The neuroscience of primate intellectual evolution: natural selection and passive and intentional niche construction

Abstract

We trained Japanese macaque monkeys to use tools, an advanced cognitive function monkeys do not exhibit in the wild, and then examined their brains for signs of modification. Following tool-use training, we observed neurophysiological, molecular genetic and morphological changes within the monkey brain. Despite being 'artificially' induced, these novel behaviours and neural connectivity patterns reveal overlap with those of humans. Thus, they may provide us with a novel experimental platform for studying the mechanisms of human intelligence, for revealing the evolutionary path that created these mechanisms from the 'raw material' of the non-human primate brain, and for deepening our understanding of what cognitive abilities are and of those that are not uniquely human. On these bases, we propose a theory of 'intentional niche construction' as an extension of natural selection in order to reveal the evolutionary mechanisms that forged the uniquely intelligent human brain.

Figure 1

(a–c) Various modes of cortical body image codings, corresponding to putative hierarchy of internal representations (on the right, see also text). (a) When monkeys use a rake to retrieve distant food, the visual receptive field (b), encompassing the somatosensory receptive field (a), of a representative intraparietal bimodal neuron extended along the rake (c) when using, but did not (d) when not using it. (b) When monkeys use a monitor (experimental set-up shown in h), a visual receptive field of representative intraparietal bimodal neuron was formed around the hand in the monitor (a) encompassing its somatosensory receptive field (g). The visual receptive field altered to match the modified appearance of the hand in the monitor (b–d), extended along the rake when used under the monitor (e), and was confined around the tip of the rake once the image was blotted out except for the tip (f). (c) Combinatory usages (sequentially from a to e) of short and long rakes. (d) The left hemisphere of a monkey brain, with arrows A and B indicating somatosensory and spatial visual processing pathways that merge at the intraparietal area indicated by the red square where neurons were recorded. CS, central sulcus; IPS, intraparietal sulcus; LS, lateral sulcus. (e) Brain activation pattern for sequential combinatory tool usages, showing prefrontal in addition to parietal activation. (a–c and e, Adapted with permission from Maravita & Iriki 2004).

Figure 2

Framework for the ‘biological science of human intellect’. See text (§2e) for details.

Figure 3

Hierarchical structure of various classes of tools.

Figure 4

Comparison of evolutionary mechanisms (a) before early hominids by ‘natural selection’ and (b) modern human intellect by ‘intentional niche construction’.