Contrasts of toolmaking stimuli with Control yielded activations in a series of cortical regions, notably including inferior frontal gyrus, dorsal premotor cortex, intraparietal sulcus and the inferior parietal lobule (Fig. 1; Table 1). Activations in these regions have commonly been reported in imaging studies of action observation (Grezes & Decety, 2001; Grafton, 2009; Caspers et al., 2010), and they are thought to comprise a network supporting action understanding through the covert simulation of observed behaviours. 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).
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 somatosensory 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’ (Umiltàet 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 supported, 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 integration 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 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. Naïve 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.
One cluster exclusive to technologically Naïve 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 Naïve 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 Naïve 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 Naïve activations match the general expectations of a simulation model of novel action understanding (Buccino et al., 2004; Vogt et al., 2007).
No activations exclusive to Trained subjects were observed in the Acheulean–Oldowan contrast. Comparison with the numerous activations 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: (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 activation 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.
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 communicative 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 activation 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.
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 & Chaminade, 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 Naïve 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 visuospatial 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 interactions 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 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.