European Journal of Neuroscience

European Journal of Neuroscience, Vol. 33, pp. 1328–1338, 2011 doi:10.1111/j.1460-9568.2011.07619.x

COGNITIVE NEUROSCIENCE

Technology, expertise and social cognition

in human evolution

Dietrich Stout,1 Richard Passingham,2 Christopher Frith,3 Jan Apel4 and Thierry Chaminade5
1
Department of Anthropology, Emory University, 1557 Dickey Drive, Atlanta, GA 30322, USA
2
Department of Experimental Psychology, University of Oxford, Oxford, UK
3
Wellcome Trust Centre for Neuroimaging, University College London, London, UK
4
Department of Archaeology and Osteology, Gotland University College, Visby, Sweden
5
Mediterranean Institute of Cognitive Neuroscience, CNRS – Université Aix-Marseille, Marseille Cedex, France

Keywords: cognitive processes, functional MRI, gesture, imitation, learning comprehension

Abstract
Paleolithic stone tools provide concrete evidence of major developments in human behavioural and cognitive evolution. Of particular
interest are evolving cognitive mechanisms implied by the cultural transmission of increasingly complex prehistoric technologies,
hypothetically including motor resonance, causal reasoning and mentalizing. To test the relevance of these mechanisms to specific
Paleolithic technologies, we conducted a functional magnetic resonance imaging study of Naı̈ve, Trained and Expert subjects
observing two toolmaking methods of differing complexity and antiquity: the simple ‘Oldowan’ method documented by the earliest
tools 2.5 million years ago; and the more complex ‘Acheulean’ method used to produce refined tools 0.5 million years ago. Subjects
observed 20-s video clips of an expert demonstrator, followed by behavioural tasks designed to maintain attention. Results show that
observational understanding of Acheulean toolmaking involves increased demands for the recognition of abstract technological
intentions. Across subject groups, Acheulean compared with Oldowan toolmaking was associated with activation of left anterior
intraparietal and inferior frontal sulci, indicating the relevance of resonance mechanisms. Between groups, Naı̈ve subjects relied on
bottom-up kinematic simulation in the premotor cortex to reconstruct unfamiliar intentions, and Experts employed a combination of
familiarity-based sensorimotor matching in the posterior parietal cortex and top-down mentalizing involving the medial prefrontal
cortex. While no specific differences between toolmaking technologies were found for Trained subjects, both produced frontal
activation relative to Control, suggesting focused engagement with toolmaking stimuli. These findings support motor resonance
hypotheses for the evolutionary origins of human social cognition and cumulative culture, directly linking these hypotheses with
archaeologically observable behaviours in prehistory.

Introduction
Neither toolmaking (Beck, 1980) nor cultural transmission (Whiten
et al., 2007) is unique to humans. Yet there is a vast gulf between the
accumulated (Tennie et al., 2009) complexity of human technology
and that of any other living species. This disparity has been attributed
to uniquely human physical (Johnson-Frey, 2003) or social (Tomasello
et al., 2005) cognition, or both (Passingham, 2008).
Motor hypotheses of action understanding (Gallese & Goldman,
1998; Blakemore & Decety, 2001) suggest a possible unification of
these explanations. The ‘Motor Cognition Hypothesis’ (Gallese et al.,
2009) proposes that human social cognition has its phylogenetic and
ontogenetic origins in ‘motor resonance’. Distinctive human capacities
for technology, language and intersubjectivity might thus have a single
origin in evolutionary modifications of a primate ‘mirror neuron
system’ (Rizzolatti & Craighero, 2004). However, it is not clear to
what extent action understanding relies on motor resonance as
Correspondence: Dr D. Stout, as above.
E-mail: dwstout@emory.edu
Received 22 April 2010, revised 15 December 2010, accepted 23 December 2010
opposed to intention reading (Saxe, 2005; Grafton, 2009), nor at
which level(s) action representations are shared between individuals
(Jacob & Jeannerod, 2005; de Vignemont & Haggard, 2008).
To address these issues, we conducted a neuroimaging study in
which human subjects observed the making of Paleolithic stone tools.
Stone toolmaking is the earliest known uniquely human behaviour
(Roux & Bril, 2005), dating back at least 2.6 million years (Semaw
et al., 2003). Previous research (Stout & Chaminade, 2007) used
FDG-positron emission tomography (PET) to study brain activation
during stone toolmaking. In the earliest, ‘Oldowan’, technology a
‘hammerstone’ held in the dominant hand is used to strike sharp
‘flakes’ from a cobble ‘core’ manipulated by the other hand. We found
this method to be associated with activation of parietal and frontal
brain regions involved in sensorimotor coordination, grip selection
and 3D shape perception. After that, 1.7 million years ago, more
complex ‘Acheulean’ technology developed. Here cores were inten-
tionally shaped into large cutting tools known as ‘handaxes’. We
found this method to be associated with activation of the right inferior
frontal gyrus (Stout et al., 2008), a region implicated in the
hierarchical organization of action (Koechlin & Jubault, 2006).

ª 2011 The Authors. European Journal of Neuroscience ª 2011 Federation of European Neuroscience Societies and Blackwell Publishing Ltd

In the present study we used functional magnetic resonance imaging
(fMRI) to compare brain activation during the observation of Oldowan
and Acheulean toolmaking. The Motor Cognition Hypothesis pro-
poses that action understanding is tied to motor expertise (Gallese
et al., 2009), but learning clearly requires understanding of actions not
yet in the observer’s repertoire. Our design crossed observer expertise
(Naı̈ve, Trained, Expert) with technological sophistication (Oldowan,
Acheulean) to examine the contribution of resonance and interpreta-
tion in understanding actions of varying familiarity and complexity.
An account in terms of motor resonance predicts expertise effects in
the putative human mirror neuron system (Rizzolatti & Craighero,
2004) and dorsolateral prefrontal cortex (Buccino et al., 2004; Vogt
et al., 2007), regardless of complexity. An inferential account (Saxe,
2005) predicts complexity effects in brain regions associated with
mental state attribution, including the medial prefrontal cortex (Frith &
Frith, 2006). A mixed model (Grafton, 2009) makes less exclusive
predictions, but might involve a shift from resonance to inference with
increasing complexity and expertise.
Methods
Paleolithic toolmaking
The Paleolithic technologies investigated here are the same that were
addressed in previous FDG-PET studies of subjects actually making
stone tools (Stout & Chaminade, 2007; Stout et al., 2008). Oldowan
flaking, known from approximately 2.6–1.6 million years ago, is a
simple process of striking sharp cutting flakes from a stone core using
direct percussion. However, even this simple technology requires
substantial visuomotor coordination, including visual evaluation of
core morphology (e.g. edge angles, location of convexities and
concavities) in order to select appropriate targets for percussion, as
well as active proprioceptive sensation and precise bimanual coordi-
nation to guide forceful blows to small targets on the core.
After approximately 1.7 million years ago, flake-based Oldowan
technology began to be replaced by ‘Acheulean’ technology, involving
the intentional shaping of cores into large cutting tools known as
‘picks’, ‘handaxes’ and ‘cleavers’. Such shaping requires greater
perceptual-motor skill to precisely control stone fracture patterns and
more complex action plans that relate individual flake removals to
each other in pursuit of a distal goal. By 500 000 years ago, some
Acheulean tools exhibit a high level of refinement that additionally
requires the careful preparation of edges and surfaces, known as
‘platform preparation’, before flake removals. Platform preparation is
often done on the face opposite a planned flake removal: the core is
flipped over (‘inverted’) and a new hammerstone and ⁄ or hammerstone
grip is selected and used to abrade ⁄ micro-flake the edge through light,
tangential blows. This preparatory operation introduces a new sub-
routine to toolmaking action plans, increasing their hierarchical depth.
It is the ‘Late Acheulean’ method that is studied here.
As in previous FDG-PET studies, the current study also includes a
control condition that consists of simple bimanual percussion of an
unmodified core without any attempt to detach flakes. This condition
is designed to include general demands of striking and manipulating a
core, while omitting any more specific demands for percussive
accuracy, core support, target selection and strategic planning involved
in actual toolmaking.
Subjects and training
Three subject groups were included in the study, comprising
technologically Naı̈ve (n = 11), Trained (n = 10) and Expert (n = 5)
ª 2011 The Authors. European Journal of Neuroscience ª 2011 Federation of European Neuroscience Societies and Blackwell Publishing Ltd
European Journal of Neuroscience, 33, 1328–1338
Technology and cognition in human evolution 1329
individuals. All subjects were right-handed by self-report and had no
history of neurological illness. The study was approved by the
National Hospital for Neurology and Neurosurgery and the Institute of
Neurology joint Ethics Committee. Twenty-one individuals with no
prior experience of stone toolmaking were recruited via advertise-
ments posted to electronic mailing lists maintained by the University
College London Functional Imaging Lab and Institute of Archaeology.
Respondents chose to participate in the Naı̈ve or Trained group.
Individuals who elected training attended 16 1-h training sessions over
an 8-week period, in groups of 2–3 subjects per session. During
training, subjects were provided with tools and raw materials for
practice, as well as demonstrations and interactive verbal and gestural
instruction by the first author. Subjects improved with training, but
none achieved expertise in shaping handaxes (Supporting Information
Fig. S1). Products of the 1st, 8th and 16th sessions of each subject
were collected for further analysis (forthcoming). Because it became
clear during training that subjects would not achieve the desired
expertise, a group of five subjects with pre-existing expertise was
included in the ongoing study. Expert subjects were drawn from the
small extant community of academic and craft stone toolmakers, and
were contacted directly. Imaging sessions for Naive, Trained and
Expert subjects were interspersed over the course of the study.
Subjects in all groups received the same instructions before
scanning, consisting of a scripted briefing, accompanying PowerPoint
presentation, and Cogent script showing instructions and exemplar
stimuli (not used in experiment) as presented in the scanner. Crucially,
instructions included a description of the methods and aims of
Paleolithic stone toolmaking so that even Naı̈ve subjects had basic
conceptual knowledge of the technology.
Stimuli
Twenty-second video clips (Supporting Information Video S1) were
extracted from full-length videos of an expert toolmaker (right-
handed) engaged in Oldowan flaking (n = 6), Acheulean shaping
(n = 6) and the Control condition (n = 6). All videos were recorded on
the same day with constant camera position and lighting. The
demonstrator was seated facing the camera, and supported the core on
his left thigh or above his lap in his left hand. The field of view
included this workspace and the full range of arm movements, but did
not extend to the face. Flint from a single quarry in Suffolk, UK was
used for all toolmaking, and video segments were deliberately selected
from early stages of flaking ⁄ shaping (e.g. prior to establishment of
symmetrical ‘handaxe’ shape) so that size, shape, colour and other
large-scale visual characteristics of cores did not differ systematically
across stimulus types. Nevertheless, action sequences portrayed in the
clips clearly reflected technological differences.
Nine types of technological action were identified in the videos, and
their frequencies in the actual stimuli used recorded using the
EthoLog 2.2.5 behavioural transcription tool (Table 1). These are:
(i) percussive strikes with the right hand; (ii) shifts of the left-hand
core grip; (iii) rotations of the core in the left hand; (iv) shifts of the
right-hand hammerstone grip; (v) inversions (flipping over) of the core
with the left hand; (vi) changing of the hammerstone (here the
demonstrator reached off camera to exchange one hammerstone for
another, see Supporting Information Video S1); (vii) abrasion ⁄ micro-
flaking of core edges with right hand; (viii) sweeping of detached
flakes and fragments off the thigh with the right hand (the
hammerstone itself or an extended finger may be used); (ix) grasping
of a detached flake or fragment with the right hand to remove it from
the thigh, usually with a side-to-side ‘scissor’ grip of index and middle
1330 D. Stout et al.

Table 1. Frequency of technological actions in fMRI stimuli indication plus a 1-s fixation screen, giving a total duration of 15 s.
Trials were interleaved so that in each session, experimental trials took
Action Hand Control Oldowan Acheulean place in blocks of two or three. Each session comprised one repetition
of each of the six conditions; the order was pseudo-randomized to
Percussion R 81 36 26
Shift core grip L 39 12 13 avoid repetition of the type of stimulus in consecutive trials and of
Rotate core L 37 16 7 individual stimulus videos within a session. Presentation of stimuli
Shift hammerstone grip R 3 0 8 and recording of participants’ responses were carried out using Cogent
Invert core L 0 2 7 (http://www.vislab.ucl.ac.uk/cogent_graphics.php) running in Mat-
Change hammerstone R 0 1 3
lab 6.5 (MathWorks).
Abrade ⁄ micro-flake R 0 0 12
Sweep R 0 14 8
Grasp flake R 0 8 3
Flakes detached N⁄A 0 29 16 fMRI recording and preprocessing
In each of the six experimental sessions, a T2*-weighted, gradient-
echo, echo-planar imaging sequence was used to acquire 164 40-slice
fingers, rarely (twice) with a pad-to-pad ‘pincer’ grip of thumb and (2 mm thickness and 1 mm gap; TE = 65 ms; a = 90 ) volumes
index finger (Supporting Information Video S1). Importantly, the total covering the whole brain and cerebellum with an in-plane resolution
number of actions declines from Control to Oldowan to Acheulean of 3 · 3 mm (64 · 64 matrix, fov 192 · 192 · 144 mm3;
stimuli. This is also true for right- and left-hand actions considered TR = 2600 ms). A high-resolution (1 · 1 · 1 mm3) structural image
separately. Thus, increasing activation across conditions must be (MPRAGE sequence) was also collected.
explained in terms of the increasing diversity and causal ⁄ intentional fMRI data were analysed using SPM8 (http://www.fil.ion.ucl.ac.uk/
complexity of actions rather than their simple quantity. spm) procedures, running in Matlab 7.6 (MathWorks), after
There are four action types that are substantially more numerous in, discarding the first four dummy volumes in each session to allow
or unique to, Acheulean stimuli: hammerstone grip shifts; hammer- for T1 equilibrium effect. Slice timing correction was applied to
stone changes; core inversions; and abrasion ⁄ micro-flaking. These correct for offsets of slice acquisition. EPI volumes were realigned to
actions are all components of the distinctive ‘platform preparation’ the first volume for each subject to correct for interscan movement,
operation discussed above, and their frequency directly reflects the and unwarped for movement-induced inhomogeneities of the magnetic
greater technological complexity of Late Acheulean toolmaking. This field using realignment parameters (Andersson et al., 2001). EPI
complexity includes increased contingency on detailed variation in volumes were stereotactically normalized into the standard space
hammerstone properties, grips and gestures, and in core morphology, defined by the Montreal Neurological Institute (MNI) using a two-step
orientation and support, as well as a greater hierarchical depth of procedure: the mean EPI image created during realignment was
action planning. coregistered with the structural image, which was spatially normalized
to the SPM T1 template using a 12-parameter affine and non-linear
cosine basis function transformation, both transformations being
fMRI paradigm subsequently applied to all EPI volumes. Normalized images were
Subjects lay supine in the 3T Siemens Allegra MRI scanner at the smoothed using an 8-mm isometric Gaussian kernel to account for
Wellcome Trust Centre for Neuroimaging, pads positioned on the side residual inter-subject differences in functional anatomy (Friston et al.,
of the head to reduce movement. Subjects underwent six sessions of 2007).
approximately 7 min, and each session comprised 12 trials, corre-
sponding to one repetition of six experimental conditions defined by a
three · two factorial plan. fMRI statistical analysis
Analysis of the functional imaging data entailed the creation of
1. Stimulus: 20-s video clips of the Control stimulus, Oldowan or
statistical parametric maps representing a statistical assessment
Acheulean toolmaking.
of hypothesized condition-specific effects (Friston et al., 1994).
2. Task: following stimulus presentation, subjects were instructed
A random effect procedure was adopted for data analysis. Within
either to simulate themselves continuing to perform the action they
individual subjects, the 20-s stimulations were modelled for the three
saw (Imagine) or to decide whether, in their opinion, the actor was
types of stimuli (Control, Oldowan, Acheulean), the 5-s tasks were
successful in achieving his goal (Evaluate).
modelled for the three types of stimuli and two tasks (Imagine, Evaluate),
Prior to entering the scanner, subjects were instructed to watch each and the motor responses were modelled as events (duration 0) irrespective
video ‘carefully’, to ‘try to understand what the demonstrator is doing’ of the experimental condition. Rest was modelled as a 12-s condition.
and that after each video they would be ‘asked to do one of two Each condition was defined with a boxcar function convolved with SPM8
things’, which were then explained. In the scanner, each trial was canonical haemodynamic response function to estimate condition-
started by the presentation of the stimulus, followed by: (i) 1.5 s of a specific effects with the General Linear Model. Low-frequency drifts
fixation cross; (ii) a written instruction indicating the Task (‘Imagine’ were removed by a high-pass filtering with a cut-off of 128 s.
or ‘Evaluate’) that remained on screen for 5 s; and (iii) a response The current analysis focused on the response to Acheulean,
screen displaying the appropriate question (‘Did you finish?’ or ‘Was Oldowan and Control stimuli, with individual subjects’ statistical
he successful?’). The side for yes and no responses was randomly maps for the four contrasts [Toolmaking: (Acheulean–Control) +
assigned to the left and right button press and indicated by the position (Oldowan–Control); Acheulean–Control, Oldowan–Control, Acheu-
of the words ‘Yes’ and ‘No’ on screen. The response screen remained lean–Oldowan] entered in second-level analyses of variance, with the
visible for 1.5 s or until subjects replied, and was followed by a group (Naı̈ve n = 11, Trained n = 10, Expert n = 5) as between-
fixation screen (minimum 1 s) for a total trial duration of 29 s. In subjects factor. As all groups comprise neurotypical adults, we
addition, each session included four 12-s rest trials, each of which hypothesized equal variance between populations in order to control
started with a 1-s ‘Rest’ indication, and ended with a 1-s ‘End of rest’ for differences in group size (Penny & Holmes, 2003).

ª 2011 The Authors. European Journal of Neuroscience ª 2011 Federation of European Neuroscience Societies and Blackwell Publishing Ltd
European Journal of Neuroscience, 33, 1328–1338

Common brain response irrespective of expertise was investigated
using a minimum statistic conjunction (Nichols et al., 2005) between
the three groups. Brain response specific of each group was assessed
by masking exclusively the effect of this group by a global null
conjunction (P < 0.05 uncorrected) of the other two groups; for
instance, the contrast between Acheulean and Oldowan in Naı̈ve is
exclusively masked by a conjunction of the same contrast in Trained
and Expert subjects. Our procedure used exclusive masking instead of
interactions, which were not significant at the threshold used, to favour
the effects within the group of interest over the reversed effects in the
other groups, which are included in the statistics of interactions
(Culham, 2006). All contrasts were thresholded at P < 0.05 FDR-
corrected with an extent threshold of 20 voxels.
Anatomical localization was performed using a brain atlas (Duver-
noy, 1999) and, in particular for inferior frontal and parietal clusters,
functional localization made use of distribution analysis of the
activated voxels on the basis of probabilistic cytoarchitectonic maps
(Eickhoff et al., 2007) implemented in SPM (Eickhoff et al., 2005).
For the sake of consistency, only anatomical labels are used in the
tables. Thus, clusters attributed to Brodmann area (BA) 44 were
labelled ‘pars opercularis’ (Amunts et al., 1999), those attributed to
BA45 were labelled ‘pars triangularis’ (Amunts et al., 1999), and
those attributed to BA6 were labelled ‘precentral gyrus’ (Geyer, 2003).
In the parietal cortex, clusters attributed to areas PF and PG (Caspers
et al., 2006) were labelled ‘inferior parietal lobule’, and those
attributed to hIP1 and hIP2 (Choi et al., 2006) were labelled ‘anterior
intraparietal sulcus’. While recognizing that functional localization
and anatomical landmarks may not strictly overlap in individuals,
these conventions were adopted in the interest of coherence in the
presentation of results. Statistical maps were rendered on FreeSurfer’s
fsaverage pial surface with 50 inflation steps (http://surfer.nmr.
mgh.harvard.edu).
Local activity
In order to assess the effect of Group, local activity in clusters of
interest was further characterized using the SPM extension toolbox
MarsBar (http://marsbar.sourceforge.net/) to extract percentage
signal change in 5-mm radius volumes centred on the maximum of
each cluster, then analysed with spss.
Fig. 1. Left: local brain activity in Toolmaking–Control irrespective of subject expertise (FDR P < 0.05, extent k > 20). Rendered with freesurfer on top, lateral and
ventral views of the two hemispheres in neurological convention (details in Methods and Table 1). Right: percent signal change across the three technologies in the
right pars triangularis (***P < 0.001; *P < 0.05).
ª 2011 The Authors. European Journal of Neuroscience ª 2011 Federation of European Neuroscience Societies and Blackwell Publishing Ltd
European Journal of Neuroscience, 33, 1328–1338
Technology and cognition in human evolution 1331
Results
Toolmaking–Control
Common response
Across all subject groups, the contrast of Toolmaking conditions with
Control yielded activations is a series of cortical regions, including a
large cluster extending from the primary visual and lateral occipital
cortices to the inferior temporal cortices, intraparietal sulci, inferior
parietal cortices and postcentral gyrii bilaterally. In the frontal cortex,
responses were found in right pars triangularis and bilateral pars
opercularis of the inferior frontal gyrus, as well as in the dorsal
precentral gyrii bilaterally (Fig. 1; Table 2).
Two-way (Stimulus, Group) analysis of variance of the extracted
percent signal change in the right pars triangularis revealed a main
effect of Stimulus (P < 0.001), with no effect of Group (P = 0.9) or
interaction between Stimulus and Group (P = 0.5; see Fig. 1, right).
All pairwise comparisons between stimuli are significant (Oldowan vs.
Control P = 0.001; Acheulean vs. Control P < 0.001; Acheulean vs.
Oldowan P = 0.016).
Effect of expertise
The exclusive masking procedure used to isolate brain responses to the
observation of Toolmaking stimuli unique to each level of expertise
identified clusters (Fig. 2; Table 2) in the bilateral ventral precentral
gyrus and left middle occipital gyrus in the Naı̈ve group, and in the left
superior parietal and right postcentral gyrus of Experts. Activations
unique to the Trained group were much more numerous particularly in
the frontal cortices, including medial frontal cortex, the right pars
orbitalis, left pars triangularis, bilateral pars opercularis, right
anterior insula, left posterior middle frontal gyrus and left precentral
gyrus, as well as left middle temporal gyrus and right inferior temporal
gyrus.
Acheulean vs. Oldowan
Common response
The minimum statistic conjunction between the three groups for the
contrast Acheulean–Oldowan identified increases in activity in the
anterior part of the left intraparietal sulcus (Fig. 3; Table 3), and in
the left prefrontal cortex within the inferior frontal sulcus.
1332 D. Stout et al.

Table 2. Brain activity in response of the observation of Toolmaking

compared with Control stimuli, common to the three groups (minimum
statistic conjunction) and by subject expertise (exclusive masking)

Location x y z Z-score Extent

Conjunction
Frontal lobe
Left Dorsal precentral gyrus )32 )8 58 4.39 421
Right Dorsal precentral gyrus 30 )8 54 4.66 1003
Right Pars opercularis 60 10 26 5.68 747
Left Pars opercularis )54 8 22 4.89 612
Right Pars triangularis 50 44 10 3.23 53
Right Insula 40 )4 8 5.40 328
Left Insula )42 )4 2 4.04 Fig. 2. Local brain activity in Toolmaking–Control for Naı̈ve (left), Trained
Parietal lobe (centre) and Expert (right) subjects (FDR P < 0.05, extent k > 20).
Left Intraparietal sulcus )26 )52 62 5.25 –
Left Postcentral gyrus )30 )44 62 5.91 19 098 the pars opercularis of the inferior frontal gyrus (Fig. 4; Table 3). The
Right Intraparietal sulcus 32 )60 56 5.39 –
Right Postcentral gyrus 36 )40 56 5.06 –
latter activation was in a similar location to that previously reported for
Right Supramarginal gyrus 66 )20 36 5.82 – the actual performance (as opposed to observation) of stone toolmaking
Left Supramarginal gyrus )64 )20 36 5.46 – (Stout & Chaminade, 2007). No cluster survived the thresholds used in
Temporal lobe this analysis for Trained subjects.
Left Inferior temporal gyrus )48 )64 )10 5.40 – In Experts (Fig. 4; Table 3), there were clusters in the right medial
Left Fusiform gyrus )48 )50 )20 5.57 – frontal and parietal cortices. The latter were localized in the inferior
Right Fusiform gyrus 34 )46 )28 5.72 – parietal lobule, and in the anterior intraparietal sulcus area hIP1 (Choi
Occipital lobe et al., 2006; see also Jubault et al., 2007).
Right Middle occipital gyrus 44 )84 12 5.23 –
Left Calcarine fissure )8 )84 4 3.40 209
Right Middle occipital gyrus 40 )78 )4 5.12 –
Discussion
Basal ganglia
Right Thalamus 14 )26 8 4.89 947 To identify brain systems involved in the observation of Paleolithic
Left Thalamus )16 )32 )4 3.32 114 toolmaking, we examined contrasts of toolmaking observation with a
Naı̈ve only control condition. Results were remarkably similar to those obtained
Left Precentral gyrus )58 )2 30 3.81 34 from previous FDG-PET studies of toolmaking execution, despite the
Right Precentral gyrus 64 0 28 3.80 29 different experimental tasks and imaging modalities used. This
Left Middle occipital gyrus )22 )88 14 4.76 31
indicates that neural systems involved in the observational under-
Trained only standing of Paleolithic toolmaking are very similar to those involved
Left Precentral gyrus )18 )10 64 4.44 242 in execution.
Left Middle frontal gyrus )24 4 54 4.19 –
Left Medial frontal cortex )12 4 48 3.95 – To investigate the effects of expertise on toolmaking observation,
Left Precentral gyrus )38 )6 42 4.04 – we examined the unique responses of each subject group (Naı̈ve,
Right Intraparietal sulcus 44 )48 40 3.83 31 Trained and Expert) to Toolmaking stimuli. This provided evidence
Left Pars opercularis )42 8 30 4.19 369 for the functional ‘reorganization’ (Kelly & Garavan, 2005) of
Right Pars opercularis 60 20 12 3.78 –
Left Pars triangularis )54 40 8 4.81 287
activation between groups, reflecting expertise-dependent shifts in
Right Anterior insula 34 20 2 3.94 165 cognitive strategy.
Right Pars orbitalis 48 48 )4 3.77 107 To investigate the specific demands of understanding increasingly
Left Middle temporal gyrus )60 )62 )6 4.04 36 complex Paleolithic technologies, we examined the contrast in brain
Right Inferior temporal gyrus 62 )56 )10 4.24 38 response to Acheulean vs. Oldowan stimuli in Naı̈ve, Trained and
Experts only Expert subjects. This revealed a significant main effect of technological
Left Superior parietal lobule )10 )52 74 4.46 159 complexity across groups, as well as distinct responses in the Naı̈ve and
Right Postcentral gyrus 48 )30 62 3.87 25
Expert groups. The localization of these expertise-dependent effects
All results are FDR P < 0.05, extent k > 20. All coordinates MNI. suggests that stone toolmaking action understanding depends on a
complex mixture of top-down, bottom-up, conceptual and embodied
In agreement with SPM whole-brain investigation, analysis of processes (cf. Grafton, 2009).
variance of activity extracted in these clusters indicated a main effect
of the stimulus (both P < 0.001), while there was no effect of Group
or interaction between Group and Stimulus (all P > 0.3) in these Contrasts of Toolmaking with Control condition
regions. Activity in Acheulean was significantly increased compared Common response
with Oldowan (P < 0.001) and Control (P < 0.05) for the left Contrasts of toolmaking stimuli with Control yielded activations in a
prefrontal cortex cluster, and all pairwise comparisons were significant series of cortical regions, notably including inferior frontal gyrus,
(P < 0.001) for the anterior intraparietal sulcus. dorsal premotor cortex, intraparietal sulcus and the inferior parietal
lobule (Fig. 1; Table 1). Activations in these regions have com-
Effect of expertise monly been reported in imaging studies of action observation
In Naı̈ve subjects, there were activations for Acheulean–Oldowan in the (Grezes & Decety, 2001; Grafton, 2009; Caspers et al., 2010),
left frontal cortex, dorsally in the superior frontal gyrus and ventrally in and they are thought to comprise a network supporting action

ª 2011 The Authors. European Journal of Neuroscience ª 2011 Federation of European Neuroscience Societies and Blackwell Publishing Ltd
European Journal of Neuroscience, 33, 1328–1338
 Technology and cognition in human evolution 1333

Fig. 3. Left: local brain activity in Acheulean–Oldowan irrespective of subject expertise (FDR P < 0.05, extent k > 20). Right: percent signal change across the
three technologies in the left anterior intraparietal sulcus (top) and inferior frontal sulcus (bottom; ***P < 0.001; *P < 0.05).

Table 3. Brain activity in response of the observation of Acheulean compared with Oldowan toolmaking stimuli, common to the three groups (minimum statistic
conjunction) and by subject expertise (exclusive masking)

Location x y z Z-score Extent

Conjunction
Left Anterior intraparietal sulcus )50 )36 42 4.74 53
Left Pars triangularis )46 32 26 6.02 94
Naı̈ve only
Left Superior frontal gyrus )24 22 56 4.21 51
Left Pars opercularis )60 12 24 4.46 83
Experts only
Right Medial frontal cortex 6 42 50 5.25 24
Right Anterior intraparietal sulcus 46 )48 46 5.65 44
Right Inferior parietal lobule 62 )52 36 4.80 22

All results are FDR P < 0.05, extent k > 20. All coordinates MNI.

understanding through the covert simulation of observed behaviours.

Fig. 4. Local brain activity in Acheulean–Oldowan for Naı̈ve (left) and Expert
(right) subjects (FDR P < 0.05, extent k > 20).
In keeping with this, the observed activations closely match (see
also Supporting Information Fig. S2; Tables S1 and S2) those
reported in previous FDG-PET studies, in which subjects actively
produced tools rather than simply observing toolmaking (Stout &
Chaminade, 2007; Stout et al., 2008).
Particularly notable is activation of the pars triangularis of the right
inferior frontal gyrus. Pars triangularis activation is more typically
associated with linguistic processing (e.g. Bookheimer, 2002; Musso
et al., 2003), but has been reported during action observation (Johnson-
Frey et al., 2003; Molnar-Szakacs et al., 2005; Caspers et al., 2010). It
has been proposed (Rizzolatti & Craighero, 2004) that such activation
reflects the ‘syntactic’ processing of hierarchically organized actions
(cf. Koechlin & Jubault, 2006). This leads to the expectation that pars
triangularis activity should respond to variation in the complexity of
observed actions (Caspers et al., 2010). Such an effect of stimulus
complexity is observed here (Fig. 1), in keeping with previous findings
of pars triangularis activation during the execution of Acheulean, but
not Oldowan, toolmaking (Stout et al., 2008; Table 2).

ª 2011 The Authors. European Journal of Neuroscience ª 2011 Federation of European Neuroscience Societies and Blackwell Publishing Ltd
European Journal of Neuroscience, 33, 1328–1338
1334 D. Stout et al.
Effect of stone toolmaking method
Across groups, the increased technological complexity of Acheulean
stimuli compared with Oldowan (Table 1) was associated with
activation of the anterior intraparietal sulcus and inferior frontal
sulcus, both in the left hemisphere (Fig. 3; Table 3). The anterior
intraparietal sulcus is a core component of the putative human mirror
neuron system (Grafton & Hamilton, 2007). It is thought to contribute
to the understanding of ‘immediate’ action goals, such as grasping to
eat vs. to place in macaque monkeys (Fogassi et al., 2005), or taking a
cookie vs. a diskette in humans (Hamilton & Grafton, 2006).
In monkeys, the anterior bank of the intraparietal sulcus changes its
connectivity and response patterns when the animals train to use tools
(Hihara et al., 2006), enabling an integration of visual and somato-
sensory stimuli. This is argued to support tool use through assimilation
of the tool into the monkey’s body schema (Maravita & Iriki, 2004),
such that ‘tools become hands’ (Umiltà et al., 2008). However, human
left anterior inferior parietal lobule displays a specific response to
observed tool use (as opposed to unassisted manual prehension) that is
absent in monkeys (Peeters et al., 2009). This suggests that hominoid
anterior inferior parietal cortex may be evolutionarily derived to play a
new role in coding the distinct functional properties of hand-held tools
(Johnson-Frey et al., 2005; Peeters et al., 2009; Jacobs et al., 2010;
Povinelli et al., 2010).
The centre of anterior inferior parietal cortex activation reported
here is somewhat posterior ()50, )36, 42 vs. )52, )26, 34) to that of
Peeters et al. (2009); however, extraction of the volume of interest
used by Peeters et al. (coordinates from Orban, pers. comm.) confirms
that the same effect of stimulus is indeed present in this region. This
response to increasingly complex Paleolithic toolmaking is consistent
with the hypothesis that human technological evolution was sup-
ported, at least in part, by the emergence of enhanced neural
mechanisms for representing the causal properties of hand-held tools
(Johnson-Frey, 2003; Wolpert, 2003; Peeters et al., 2009).
The main effect in the prefrontal cortex was centred on the inferior
frontal sulcus. In macaques, this region is heavily interconnected with
the anterior inferior parietal lobule (Pandya & Seltzer, 1982) and the
parietal operculum (Preuss & Goldman-Rakic, 1989), in keeping with
the co-activation observed here, and suggesting involvement in the
integration of visuospatial and somatosensory information. In an fMRI
study with macaques, there was activation in this area during the
observation of actions (Nelissen et al., 2005). In contrast to more the
posterior premotor cortex (F5c) where mirror neurons were originally
recorded, the ventral prefrontal cortex also responded to abstract or
context-free stimuli, including isolated hands, robotic hands and
shapes (Nelissen et al., 2005), indicating representation and integra-
tion of actions at a relatively high level. In humans, activation of
similar coordinates is reported during observation and preparation to
imitate complex hand postures (guitar chords), perhaps indicating a
role for this region in the selection and combination of motor elements
into novel actions (Vogt et al., 2007).
It is thus likely that the increase in prefrontal activation for
Acheulean–Oldowan reflects the greater temporal and relational
complexity of Acheulean toolmaking actions, which, to a greater
extent than Oldowan flaking, are organized into flexible and internally
variable action chunks, such as ‘platform preparation’ vs. ‘primary flake
removal’ (Pelegrin, 2005; Stout, 2011). No significant prefrontal
activation was observed for Oldowan–Control, in keeping with
previous conclusions regarding the relative simplicity of Oldowan
action sequences (Stout & Chaminade, 2007; Stout et al., 2008).
On this interpretation, the anterior inferior parietal cortex and the
inferior frontal sulcus form a parieto-frontal circuit involved in
ª 2011 The Authors. European Journal of Neuroscience ª 2011 Federation of European Neuroscience Societies and Blackwell Publishing Ltd
representing episode-specific intentions, causal relations and multi-
component action sequences during toolmaking observation. The
apparent abstraction (Hamilton & Grafton, 2006; Badre & D’Esposito,
2009) of causal ⁄ intentional processing in this circuit may be compared
with a proposed ‘intermediate’ level representing ‘intentions in action’
as goal-oriented sequences of motor commands and predicted
outcomes (de Vignemont & Haggard, 2008).
Expertise effects on response to stimuli
Varying expertise across subject groups was associated with qualitative
shifts in the set of brain regions activated in response to Acheulean
compared with Oldowan stimuli (Fig. 4; Table 3). These differences
suggest a functional reorganization (Kelly & Garavan, 2005) involving
the adoption of different cognitive strategies for action understanding.
Naı̈ve subjects show activation in core motor resonance structures
together with the ventral prefrontal cortex, as expected for a low-level
strategy of novel action understanding through kinematic simulation.
Trained subjects show strong, statistically indistinguishable responses
to both Oldowan and Acheulean stimuli, perhaps reflecting the
particular social context and motivational set associated with training.
Finally, Expert subjects display activation in the medial prefrontal
cortex, a classic ‘mentalizing’ region, suggesting a relatively high-
level, inferential strategy of intention reading.
Naı̈ve subjects
One cluster exclusive to technologically Naı̈ve subjects occurred in the
pars opercularis of the left posterior inferior frontal gyrus (Fig. 4,
left). Pars opercularis is another core component of the putative
human mirror neuronal system (Rizzolatti & Craighero, 2004), which,
in contrast with the performance-monitoring functions of the anterior
inferior parietal cortex described above, is thought to be responsible
for the generation of the kinematic models used to execute (Fagg &
Arbib, 1998) or simulate (Carr et al., 2003; Grafton & Hamilton,
2007; Kilner et al., 2007) motor acts.
Also unique to Naı̈ve subjects was activation of the superior frontal
gyrus, anterior to the frontal eye field (Lobel et al., 2001). Activation
of this area is associated with the selection among competing
responses (Petrides, 2005), and the more superior portion activated
here is especially involved in the spatial domain (Volle et al., 2008).
During imitation, this region may serve to maintain a representation of
the observed goal in short-term working memory for later execution
(Chaminade et al., 2002). Co-activation of the superior frontal gyrus
and posterior inferior frontal gyrus may thus reflect Naı̈ve reliance on
kinematic simulation and top-down direction of attention to task-
relevant spatial cues. When combined with the anterior inferior
parietal and ventral prefrontal activations observed across all groups,
these Naı̈ve activations match the general expectations of a simulation
model of novel action understanding (Buccino et al., 2004; Vogt
et al., 2007).
Trained subjects
No activations exclusive to Trained subjects were observed in the
Acheulean–Oldowan contrast. Comparison with the numerous activa-
tions observed in the contrast of Toolmaking–Control for Trained
subjects (Table 2; Fig. 2) indicates that this result derives from the
presence of similar responses to Oldowan and Acheulean stimuli
rather than from the absence of significant differences from Control.
This is corroborated by the observation of similar activations in
separate contrasts of Oldowan–Control and Acheulean–Control
(Supporting Information Figs S3 and S4; Tables S1 and S2). The
Trained response to both Oldowan and Acheulean stimuli includes:
European Journal of Neuroscience, 33, 1328–1338

(i) clusters in the anterior insula, lateral premotor cortex, frontal
eye field and supplementary eye field likely related to attentional
and affective engagement with the stimuli; and (ii) ventral
prefrontal clusters likely associated with parsing of observed action
sequences.
Insular activations unique to Trained subjects are in an anterior
region associated with interoception, subjective feeling and perceptual
awareness (Kikyo et al., 2002; Ploran et al., 2007; Craig, 2009).
Activations of the left medial frontal cortex (close to y = 0) and
posterior middle frontal gyrus appear to fall within the supplementary
and frontal eye fields (Tehovnik et al., 2000), functional regions
associated with saccades, visual attention and visual learning
(Tehovnik et al., 2000; Grosbras et al., 2005). Together with activa-
tion of the precentral gyrus, a region commonly recruited during
action observation (Grezes & Decety, 2001; Caspers et al., 2010),
these activations likely indicate intense engagement by Trained
subjects with the Toolmaking stimuli. These effects of training were
not predicted, but are consistent with the pragmatic social and
motivational context created by the training programme.
Also unique to Trained subjects were inferior frontal gyrus
activations of bilateral pars opercularis, left pars triangularis and
right pars orbitalis. These are probably best understood in terms of the
putative role of the inferior frontal gyrus in the multi-level processing
of stimuli along a posterior to anterior gradient of increasing
hierarchical complexity (Koechlin & Jubault, 2006; Caspers et al.,
2010), and may reflect the intense processing of all Toolmaking
stimuli by highly motivated Trained subjects.
Expert subjects
Activations exclusive to Expert subjects were observed in the medial
frontal cortex, anterior intraparietal sulcus and inferior parietal lobule of
the right hemisphere (Fig. 4, right). The medial frontal cortex is a core
element in the network of brain regions associated with the attribution of
mental states (Frith & Frith, 2006), suggesting that Expert subjects rely
on top-down interpretation of the demonstrator’s intentions in order to
differentiate Acheulean from Oldowan toolmaking. The activation is
centred at the border between a posterior region associated with the
attribution of ‘private’ action intentions and an anterior region
associated with communicative intentions (Grèzes et al., 2004a,b;
Amodio & Frith, 2006), in a position closely approximating that
activated when mentalizing about the internal states of a dissimilar other
(Mitchell et al., 2006). It may reflect inference about the private
technological ‘prior intentions’ of the demonstrator (Chaminade et al.,
2002), rather than meta-cognition about the demonstrator’s communi-
cative intentions toward the observer (Amodio & Frith, 2006: 274).
Activation of the right anterior intraparietal sulcus in Experts is
comparable to expertise effects found in studies of dance observation
(Calvo-Merino et al., 2005, 2006; Cross et al., 2006). The more anterior
location the current activation may reflect somatotopy of response to the
observation of upper vs. lower limb actions (Buccino et al., 2001). This
particular region of right anterior intraparietal sulcus has also been
linked with the preparation of successive sensorimotor task-sets during
action sequence execution (Jubault et al., 2007).
Also activated in Experts was a region of right inferior parietal
lobule known to support the stimulus-driven allocation of spatial
attention (Corbetta & Shulman, 2002; Mort et al., 2003) during
visuospatial sequence learning (Rosenthal et al., 2009). This activa-
tion is posterior to the region associated with action outcome
monitoring by Hamilton & Grafton (2008), and together with the
right anterior intraparietal sulcus activation probably reflects Expert
recognition of familiar toolmaking action sequences.
ª 2011 The Authors. European Journal of Neuroscience ª 2011 Federation of European Neuroscience Societies and Blackwell Publishing Ltd
European Journal of Neuroscience, 33, 1328–1338
Technology and cognition in human evolution 1335
Broader implications
Contrasts with Control show that the observation of Paleolithic
toolmaking recruits cognitive control mechanisms in the pars
triangularis of the right inferior frontal gyrus, and that this response
increases with the technological complexity of the observed actions.
This matches results from earlier studies of subjects actively making
stone tools, and is consistent with an evolutionary scenario in which
manual and perceptual-motor adaptations were critical to the earliest
stages of human technological evolution (Wynn & McGrew, 1989;
Ambrose, 2001; Byrne, 2004; Bril & Roux, 2005; Stout & Chamin-
ade, 2007), but later developments were more dependent on enhanced
cognitive control (Faisal et al., 2010; Stout, 2010). These findings
support long-standing intuitions regarding the cognitive sophistication
of Acheulean technology (e.g. Oakley, 1954; Wynn, 1979; Gowlett,
1986), and specifically highlight the complex hierarchical organization
(Holloway, 1969; Stout et al., 2008) of Acheulean action sequences.
This interpretation is further supported by the main effect of stimulus
in the anterior inferior parietal and ventral prefrontal cortices across
subject groups.
Differing responses to stimulus complexity between groups provide
insight into the effects of expertise on action observation strategies.
Activations specific to Naı̈ve subjects suggest a strategy reliant on
kinematic simulation (inferior frontal gyrus) and the top-down
direction of visuospatial attention (superior frontal gyrus). This
supports an account of early observational learning in which
simulation of low-level action elements interacts with representations
of mid-level intentions in action to produce a ‘best-fit’ understanding
of complex, unfamiliar actions (cf. Vogt et al., 2007).
Interestingly, Trained subjects responded equally to Oldowan and
Acheulean stimuli, activating a set of frontal regions related to
subjective awareness, visual attention and multi-level action parsing.
This unexpected result may reflect a strong motivation to attend to,
analyse and understand all Toolmaking stimuli, generated by the social
and pragmatic context of being a ‘learner’ (cf. Lave & Wenger, 1991;
Stout, 2002). There is increasing awareness of the importance of such
social and affective dimensions in understanding human cognitive
evolution (Holloway, 1967; Hare & Tomasello, 2005; Burkart et al.,
2009; Stout, 2010).
Unlike Naive and Trained subjects, Experts recruited a mixture of
bottom-up, familiarity-based posterior parietal mechanisms for visuo-
spatial attention (right inferior parietal lobule) and sensorimotor
matching (anterior intraparietal sulcus) with high-level inference
regarding technological ‘prior intentions’ in the medial frontal cortex.
In this context, shared pragmatic skills may provide the foundation for
sharing of higher level intentions, in keeping with the Motor
Cognition Hypothesis (Gallese et al., 2009). More broadly, the
apparent shift in observation strategy from Naive kinematic simulation
to Expert mentalizing is consistent with a ‘mixed’ model of action
understanding (Grafton, 2009) involving contextually variable inter-
actions between bottom-up resonance and top-down interpretation.
Complex, pragmatic skills like stone toolmaking can only be
acquired through deliberate practice (Pelegrin, 1990; Whittaker, 1994)
and experimentation (Ericsson et al., 1993), leading to the discovery of
subtle causal relations that would remain ‘opaque’ (Gergely & Csibra,
2006) to observation and simulation alone. Mid-level ‘intentions in
action’ represented in the anterior inferior parietal and the ventral
prefrontal cortices, though likely to be inaccurate at first, appear to be
important across skill levels and may play an important role in guiding
such practice, perhaps contributing to the high fidelity of human social
learning (the ‘ratchet effect’: Tomasello, 1999; Tennie et al., 2009). The
effect of Toolmaking complexity in the anterior inferior parietal lobule
1336 D. Stout et al.
in particular suggests that this phylogenetically derived (Peeters et al.,
2009) region may have played a key role in human technological
evolution 2.6–0.5 million years ago.
Supporting Information
Additional supporting information may be found in the online version
of this article:
Fig. S1. Handaxes produced (a–c) by Trained subjects, (d) by the
expert demonstrator, and (e) from the Middle Pleistocene (approxi-
mately 500 000 years ago) site of Boxgrove, West Sussex, UK.
Fig. S2. Local brain activity in Oldowan–Control (left) and Acheu-
lean–Control (right) irrespective of subject expertise (FDR P < 0.05,
extent k > 20). To more directly compare current results with previous
FDG-PET studies of Oldowan and Acheulean toolmaking execution,
we examined separate contrasts of Oldowan and Acheulean toolmak-
ing with the Control. This yielded activations of left ventral premotor
cortex in both contrasts (Oldowan: )56, 8, 22; Acheulean: )58, 10,
32), and of right pars triangularis in the Acheulean (46, 36, 4) but not
Oldowan contrast. This directly matches results from the execution of
Oldowan (ventral premotor cortex: )52, 6, 28) and Acheulean (ventral
premotor cortex: )52, 6, 28; pars triangularis: 48, 34, 10) toolmaking
(Stout et al., 2008; Table 2).
Fig. S3. Local brain activity in Oldowan–Control for Naı̈ve (left),
Trained (centre) and Expert (right) subjects (FDR P < 0.05, extent
k > 20).
Fig. S4. Local brain activity in Acheulean–Control for Naı̈ve (left),
Trained (centre) and Experts (right) subjects (FDR P < 0.05, extent
k > 20).
Table S1. Brain activity in response of the observation of Oldowan
compared with Control stimuli, common to the three groups
(minimum statistic conjunction) and by subject expertise (exclusive
masking). All results are FDR P < 0.05, extent k > 20.
Table S2. Brain activity in response of the observation of Acheulean
compared with Control stimuli, common to the three groups
(minimum statistic conjunction) and by subject expertise (exclusive
masking). All results are FDR P < 0.05, extent k > 20.
Video S1. Examples of Control, Oldowan and Acheulean stimuli used
in the experiment.
Please note: As a service to our authors and readers, this journal
provides supporting information supplied by the authors. Such
materials are peer-reviewed and may be re-organized for online
delivery, but are not copy-edited or typeset by Wiley-Blackwell.
Technical support issues arising from supporting information (other
than missing files) should be addressed to the authors.
Acknowledgements
This research was funded by European Union project HANDTOMOUTH. We
thank Bruce Bradley for acting as the expert demonstrator, and Stefan Vogt and
an anonymous reviewer for helpful comments.
Abbreviations
BA, Brodmann area; fMRI, functional magnetic resonance imaging; PET,
positron emission tomography.
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