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.

Functional connectivity associated with hand shape generation: Imitating novel hand postures and pantomiming tool grips challenge different nodes of a shared neural network

“…Posterior temporal lobe activation is typically found in studies assessing semantic action knowledge and recent publications emphasized the visual format of these action representations in pMTG (Binkofski and Buxbaum, 2013;Buxbaum et al, 2014;Kable et al, 2005;Kalenine et al, 2010). The proposed functional link between pMTG and extrastriate regions is in agreement with the finding that the highest (of albeit weak) pMTG resonance was observed with the lingual gyrus and the inferior precunei, whereas correlations of pMTG with the frontal and parietal ROIs were very modest.…”

“…The proposed functional link between pMTG and extrastriate regions is in agreement with the finding that the highest (of albeit weak) pMTG resonance was observed with the lingual gyrus and the inferior precunei, whereas correlations of pMTG with the frontal and parietal ROIs were very modest. The strong relation of the posterior temporal region with human tool use is demonstrated by the finding that lesions to the left posterior temporal gyrus were associated with poor toolrelated gesture performance (Buxbaum et al, 2014;Hoeren et al, 2014). In a recent study combining fMRI and DTI, Vry and colleagues stressed the relevance of the infra-Sylvian ventral pathway supporting the semantic operations of pantomimed gestures.…”

“…Neuropsychological research in patients with apraxia revealed (double) dissociations between impaired gesture imitation and defective (pantomime of) tool use, between poor imitation of meaningful and meaningless gestures, and even between impaired copying of meaningless hand versus finger postures (Bartolo et al, 2001;Goldenberg and Hagmann, 1997;Goldenberg and Karnath, 2006). Two major elements considered in most theoretical models of praxis include a representational or semantic component and a kinematic or action production component (Buxbaum, 2001;Buxbaum et al, 2014;Cubelli et al, 2000;Rothi et al, 1991;Roy and Hall, 1992). The semantic component refers to stored action knowledge about familiar objects gained over repetitive encounters, i.e.…”

“…The ventro-dorsal stream connects temporal regions with the inferior parietal cortex and ventral premotor cortex, and supports conceptual representations of skilled actions involving familiar objects (Binkofski and Buxbaum, 2013;Buxbaum and Kalenine, 2010;Vingerhoets, 2014). Recent voxel-based lesion-symptom mapping (vlsm) studies have employed the imitation of meaningless gestures and the pantomiming of tool use to test the integrity of the dorso-dorsal and ventro-dorsal streams respectively (Buxbaum et al, 2014;Hoeren et al, 2014). Buxbaum et al reported that imitation of meaningless gestures relied predominantly on the inferior parietal lobule and that gesture to the sight of tools depended on posterior temporal activation (Buxbaum et al, 2014).…”

“…Recent voxel-based lesion-symptom mapping (vlsm) studies have employed the imitation of meaningless gestures and the pantomiming of tool use to test the integrity of the dorso-dorsal and ventro-dorsal streams respectively (Buxbaum et al, 2014;Hoeren et al, 2014). Buxbaum et al reported that imitation of meaningless gestures relied predominantly on the inferior parietal lobule and that gesture to the sight of tools depended on posterior temporal activation (Buxbaum et al, 2014). Hoeren et al found that imitation of meaningless gestures was impaired following damage to the posterior intraparietal sulcus and the superior parietal lobule, whereas tool pantomiming suffered with lesions of the supramarginal gyrus and areas of the ventral stream (Hoeren et al, 2014).…”