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Left anterior supramarginal gyrus activity during tool use action observation after extensive tool use training

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Abstract

The advanced use of complex tools is considered a primary characteristic of human evolution and technological advancement. However, questions remain regarding whether humans possess unique underlying brain networks that support advanced tool-using abilities. Specifically, previous studies have demonstrated the presence of a structurally and functionally unique region in the left anterior supramarginal gyrus (aSMG), that is consistently active during tool use action observation. This region has been proposed as a primary hub for integrating semantic and technical information to form action plans with tools. However, it is still largely unknown how tool use motor learning affects left aSMG activation or connectivity with other brain regions. To address this, participants with little experience using chopsticks observed an experimenter using chopsticks to perform a novel task while undergoing two functional magnetic resonance imaging (fMRI) scans. Between the scans, participants underwent four weeks of behavioral training where they learned to use chopsticks and achieve proficiency in the observed task. Results demonstrated a significant change in effective connectivity between the left aSMG and the left anterior intraparietal sulcus (aIPS), a region involved in object affordances and planning grasping actions. These findings suggest that during unfamiliar tool use, the left aSMG integrates semantic and technical information to communicate with regions involved with grasp selection, such as the aIPS. This communication then allows appropriate grasps to be planned based on the physical properties of the objects involved and their potential interactions.

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The datasets generated during and/or analysed during the current study are available from the corresponding author on reasonable request.

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Acknowledgements

Partially funded by a Center for Brain and Behavior Student Research Grant to TJB.

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All authors contributed to the study. All authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

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Correspondence to Lee A. Baugh.

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The authors declare no financial or non-financial interests that are directly or indirectly related to the work submitted for publication.

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Communicated by Bill J Yates.

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Bosch, T.J., Fercho, K.A., Hanna, R. et al. Left anterior supramarginal gyrus activity during tool use action observation after extensive tool use training. Exp Brain Res 241, 1959–1971 (2023). https://doi.org/10.1007/s00221-023-06646-1

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  • DOI: https://doi.org/10.1007/s00221-023-06646-1

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