Object-oriented hand dexterity and grasping abilities, from the animal quarters to the neurosurgical OR: a systematic review of the underlying neural correlates in non-human, human primate and recent findings in awake brain surgery

• Published in: Frontiers in integrative neuroscience 2024-02, Vol.18, p.1324581-1324581
• Main Authors: Tariciotti, Leonardo, Mattioli, Luca, Viganò, Luca, Gallo, Matteo, Gambaretti, Matteo, Sciortino, Tommaso, Gay, Lorenzo, Conti Nibali, Marco, Gallotti, Alberto, Cerri, Gabriella, Bello, Lorenzo, Rossi, Marco
• Format: Article
• Language: English
• Subjects: Animal cognition; awake surgery; Behavior; Brain architecture; Brain mapping; Brain surgery; Brain tumors; Functional magnetic resonance imaging; Grasping; grasping network; Hand; hand manipulation; Literature reviews; Monkeys & apes; Motor ability; motor cognition; Neuroscience; Neurosurgery; object-oriented hand manipulation; Primates; Quality of life; Sensorimotor system; Systematic review
• ISSN: 1662-5145; 1662-5145
• DOI: 10.3389/fnint.2024.1324581

The sensorimotor integrations subserving object-oriented manipulative actions have been extensively investigated in non-human primates via direct approaches, as intracortical micro-stimulation (ICMS), cytoarchitectonic analysis and anatomical tracers. However, the understanding of the mechanisms underlying complex motor behaviors is yet to be fully integrated in brain mapping paradigms and the consistency of these findings with intraoperative data obtained during awake neurosurgical procedures for brain tumor removal is still largely unexplored. Accordingly, there is a paucity of systematic studies reviewing the cross-species analogies in neural activities during object-oriented hand motor tasks in primates and investigating the concordance with intraoperative findings during brain mapping. The current systematic review was designed to summarize the cortical and subcortical neural correlates of object-oriented fine hand actions, as revealed by fMRI and PET studies, in non-human and human primates and how those were translated into neurosurgical studies testing dexterous hand-movements during intraoperative brain mapping. A systematic literature review was conducted following the PRISMA guidelines. PubMed, EMBASE and Web of Science databases were searched. Original articles were included if they: (1) investigated cortical activation sites on fMRI and/or PET during grasping task; (2) included humans or non-human primates. A second query was designed on the databases above to collect studies reporting motor, hand manipulation and dexterity tasks for intraoperative brain mapping in patients undergoing awake brain surgery for any condition. Due to the heterogeneity in neurosurgical applications, a qualitative synthesis was deemed more appropriate. We provided an updated overview of the current state of the art in translational neuroscience about the extended frontoparietal grasping-praxis network with a specific focus on the comparative functioning in non-human primates, healthy humans and how the latter knowledge has been implemented in the neurosurgical operating room during brain tumor resection. The anatomical and functional correlates we reviewed confirmed the evolutionary continuum from monkeys to humans, allowing a cautious but practical adoption of such evidence in intraoperative brain mapping protocols. Integrating the previous results in the surgical practice helps preserve complex motor abilities, prevent long-term disability and poor quality of life