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Barrett-The Evolution of Cognition - 4E Perspective
Barrett-The Evolution of Cognition - 4E Perspective
Keywords: cognitive evolution, skin-brain thesis, minimal cognition, sensorimotor coordination, myoepithelia,
Umwelt, biogenic, radical, enactivism, evolutionary continuity, nervous systems
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So far, so good. The problem is that, as Rowlands (2003, p. 167) has pointed out, there is
very little consensus on what entitles something to be called a cognitive process; often,
he says, we simply point toward the set of abilities we consider to be cognitive, like
reasoning and language, and leave it at that, without specifying exactly why such
processes count and others don’t. Deciding what counts as cognitive therefore becomes
rather fraught at times, with a continual battle over whether a particular behavior is the
result of a cognitive process or “merely” the outcome of associative learning (e.g.,
Buckner 2011; Byrne and Bates 2006). This state of affairs is made even more confusing
by the fact that the leading textbook on comparative cognition undercuts this distinction
by defining cognition as “any process by which animals acquire, process, store, and act
on information from the environment” (Shettleworth 1999), which would seem to render
debates over whether a particular result supports an associative or cognitive account
redundant, if not incoherent.
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Despite these various efforts, then, it seems that, as van Duijn et al. (2006) suggest, we
still lack a means of navigating between overly “mindless” accounts of behavior versus
“mindful” accounts that involve the use of mentalistic terms, where the latter, as Penn
(2011) points out, fail to identify any cognitive process at all, but simply fall back on folk
psychological descriptors (see also Ramsey 2007). In particular, we seem to lack the
appropriate vocabulary to discuss the abilities of simple creatures in ways that capture
the flexibility of their behavior, but that do not generate an inappropriately “mentalistic”
view of matters (van Duijn et al. 2006).
Determining when or why an organism can be deemed cognitive is, therefore, not clear-
cut, and tracing the evolutionary origins of cognition accordingly is more difficult.
Perhaps this is why accounts of cognitive evolution are sometimes couched in terms of
brain size (Roth and Dicke 2005; Dunbar and Shultz 2007). Brain size is, of course, more
easily and unambiguously measured than cognitive capacity, and has the advantage that
it can be obtained from species that are long dead and fossilized, as well as from extant
species. Although measuring brains avoids the difficulty of defining cognitive processes,
this approach rests on the assumption that brain capacity is an accurate proxy for
cognitive abilities. As van Duijn et al. (2006, p. 163) point out, however, it appears that
our best reason for linking brains and cognition is that it “seems so obviously true”: those
animals we characterize as obviously cognitive, like humans and apes, have very large
brains for their body size, making the connection seem entirely logical. Creatures like
bacteria, which lack nervous tissue cannot, by definition, engage in a cognitive process,
and this also seems reassuringly logical. Equating brains (and nervous systems) with
cognition thus provides another (simple) means by which different creatures can be
sorted into those that are cognitive and those that are not.
The problem with this solution is that bacteria have revealed themselves capable of a
remarkable flexibility in behavior, despite lacking the only structure, i.e., a nervous
(p. 721) system, allegedly capable of producing such flexibility (e.g., Shapiro 2007). The
brain = cognition equation is also undermined by creatures like salticid spiders, which
possess brains that are absolutely tiny, no bigger than a poppy seed, yet are capable of
remarkably flexible hunting tactics, including the ability to engage in deceptive mimicry,
create diversions to distract prey, and take long, complex detours in order to better
position themselves for prey capture (Tarsitano and Jackson 1994; Tarsitano 2006; Barrett
2011). If a certain degree of behavioral flexibility is possible without brains, or with only
very small ones, then the idea that more brain means more cognition seems rather shaky,
as is our ability to distinguish cognitive from noncognitive creatures using simple metrics.
The situation is made even worse by the fact that, among creatures in possession of fully
fledged brains, the manner in which cognitive capacity can be mapped onto brain
structure is a highly vexed issue—Healy and Rowe (2007, 2013), for example, identify a
number of problematic assumptions within the literature and dispute the idea that smart
behavior maps onto brain anatomy in the way some have argued. Even within the context
of this debate, however, the essential assumption that brains are the organs of cognition
remains intact: elsewhere, these same authors have argued for better controlled
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The rise of 4E cognition (embodied, embedded, enactive, and extended) has raised
awareness of the inconsistencies and problems of the traditional cognitivist view, making
it clear that brains cannot be divorced from their bodily and environmental contexts
(Clark 1997; Gallagher 2005; Rosch, Thompson, and Varela 1992; Chemero 2009; Hutto
and Myin 2012; Barrett 2011). Whatever cognition might be, it is not best captured by a
purely brain-based computational perspective that places brains at a remove from the
rest of the body and the worlds they inhabit. This is true of humans, but even more so for
other creatures, given that the computational views on offer take some quite peculiarly
human abilities as a benchmark for cognitive processes in general; these might not apply
to other animals, or at least they might not operate in quite the same way. 4E cognition
thus offers an alternative to the anthropogenic approach, by providing a bottom-up or
“biogenic” perspective on cognitive evolution, where the principles of biological
organization, and their links to fitness, are taken to be the most productive means by
which we can understand what cognition is, what it does, and how and why it evolved
(Lyon 2006). A 4E biogenic approach thus seems worth considering, given that—although
psychologists readily accept that cognition occurs in a biological context—the inherent
anthropocentrism of the representational, computational view of cognition is less widely
recognized, even among authors who attempt a more ecological approach. Hence, many
authors clearly consider representational and computational theories of cognition to be
“species neutral,” when in fact these are highly human-oriented and hence much less
“biogenic” than they imagine. In what follows, I first consider some ideas relating to the
minimal criteria for cognition, before going on to discuss how cognitive evolution can be
conceived within a 4E framework. I conclude (p. 722) with a short consideration of why
more radical forms of embodied cognitive science may represent the way forward.
Cognition as Coordination
If we move away from thinking of cognition as brain-bound computational processes, and
move toward a more functional definition, the line between cognitive and noncognitive
creatures becomes increasingly blurred. Lyon (2006), for example, defines cognition as
the “capacity to infer relations between external circumstance and internal need to
facilitate agency” whose function is to “enable successful action and interaction in a
niche.” Anderson (2003) offers an even simpler definition of cognition as “situated
activity.” It is not immediately apparent that, under these definitions, cognition depends
on the possession of a particular kind of brain or nervous system organization, or that
there are particular kinds of representational or computational processes that qualify as
cognitive while others don’t.
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Brooks (1991, 1999), for example, famously rejected the idea that representation and
reason were necessary for intelligent behavior, and sought instead to study the adaptive
behavior of whole agents operating in an uncontrolled real-world environment (see also
Beer 1996; Pfeifer and Scheier 2001; Pfeifer and Bongard 2006). Brooks’s work
demonstrated that perception and action could often be so closely intertwined that there
was no need for “cognition”: the discrete action-producing systems of his robots resulted
in adaptive, robust behavior in the complete absence of a central processing unit that
could integrate inputs, plan, and produce coordinated action. His robots did not need a
complete internal representation of the world in order to produce coherent behavior.
Instead, they were “situated”: sensitive to relevant information in their surroundings,
with tightly coupled perception-action mechanisms that were, in turn, directly coupled to
an environment that they dynamically and frequently sampled. As Chemero (2013)
suggests, Brooks’s work was thus a logical extension of Gibson’s (1979) anti-
representational ecological theory of perception (where psychological phenomena are
seen as relations between an organism’s physical constitution and its environment) along
with Barwise and Perry’s (1983) notion of situation semantics (the idea that the meaning
of thoughts and utterances has nothing to do with mental representations, but with the
relationship between thinkers/speakers and their environment). For Brooks, like his
predecessors, intelligence was a relational property: it came about via possessing a
particular physical constitution operating within a particular environment.
This last point is key, as it helps illustrate how the rationale for Brooks’s research
program was genuinely evolutionary. As he pointed out, most of the four billion years of
life on earth has been spent refining the perception and action mechanisms that permit
organisms to cope with a dynamic, ever-changing environment (Brooks 1999). These
seemingly more “primitive” nonrepresentational forms of intelligence therefore must
have been the more difficult forms to evolve and implement, whereas the highly (p. 723)
representational processes that we humans deem intelligent—language, mathematical
reasoning, symbolic logic—must have been relatively easy to set in place. Following this
reasoning, Brooks decided to focus on insect-level intelligence, arguing it was essential to
understand the 97 percent of behavior that was controlled by nonrepresentational
processes, in order to understand the remaining 3 percent that could be deemed
representational (where these values refer to humans). As such, Brooks’s work
represented an early attempt to rid artificial intelligence of its anthropocentric
orientation, grounding cognition in biological processes, and not human artifacts.
This proposal was met with skepticism by some, however, who considered it unlikely that
insect intelligence would scale up to human intelligence. As Kirsh (1991, p. 162) put it:
“Insect ethologists are not cognitive scientists.” This latter pronouncement seems
increasingly insecure in the face of scientific findings that make a strong case for insect
cognition (e.g., Leadbeater and Chittka 2007; Lihoreau et al. 2012). One could argue,
though, that the decision to pursue insect-level intelligence as the basis of intelligent
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“cognitive” behavior was somewhat arbitrary, given that insects themselves appear pretty
late in the day, evolutionarily speaking.
Indeed, some in the classic enactivist camp suggest that any attempt to distinguish
cognition from other kinds of processes is, essentially, meaningless, and consider all life
to be inherently cognitive (Rosch et al. 1992). More specifically, Thompson (2007) offers
us the position that “life and mind share a set of basic organizational properties, and the
organizational properties of mind are an enriched version of those fundamental to life.
Mind is life-like, and life is mind-like” (p. 128). The problem with this position is that, if
everything is cognitive, then nothing is (van Duijn et al. 2006): we are left no means of
coming to grips with why a sea urchin differs from a shark or a slow worm from a squirrel
monkey. If we want to understand differences between minimally cognitive systems and
more advanced systems, van Duijn et al. (2006, p. 159) argue, then “it seems important to
differentiate between the cognitive processes of the rabbit and those of the carrot”: we
need to distinguish the subset of living systems that can be classified as cognitive
systems, and make clear the basis on which we make such a classification.
As noted earlier, one means of doing so is to assume minimal cognition requires the
possession of a nervous system. Moreno and colleagues, for example, argue that the
sensorimotor behavior of creatures without a nervous system is simply an extension of
their metabolic processes whereas, on their account, minimal cognition requires “meta-
metabolic functions” that can transcend these processes, generating an autonomous
sensorimotor domain that can sustain an “independent domain of patterns” (Moreno et al.
1997; Moreno and Etxeberria 2005). As van Duijn et al. (2006) point out, however, several
authors have now questioned whether a nervous system is essential for cognitive (i.e.,
meta-metabolic) behaviors, arguing that the evolution of nervous systems represents the
augmentation of abilities that already exist in unicellular organisms, rather than nervous
systems marking the crossing of some “cognitive Rubicon” (Lyon 2006; Taylor 2004).
To make this point more forcefully, van Duijn et al. (2006) give the specific example of the
sensorimotor abilities of the bacterium, Escherichia coli, and its two-component (p. 724)
signal transduction (TCST) system. In brief, and to oversimplify a little, chemotaxis in E.
coli relies on two interacting signaling pathways, a fast one (of the order of milliseconds)
that mediates perception, and a slower one (of the order of seconds) that mediates
adaptation to the signals in the environment (and therefore constitutes a form of
memory). The perception pathway consists of surface receptors for chemical attractants
or repellents, the occupation of which triggers phosphorylation of other molecules inside
the bacterium, and influences the direction in which the cells’ flagella rotate (so
controlling whether the organism “runs” or “tumbles”). The adaptation process involves
the methylation of occupied receptors. As this process is slower than the perceptual
process, the number of methylated receptors registers the concentration of chemicals in
the environment a few seconds previously. The receptors are continuously methylated and
demethylated in response to the occupation of receptor sites by attractants and repellant
chemicals as the organism moves through the environment while, at the same time,
receptor occupation and levels of methylation influence chemical processes inside the cell
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which, in turn, influence how the organism moves. The interaction and feedback between
the two systems thus produces a dynamic form of molecular memory. The difference
between the current state of the receptors and the internal level of methylation means
that the organism becomes sensitive to the relative concentration of chemicals in the
environment, rather than their absolute value, and hence can register any large-scale
abrupt changes in chemical concentration but will adapt to a constant level of signal.
This, in turn, means that organisms can move toward high concentrations of attractants
and away from repellents, but will remain in an environment with an optimum
concentration of attractants.
Van Duijn et al. (2006, p. 163) use this example to undercut the intuitively appealing idea
that minimally cognitive behavior requires a nervous system. Chemotaxis is more than
just an aspect of the cell’s metabolism because it involves physical changes of the
organism in relation to the environment that are distinct from metabolic processes.
Metabolic processes benefit from the changes in the environment the organism produces,
but the changes produced (moving toward a food source or away from a noxious stimulus)
are not themselves part of metabolism. Thus, they fulfill Moreno and colleagues’
requirement of autonomy and “meta-metabolic functions.” Given this, van Duijn et al.
(2006) suggest that sensorimotor coordination offers a conceptually clearer and more
effective starting point for minimal cognition.
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Keijzer et al. (2013) put forward a two-phase evolutionary process. The first (hypothetical)
phase involved the evolution of excitable myoepithelia (epithelia with contractile
properties that can conduct electrical activity across their surface) that was capable of
chemical transmission between cells. This myoepithelia is thought to have comprised an
unbroken sheet of protonervous and muscle tissue, with each cell signaling to its
immediate neighbors. Keizer et al. (2013) refer to these muscle surfaces as “Pantin
surfaces” (p. 726) (in honor of Carl Pantin, who first had the idea that the need for
mobility drove nervous system evolution; Pantin 1956), each of which has a specific size,
shape, and extension for each species (and indeed each individual, given that these will
not be identical to each other). They refer to the self-organized waves of coordinated
contraction that the surface produces as “patterning.” This aspect of the hypothesis is
therefore of particular relevance to an embodied perspective, because such patterning is
argued to be particular to the Pantin surface that produces it, i.e., it inherently reflects
the structure of an animal’s body. Patterning cannot, therefore, be interpreted as some
form of generic motor output function (e.g., feeding, mating), but should be viewed more
like the action of an organ: as a single coordinated system of movement that is
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The same goes for sensory capacities (Keijzer 2015). In order for patterning over the
Pantin surface to remain functional, the organism must be sensitive to disturbances in
such patterning (e.g., due to growth, short-term changes in activity, temperature,
chemical concentrations), as this will allow it to compensate and restore functionality.
The animal must therefore be sensitive to the ongoing dynamical changes in contraction
and extension across its Pantin surface, so that it can influence the processes that
produce and maintain these same contractions. This sensitivity to its own bodily dynamics
naturally incorporates sensitivity to any external disturbances that hinder or enhance
bodily contractions and extensions. Thus, the animal can sense the environment via the
skin-brain despite the absence of any dedicated external receptors. In this view, the
“animal body itself becomes a sensing device through its use of contractile tissues and
the environmental feedback this generates, both within and external to the body.” (Keijzer
2015, p. 14).
In the second phase of evolution, Keijzer et al. (2013) argue that a comparatively small
number of more specialized signaling cells evolved, with elongated axodendritic
processes (i.e., neurons) that enabled them to signal to non-adjacent cells. This would
give rise to a diffusely connected nerve net spread over the entire body. The advantage of
such nerve nets is that they would add to the self-organizing properties of existing
epithelial and muscular tissues. Specifically, Keijzer et al. (2013) argue that the addition
of long-range neural processes could thus enable wave-like patterning across larger
Pantin surfaces, releasing a constraint on size, as well as offering greater flexibility: in
contrast to sheet-like myoepithelia, nerve nets can take many forms, so removing
constraints on body form. Rather than providing specific, more precise connections from
sensors to effectors, as an input-output view of nervous system evolution would argue,
the function of nerve nets was to control, modify, and extend self-organized patterning
across a Pantin surface. Much like the memory system of E. coli, then, diffuse nerve nets
offered organisms an extra loop of control over behavior.
With diffuse neural nets in place, Keijzer et al. (2013) suggest that, evolutionarily, the
contractile apparatus could be cut loose from its placement on the animal’s skin and
repositioned as internal muscle. The general differentiation of muscle from skin would
then give rise to more complex nervous systems, and the kinds of animal bodies that we
(p. 727) are familiar with today, which fit well with the input-output conduction view of
nervous systems (see also Jekely et al. 2015). Thus, there is nothing in the SBT that
suggests we should abandon the conduction view. Rather the SBT offers a different, more
embodied standpoint from which to consider possible hypotheses about the origins of
nervous systems, and how we can think about cognitive processes. The SBT does,
however, present a major contrast to the one-size-fits-all view of classical cognitivism,
which “casts the operation of basic nervous systems in terms of abstract computational
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functions.” Instead, “the SBT draws it as a producer of complex but concrete dynamical
patterns of activation” (Keijzer et al. 2013, p. 15).
It is important to emphasize the nervous system as a whole, and not just the brain,
because species with larger brains also tend to have more elaborate sensory apparatus.
Although we often speak of humans having a poorer sense of smell, or less sensitive
hearing, than other creatures, our senses of smell and hearing are actually pretty good,
and we also have good vision, along with a sense of touch, taste, and balance. There is
often the assumption that more brain tissue allows animals to engage in more complex
“thinking” processes, but the control of complex sensorimotor systems also requires a lot
of neural tissue. So, in order to employ our receptors effectively, they are incorporated
into perceptual systems (e.g., we have two eyes in our head, that in turn is positioned on
a moveable neck, which is attached to a body that can move in a variety of ways) that
allow us to actively explore and sample the environment, and not passively receive it
(Gibson 1979). Part of the reason why human brains are so big, then, is to help control
and coordinate our sensory and motor apparatus. This, in turn, is partly why humans
show such high levels of behavioral flexibility: our greater sensitivity to many different
(p. 728) aspects of our environments expands our Umwelt—the term used by Uexküll
(2014) to capture the notion that organisms are sensitive only to those aspects of the
environment that hold significance for their survival and reproduction. This also helps us
recognize why other animals, with different kinds of sensorimotor systems, which have
developed to differing degrees, vary in their flexibility and problem-solving capacities.
An embodied perspective on comparative cognition therefore includes the idea that other
features of an animal’s anatomy can contribute to successfully navigating the world,
including how morphology itself can contribute to successful problem-solving. For
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example, New Caledonian crows are large-brained birds, and have exceptionally good
tool-using abilities compared to other members of the crow family, despite the fact that
these are similarly large-brained. This is partly because they have much greater
convergence (binocular vision) and straighter beaks (Troscianko et al. 2012). It is much
easier for New Caledonian crows to visually guide the stick-like tools they use to obtain
food than it is for other crow species, and this helps explain why they perform so much
better on tool-using problems than other corvids in the laboratory, but show comparable
performance on non-tool-using tasks.
Once one is attuned to the idea that behavioral flexibility is a property of bodies as well as
brains, and that the exploitation of environmental structure can serve a similar function,
examples appear all over the place—from the plant hoppers that have a gearing
mechanism in their legs that synchronize their jumping movements more precisely than
neural control can achieve (Burrows and Sutton 2013), to the seahorses that have square
rather than cylindrical tails (Porter et al. 2015), which improve their ability to maintain a
controlled grasp onto coral reefs, to the way that mudskippers (fish with the ability to
feed on land) form a “hydrodynamic tongue” to help capture food: the fish emerge onto
land and eject a mouthful of water, using a pattern of motion that shows a clear
resemblance to the way newts protrude their sticky tongues to capture prey (Michel et al.
2015). From an evolutionary comparative perspective, a 4E approach allows us to
appreciate the capacities of other species on their own terms: it brings the organism’s
body and environment into clear focus, in a way that allows the anthropocentric biases of
the cognitivist position to be circumvented, and (hopefully) overcome.
One reason is because, as Chemero (2013, p. 147) notes, CEC maintains a commitment to
a computational theory of mind, “embracing some of the ideas of Gibson, Barwise and
Perry and Brooks, but backpedaling on the strongest claims these authors made.” Given
this, REC should not be seen as the radicalization of Clark-style embodied cognitive
science (as is often assumed); rather, Clark-style CEC should be seen as a watered-down
version of REC. Hence, in Chemero’s (2013) view, it is the computational elements of CEC
that actually requires justification, and not the radical anti-representational stance, which
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Rejecting the notion of contentful representation for “basic minds” (i.e., those that are
non- or prelinguistic) thus seems to offer the same horizon-expanding promise as the SBT.
REC presents a new way of thinking about and conceiving of cognition, of understanding
what minds are and how they become more elaborate. A representational stance, in
contrast, seems to lead inexorably to an intellectualist view of other animals (and indeed
our own species; Barrett 2011), in ways that may hinder rather than help understand
cognitive evolution.
As I have argued elsewhere, the search for the precursors of our own cognitive and
linguistic abilities in other animals reflects the same “explanatory need” that plagues
studies of human cognition (Hutto 2013a): contentful representations are deemed to be
present because a need for them has been established by a logical argument that simply
insists this must be the case (Barrett 2015b). Specifically, the logic of evolutionary
continuity is used to insist that, as human contentful representational knowledge could
not have sprung from nowhere, then its precursors must be found in other species.
For example, Dorothy Cheney and Robert Seyfarth, pioneers and leaders in the field of
comparative cognition, have argued that baboon social knowledge “reveal[s] a
hierarchical, rule-governed structure with many properties similar to those found in
human language” (Seyfarth et al. 2005, p. 264), as well as suggesting that vervet alarm
calls are “best described as a proposition” and that “non-human primates certainly act as
if they are capable of thinking (as it were) in sentences” (Cheney and Seyfarth 2005, pp.
150–1). But it is only the assumption that nonhuman minds must contain content-bearing
representations that makes it necessary to characterize monkeys as possessing this kind
of knowledge, when many aspects of their behavior actually speak against this view.
Cheney and Seyfarth (2005) freely admit that their monkeys seem “unaware of their
effects on their audiences’ knowledge and beliefs” (p. 139), and do not “know that” others
have beliefs and knowledge, nor do they show any evidence of “knowing that” they
themselves possess knowledge and beliefs (Cheney and Seyfarth 1992; Cheney and
Seyfarth 2008). Indeed, it is this mismatch that requires certain concepts either to be
modified or watered down (e.g., a proposition is simply “a single utterance or thought
that simultaneously incorporates a subject and a predicate,” with no conditions of
(p. 730) satisfaction or truth-preserving component; Cheney and Seyfarth 2005, pp. 150–
1). As a result, it is unclear the extent to which these concepts can contribute to an
understanding of either monkey or human cognitive evolution.
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by some as the first enactivist; Moyal-Sharrock 2013) argues, our most basic beliefs, our
“hinge certainties,” are non-epistemic and non-propositional: it is action that lies at the
base of our knowledge (Wittgenstein 1974, p. 204). If this is correct, then it makes no
sense to look for the precursors of human knowledge and linguistic thought in the
(putative) thought processes of the living primates (or other organisms). For RECers,
there are no precursors of this nature, and whatever we share in common with other
species is to be found by seeking similarity in the nonrepresentational ways they act and
control behavior, as these will form the common ground between humans and other living
beings. In other words, we have to get our continuity the right way around, and the
dominant computational view of mind seems to get it wrong.
REC is therefore attractive because it is explicitly pluralist in its approach. It does not
argue against all forms of representational thought—only the notion that basic minds
must possess content (Chemero 2009; Hutto and Myin 2012; Hutto 2013b). Linguistic,
socioculturally scaffolded minds like ours clearly deal in rules and representations (else
you would not be able to read and comprehend the words on this page), and it is quite
clear that some of the interesting issues of human psychology are best understood using
a representational framework. It is a mistake, however, to assume that, given this state of
affairs pertains in the human species, that contentful thought must therefore characterize
cognition across the animal kingdom.
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these abilities to emerge late, and builds them on top of basic minds, rather than
extending content-dependent processes far back into the evolutionary past.
Acknowledgments
Thanks to Jessica Parker, Gert Stulp, and an anonymous reviewer for comments on an
earlier draft. This work was supported by the Canada Research Chairs and NSERC
Discovery Grant Programs.
References
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Barrett, L. (2015a). A better kind of continuity. The Southern Journal of Philosophy, 53,
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