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Neuroimage. 2019 Sep 23:116215. doi: 10.1016/j.neuroimage.2019.116215. [Epub ahead of print]

Large scale networks for human hand-object interaction: Functionally distinct roles for two premotor regions identified intraoperatively.

Author information

1
Laboratory of Motor Control, Department of Medical Biotechnologies and Translational Medicine, Università degli Studi di Milano, Humanitas Reasearch Hospital, IRCCS, Milan, Italy. Electronic address: luciano.simone52@gmail.com.
2
Laboratory of Motor Control, Department of Medical Biotechnologies and Translational Medicine, Università degli Studi di Milano, Humanitas Reasearch Hospital, IRCCS, Milan, Italy.
3
Unit of Neurosurgical Oncology, Department of Oncology and Hemato-Oncology, Università degli Studi di Milano, Humanitas Reasearch Hospital, IRCCS, Milan, Italy.
4
Department of Neuroscience (DNS), University of Padova, Padua, Italy.

Abstract

The development of awake intraoperative brain-mapping procedures for resection of brain tumors is of growing interest in neuroscience, because it enables direct testing of brain tissue, previously only possible in non-human primates. In a recent study performed in this setting specific effects can be induced by direct electrical stimulation on different sectors of premotor cortex during the execution of a hand manipulation task. Specifically, direct electrical stimulation applied on a dorsal sector of precentral cortex led to an increase in motor unit recruitment in hand muscles during execution of a hand manipulation task (Recruitment sector). The opposite effect was elicited when electrical stimulation was delivered more ventrally on the precentral cortex (Suppression sector). We studied whether the different effects on motor behavior induced by direct electrical stimulation applied on the two sites of the precentral cortex underlie differences in their functional connectivity with other brain areas, measured using resting state fMRI. Using healthy adults scanned as part of the Human Connectome Project, we computed the functional connectivity of each sector used as seeds. The functional connectivity patterns of the two intraoperative seeds was similar but cross-comparison revealed that the left and right Recruitment sectors had stronger functional connections with the hand region of the sensorimotor cortex, while the right Suppression region displayed stronger functional connectivity with a bilateral set of parieto-frontal areas crucial for the integration of perceptual and cognitive hand-related sensorimotor processes required for goal-related hand actions. Our results suggest that analyzing data obtained in the intraoperative setting with resting state functional magnetic resonance imaging in healthy brains can yield useful insight into the roles of different premotor sectors directly involved in hand-object interaction.

KEYWORDS:

Direct electrical stimulation; Functional connectivity; Hand manipulation; Motor unit recruitment; Parieto-frontal system

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