Comparative evidence provides insight into the deep evolutionary origins of human cognition, but it cannot reveal details of the timing and context of more recent developments. Such evidence comes instead from the physical remains comprising the human paleontological and archeological records. Paleoneurological investigation of hominin cranial remains provides direct, if limited, evidence of brain evolution, whereas archeology provides evidence of past behavior.
Hominin cranial fossils preserve evidence of (a) overall brain size, (b) cerebral asymmetry, and (c) cortical sulcal patterns that leave impressions on the endocranial surface. As reported by Holloway, Broadfield, and Yuan (2004), currently available fossils suggest three major stages of hominin brain evolution. Stage 1, from approximately 3.5–2.0 million years ago (mya), consists of brain reorganization without substantial expansion and includes the relative expansion of posterior parietal association cortex at the expense of occipital visual cortex. This reorganization may have been an important precondition (Stout & Chaminade, 2007) for the emergence of stone tool making by 2.6 mya (Semaw et al., 2003). Stage 2, from 2.0 to 0.5 mya, begins with a sudden increase in brain size (500–750 ml) associated with the appearance of Homo habilis, followed by more gradual expansion (800–1,000 ml) related to body size increases in Homo erectus. Homo habilis also sees the first appearance of modern-human-like cerebral asymmetries, including enlargement of the Broca’s cap region of left LPFC. Stage 3, from 0.5 to 0.02 mya, consists of a rapid but continuous increase in brain size (1,000 to 1,500 ± 200 ml) without associated changes in body size. Finally, over the past 15,000 years, decreasing body size has brought human mean brain size down to around 1,400 ml.
Aside from enlargement of Broca’s cap in Homo habilis, evidence of frontal lobe size and organization from paleoneurology is limited. The fact that modern human frontal lobes are no bigger than expected for an ape brain of comparable size (Semendeferi et al., 2002) strongly suggests that this was also the case for ancestral hominins; however, much less can be said about the volume of specific regions of prefrontal cortex. There is some suggestion that Stage 1 involved a change in prefrontal lobe shape (Falk et al., 2000), perhaps indicative of functional reorganization, but this remains a tentative assessment (Holloway et al., 2004). The functional implications of an enlarged Broca’s cap in Stage 2 are also unclear, they but might suggest adaptations for language, gesture (Arbib, 2005), and/or instrumental action with objects (Stout & Chaminade, 2009). Paleoneurology thus provides invaluable evidence for broad patterns in hominin brain expansion, but it leaves many details about the evolution of particular systems and abilities unanswered. To some extent, these gaps may be filled through consideration of behavioral evidence from the archeological record.
The archeological record of human evolution is dominated by durable stone artifacts that have survived to be recovered by modern researchers. Fortunately for us, these tools and the refuse from their production can provide a surprisingly detailed record of individual actions and goal-directed sequences (e.g., Delagnes & Roche, 2005) going back as much as 2.6 million years. Somewhat less fortunately, there is no generally accepted method for inferring the cognitive processes underlying these reconstructed behaviors (Wynn, 2009), and widely divergent interpretations of the same evidence persist (e.g., Mithen, 1996; Noble & Davidson, 1996; Read & van der Leeuw, 2008; Wynn, 2002; Wynn & Coolidge, 2004). One response has been to develop an additional empirical basis for interpretation by using functional brain imaging to identify the neural correlates of particular Paleolithic technologies (Stout & Chaminade, 2007, 2009; Stout, Toth, Schick, & Chaminade, 2008; Stout, Toth, Schick, Stout, & Hutchins, 2000).
At first glance, the cognitive and behavioral complexity of Paleolithic tool production is easily underestimated. For example, the earliest known (Oldowan) stone tools consist of nothing more than sharp stone flakes struck from river cobbles (Semaw, 2006; Toth, 1985). However, even this simple technology requires substantial visuomotor coordination that must be developed through practice. Typically, flakes are produced by striking a cobble “core” held in one hand with a “hammerstone” held in the other. This requires 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 precise bimanual coordination to deliver highly forceful blows to small targets on the core. When these aspects of Oldowan skill are underdeveloped, as in trained apes or humans with insufficient experience, the products are diagnostically different from those found in the early archeological record (Stout & Chaminade, 2007; Toth, Schick, & Semaw, 2006).
In keeping with these behavioral observations, functional imaging studies indicate that proficient Oldowan flaking is especially reliant on posterior parietal mechanisms for object perception and bodily awareness and on ventral premotor control of manual prehension (Stout & Chaminade, 2007; Stout et al., 2008). This includes activation of portions of dorsal intraparietal sulcus that comprise a phylogenetically new functional area in humans, with novel response properties to central visual field stimuli and three-dimensional forms that are absent in monkeys (Orban et al., 2006). This leads to the conjecture that the emergence of Oldowan technology at 2.6 mya may have been enabled at least in part by the expansion of posterior parietal cortex in Holloway’s Stage 1. In contrast, imaging results do not indicate any exceptional demands of Oldowan flaking on PFC.
This likely reflects the fact that Oldowan action sequences are relatively simple and can be fully accounted for in terms of the following: (a) responsiveness to current core configurations and (b) a simple (Markovian) chaining together of flake removals in which the location of the next removal is determined from the previous one according to a simple rule (e.g., vertically adjacent, horizontally adjacent, alternate face) (cf. Delagnes & Roche, 2005; Wynn & McGrew, 1989). This suggests that the need for control processes like task shifting or the updating of working memory representations should be quite limited. Unfortunately, such interpretations are difficult to test given the lack of well-defined behavioral or neural criteria for identifying the recruitment of these putative cognitive functions. Alternatively, one might characterize Oldowan flaking as involving action selection based on sensory information and immediate context without the need to consider more temporally extended contingencies relating to past behaviors or ongoing subgoals. This assessment implicates the “sensory” and “contextual” levels of processing specified in the PFC model of Koechlin and Summerfield (2007), and it is in close agreement with the experimentally observed activations in motor (Brodmann area [BA] 4) and premotor (border between BA 6 and 44) cortex as well as the absence of activation in PFC.
Both interpretations support earlier characterizations (Bril & Roux, 2005; Wynn & McGrew, 1989) suggesting that Oldowan flaking does not directly implicate cognitive control demands beyond those seen in ape extractive foraging (e.g., Byrne & Russon, 1998). However, Oldowan flaking and ape foraging both exist in a broader behavioral context. For Oldowan and later stone technologies, this minimally includes the initial selection and transport of raw materials (Stout, Quade, Semaw, Rogers, & Levin, 2005), the effective use of tools after production (Schick & Toth, 2006), and the prior acquisition of relevant technological skills and knowledge (Stout, 2005). The details and cognitive implications of this broader context are not well known, but skill acquisition stands out as a key issue.
Available evidence indicates that it takes more than a few hours of practice to master even simple Oldowan flake production. Although novice flakers rapidly learn to identify and select appropriate targets (Stout & Chaminade, 2007), it takes much longer to develop the bodily techniques needed to reliably deliver forceful and accurate blows (Stout et al., 2008). Such skill acquisition requires the discovery of appropriate techniques through behavioral experimentation (Ericsson, Krampe, & Tesch-Romer, 1993) with various different grips, postures, and angles of percussion, as well as with hammerstones of varying size, shape, and density. Discovery of optimal techniques can be facilitated by explicit instruction or imitation of an expert model, but it minimally requires focused attention, self-monitoring, and the inhibition of automatic reactions during repetitious practice (Ericsson et al., 1993; Rossano, 2003). The necessity of such practice implies additional demands on both VMPFC and LPFC to support the full range of Oldowan behavior.
Functional imaging studies have not yet addressed the next major technological development in human evolution: the appearance by ∼1.7 mya (Roche et al., 2003) of intentionally shaped “large cutting tools” characteristic of the early Achuelean (Clark, 1994). The earliest Acheulean tools come in a variety of forms, including pointed, trihedral “picks” made from large cobbles and flatter, two-sided “handaxes” made by trimming the edges of very large (>15 cm) flakes produced from boulder cores. Both methods require a new level of hierarchical control over individual flake removals, which must be subordinated to the broader goal of shaping the piece. This might be expected to involve LPFC in the assembly of individual removals into a coherent action “chunk” (Koechlin & Jubault, 2006) and/or the management of increasingly abstract relations (Badre & D’Esposito, 2007) between individual flake removals and overall core shape. The latter could also be thought of as an increase in demands for the updating (sensu Miyake et al., 2000) or active use (Passingham & Sakai, 2004) of working memory representations. These intuitions make specific predictions regarding patterns of LPFC activation that should be testable in future research. It is also possible that the production of handaxes from large flakes produced in a previous technological operation implies an additional level of temporally extended “episodic” control (Koechlin & Summerfield, 2007). Unfortunately, this is likely to be much more difficult to test.
Brain activation data have recently become available for later Acheulean tool making, and they do provide evidence of associated LPFC activation (Stout et al., 2008). Later Acheulean handaxes, clearly present by ∼0.5 mya (e.g., Roberts & Parfitt, 1999), are much more refined than earlier examples, with sharper, more regular edges and a thinner cross-section. Such characteristics are very difficult to produce and clearly reflect intentional effort on the part of tool-makers (Edwards, 2001). There is some debate over the cognitive and/or functional implications of the symmetry seen in these forms (Machin, Hosfield, & Mithen, 2007; Wynn, 2002 and comments); however, it is the thinning of the cross-section that seems to present the greatest challenge for modern knappers (Winton, 2005). Thinning requires tool makers to strike very long flakes traveling more than halfway across the core surface. This in turn requires the careful preparation of edges and surfaces (platform preparation) through abrasion and/or micro-flaking before flake removal. Such platform preparation introduces a new subroutine into tool production, further increasing its hierarchical complexity and likely implicating additional demands for task shifting and inhibition of common actions that are inappropriate in a specific context. As expected for this level of hierarchical processing (Koechlin & Jubault, 2006), later Acheulean handaxe making is associated with activation of right BA 45 (i.e., the right homolog of anterior Broca’s area).
Although this brief review merely brushes the surface of the Paleolithic archaeological record, it is clear that technological changes over the past 2.6 million years provide evidence of increasing demands for cognitive control. These changes are consistent with a gradual evolution of LPFC function, although the role of technological change as cause, consequence, or indirect correlate of cognitive change remains unclear. Implications for VMPFC are less clear but should not be underestimated. Levels of tool-making performance evident by later Acheulean times are achieved by modern practitioners only after hundreds of hours of practice, and they are clearly indicative of well-developed capacities for self-regulation. Although perhaps not decisive, the expression of such skills strongly suggests learning facilitated by the instruction and/or imitation of an expert model (Stout, 2005). For example, independent rediscovery of effective later Achuelean thinning techniques can take years (Callahan, 1979) if it ever happens at all. Increasingly skilled technical performance in prehistory thus provides strong evidence of multilevel sensorimotor integration and somewhat weaker evidence of the social (Stout, 2005) and cognitive (Rossano, 2003) skills needed to establish, maintain, and learn from interactions with expert models. LPFC and VMPFC may make dissociable contributions to human cognitive control, but it appears to be their synergistic interaction that enables the complexity of modern human cognition and culture.