Tool use and syntactic skills improve each other via shared neural patterns in the basal ganglia

Claudio Brozzoli, Simon Thibault, Veronique Boulenger and Alice Roy

Longstanding theories have claimed a motor origin of language during evolution (1-2). The
advent and refinement of tool use may have offered the neural niche for the coevolution of
new cognitive skills serving both motor and communicative aims (3-6). Functions responding
to demands of the motor system would therefore have met communicative needs and
progressively been exapted and recycled for language (5, 7). Studies have shown that tool use
and syntactic processing of language display neural similarities in the basal ganglia (BG) and
the left inferior frontal gyrus. These lines of research have yet grown apart, and the
anatomical overlap between tool use and syntax remains anecdotal. Here, we questioned the
extent and functional relevance of this potential overlap in healthy right-handed participants
(20-40yo). Then, we behaviorally assessed cross-domain transfer from tool-use learning to
syntactic processing and from syntax training to tool-use ability. Using fMRI (n=20), we
examined object and subject relatives comprehension and, as a control, working memory
(WM). Additionally, participants performed a motor task using a tool or the free hand. We
examined the anatomical overlap between tool use and syntax activations, together with its
functional relevance, through conjunction and representational similarity analyses (RSA). In a
first behavioral experiment (n=78), we tested cross-domain benefits of motor training onto
syntax. Motor training consisted of inserting pegs with either the tool or the free hand. In a
further experiment (n=39), we controlled for motor difficulty as an unspecific factor of
transfer, by comparing two groups trained as previously (tool or free hand) with a third group
undergoing a hand training mimicking tool-use constraints. Finally, we tested the transfer in
the opposite direction (n=48), by assessing tool-use abilities after training with complex
syntactic structures (i.e. object relatives), or as a control, with simpler ones (i.e. subject
relatives). Tool-use planning and syntax networks both involved the left fronto-parietal cortex
and BG. Activity overlapped in the left caudate and the bilateral pallidum, where RSA
showed stronger patterns similarity between object relatives and tool use. No overlap was
found with hand planning nor between tool-use planning and WM. Behavioral experiments
showed that performance for most complex syntactic structures significantly improved only
after tool use, as compared to both free and constrained hand training. Furthermore, we
showed these benefits were bi-directional: training complex syntax improved tool-use
abilities, whereas training simpler syntax did not. Overall, our findings highlight the
functional overlap between tool-use planning and complex syntactic processing within the
BG. Behaviorally, this is reflected by bi-directional cross-domain transfer, where tool use
benefits to syntax and vice-versa. This network might subserve similar functions for tool use
and syntactic comprehension, such as handling complex hierarchical sequences, either in the
motor or linguistic domain. Accordingly, we posit the existence of a supramodal syntactic
function supported by the BG, the neural niche for a crucial co-evolution of motor and
linguistic functions.

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