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Propagating motor cortical patterns of excitability are ubiquitous across human and non-human primate movement initiation.

ABSTRACT: A spatiotemporal pattern of excitability propagates across the primary motor cortex prior to the onset of a reaching movement in non-human primates. If this pattern is a necessary component of voluntary movement initiation, it should be present across a variety of motor tasks, end-effectors, and even species. Here, we show that propagating patterns of excitability occur during the initiation of precision grip force and tongue protrusion in non-human primates, and even isometric wrist extension in a human participant. In all tasks, the directions of propagation across the cortical sheet were bimodally distributed across trials with modes oriented roughly opposite to one another. Propagation speed was unimodally distributed with similar mean speeds across tasks and species. Additionally, propagation direction and speed did not vary systematically with any behavioral measures except response times indicating that this propagating pattern is invariant to kinematic or kinetic details and may be a generic movement initiation signal.

SUBMITTER: Balasubramanian K

PROVIDER: S-EPMC10105290 | biostudies-literature | 2023 Apr

REPOSITORIES: biostudies-literature

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Propagating motor cortical patterns of excitability are ubiquitous across human and non-human primate movement initiation.

Balasubramanian Karthikeyan K Arce-McShane Fritzie I FI Dekleva Brian M BM Collinger Jennifer L JL Hatsopoulos Nicholas G NG

iScience 20230329 4

A spatiotemporal pattern of excitability propagates across the primary motor cortex prior to the onset of a reaching movement in non-human primates. If this pattern is a necessary component of voluntary movement initiation, it should be present across a variety of motor tasks, end-effectors, and even species. Here, we show that propagating patterns of excitability occur during the initiation of precision grip force and tongue protrusion in non-human primates, and even isometric wrist extension i ...[more]

PMID: 37070071

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Project description:To offer engaging neurorehabilitation training to neurologic patients, motor tasks are often visualized in virtual reality (VR). Recently introduced head-mounted displays (HMDs) allow to realistically mimic the body of the user from a first-person perspective (i.e., avatar) in a highly immersive VR environment. In this immersive environment, users may embody avatars with different body characteristics. Importantly, body characteristics impact how people perform actions. Therefore, alternating body perceptions using immersive VR may be a powerful tool to promote motor activity in neurologic patients. However, the ability of the brain to adapt motor commands based on a perceived modified reality has not yet been fully explored. To fill this gap, we "tricked the brain" using immersive VR and investigated if multisensory feedback modulating the physical properties of an embodied avatar influences motor brain networks and control. Ten healthy participants were immersed in a virtual environment using an HMD, where they saw an avatar from first-person perspective. We slowly transformed the surface of the avatar (i.e., the "skin material") from human to stone. We enforced this visual change by repetitively touching the real arm of the participant and the arm of the avatar with a (virtual) hammer, while progressively replacing the sound of the hammer against skin with stone hitting sound via loudspeaker. We applied single-pulse transcranial magnetic simulation (TMS) to evaluate changes in motor cortical excitability associated with the illusion. Further, to investigate if the "stone illusion" affected motor control, participants performed a reaching task with the human and stone avatar. Questionnaires assessed the subjectively reported strength of embodiment and illusion. Our results show that participants experienced the "stone arm illusion." Particularly, they rated their arm as heavier, colder, stiffer, and more insensitive when immersed with the stone than human avatar, without the illusion affecting their experienced feeling of body ownership. Further, the reported illusion strength was associated with enhanced motor cortical excitability and faster movement initiations, indicating that participants may have physically mirrored and compensated for the embodied body characteristics of the stone avatar. Together, immersive VR has the potential to influence motor brain networks by subtly modifying the perception of reality, opening new perspectives for the motor recovery of patients.

Dataset Information

Propagating motor cortical patterns of excitability are ubiquitous across human and non-human primate movement initiation.

Publications

Propagating motor cortical patterns of excitability are ubiquitous across human and non-human primate movement initiation.

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