Critical brain regions for tool-related and imitative actions: a componential analysis

Abstract

Numerous functional neuroimaging studies suggest that widespread bilateral parietal, temporal, and frontal regions are involved in tool-related and pantomimed gesture performance, but the role of these regions in specific aspects of gestural tasks remains unclear. In the largest prospective study of apraxia-related lesions to date, we performed voxel-based lesion-symptom mapping with data from 71 left hemisphere stroke participants to assess the critical neural substrates of three types of actions: gestures produced in response to viewed tools, imitation of tool-specific gestures demonstrated by the examiner, and imitation of meaningless gestures. Thus, two of the three gesture types were tool-related, and two of the three were imitative, enabling pairwise comparisons designed to highlight commonalities and differences. Gestures were scored separately for postural (hand/arm positioning) and kinematic (amplitude/timing) accuracy. Lesioned voxels in the left posterior temporal gyrus were significantly associated with lower scores on the posture component for both of the tool-related gesture tasks. Poor performance on the kinematic component of all three gesture tasks was significantly associated with lesions in left inferior parietal and frontal regions. These data enable us to propose a componential neuroanatomic model of action that delineates the specific components required for different gestural action tasks. Thus, visual posture information and kinematic capacities are differentially critical to the three types of actions studied here: the kinematic aspect is particularly critical for imitation of meaningless movement, capacity for tool-action posture representations are particularly necessary for pantomimed gestures to the sight of tools, and both capacities inform imitation of tool-related movements. These distinctions enable us to advance traditional accounts of apraxia.

Keywords: action; apraxia; gesture; imitation; tools.

Figure 1

Illustration of the 71 left-hemisphere lesions displayed on a template brain. Lesions are represented on the surface of the brain but display both cortical and subcortical damage to an 8-voxel search depth.

Figure 2

Examples of hand and arm posture errors made by study participants on the pantomime to sight of tool task (GestTool). (A) Hand and arm posture errors. In pantomiming eating with a fork, the participant shakes fist with thumb out (hand posture error) and maintains arm in a fixed position lateral to the body throughout (arm posture error). (B) Hand posture error. In pantomiming winding a watch, the participant forms a static precision grip (‘pinch’) and rotates the entire hand in a circle parallel to the watch-face.

Figure 3

Map depicting lesion overlap of the 71 participants. Only voxels lesioned in at least five subjects were included. The regions rendered in purple and blue correspond to an overlap of 5–15 participants. The regions rendered in aqua and green correspond to an overlap of 16–23 participants. Regions rendered in warm colours (yellow to dark red) were lesioned in at least one-third of the sample (overlap of ≥ 24 participants).

Figure 4

Maps of the reliability (Z-scores) of the difference between patients with and without lesions in each voxel in (A) gesture to the sight of tools (GestTool), (B) imitation of tool-related gestures (ImTool), and (C) imitation of novel gestures (rendered on the MNI space ch2bet volume). For each of the three maps, voxels rendered in warm/hot colours correspond to Z-scores > 3.02, 2.7, and 2.7, respectively, that reached the FDR-corrected threshold of q < 0.05. Voxels rendered in blue correspond to voxels associated with FDR-corrected thresholds between q = 0.05 and q = 0.1.

Figure 5

Maps of the conjunction of the voxels reaching the FDR-corrected threshold of P < 0.05 in two of the three gesture conditions. (A) Conjunction of voxels meeting the threshold for the two tool-related tasks (gesture to the sight of tools and imitation of tool-related gestures). (B) Conjunction of voxels meeting the threshold for the two imitation tasks (imitation of tool-related gestures and imitation of novel gestures).

Figure 6

Maps of the reliability (Z-scores) of the difference between patients with and without lesions in each voxel in (A) posture scores on ImTool controlling for posture scores on ImNov, (B) kinematic scores on ImTool controlling for kinematic scores on GestTool (rendered on the MNI space ch2bet volume). For each of the two maps, voxels rendered in warm/hot colours correspond to Z-scores > 3.4 and 2.9, respectively, that reached the FDR-corrected threshold of q < 0.05. Voxels rendered in blue correspond to voxels associated with FDR-corrected thresholds between q = 0.05 and q = 0.1.