Neural bases of imitation and pantomime in acute stroke patients: distinct streams for praxis

Abstract

Apraxia is a cognitive disorder of skilled movements that characteristically affects the ability to imitate meaningless gestures, or to pantomime the use of tools. Despite substantial research, the neural underpinnings of imitation and pantomime have remained debated. An influential model states that higher motor functions are supported by different processing streams. A dorso-dorsal stream may mediate movements based on physical object properties, like reaching or grasping, whereas skilled tool use or pantomime rely on action representations stored within a ventro-dorsal stream. However, given variable results of past studies, the role of the two streams for imitation of meaningless gestures has remained uncertain, and the importance of the ventro-dorsal stream for pantomime of tool use has been questioned. To clarify the involvement of ventral and dorsal streams in imitation and pantomime, we performed voxel-based lesion-symptom mapping in a sample of 96 consecutive left-hemisphere stroke patients (mean age ± SD, 63.4 ± 14.8 years, 56 male). Patients were examined in the acute phase after ischaemic stroke (after a mean of 5.3, maximum 10 days) to avoid interference of brain reorganization with a reliable lesion-symptom mapping as best as possible. Patients were asked to imitate 20 meaningless hand and finger postures, and to pantomime the use of 14 common tools depicted as line drawings. Following the distinction between movement engrams and action semantics, pantomime errors were characterized as either movement or content errors, respectively. Whereas movement errors referred to incorrect spatio-temporal features of overall recognizable movements, content errors reflected an inability to associate tools with their prototypical actions. Both imitation and pantomime deficits were associated with lesions within the lateral occipitotemporal cortex, posterior inferior parietal lobule, posterior intraparietal sulcus and superior parietal lobule. However, the areas specifically related to the dorso-dorsal stream, i.e. posterior intraparietal sulcus and superior parietal lobule, were more strongly associated with imitation. Conversely, in contrast to imitation, pantomime deficits were associated with ventro-dorsal regions such as the supramarginal gyrus, as well as brain structures counted to the ventral stream, such as the extreme capsule. Ventral stream involvement was especially clear for content errors which were related to anterior temporal damage. However, movement errors were not consistently associated with a specific lesion location. In summary, our results indicate that imitation mainly relies on the dorso-dorsal stream for visuo-motor conversion and on-line movement control. Conversely, pantomime additionally requires ventro-dorsal and ventral streams for access to stored action engrams and retrieval of tool-action relationships.

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

“…Figure 4B, on the other hand, suggests that disruption of the medial occipital cortices would impair the tool pantomime task, as would damage to the right or left IPL. Only the latter observation is confirmed by the vlsm study of Hoeren et al (Hoeren et al, 2014). In addition, the connectivity schema would predict that left frontal damage is also likely to impair tool pantomiming, a repeated observation that has been hotly debated in the past Haaland et al, 2000).…”

“…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.…”

“…Finally, Figure 4A also suggests that damage to either IPL could have a detrimental impact given its strong and asymmetric connection with left PPCG. Both vlsm studies (that included only left brain damaged patients) mentioned the adverse effect of left IPL damage on the imitation of novel gestures (Buxbaum et al, 2014;Hoeren et al, 2014). Previous research also reported that patients with right brain damage perform more poorly in finger configuration tasks compared to hand configuration tasks (Goldenberg, 1996).…”

Shared neural substrates of apraxia and aphasia

“…Among the possible comparisons between different instances of apraxia the opposition of imitation of meaningless gestures to pantomime of tool use has raised particular interest (Duffy and Duffy, 1981;Goldenberg and Hagmann, 1997;Buxbaum et al, 2014;Hoeren et al, 2014;Weiss et al, in press). In the traditional dichotomy of ideational and ideo-motor apraxia both were classified as manifestations of ideo-motor apraxia, but their cognitive demands differ.…”

“…Group studies of patients with left brain damage (LBD) agree that correlations with severity of aphasia are generally stronger for pantomime of tool use than for imitation of meaningless gestures (Duffy and Duffy, 1981;Wang and Goodglass, 1992;Goldenberg, et al, 2003;Hoeren et al, 2014;Weiss et al, in press). Results are less unequivocal for the question whether imitation of meaningless gestures might also show some correlations at least to single aspects of linguistic capabilities.…”