Acquisition of Paleolithic toolmaking abilities involves structural remodeling to inferior frontoparietal regions

Abstract

Human ancestors first modified stones into tools 2.6 million years ago, initiating a cascading increase in technological complexity that continues today. A parallel trend of brain expansion during the Paleolithic has motivated over 100 years of theorizing linking stone toolmaking and human brain evolution, but empirical support remains limited. Our study provides the first direct experimental evidence identifying likely neuroanatomical targets of natural selection acting on toolmaking ability. Subjects received MRI and DTI scans before, during, and after a 2-year Paleolithic toolmaking training program. White matter fractional anisotropy (FA) showed changes in branches of the superior longitudinal fasciculus leading into left supramarginal gyrus, bilateral ventral precentral gyri, and right inferior frontal gyrus pars triangularis. FA increased from Scan 1-2, a period of intense training, and decreased from Scan 2-3, a period of reduced training. Voxel-based morphometry found a similar trend toward gray matter expansion in the left supramarginal gyrus from Scan 1-2 and a reversal of this effect from Scan 2-3. FA changes correlated with training hours and with motor performance, and probabilistic tractography confirmed that white matter changes projected to gray matter changes and to regions that activate during Paleolithic toolmaking. These results show that acquisition of Paleolithic toolmaking skills elicits structural remodeling of recently evolved brain regions supporting human tool use, providing a mechanistic link between stone toolmaking and human brain evolution. These regions participate not only in toolmaking, but also in other complex functions including action planning and language, in keeping with the hypothesized co-evolution of these functions.

The evolution of cognitive mechanisms in response to cultural innovations

“…This scenario is quite consistent with mounting evidence and recent views of experience-based imitation and emulation (110,111). It also suggests that similar processes are involved both in language learning and in complex imitation, which is in line with recent views according to which tool-making possibly preadapted the brain to language learning (27). Finally, our process-level approach may also help to explain recent new studies linking neuroanatomical changes in the brain to Paleolithic tool-making ability.…”

“…Finally, our process-level approach may also help to explain recent new studies linking neuroanatomical changes in the brain to Paleolithic tool-making ability. These studies found that the acquisition of tool-making abilities by experimental subjects involved specific structural changes in the brain (27) and that these structures and regions in the brain are more developed in humans than in chimpanzees (28). This evidence for a short-term plastic response colocalized with structures that underwent recent evolutionary change strongly suggests a process akin to the Baldwin effect, in which genetic variants are selected based on how well they support the required plastic changes (92,93).…”

“…This evidence includes signs of selection on genes implicated in brain growth, learning, and cognition (22)(23)(24) that may be attributed to human culture (21), and differences in gene expression in the brain between human and nonhuman primates (25,26) that may be interpreted similarly. There is also recent evidence relating structural changes in the human brain to Paleolithic tool-making abilities (27,28), but additional work is still needed to clarify the direction of causation between culture and cognition (we will return to discuss these findings toward the end of the paper). Finally, when animal culture is considered, a recent study (29) suggests an effect of culture on learning in songbirds: a larger repertoire size is found in species that developed open-ended learning ability.…”

Evolutionary neuroscience of cumulative culture

“…Experiments by Bril and colleagues have shown that fracture prediction and control is a demanding perceptual-motor skill reliably expressed only in expert knappers (28,29). Building on this work, Stout and colleagues (31,36,37) found that even 22 mo (x̄= 167 h) of knapping training produced relatively little evidence of perceptual-motor improvement, in contrast to clear gains in conceptual understanding.…”

“…Enlarged ape and human brains are expected to be more developmentally plastic and subject to inflection by somatic [e.g., bipedal locomotion, hand morphology (92)] and sensorimotor adaptations, and developmental niche construction (70). In fact, research with modern humans has shown that the acquisition of Paleolithic tool-making skills elicits plastic remodeling of dorsal stream white matter connections, including SLFIII's projection into the right vlPFC, even in adults (37). Functionally, the gray matter targeted by this projection is recruited by execution (93) and observation (83) of relatively complex tool-making sequences of the kind that appeared with Late Acheulean handaxe technology after about 0.7 Mya (50).…”