained mysterious. It is not sufficient to note the correlation with
visual experiences during altered states of consciousness. Even if we accept that internally oriented visual
perception is possible during altered states of consciousness, this does not in itself explain why those perceptual
experiences are more frequently expressed artistically.
Why should these particular patterns be preferred over
other kinds of ordinary and non-ordinary visual experiences? This selective bias must therefore be accounted
for in terms of the value these patterns have had for the
artists who made them.

Adaptive Behavior 21(3)

This consideration places a significant constraint on
our explanation from the side of cultural practices,
because the artists must have valued their altered visual
experiences. Some researchers have tried to address this
constraint by appealing to social practices. For example, Lewis-Williams (2002) argued that the value of the
experiences derives from their value as a tool to enforce
social hierarchies by restricting access to elite individuals via prohibition. But this only shifts the original
problem without resolving it, because we must then
explain why people would value these experiences as
worthy of restriction to elites.
One promising alternative is to assume that when
these visual patterns are seen during altered states of
consciousness they are directly experienced as highly
charged with significance. In other words, the patterns
are directly perceived as somehow meaningful and
thereby offer themselves as salient motifs for use in
rituals. This possibility seems to accord with verbal
reports about the range of emotional effects that can be
elicited by a variety of non-ordinary experiences (e.g.,
Dobkin de Rios & Janiger, 2003; Huxley, 1956;
Shanon, 2002; Strassman, 2001). This appeal to an
intrinsic value places constraints on the underlying
neural dynamics. We therefore need to discuss how
value could be realized in neurobiology, and then we
determine whether this neurological mechanism is compatible with the neurological mechanism underlying the
experience of the most common forms of geometric
phenomena.

4.2 Sketches of an enactive neurobiological account

of value
In the history of cognitive science, the question of value
has been a profoundly puzzling one. The computational theory of mind holds that cognition is rule-based
manipulation of abstract symbols, as epitomized by the
digital computer program. However, this logical syntax
leaves the concrete meaning of the symbols unaccounted for; they are simply empty placeholders. This
problem of meaning has resulted in major stumbling
blocks in theory of mind, as well as in the practice of
AI and robotics, such as the symbol grounding problem and the frame problem. The enactive critique of
these theoretical and practical problems is centered on
the grounding of value in the self-maintenance of
autonomous forms of biological organization (for a
review, see Froese & Ziemke, 2009).
Most importantly, the enactive approach tries to
provide a viable alternative by defining value in operational terms. A good starting point is the work by Di
Paolo, Rohde and De Jaegher (2010, p. 48): We propose to define value as the extent to which a situation
affects the viability of a self-sustaining and precarious
network of processes that generates an identity. There

Froese et al.
are a number of entangled concepts implicated in this
definition, which cannot be unpacked in detail here.
We briefly summarize the main ideas. To start with,
the networks identity is not a reified entity; it can be
defined as operational closure, i.e., the mutual dependence of the processes of the network on each other for
their existence. This co-dependence provides them with
an internal relationship that integrates them with each
other and that does not depend on a unifying distinction by an external observer. And this co-dependence
also makes the networks identity precarious, since its
existence is not externally guaranteed but must be selfsustained by its own ongoing activity. In other words,
the network is only viable within certain boundary conditions. The value of an event is therefore defined
in relation to its impact on these conditions, i.e.,
whether it contributes to the self-sustaining of the identity or not.
The paradigmatic example of this kind of valuegenerating system is the minimal living system (Weber
& Varela, 2002). But the same kind of organization can
also be found in the nervous system, where we have the
temporary emergence of cell assemblies (Varela,
Lachaux, Rodriguez, & Martinerie, 2001). The firing
patterns of some neurons (or of collections of neurons)
can become entrained with each other, thereby constituting a precarious, self-sustaining network of processes, which in this case is a neurocognitive identity
(Varela, 1997). This kind of neural pattern is therefore
a suitable candidate for a process of value-generation.
Now if we consider the models of the neural mechanisms underlying some of the common geometric hallucinations, we also find the same kind of self-sustaining
cell assembly. Moreover, it is likely that the assemblys
robustness is enhanced considerably, because activity in
the visual brain regions during altered states is generally
assumed to be disinhibited. In addition, under these
conditions the sensory input from external events no
longer has the power to modulate the cell assemblys
boundary conditions, thus enhancing its viability. In
the most extreme cases, this kind of autonomous, selfsustaining network can manifest itself in a complete loss
of sensorimotor interaction. For example, it has long
been known that seeing flickering light at certain frequencies can induce neural entrainment and geometrical hallucinations (for recent work in this area, see, e.g.,
Billock & Tsou, 2007), but when the brain as a whole
becomes too entrained with those frequencies it can
cause an epileptic fit. According to the enactive account
of value, we would expect these kinds of geometric
experiences to be experienced as significant, and the
non-ordinary experiences encountered before or during
epileptic fits as intensely meaningful.5
Verbal reports of people with epilepsy confirm this
hypothesis. Sometimes the seizures leave people unconscious, but when they do have experiences during the
prodromal phase and at the onset of the epileptic fit

209
they are complex in many ways (Le Van Quyen, 2010;
Petitmengin et al., 2007). What is particularly remarkable is the reported vividness or intensity of these
experiences. The content of the experiences depends on
the person and the precise brain region of the epileptic
discharge, but commonalities can be identified.
Consider, for example the case of emotional experience:
Special emotional auras consist of an attack of anguish
and terror that suddenly takes over the consciousness with
such intensity that the subject has the impression she or he
is losing control of the situation, which will have a terrible
end, perhaps madness or even death. In other emotional
auras, the experience consists of a sudden state of joy with
no apparent cause, and it takes over the consciousness
passively for a few short moments, filling it with awe and
strangeness. (Le Van Quyen, 2010, pp. 247248)

Clearly, neurophenomenology is currently not

advanced enough to explain the particular content of
these experiences, but it does successfully explain why
the experiences are characterized by such an intensely
felt significance. Generalizing this insight to the experiences of geometric hallucinations, we can predict that
these, too, are felt with an increased intensity of significance, as long as self-sustaining processes of neural
activity generate them. In other words, intrinsic value is
built into the experience of some altered states of consciousness from the start. The ambivalence of the nonordinary experiences reported by Le Van Quyen, i.e.,
whether they are experienced as good or bad, is not
specific to altered states of consciousness induced by
epilepsy, but is characteristic of altered states more generally (Huxley, 1956). Perhaps this inherent polarity of
consciousness alteration, which Huxley famously contrasted as scenarios of heaven and hell, has to do
with the fact that the organism is a whole meshwork of
self-sustaining processes (Varela, 1991), and the intrinsic value of a specific self-sustaining neural process has
to be balanced against the needs of the other selfsustaining processes of the organism as a whole.

4.3 Ideas for an enactive neurobiological account

of imagination
The problem of explaining the origins of the human
imagination is related to the transformation of basic
sense-making of the here and now to the enaction of
the absent and imaginary (Froese, 2012). We speculate
that one manner of realizing this transformation is to
mediate the organisms sensorimotor interactions in
such a way that the autonomous dynamics of the nervous system temporarily become decoupled from the
environment. Abstract forms of cognition are likely to
be facilitated during such highly introverted states of
consciousness, which would also help to explain their
prehistoric origin.

210
As we have already indicated, a basic dynamic
neural mechanism for realizing a temporary mode of
environmental decoupling can be derived from the existence of self-sustaining processes of neural activity.
These neural processes might not always be easily identifiable in terms of spatial patterns, especially when we
are considering parts of the nervous system that do not
exhibit such a regular spatial embedding as the retina
or V1.6 Nevertheless, it is helpful to think of these
neural processes in terms of an analogy with chemical
reactiondiffusion systems, which are formally closely
related to the activationinhibition models of the visual
system (H. R. Wilson, 1999, pp. 267268). Chemical
reactiondiffusion systems are a well-researched area,
both formally and empirically, and therefore provide a
useful source of inspiration. For example, it has been
demonstrated that chemical Turing patterns, and especially spiral patterns, are highly robust against the influence of external perturbations such as attacks by
parasitic chemical species (Boerlijst & Hogeweg, 1991).
Accordingly, it seems plausible that the disinhibition of
the visual cortex during altered states, perhaps via topdown projections from prefrontal cortex to the pathway
from retina to V1 regions, could lead to Turing patterns
of neural activity in V1 that are robust against perturbations from visual sensory input, thereby effectively shutting down external visual influence (Butler et al., 2012).
The analogy with chemical reactiondiffusion systems also suggests that some of these neural Turing patterns may even exhibit their own self-individuated
spatiotemporal identity, as well as the ability to engage
in adaptive interactions with other emergent processes
and structures. These kinds of emergent behaviors have
been demonstrated to occur in chemical reaction
diffusion systems, including self-moving droplets with
tail structures (Froese, Virgo, & Ikegami, in press). It is
therefore tempting to speculate that some neural Turing
patterns can adapt to, and perhaps even make sense of,
the brains own activity and structures during altered
states of consciousness. Could this help to explain the
commonly reported transition from purely geometric
hallucinations to iconic hallucinations that appear to
exhibit their own agency (Lewis-Williams, 2002)?
Future work in systems neuroscience needs to verify
if any of these possibilities are borne out by the empirical evidence. Nevertheless, an enactive approach is
compatible with current models of the neural mechanisms underlying geometric hallucinations, and already
has more explanatory power than merely assuming a
direct structural isomorphism between visual experience and brain activity: (1) it allows for the possibility
that the patterns of non-ordinary visual experience are
more varied and richly detailed than the underlying
neural patterns; (2) it can help to explain why these patterns were taken to be highly significant; and (3) it suggests that there may have been a functional link
between the ritualistic alteration of consciousness and

Adaptive Behavior 21(3)

the origin of abstract cognition and symbolic practices
in terms of temporary environmental decoupling of
neural processing.

5 Conclusion
We have criticized some of the current theories that
have been proposed to explain the origins of symbolic
practices, especially as exemplified by Lewis-Williams
account. We have argued that Lewis-Williams insistence on social conflict and class struggle as the primary driving force behind changes in the first symbolic
practices is not compelling for a variety of reasons.
Nevertheless, his claim that the cultivation of altered
states of consciousness was involved in the origins of
the first symbolic material cultures may still turn out to
be correct, although for alternative reasons which he
fails to consider.
On the basis of a review of current mathematical
models of neural mechanisms underlying geometric hallucinations, we proposed a neurophenomenological
approach that emphasizes the enactive account of
sense-making and value. In particular, by considering
some kinds of altered state of consciousness as largely
internally mediated forms of perceptual sense-making,
we can better account for the richness of non-ordinary
experiences. Furthermore, the value generated by selfsustaining cell assemblies may help to explain the
selective bias of the first artists for the kinds of geometric
patterns that are typically experienced during these
altered states of consciousness. The enactive approach
also supports the idea that such altered states could have
significantly influenced the operation of the nervous system, especially by temporarily decoupling the autonomous activity of the brain from the usual environmental
influences. This switch from immediate sensorimotor
sense-making, which is normally directed toward the
external here and now, to a more internally mediated,
decoupled sense-making of mental and bodily structures
could thereby have facilitated the creation and diversification of abstract cognition and symbolic practices.
Notes
1. Some researchers prefer the hypothesis that these prehistoric patterns are highly abstract representations of normal perceptual experience rather than direct expressions
of abnormal hallucinatory experience. For example,
spiral patterns could be derived from swirling water
flows, swirling winds, winding stems of vines and winding
snakes (Takaki & Ueda, 2007, p. 133). However, this
hypothesis presupposes a process of geometric abstraction. Moreover, other common kinds of prehistoric patterns are not so readily found in nature. Most
importantly, even if all of the patterns could be
abstracted from environmental phenomena, the problem
of explaining the cross-cultural significance of these patterns would remain the same.

Froese et al.
2. Note that the engraved pattern shown in Figure 1 can be
interpreted as a lattice pattern made of triangles (i.e., one
of Kluvers form constants).
3. In this respect it is suggestive that even the hallucinatory
experience of small spots of light (phosphenes), induced
by applying transcranial magnetic stimulation (TMS)
over the human visual cortex, apparently cannot be
reduced to a local neural mechanism, but arises only after
more widespread recurrent processing (P. C. J. Taylor et
al., 2010). A distribution across multiple neural substrates
also helps to explain how such simple geometric hallucinations can be transformed into full-blown iconic hallucinations, for example under certain kinds of pathological
conditions (J.-P. Taylor et al., 2011).
4. This shift in explanatory approach helps us to resolve one
of the major outstanding puzzles of the current neuroscience of geometric hallucinations, namely the apparent mismatch between the resolution of neural Turing
patterns and visually experienced patterns. However, it is
not a solution to the explanatory gap of the mind-body
problem as such. We thank Julien Hubert for helping us
to clarify this important difference.
5. Strictly speaking, the enactive approach only predicts that
there is value for the self-sustaining neural process itself.
More remains to be said about how this value also
becomes significant from the perspective of the selfsustaining organism as a whole. But considering that
neural processes are constitutive of the whole organism
(Varela, 1991), it seems reasonable to assume that their
values are also constitutive of the values of the whole
organism. Nevertheless, future work on an enactive theory of the personal self is needed in order to better connect these distinct levels of description. Thanks to
Nathaniel Virgo for highlighting this issue.
6. Thanks to Chris Buckley for pressing this point during
several discussions.

Acknowledgments
We thank Chris Buckley, daboo, Julien Hubert, Guillaume
Dumas, Etienne Roesch, Nathaniel Virgo and one anonymous reviewer for their thoughtful comments on an earlier
draft of this paper. Many ideas of this paper took shape during several seminars of the Ikegami Laboratory, and they
have benefited from generous audience feedback.

Funding
Tom Froese and Alexander Woodward were each financially
supported by a Grant-in-Aid of the Japanese Society for the
Promotion of Science (JSPS) during the initial phase of this
work.

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About the Authors

Tom Froese 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 consciousness 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 (20102012). Currently,
he is a postdoctoral researcher at the self-organizing systems laboratory of the Instituto de
Investigaciones en Matematicas Aplicadas y en Sistemas, Universidad Nacional Autonoma
de Mexico, Mexico (20122013). 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 laboratory of the University of Tokyo (since 2010). His research into computer vision has led him
to ask questions about the nature of visual perception in living systems. Current research
focuses on computer vision, neural networks and reservoir computing, subjective time in the
brain, scientific computing on the GPU, and a maximalist approach to artificial life.

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Takashi Ikegami received his doctorate in physics from the University of Tokyo. His
research interest is to build and study artificial life systems ranging from chemical droplets
and evolutionary robotics to Web dynamics. Some of these results have been published in
Life emerges in motion (Seido, 2007) and also The Sandwich theory of life (Kodansha, 2012).
Takashi Ikegami gave the keynote address at the 20th anniversary of the Artificial Life conference in Winchester, UK. He is also a member of the editorial boards of Artificial Life,
Adaptive Behavior and BioSystems.