Distinct Contributions of Dorsal and Ventral Streams to Imitation of Tool-Use and Communicative Gestures

Abstract

Imitation of tool-use gestures (transitive; e.g., hammering) and communicative emblems (intransitive; e.g., waving goodbye) is frequently impaired after left-hemispheric lesions. We aimed 1) to identify lesions related to deficient transitive or intransitive gestures, 2) to delineate regions associated with distinct error types (e.g., hand configuration, kinematics), and 3) to compare imitation to previous data on pantomimed and actual tool use. Of note, 156 patients (64.3 ± 14.6 years; 56 female) with first-ever left-hemispheric ischemic stroke were prospectively examined 4.8 ± 2.0 days after symptom onset. Lesions were delineated on magnetic resonance imaging scans for voxel-based lesion-symptom mapping. First, while inferior-parietal lesions affected both gesture types, specific associations emerged between intransitive gesture deficits and anterior temporal damage and between transitive gesture deficits and premotor and occipito-parietal lesions. Second, impaired hand configurations were related to anterior intraparietal damage, hand/wrist-orientation errors to premotor lesions, and kinematic errors to inferior-parietal/occipito-temporal lesions. Third, premotor lesions impacted more on transitive imitation compared with actual tool use, pantomimed and actual tool use were more susceptible to lesioned insular cortex and subjacent white matter. In summary, transitive and intransitive gestures differentially rely on ventro-dorsal and ventral streams due to higher demands on temporo-spatial processing (transitive) or stronger reliance on semantic information (intransitive), respectively.

Repetitive transcranial magnetic stimulation reveals a role for the left inferior parietal lobule in matching observed kinematics during imitation

“…There is also evidence, at least for tool‐related actions, that damage to the left IPL is more reliably associated with deficits in action performance, rather than action recognition (Tarhan et al ., ), potentially confirming the priority that the left IPL places on processing movement during imitation, rather than semantic information (which may be more reliably served by the temporal lobe, e.g. Dressing et al ., ; Kalénine et al ., ).…”

“…However, there is evidence that damage to the IPL can be associated with deficits in both the imitation of communicative and tool‐use gestures (e.g. Dressing et al ., ), implying that our findings may be applicable beyond the specific action types used in this experiment. We do, of course, suggest further testing this hypothesis.…”

“…Similar results were found in a more recent voxel‐based lesion‐symptom mapping study by Dressing et al . (). Buxbaum et al .…”

A kinematic examination of dual-route processing for action imitation

“…In addition, given the potential interactions between kinematic and semantic processing revealed by apraxia (Buxbaum et al, 2014;Dressing et al, 2016), further work using motion-tracking could be useful for understanding the neural control of imitation of different action types, particularly if combined with neuropsychological assessments or neuroimaging.…”

“…However, the spatial and kinematic elements of an observed action may be particularly useful for meaningless action imitation, and some apraxia research supports the idea that there may also be postural and kinematic dissociations in apraxic imitation deficits (Buxbaum et al, 2014;Dressing et al, 2016). Despite this, little research has been done to objectively characterize the kinematics of meaningful and meaningless action imitation in healthy individuals.…”