Changes in Frontoparietotemporal Connectivity following Do-As-I-Do Imitation Training in Chimpanzees (Pan troglodytes)

Abstract

Changes in fronto-parieto-temporal connectivity following Do-As-I- Human imitation is supported by an underlying 'mirror system' principally 3 composed of inferior frontal (IF), inferior parietal (IP), and superior temporal (ST) 4 cortical regions. Across primate species, differences in fronto-parieto-temporal 5 connectivity have been hypothesized to explain phylogenetic variation in imitative 6 abilities. However, if and to what extent these regions are involved in imitation in non-7 human primates is unknown. We hypothesized that 'Do As I Do' (DAID) imitation 8 training would enhance white matter integrity within and between fronto-parieto-9 temporal regions. To this end, four captive chimpanzees (Pan troglodytes) were trained 10 to reproduce 23 demonstrated actions, while four age/sex-matched controls were trained 11 to produce basic husbandry behaviors in response to manual cues. Diffusion tensor 12 images were acquired before and after 600 minutes of training over an average of 112 13 days. Bilateral and asymmetrical changes in fronto-parieto-temporal white matter 14 integrity were compared between DAID trained subjects and controls. We found that 15 imitation trained subjects exhibited leftward shifts in both mean fractional anisotropy and 16 tract strength asymmetry measures in brain regions within the mirror system. This is the 17 first report of training-induced changes in white matter integrity in chimpanzees and 18suggests that fronto-parieto-temporal connectivity, particularly in the left hemisphere, 19 may have facilitated the emergence of increasingly complex imitation learning abilities.

The pervasive role of social learning in primate lifetime development

“…Direct evidence that apes can imitate bodily actions, even if with lower fidelity than children, comes from “Do-as-I-do” experiments in which the subject is taught to try to replicate a training set of bodily actions when requested, then tested on a novel battery of manual, facial and gross bodily movements. These were first reported for a young home-reared chimpanzee by Hayes and Hayes ( 1952 ), then later replicated with non-enculturated “lab” chimpanzees by Custance et al ( 1995 ) and Pope et al ( 2018 ) as well as with an enculturated adult orangutan by Call ( 2001 ). Evidence that chimpanzees observing others are cognitively encoding what they see in terms of actions comes from a case where in one juvenile this “spilled over” the normal inhibition that occurs while watching an act that may later be imitated.…”

Social Learning Strategies: Bridge-Building between Fields

“…In macaques and chimpanzees, most of this circuitry consists of frontal-temporal connections, whilst humans have more substantial temporal-parietal and frontal-parietal connections. Moreover, humans' comparatively expanded and plastic association cortex [122] may imply a greater role for developmental scaffolding [123] upon brain architecture underlying social learning capacities in humans versus nonhumans (but see [124]). Finally, connectome studies are revealing dedicated networks of neural connections underlying behavioral innovation [125], that link to regions of the primate brain (such as the lateral prefrontal cortex) that have expanded disproportionately during human evolution [126].…”

Teaching and curiosity: sequential drivers of cumulative cultural evolution in the hominin lineage

“…Evidence for action copying in wild great apes (and, likewise, unenculturated captive apes) is debated, but weak at best (CT et al unpublished data), whereas enculturated great apes, i.e. individuals that grew up with humans and were treated much like human babies are, do show evidence of action copying (Russon and Galdikas 1993;Tomasello et al 1993;Subiaul 2016), along with the requisite changes in brain structure that are required and that resulted from such "training" (Bard and Hopkins 2018;Pope et al 2018). This indicates that apes can be induced to socially construct the ability to imitate by exposure to rich inputs, perhaps especially numerous novel actions and/or long sequences of actions with unexpected outcomes.…”