The parietal architecture binding cognition to sensorimotor integration: a multimodal causal study

Despite human's praxis abilities are unique among primates, comparative observations suggest that these cognitive motor skills could have emerged from exploitation and adaptation of phylogenetically older building blocks, namely the parieto-frontal networks sub-serving prehension and manipulation. Within this framework, investigating to which extent praxis and prehension-manipulation overlap and diverge within parieto-frontal circuits could help in understanding how human cognition shapes hand actions. This issue has never been investigated by combining lesion mapping and direct electrophysiological approaches in neurosurgical patients. To this purpose, seventy-nine right-handed left-brain tumor patients candidate for awake neurosurgery were selected based on inclusion criteria. First, a lesion mapping was performed in the early post-operative phase to localize the regions associated to an impairment in praxis (imitation of meaningless and meaningful intransitive gestures) and visuo-guided prehension (reaching-to-grasping) abilities. Then, lesion results were anatomically matched with intraoperatively identified cortical and white matter regions, whose direct electrical stimulation impaired hand-manipulation task. The lesion mapping analysis showed that prehension and praxis impairments occurring in early post-operative phase were associated to specific parietal sectors. Dorso-mesial parietal resections, including the superior parietal lobe and precuneus, affected prehension performance, while resections involving rostral intraparietal and inferior parietal areas affected praxis abilities (covariate clusters, 5000 permutations, CFWER p < 0.05). The dorsal bank of the rostral intraparietal sulcus was associated to both prehension and praxis (overlap of non-covariate clusters). Within praxis results, while resection involving inferior parietal areas affected mainly the imitation of meaningful gestures, resection involving intraparietal areas affected both meaningless and meaningful gesture imitation. In parallel, the intraoperative electrical stimulation of the rostral intraparietal and the adjacent inferior parietal lobe with their surrounding white matter during hand-manipulation task evoked different motor impairments, i.e. the arrest and clumsy patterns respectively. When integrating lesion mapping and intraoperative stimulation results, it emerges that imitation of praxis gestures first depends on the integrity of parietal areas within the dorso-ventral stream. Among these areas, the rostral intraparietal and the inferior parietal area play distinct roles in praxis and sensorimotor process controlling manipulation. Due to its visuo-motor "attitude", the rostral intraparietal sulcus, putative human homologue of monkey AIP, might enable the visuo-motor conversion of the observed gesture (direct pathway). Moreover, its functional interaction with the adjacent, phylogenetic more recent, inferior parietal areas might contribute to integrate the semantic-conceptual knowledge (indirect pathway) within the sensorimotor workflow, contributing to the cognitive up-grade of hand-actions.