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
IntroductionThe 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 me...
| Main Authors: | , , , , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Frontiers Media S.A.
2024-02-01
|
| Series: | Frontiers in Integrative Neuroscience |
| Subjects: | |
| Online Access: | https://www.frontiersin.org/articles/10.3389/fnint.2024.1324581/full |
| _version_ | 1797307029395603456 |
|---|---|
| author | Leonardo Tariciotti Luca Mattioli Luca Viganò Matteo Gallo Matteo Gambaretti Tommaso Sciortino Lorenzo Gay Marco Conti Nibali Alberto Gallotti Gabriella Cerri Lorenzo Bello Marco Rossi |
| author_facet | Leonardo Tariciotti Luca Mattioli Luca Viganò Matteo Gallo Matteo Gambaretti Tommaso Sciortino Lorenzo Gay Marco Conti Nibali Alberto Gallotti Gabriella Cerri Lorenzo Bello Marco Rossi |
| author_sort | Leonardo Tariciotti |
| collection | DOAJ |
| description | IntroductionThe 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.MethodsA 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.ResultsWe 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.DiscussionThe 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 and allow the maximal safe resection of intrinsic brain tumors. |
| first_indexed | 2024-03-08T00:50:27Z |
| format | Article |
| id | doaj.art-ddf1dc7f2b384b55a0dca90195a6c9e8 |
| institution | Directory Open Access Journal |
| issn | 1662-5145 |
| language | English |
| last_indexed | 2024-03-08T00:50:27Z |
| publishDate | 2024-02-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Integrative Neuroscience |
| spelling | doaj.art-ddf1dc7f2b384b55a0dca90195a6c9e82024-02-15T05:10:44ZengFrontiers Media S.A.Frontiers in Integrative Neuroscience1662-51452024-02-011810.3389/fnint.2024.13245811324581Object-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 surgeryLeonardo Tariciotti0Luca Mattioli1Luca Viganò2Matteo Gallo3Matteo Gambaretti4Tommaso Sciortino5Lorenzo Gay6Marco Conti Nibali7Alberto Gallotti8Gabriella Cerri9Lorenzo Bello10Marco Rossi11Neurosurgical Oncology Unit, Department of Oncology and Hemato-Oncology, Università degli Studi di Milano, Milan, ItalyNeurosurgical Oncology Unit, Department of Oncology and Hemato-Oncology, Università degli Studi di Milano, Milan, ItalyNeurosurgical Oncology Unit, Department of Oncology and Hemato-Oncology, Università degli Studi di Milano, Milan, ItalyNeurosurgical Oncology Unit, Department of Oncology and Hemato-Oncology, Università degli Studi di Milano, Milan, ItalyNeurosurgical Oncology Unit, Department of Oncology and Hemato-Oncology, Università degli Studi di Milano, Milan, ItalyNeurosurgical Oncology Unit, Department of Oncology and Hemato-Oncology, Università degli Studi di Milano, Milan, ItalyNeurosurgical Oncology Unit, Department of Oncology and Hemato-Oncology, Università degli Studi di Milano, Milan, ItalyNeurosurgical Oncology Unit, Department of Oncology and Hemato-Oncology, Università degli Studi di Milano, Milan, ItalyNeurosurgical Oncology Unit, Department of Oncology and Hemato-Oncology, Università degli Studi di Milano, Milan, ItalyMoCA Laboratory, Department of Medical Biotechnology and Translational Medicine, Università degli Studi di Milano, Milan, ItalyNeurosurgical Oncology Unit, Department of Oncology and Hemato-Oncology, Università degli Studi di Milano, Milan, ItalyNeurosurgical Oncology Unit, Department of Medical Biotechnology and Translational Medicine, Università degli Studi di Milano, Milan, ItalyIntroductionThe 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.MethodsA 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.ResultsWe 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.DiscussionThe 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 and allow the maximal safe resection of intrinsic brain tumors.https://www.frontiersin.org/articles/10.3389/fnint.2024.1324581/fullgrasping networkobject-oriented hand manipulationhand manipulationmotor cognitionbrain mappingawake surgery |
| spellingShingle | Leonardo Tariciotti Luca Mattioli Luca Viganò Matteo Gallo Matteo Gambaretti Tommaso Sciortino Lorenzo Gay Marco Conti Nibali Alberto Gallotti Gabriella Cerri Lorenzo Bello Marco Rossi 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 Frontiers in Integrative Neuroscience grasping network object-oriented hand manipulation hand manipulation motor cognition brain mapping awake surgery |
| title | 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 |
| title_full | 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 |
| title_fullStr | 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 |
| title_full_unstemmed | 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 |
| title_short | 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 |
| title_sort | 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 |
| topic | grasping network object-oriented hand manipulation hand manipulation motor cognition brain mapping awake surgery |
| url | https://www.frontiersin.org/articles/10.3389/fnint.2024.1324581/full |
| work_keys_str_mv | AT leonardotariciotti objectorientedhanddexterityandgraspingabilitiesfromtheanimalquarterstotheneurosurgicalorasystematicreviewoftheunderlyingneuralcorrelatesinnonhumanhumanprimateandrecentfindingsinawakebrainsurgery AT lucamattioli objectorientedhanddexterityandgraspingabilitiesfromtheanimalquarterstotheneurosurgicalorasystematicreviewoftheunderlyingneuralcorrelatesinnonhumanhumanprimateandrecentfindingsinawakebrainsurgery AT lucavigano objectorientedhanddexterityandgraspingabilitiesfromtheanimalquarterstotheneurosurgicalorasystematicreviewoftheunderlyingneuralcorrelatesinnonhumanhumanprimateandrecentfindingsinawakebrainsurgery AT matteogallo objectorientedhanddexterityandgraspingabilitiesfromtheanimalquarterstotheneurosurgicalorasystematicreviewoftheunderlyingneuralcorrelatesinnonhumanhumanprimateandrecentfindingsinawakebrainsurgery AT matteogambaretti objectorientedhanddexterityandgraspingabilitiesfromtheanimalquarterstotheneurosurgicalorasystematicreviewoftheunderlyingneuralcorrelatesinnonhumanhumanprimateandrecentfindingsinawakebrainsurgery AT tommasosciortino objectorientedhanddexterityandgraspingabilitiesfromtheanimalquarterstotheneurosurgicalorasystematicreviewoftheunderlyingneuralcorrelatesinnonhumanhumanprimateandrecentfindingsinawakebrainsurgery AT lorenzogay objectorientedhanddexterityandgraspingabilitiesfromtheanimalquarterstotheneurosurgicalorasystematicreviewoftheunderlyingneuralcorrelatesinnonhumanhumanprimateandrecentfindingsinawakebrainsurgery AT marcocontinibali objectorientedhanddexterityandgraspingabilitiesfromtheanimalquarterstotheneurosurgicalorasystematicreviewoftheunderlyingneuralcorrelatesinnonhumanhumanprimateandrecentfindingsinawakebrainsurgery AT albertogallotti objectorientedhanddexterityandgraspingabilitiesfromtheanimalquarterstotheneurosurgicalorasystematicreviewoftheunderlyingneuralcorrelatesinnonhumanhumanprimateandrecentfindingsinawakebrainsurgery AT gabriellacerri objectorientedhanddexterityandgraspingabilitiesfromtheanimalquarterstotheneurosurgicalorasystematicreviewoftheunderlyingneuralcorrelatesinnonhumanhumanprimateandrecentfindingsinawakebrainsurgery AT lorenzobello objectorientedhanddexterityandgraspingabilitiesfromtheanimalquarterstotheneurosurgicalorasystematicreviewoftheunderlyingneuralcorrelatesinnonhumanhumanprimateandrecentfindingsinawakebrainsurgery AT marcorossi objectorientedhanddexterityandgraspingabilitiesfromtheanimalquarterstotheneurosurgicalorasystematicreviewoftheunderlyingneuralcorrelatesinnonhumanhumanprimateandrecentfindingsinawakebrainsurgery |