Abstract

Producing a tool use gesture is a complex process drawing upon the integration of stored knowledge of tools and their associated actions with sensory–motor mechanisms supporting the planning and control of hand and arm actions. Understanding how sensory–motor systems in parietal cortex interface with semantic representations of actions and objects in the temporal lobe remains a critical issue and is hypothesized to be a key determinant of the severity of limb apraxia, a deficit in producing skilled action after left hemisphere stroke. We used voxel-based and connectome-based lesion-symptom mapping with data from 57 left hemisphere stroke participants to assess the lesion sites and structural disconnection patterns associated with poor tool use gesturing. We found that structural disconnection among the left inferior parietal lobule, lateral and ventral temporal cortices, and middle and superior frontal gyri predicted the severity of tool use gesturing performance. Control analyses demonstrated that reductions in right-hand grip strength were associated with motor system disconnection, largely bypassing regions supporting tool use gesturing. Our findings provide evidence that limb apraxia may arise, in part, from a disconnection between conceptual representations in the temporal lobe and mechanisms enabling skilled action production in the inferior parietal lobule.

Highlights

  • The ability to produce skilled object-directed action in order to satisfy behavioral goals is a cornerstone of high-level cognitive and motor function, referred to as praxis

  • Performance when gesturing tool use is a sensitive assay of the contributions of the indirect route, as the visual input must interface with the semantic system for accurate demonstration of tool use

  • Two SVR-VLSM analyses were conducted; in the first analysis we identified voxels in which lesions were associated with worse performance when gesturing tool use to the sight of objects

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Summary

Introduction

The ability to produce skilled object-directed action in order to satisfy behavioral goals is a cornerstone of high-level cognitive and motor function, referred to as praxis. The indirect route provides a processing advantage when generating a meaningful gesture (e.g., hammering a nail), because the implementation of that gesture is facilitated by semantic memory, including the retrieval of the visual appearance of a gesture (e.g., that a swung hammer moves in a particular trajectory), function knowledge retrieval (e.g., that the function of the act of hammering is to pound in nails), and the retrieval of postural knowledge (e.g., that the configuration of the hand and fingers are positioned in a non-arbitrary manner in order to functionally grasp and manipulate a hammer; e.g., see Bracci & Peelen, 2013). Imitation of meaningless gestures provides a means with which to evaluate the integrity of the direct route, because the transformation of visual input into sensory-motor plans occurs without access to semantic information (for review, see Binkofski & Buxbaum, 2013)

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