Abstract

Sophisticated tool use is a defining characteristic of the primate species but how is it supported by the brain, particularly the human brain? Here we show, using functional MRI and pattern classification methods, that tool use is subserved by multiple distributed action-centred neural representations that are both shared with and distinct from those of the hand. In areas of frontoparietal cortex we found a common representation for planned hand- and tool-related actions. In contrast, in parietal and occipitotemporal regions implicated in hand actions and body perception we found that coding remained selectively linked to upcoming actions of the hand whereas in parietal and occipitotemporal regions implicated in tool-related processing the coding remained selectively linked to upcoming actions of the tool. The highly specialized and hierarchical nature of this coding suggests that hand- and tool-related actions are represented separately at earlier levels of sensorimotor processing before becoming integrated in frontoparietal cortex. DOI:http://dx.doi.org/10.7554/eLife.00425.001.

Highlights

  • Tool use, whether using a stone, stick, rake, or pliers, provides an extension of the body (Van LawickGoodall, 1970) and involves, among other things, the transfer of a proximal movement goal for the hand into a more distal goal for the tool (Johnson and Grafton, 2003; Arbib et al, 2009)

  • Than across-effector decoding (p

  • We employed functional magnetic resonance imaging (fMRI) multi-voxel pattern analysis (MVPA) in order to examine whether planned object-directed hand actions were represented in an effector-specific or effectorindependent manner in human frontoparietal and occipitotemporal cortex

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Summary

Introduction

Whether using a stone, stick, rake, or pliers, provides an extension of the body (Van LawickGoodall, 1970) and involves, among other things, the transfer of a proximal movement goal for the hand into a more distal goal for the tool (Johnson and Grafton, 2003; Arbib et al, 2009). A compelling demonstration that this transfer might occur at the cortical level comes from neural recordings of grasping neurons in the ventral premotor cortex (PMv) and motor cortex (M1) of macaque monkeys trained to use pliers (Umilta et al, 2008) In both these areas, many neurons that encoded the specifics of hand grasping subsequently encoded tool grasping, even when use of the specific tool (reverse pliers that close as the hand grip opens) required hand kinematics opposite to those required when grasping with the hand alone. Many neurons that encoded the specifics of hand grasping subsequently encoded tool grasping, even when use of the specific tool (reverse pliers that close as the hand grip opens) required hand kinematics opposite to those required when grasping with the hand alone These findings suggest that tool use is supported by an effector-independent level of representation, in which the overall goal of the motor act is coded separately from the precise hand kinematics required to operate the tool. How well does this single mechanism explain the neural substrates of tool use in humans, within established networks that have been identified for tools (Lewis, 2006), hand actions (Culham et al, 2006), and body perception (Peelen and Downing, 2007)?

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