doi:10.1093/scan/nsq036
SCAN (2010) 5,168 ^179
The culture ready brain
Charles Whitehead
London
In this article, I examine two hypotheses of language origins: the extended mirror system hypothesis and the vocal
grooming hypothesis. These conflict in several respects, partly because their authors were trained in different disciplines
and influenced by different kinds of evidence. I note some ethnographic/linguistic and psychological issues which, in my
view, have not been sufficiently considered by these authors, and present a ’play and display’ hypothesis which aims to
explain the evolution, not of language, but of the ’culture ready brain’with apologies to Arbib for so extending his original
concept. In the second half of the article, I will test all three hypotheses against the available fossil, archaeological and
neuroimaging evidence.
Keywords: mirror neurones; social displays; social mirrors; language origins; brain evolution
THE EXTENDED MIRROR SYSTEM HYPOTHESIS
The discovery of mirror neurones led Arbib and Rizzolatti
(1997) to propose a mirror system hypothesis of language,
according to which:
the parity requirement for language in humansthat what counts
for the ‘‘communicator’’ [e.g. speaker] must count approximately
the same for the ‘‘communicatee’’ [e.g., hearer]is met because
Broca’s area evolved atop the mirror system for grasping
with its capacity to generate and recognize a set of actions
(Arbib, 2006).
However, mirror neurones for graspingcommon to
monkeys as well as humanscannot be sufficient to explain uniquely human abilities such as language. To bridge
this explanatory gap, Arbib (2002) proposed seven evolutionary stages, which constitute his extended mirror system hypothesis, namely:
S1:
S2:
S3:
S4:
S5:
S6:
S7:
a control system for grasping,
a mirror system for grasping,
a simple imitation system for grasping,
a complex imitation system for grasping,
protosign,
protolanguage,
language.
This is in fact several hypotheses, but there is one core
underlying idea. Arbib suggests that brain expansion in apes
and humans involved expansion and reduplication of mirror
systems, with duplicated systems subsequently evolving to
serve different functions.
Received 14 April 2009; Accepted 22 March 2010
Advance Access publication 16 June 2010
The studies of role-play (Whitehead, 2003) and pretend play (Whitehead et al., 2009) were conducted at
the Wellcome Trust Centre for Neuroimaging at UCL, and funded by the Wellcome Trust.
Correspondence should be addressed to Charles Whitehead, 19 Rydal Road, London SW16 1QF, UK.
Email: [email protected]
Accepting S1 and S2 as uncontroversial, I will discuss
S3–S7 under three headings:
Imitation (S3–S4)
Arbib (2006) notes that there is no significant imitation
in monkeys, and limited imitative ability in apes. Where
chimpanzees typically took 12 trials to learn to imitate a
behaviour (Myowa-Yamakoshi and Matsuzawa, 1999),
humans can acquire longer sequences of more abstract actions in a single trial. Arbib therefore postulates a simple
imitative system (S3) which evolved in an ape/human
common ancestor, and a complex imitative system (S4)
unique to humans.
Mimesis (S5a–b)
To explain the transition from imitation to communication,
Arbib et al. (2008) divide ‘protosign’ into three subsidiary
stages:
S5a: pantomime of manual praxic actions,
S5b: pantomime of actions not in repertoire,
S5c: protosign.
By ‘pantomime’ Arbib means mimetic gesture. Mimesis
is voluntary representation by resemblance (e.g. ‘drawing
pictures in the air’ with the hands: Burling, 1993). Arbib
does not explain the transition from imitation (S4) to mimesis (S5a), or why any selfish hominid would wish to share
its praxic skills.
In S5b, praxic communication becomes extended to
include the miming of actions outside the normal repertoiresuch as flapping the arms to represent the flight of a
bird. Imitation of other species, such as turtles or sharks,
occurs in dolphins (Tayler and Saayman, 1973). When a
group of dolphins all follow and mimic a turtle, they are
not exchanging useful information about turtles. Such collective behaviour implicates play or performance (see below)
rather than communication. Playan essential aspect of
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The culture ready brain
social learning in primatesis a whole-body affair, and it is
phylogenetically older than mimesis, which occurs in apes
but not in monkeys. Furthermore, apes do not use mimesis
to convey information about the world, but to manipulate
others (Mithen, 2006). For example, Kubie the gorilla,
touches Zara lightly and moves his hand in the direction
he wants her to move (Tanner and Byrne, 1996). This
raises questions concerning the social changes required for
mimesis, the associated cortical mechanisms, the relevance of
grasping behaviour, and the evolutionary sequence postulated by Arbib.
Conventionalization (S5c–S7)
Arbib (2002) suggests that mimesis is slow, inefficient,
and subject to misinterpretation. Hence the need for
conventionalized signals (S5c) to ‘formalize, disambiguate
and extend pantomime’for example, to disambiguate
‘bird’ from ‘flight’. However, the essential difference between mimesis and language is not one of efficiency but
functiona mimed demonstration can be ‘worth a thousand
words’. Mimetic signals refer to concrete things, agents or actions, whereas language is specialized for abstractiongeneralized concepts, ideas and beliefs (Whitehead,
2008a).
Arbib (2008) suggests that conventionalized protosign
(S5c) is subsequently extended into and combined with ‘protospeech’. Conventionalized manual, facial and vocal signals
(protowords) then become separated from pantomime and
coalesce to form ‘protolanguage’ (S6).
The final transitionfrom protolanguage (S6) to fully
syntactical language of modern type (S7)is entirely
cultural. An important feature of Arbib’s hypothesis is the
distinction between a biologically evolved language ready
brain and, for example, Dunbar’s biologically evolved
language.
THE VOCAL GROOMING HYPOTHESIS
Robin Dunbar’s Vocal Grooming Hypothesis is rooted in
research related to primate group sizes. Dunbar (1993)
demonstrated that, in living monkeys and apes, there is a
positive linear correlation between mean group size and ratio
of neocortical to whole brain volume. This, he infers, reflects
increasing cognitive demand with increasing group size, due
to increasing social complexity.
Projecting Dunbar’s graph to intersect with human
neocortical ratio predicts that the optimal group size for
humans is around 150now known as ‘Dunbar’s number’.
Subsequent research on a range of human groups confirmed
that the mean number of people having social contact with
each other was between 100 and 200 (Hill and Dunbar,
2003).
The ’grooming gap’
Dunbar further showed that the time animals spent grooming each other also correlated with group size. The time
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available for grooming, however, is not infinitely elastic.
Feeding, resting and journeying between food sites make
irreducible time demands. Dunbar found that the maximum
time spent grooming in any modern primate group is 20%
of the day. This suggests that groups requiring more than
20% grooming time would fragment into smaller groups,
and there is a ‘glass ceiling’ on group size at around
80 individuals.
Again, projecting the grooming time vs group size plot
to the level of ‘Dunbar’s number’ implied that, if human
sociality depended on the standard primate mechanism, we
would need to spend around 43% of the day grooming each
other. However, from studies in seven societies, Dunbar
(1998) concluded that humans actually spend around 20%
of their time in social interaction, which coincides with the
primate grooming maximum.
Thus we have a ‘grooming gap’ which requires explanation. Dunbar’s solution to this is his vocal grooming
hypothesis, according to which language originated as a
time-saving substitute for one-to-one grooming, allowing
several individuals to be ‘groomed’ simultaneously, and leaving the groomer free to engage in other activities whilst
grooming.
The origins of vocal grooming
Aiello and Dunbar (1993) used Dunbar’s findings to predict
group size and grooming time for all hominid crania in their
sample (n ¼ 85). They concluded that ‘the evolution of
human language involved a gradual and continuous transition from non-human primate communication systems’.
This gradual process divides into two phases. First, early
Homo, with average grooming times approaching 23%,
would have needed vocal grooming in which ‘tone and emotion would be the essential components’that is, something
analogous to the ‘gossiping’ exchanges and choral ‘song’ displays in gelada baboons, who in fact maintain human-sized
groups. Second, archaic Homo sapiens, with average grooming times within the modern range, would need speech capable of communicating social information. The authors do
not explain why archaic H. sapiens should require speech
when geladas can maintain equally large groups without it.
The ’extended’ vocal grooming hypothesis
Two particularly serious problems with the vocal grooming
hypothesis concern the inadequacy of language as a grooming substitute:
First, grooming functions to prevent the problem of
freeriders by being costly in terms of time budgets. Words
are cheapthey are just too time-saving, and it is too easy to
lie. So we have the problem of explaining how such inexpensive and potentially dishonest signals can demonstrate
commitment.
Secondly, grooming cements social bonds by raising
endorphin levels. Speech lacks the requisite psychopharmacological properties.
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To address these problems, Dunbar added three new
phases to his hypothesis:
(1) Human laughter has an unvoiced homologue in chimpanzees. Dunbar (2009) therefore suggests that laughter
probably achieved a recognisably human form at an early
date, perhaps in early Homo erectus. Modern laughter
often occurs in rhythmic chorusing bouts, and this
may have scaffolded the emergence of his second
phasesong-and-dance display.
(2) Dunbar (2009) notes that evidence for modern vocal
capacities (expanded hypoglossal and upper thoracic
vertebral canals) first appears in archaic H. sapiens by
0.5 million years ago (mya). He notes that this evidence
does not discriminate between song and speech, but suggests song and dance probably emerged at this time because of their obvious grooming advantage over
languagein common with laughter, song and dance
provide the requisite discharge of endorphins.
(3) He then observes that religious techniquessuch as
meditation, fasting and flagellationbecause they are arduous or painfulare likely to raise endorphin levels
(Dunbar, in press). Perhaps religion evolved as the
‘opium of the people’ in more senses than one.
Dunbar’s complex ideas on religion are beyond the scope
of this article. However, his speculations concerning the religious capacities of different hominids seem to add several
additional steps to his thesis. But no matter how many stages
you insert in the progression towards language, it still remains a poor substitute for grooming.
What seems striking about the Vocal Grooming
Hypothesis, in its final extended form, is that language has
almost become an appendagesimply included because it is
necessary for ‘communal religion’.
LINGUISTIC AND ETHNOGRAPHIC ISSUES
Chomsky (2005) describes language as ‘a system of discrete
infinity’. That is, phonemes can be combined to make words,
words to make sentences, sentences to make narratives, and
so onin principle to infinity. Digital codes such as language
are discontinuous with all other communication systems,
which use sliding scales of size, rhythm, pitch, timbre, etc.
(Burling, 1993). Chomsky points out that you cannot get
from an analogue to a digital system by a gradual transition,
or by a series of intermediate steps. The origin of language
has to be instantaneous, because a system is either digital or
it is not.
The idea that cultureand languagehad a ‘big bang’
origin has a long history in social anthropology, where culture is conceived as ‘anti-biological’: ‘in apes, sex controls
society, but in humans, society controls sex’ (Sahlins, 1960).
The anti-biological features of human culturesuch as
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concealment of the genitals and classificatory kinshipimply
that human culture began at some revolutionary moment by
inverting an ancient primate social order (review:
Whitehead, 2008b).
Such ideas originate with Durkheim (1912), who argued
that this revolutionary change was accomplished by ritual,
and that language could only have a ritual origin. What
distinguishes language from the vocalizations of animals,
he argued, is displaced referenceconveying things known,
imagined or imaginary. In order to encrypt an intangible,
group members would have to engage in a recurring pantomime with self-evident meaning, where participants would
know that the same meaning was present in the minds of all.
Then it would become possible to refer to that meaning in a
cryptic manner.
Speech–act theory points to the same conclusion (e.g.
Grice, 1969; Searle, 1969; Austin, 1978). Language could
not function without a ‘social contract’ because words are
cheap. Like paper banknotes, they could not be taken at face
value unless backed by a source of genuine worth or sanctions against lying. In societies without police, gaols and
judicial systems, this can only be accomplished through
ritual and ritually-constructed supernatural beliefs (Knight,
1998).
PSYCHOLOGICAL AND DEVELOPMENTAL ISSUES
Mirror systems in the brain are implied by social mirror
theory, which holds that ‘mirrors in the mind depend on
mirrors in society’ (Whitehead, 2001). Shared social displays
make experiential states salient so that we begin to notice
them simultaneously in ourselves and others (Dilthey,
1883–1911). However, the discovery of mirror neurones in
grasping cortex led the Parma team to favour simulation
theory (Harris, 1991), according to which self-awareness is
a given, and other-awareness is inferred by ‘mentally simulating’ others. In Harris’s theory, pretence and imagination
are involved in mental simulation, but the Parma group
emphasizes visuomotor mirroring, which could implicate
any kind of shared behaviour. Developmental psychologists
such as Gratier and Trevarthen (2008) have stressed the importance of displays in the development of social insight,
whilst evidence that self-awareness and other-awareness
emerge simultaneously (Gopnik and Meltzoff, 1994) favours
social mirror theory.
Social displays include any behaviour that makes experiential states observable, and so broaden the focus of investigation beyond language. Burling (1993) notes that we have
at least three modes of communication: affective, mimetic
and conventional. But we also have two other kinds of display which have functions over and above communication,
and they too have the same three modalities. Play is exploratory and experimental, and, in the case of pretend play, creates a world of shared imagination. Performance combines
the functions of communication and play with two
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Table 1 Illustrative examples of social display
Communication
Play
Performance
Implicit
Gesture-calls (e.g. laughing, crying)
Embodied play (e.g. contingent
mirror play)
Song-and-dance display
Making marks
Mimetic
Projective
Introjective
Iconic gesture-calls
Projective pretend play
Role-play
Making representational images
Pantomime
Conventional
Analogical codes (e.g. pictographic writing)
Collecting behaviour
Ritual/ceremony
Iconography
Emblems
‘Fine art’
Music
Cryptic codes (e.g. language, phonetic
alphabets, mathematical denotations)
Play scripts
Myth
Literary and dramatic arts
Economico-moralcodes
Games-with-rules
Socio-economic personae
Wealth displays (material, moral,
aesthetic, cultural; spiritual; etc.)
Source: Whitehead (2001): based on data in Bourdieu (1972), Burling (1993), Huizinga (1955), Jennings (1990, 1991), Winnicott (1974).
otherssocial grooming and entrainmentensuring two or
more individuals are functioning as one (Whitehead, 2001).
What is remarkable and unique to humans is far more
than just language. We have elaborated to an exceptional
degree an unprecedented variety of social displays. According to social mirror theory, the reason for our high levels of
self- and other-consciousness is this formidable armamentarium of displays.
Table 1 summarizes our three types and three modes of
social display, with some illustrative examples.
A ’PLAY AND DISPLAY’ HYPOTHESIS
Whitehead (2003, 2008a) has proposed a ‘play and display’
hypothesis, holding that the proliferation of social displays
was a major factor in human brain expansion.
Our prodigious repertoire of displays could not have
emerged all at once, and must have evolved in a logical
order. Communication has to be primary, because it is so
widespreadeven cells communicate chemically. If performance is a playful extension of communication, it must be the
most recent. A similar argument applies to modes of display.
Implicit signals are common, mimesis is rare, and both have
to be in place before they can be conventionalized to sustain
and constitute modern human culture.
Whitehead further argued that play and performance in
one mode could scaffold the emergence of communication
in a ‘higher’ mode. Song-and-dance display, for example,
creates the preconditionssocial trust, social insight and
voluntary control over displaysfor a major expansion of
mimetic abilities. Similarly, ritual pantomime (mimetic performance) is a likely prerequisite for language (conventional
communication), as argued by Durkheim (1912) and Knight
Table 2 Hypothetical evolutionary sequence of social displays
Communication
Play
Performance
Implicit
Mimetic
Conventional
(1991). If so, the result is a spiral evolution of displays as
shown in Table 2.
This spiral of display behaviours suggests three Rubicons
during human evolution. The first, resulting from the emergence of song-and-dance display, would be expected to lead
to brain expansion, as would the second, marked by a major
elaboration of mimetic abilities up to the modern human
level of role-play. There are four reasons why this might be so:
(1) Multimodal integration. Dance and role-play require fine
motor control of multiple independent sets of muscles
throughout the body, co-ordinated with proprioceptive,
auditory, and visual feedback. Song-and-dance display
would be expected to lead to expansion of multimodal
areas such as the inferior parietal lobule, and higher level
sensorimotor areaspossibly pre-adapting the brain for
role-play.
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(2) Timing precision. Calvin (1983) has shown that the
‘release window’ involved in throwing a missile at a
target, which is shorter than the firing times of individual neurones, requires massive neuronal ‘redundancy’
exploiting the statistical accuracy of large numbersto
achieve the necessary precision. Richman (1978) showed
that the synchronized choral displays of gelada baboons
also involve millisecond timing precision. In the case of
human performancethat of a concert pianist for examplethe subtleties of rhythm, rubato and the characteristic ‘pulse’ which distinguishes the work of individual
western composers (Clines, 1977; Brown, 1991) demands fine timing precision not only in the performer
but also in the listener, involving muscle tone throughout the body (Storr, 1993).
(3) Performative skills. An imaging study of cello players
showed that the cortical representations of the fingers
of the left hand were larger than those of the right,
and this difference correlated with the age at which cellists began to play (Elbert et al., 1995). Another study
assessed the effects of skill acquisition in a finger tapping
task (Karni et al., 1995). The increased skill was associated with a 25% increase in area of the cortical representations of the fingers. The results were consistent with
findings in monkeys relating to both motor and perceptual skill learning. Humans are capable of learning an
extraordinary variety of motor and cognitive skills,
including those required for performative displays.
Presumably our large brains, in part, pre-adapt us for
such acquired skills.
(4) Modelling other people. Role-play and ‘theatre of mind’
(ThoM) involve whole-system mind and body representations of multiple personae. Imagined peoplesuch as
characters in a novelcommonly behave as though they
have minds, desires and beliefs of their own. To process
multiple mind/body representations in parallel would
presumably require comprehensive expansions of all
brain structures required for a ‘toy person’ to behave
realistically. This ‘chimerical brain’ hypothesis is consistent with experimental data suggesting multiple dissociated self-representations in normal human minds
(Oakley and Eames, 1985; Bliss, 1986; Hilgard, 1986;
Laughlin et al., 1992; Mitchell, 1994).
All the above implicit and mimetic abilities, expanded
across the first two Rubicons, would lay the foundations
for the thirdritual-based culture, establishing a ‘social contract’ on which the emergence of language depends. This
would not be expected to lead to brain expansioncontraction is more likely because brain tissue is expensive (Aiello
and Wheeler, 1995). Societies whose members are controlled
‘from the outside’ by rulesbacked by social or sacred sanctionsmay not need such highly skilled or finely timed
performances to maintain social cohesion.
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ARCHAEOLOGICAL AND FOSSIL EVIDENCE
Figure 1 shows cranial capacities in fossil hominids since
3.5 mya. As predicted by the ‘play and display’ hypothesis,
there appear to have been two periods of accelerated brain
expansion: the first in habiline species between 2.5 and 2.0
mya, and the second from 700 thousand years ago (kya) in
archaic H. sapiens.
There is also evidence of structural brain changes across
these periods, and they coincide with periods of cooling
world climates and archaeological evidence of behavioural
change.
There is also evidence of a third grade shift, though
this did not coincide with the emergence of modern
human culture. The rate of brain expansion appears to plateau around 50 kya, with an average of 1500 cm3 (Figure 2).
After 10 kyaroughly coinciding with the agricultural revolutionbrain volumes fell to their present average level of
1350 cm3.
Figure 3 shows endocranial casts from three fossil hominids, compared with those from a chimpanzee and a contemporary human.
Fig. 1 Hominid cranial capacities over the last 3.5 mya (data from De Miguel
and Henneberg, 2001).
Fig. 2 Hominid cranial capacities from 200 to 10 kya (bold rule indicates 1350 cm3
average for living humans) (data from De Miguel and Henneberg, 2001).
The culture ready brain
Fig. 3 Endocranial casts (after Holloway, 1974).
Apith crania are slightly larger than those of chimps, the
main differences being: bilateral transverse expansion,
mainly due to increased bulk of the parietal and temporal
lobes, and possibly enlarged premotor cortices; increased
height, mainly of the parietal lobes; and a well-developed
superior parietal lobule (Tobias, 1987). These enlargements
include motor and parietal areas central to Arbib’s extended
mirror system hypothesis.
The H. erectus cast reflects changes that occurred in habilines. From an examination of six habiline cranial casts,
Tobias (1987) notes a number of new features not present
in apiths, including a modern pattern of left-right asymmetries, increased bulk of frontal and parietal lobes, a prominent inferior parietal lobule, and pronounced enlargement of
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Broca’s and Wernicke’s ‘speech’ areas. Tobias infers that
Homo habilis could speak, but homologous swellings can
be seen in macaques (Deacon, 1992), and, in all primates
other than ourselves, implicit vocalizations are processed in
the left hemisphere (Falk, 1987). The expanded ‘speech’ and
inferior parietal areas are consistent with song-and-dance
display in habilines rather than archaic humans as suggested
by Dunbar.
There is also archaeological evidence for major behavioural change just before the first grade-shift. The earliest unequivocal stone tools appear around 2.7 mya (Bilsborough,
1992). These were used for butchering meat, and the butchery scatters were all at riverside sites. There are two points to
note here.
Firstly, chimpanzees cannot butcher meat because they
cannot trust each other to share such a valuable resource.
When chimpanzees capture an animal they tear it apart
and eat it in a general mêlée (Teleki, 1973, 1981; Strum
1981)they are grabbing their share before the others eat it.
Secondly, if you are a prey animal you do not linger
near water where large carnivores are likely to drink (Potts,
1994). Still less would you sit around butchering meat,
releasing an alluring smell that could travel a long way
downwind.
These two points suggest that the earliest stone tool
makers had developed levels of social trust unprecedented
in any non-human primate, and an ability to deal with dangerous predators which were larger, faster, and better armed
with teeth, claws and muscle, than any hominid. This suggests an ability to maintain large, well-coordinated groups,
and a requirement to do so. By Dunbar’s own reasoning one
would expect song-and-dance display by 2.7 rather than
0.5 mya.
Following the first grade-shift there was little change in
H. erectus for around 1.5 million years. Then, during the
second grade shift, all the previously expanded cortices
became further enlarged, together with at least proportionate
increase in prefrontal lobes.
During this second grade shift we find the first unequivocal evidence for new kinds of display behaviour.
Pigmentsespecially red ochre and haematite, perhaps serving as body paintwere increasingly used by African and
European hominids from around 300 kya (Watts, 1999), and
late H. erectus was assembling collections of non-utilitarian
objects, such as attractive pebbles, crystals, shells, whale teeth
and fossils (Hayden, 1993).
From around 125 kya, Neanderthals engraved geometric
patterns on bones and rocks (Marshack, 1976, 1990).
Analogous evidence from Africa is scarce but present. The
first putative iconic objectthe Berekhat Ram ‘figurine’predates 270 kya and comes from an Acheulian site
(Schepartz, 1993). This might be better interpreted as a
‘doll’ than as ‘fine art’ which would imply social hierarchy
and class politics of a distinctly modern kind (Whitehead,
2003).
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Fig. 4 Peak activations in nine studies involving tool use or hand-object manipulation.
Whitehead (2003) has further argued that all this display
material implicates increasing mimetic and pretend play
abilities, particularly in the light of negative evidence from
earlier periods. The stereotypical character of Acheulian
toolswhich persisted unchanged for more than a million
yearssuggests extraordinary social conformity. The play
and display hypothesis would associate this with a cohesive
‘song-and-dance’ rather than a more flexible ‘pretend play
and mimetic’ culture.
If social displays implicate mirror systems, then the fossil
and archaeological evidence is consistent with Arbib’s central
thesis of expanding and proliferating mirror systems. The
above evidence also favours the sequence and timing of display behaviours proposed by the play and display rather than
the extended vocal grooming hypothesis.
NEUROIMAGING EVIDENCE
Tool use and object manipulation
Buccino and colleagues (2001) conducted an imaging study
of object manipulations using hands, feet and mouth, and
found associated brain activations which mapped onto parietal and opercular prefrontal areas in a somatotopic fashion,
resembling a classic motor homunculus, and suggesting that
there are mirror systems for many types of body movementnot just manual grasping.
Nevertheless, the discovery of a manual grasping mirror
system led to more than 40 imaging studies of hand actions,
tool use and object manipulation (Grèzes and Decety, 2001).
Table 3 Contrasts used in nine tool use and object manipulation studies
Planning and naming tools
Johnson-Frey et al. (2005) Planning to mime tool use vs planning a meaningless
hand movement: R and L hand
Fridman et al. (2006)
Planning a tool-use gesture vs planning a communicative gesture: R hand only
Kan et al. (2006)
Naming tools vs naming animals
Martin et al. (1996)
Naming tools vs naming animals
Executing/miming tool use or object manipulation
Choi et al. (2001)
Miming tool use vs oppositional thumb–index finger
movements: R and L hand
Inoui et al. (2001)
Using tongs vs using fingers to manipulate an object:
R and L hand
Ohgami et al. (2004)
Miming tool use vs mimetic gesture representing an
object: R and L hand
Johnson-Frey et al. (2005) Miming tool use vs a meaningless hand movement:
R and L hand
Fridman et al. (2006)
Miming tool use vs a communicative gesture: R hand
only
Naito and Ehrsson (2006) Illusory hand flexion with ball vs illusory hand flexion
without ball: R and L hand
Observing tool use
Lotze et al. (2006)
Observing tool use or instrumental actions with
objects vs expressive gestures
Figure 4 shows major centres of brain activity from nine
of these studies, six of which involved using and/or planning
to use tools, whilst two involved naming tools and the other
hand-object interactive movement. Table 3 shows the contrasts used in these studies.
The culture ready brain
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Fig. 5 Main activation loci from four studies of dance.
Peak activations in these studies clustered in opercular
prefrontal and superior parietal areas, corresponding to the
assumed grasping mirror system. Most of the activity is in
the left hemisphere, whereas studies of non-praxic hand actions show more bilateral activity (Grèzes and Decety, 2001).
Note that there is very little activation of medial or prefrontal areas other than opercular.
Dance
To date there have only been four imaging studies of dance.
Three of these (Calvo-Merino et al., 2005, 2006; Cross et al.,
2006) were primarily intended to investigate mirror systems
rather than dance as such. Participants observed videos of
familiar vs unfamiliar dance moves: the former showed
greater activity than the latter. In the fourth study (Brown
et al., 2006) participants performed tango steps on a sloping
board, and metric dance was contrasted with non-metric
dance, self-paced dance, isometric muscle contractions; and
a resting baseline. Figure 5 shows activation loci associated
with familiar vs unfamiliar dance moves, plus, from the
Cross et al. study, all dance vs rest (observing) and, from
the Brown et al. study, all metric dance contrasts, plus
non-metric dance vs isometric muscle contractions
(executing).
Unsurprisingly, dance activates the opercular prefrontal
and parietal areas associated with tool-use, mainly in the
left hemisphere. Overall, however, there is fairly widespread
activity in both hemispheres. Note the superior temporal
cluster, most evident in the right hemisphere. Since the
three studies of observing dance used silent videos as stimuli,
this cannot be a result of heard music, though it could indicate imagined music.
For two observing dance studies the activations shown
represent dance minus dance, which may account for less
inferior parietal activity than would be expected for a
performative display requiring considerable multimodal
integration. In any case, the observing dance studies
lacked musical accompaniment, and the dance execution
study had no visual feedback, so none were truly
multimodal.
A further difference between dance and tool-use is the
broad scatter of medial prefrontal, parietal and temporal
activations.
It is unsurprising that a complex multimodal activity such
as dance should involve more widespread cortical activation than tool use. Yet for decades palaeoanthropological debates about ‘cognitive evolution’ have been dominated by
discussions of tool-making and tool-use, with corresponding
concerns that technological innovations do not correlate
with brain expansion (Mellars and Stringer, 1989). Interest
in the evolution of dance is relatively recent (Whitehead,
2003; Mithen, 2006; Dunbar, 2009). To my knowledge, no
previous author has suggested a role for dance display in
brain expansion.
Several of the brain structures activated by dance have also
been implicated in studies of pretend play. This is consistent
with the suggestion that performance in one mode may scaffold the later emergence of a higher mode.
176
SCAN (2010)
Pretend play
The first imaging study of pretence (Whitehead, 2003)
involved six drama students imagining themselves performing Hamlet and Lady Macbeth in rehearsed extracts from
Shakespeare’s plays, cued from a rolling text. The role-play
tasks were contrasted with readings from control texts, selected for their apparently uninvolving character. Although
participants found the role-play tasks considerably more demanding than the control tasks, we found more brain activity during the control tasks.
A possible explanation for this unexpected finding
might be that role-play (i.e. ‘ThoM’) is the default activity
of the brain in awake adults. Such an idea is consistent
with evidence that brain areas supporting default activity
are involved with thinking about the self and others
(D’Argembeau et al., 2005), watching social scenarios
(Iacoboni et al., 2004), and following or constructing narratives (Mar, 2004).
Many authors assume continuity between role-play, narrative and default activity (Mar, 2004). If so, all three would
be expected to show significant overlap in imaging studies.
Interestingly, narrative and default areas were activated in the
role-to-control switch during the role-play study. One tentative suggestion is that the role-to-control switch involved
increased activity in role-play areas as they were being
dissociated. Clearly this suggestion needs to be tested by a
more definitive study. However, the role-to-control
switch findings are provocative and I have included them
in Figure 6.
C.Whitehead
The role-play study was followed by two larger studies
where participants observed videos of pretend actions contrasted with instrumental actions. In the first of these
(German et al., 2004), an actor manipulated an object (e.g.
placing a book on a shelf) or pretended to do so (e.g. placing
an imaginary book on the shelf). One criticism of this study
was that brain activity associated with the pretend action
might have been due to its unfamiliarity. To correct for
such a possibility, the second study (Whitehead et al.,
2009) included two control conditions: using a familiar
object in the normal way (e.g. using a pen to write with)
and in an unusual way (e.g. using the pen to stir coffee). The
pretend condition involved pretending the object was something else (e.g. pretending the pen was an aeroplane). We
found minimal differences between the two instrumental
tasks. Figure 6 shows peak activity for the pretend minus
instrumental tasks in these two studies. The square markers
represent a second task in the Whitehead et al. study.
Participants were shown a picture of the object used in the
previous action video and were required to name its use (e.g.
‘pen’, ‘coffee spoon’ or ‘aeroplane’). Pretend use was contrasted with usual plus unusual use.
The two studies of observing pretence showed similar patterns of activation, with several areas close to those associated with dance: bilateral opercular prefrontal; right
superior temporal; and bilateral temporal poles. In contrast
to dance, these two studies showed relatively extensive activity in ventromedial and orbital prefrontal cortex. Two dance
studies (Brown et al., 2006; Cross et al., 2006) contrasted
Fig. 6 Main activation loci from three studies of pretence. Red, observing projective pretence (Whitehead et al., 2009); Orange, observing projective pretence (German
et al., 2004); Maroon, role-to-control switch (Whitehead, 2003).
The culture ready brain
SCAN (2010)
Table 4 Regions of interest associated with three forms of social display,
compared with tool use, deactivation areas and ToM
Tool Dance Pretend Narrative Deactivation ToM
use
play
areas
Superior parietal
L
Prefrontal operculum
L
Inferior parietal
L
Posterior cingulate/precuneus
Superior temporal
Temporal pole
Ventromedial/orbital prefrontal
Dorsolateral frontal
R<L
R<L
R<L
RþL
R>L
RþL
R>L
RþL
RþL
R
R
RþL
R
R>L
RþL
RþL
RþL
RþL
R>L
R>L
RþL
RþL
R
RþL
RþL
RþL
RþL
RþL
Deactivation areas may equate with ‘theatre of mind’ (ThoM). R, right hemisphere;
L, left hemisphere. Italics, role-to-control switch only.
dance with a resting baseline, and these did not show such
rostral ventromedial or orbital prefrontal activation.
Observing pretence activated temporal and prefrontal
areas frequently associated with ‘theory of mind’ (ToM).
German et al. inferred that ToM is automatically engaged
when people observe pretend actions. This would be consistent with Leslie’s (1987) view that children show precocious
mentalizing abilities in the context of pretend play.
However, ToM engages a subset of the brain structures
implicated in the pretend play studies (Table 4). Social
mirror theory and Lillard’s (2001) ‘twin earth’ model both
imply that pretend play is the primary phenomenon,
enabling children to acquire ToM. Whether ToM is necessary for pretend play, or the converse is true, remains an
open question.
The two studies of observing pretence also implicated
brain regions repeatedly associated with narrative and
default activity. If future research confirms that the
role-to-control switch in the Whitehead et al. study does
indeed represent role-play, the overlap between narrative,
default activity and pretence would be considerably
increased (Table 4).
Comment on the imaging evidence
Table 4 summarizes the brain regions implicated in the
above imaging research, showing areas of overlap and difference. In view of the paucity of studies of dance and pretence,
and the fact that different controls were used, conclusions
based on this data are necessarily tentative. Although Table 4
does not take account of fine-grained functional differences
within the broad areas shown, it does suggest a plausible
evolutionary sequence, and possible directions for future
investigation.
Imaging research suggests that there may be up to five
distinct mirror systems in modern human brains, each of
which partially incorporates phylogenetically older ones.
The first two systems, which we share with monkeys,
would be those for reading body actions and affective signals.
177
A possible third would be a song-and-dance system, a fourth:
a mimetic and pretend play system, and a putative fifth: a
role-play system.
CONCLUSIONS
The evidence reviewed here broadly supports an extended
mirror system hypothesis, though Arbib’s more controversial
steps of protosign (S5) and protolanguage (S6) seem questionable. I have also argued that we need to take into account
a broad range of display behaviours in explaining the evolution of the ‘language ready brain’. Anthropological and
linguistic data favour Arbib’s hypothesis of language as a
cultural invention.
All the evidence reviewed above is consistent with the
vocal grooming and play and display hypotheses, with cranial cast and archaeological data favouring the earlier date
for song-and-dance display proposed by Whitehead.
Overall, this article supports Arbib’s notion of a ‘language
ready brain’, as opposed to the evolution of language per se.
However, taking into account our rich repertoire of social
displays, ‘culture ready brain’ might be a more appropriate
term. Trevarthen (1995), after 30 years researching human
infants in different cultures, claimed that human children are
born ‘hungry for culture’. At least, I would claim, they are
born hungry for socialization, and were things otherwise,
human culture would be impossible.
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