Epidural cerebellar stimulation drives widespread neural synchrony in the intact and stroke perilesional cortex

Abbasi, Aamir; Danielsen, Nathan P.; Leung, Jennifer; Muhammad, A.K.M. Ghulam; Patel, Saahil; Gulati, Tanuj

doi:10.1186/s12984-021-00881-9

“…This work also boosted M1 LFOs through electric stimulation to promote recovery. Recently, there has also been an interest in cerebellar stimulation for stroke recovery ( Machado et al, 2009 ; Shah et al, 2017 ; Abbasi et al, 2021 ), but a biomarker in cortico-cerebellar networks that can be a target for closed-loop electric stimulation for stroke recovery is lacking. Future work can test whether the LFOs we found in cortico-cerebellar networks of healthy animals with skill consolidation here can also serve as a biomarker for motor function during recovery from stroke.…”

Section: Discussionmentioning

confidence: 99%

Emergent Low-Frequency Activity in Cortico-Cerebellar Networks with Motor Skill Learning

Fleischer

¹

,

Abbasi

²

,

Fealy

³

et al. 2023

eNeuro

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The motor cortex controls skilled arm movement by recruiting a variety of targets in the nervous system, and it is important to understand the emergent activity in these regions as refinement of a motor skill occurs. One fundamental projection of the motor cortex (M1) is to the cerebellum. However, the emergent activity in the motor cortex and the cerebellum that appears as a dexterous motor skill is consolidated is incompletely understood. Here, we report on low-frequency oscillatory (LFO) activity that emerges in cortico-cerebellar networks with learning the reach-to-grasp motor skill. We chronically recorded the motor and the cerebellar cortices in rats which revealed the emergence of coordinated movement-related activity in the local-field potentials (LFPs) as the reaching skill consolidated. Interestingly, we found this emergent activity only in the rats that gained expertise in the task. We found that the local and cross-area spiking activity was coordinated with LFOs in proficient rats. Finally, we also found that these neural dynamics were more prominently expressed during accurate behavior in the M1. This work furthers our understanding on emergent dynamics in the cortico-cerebellar loop that underlie learning and execution of precise skilled movement.Significance StatementMovement execution involves parallel processing across brain regions, with the motor cortex (M1) being a key hub that recruits several subcortical nodes. The cerebellar cortex is a principal receiver of M1 projections via pons, but the emergent dynamics in these regions with motor skill learning is incompletely understood. We performed simultaneous recordings of M1 and cerebellum in a reach-to-grasp task. We found low frequency activity and coordinated neural dynamics emerged within and across regions with skillful task execution. Recent interest in modulating cortico-cerebellar networks for motor-recovery post-injury/stroke make this work an important precursor to assessing whether similar low-frequency activity in cortico-cerebellar networks can serve as a biomarker of motor recovery and help optimize modulation of these networks.

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“…This work also boosted M1 LFOs through electric stimulation to promote recovery. Recently, there has also been an interest in cerebellar stimulation for stroke recovery [58][59][60] , but a biomarker in corticocerebellar networks that can be target for closed-loop electric stimulation for stroke recovery is lacking. Future work can test if the LFOs we found in cortico-cerebellar networks of healthy animals with skill consolidation here can also serve as a biomarker for motor function during recovery from stroke.…”

Section: Coordinated Oscillatory Dynamics Across Motor Networkmentioning

confidence: 99%

Emergent low-frequency activity in cortico-cerebellar networks with motor skill learning

Fleischer

¹

,

Abbasi

²

,

Fealy

³

et al. 2022

Preprint

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The motor cortex controls skilled arm movement by recruiting a variety of targets in the nervous system, and it is important to understand the emergent activity in these regions as refinement of a motor skill occurs. One fundamental projection of the motor cortex is to the cerebellum. However, the emergent activity in the motor cortex and the cerebellum that appears as a dexterous motor skill is consolidated is incompletely understood. Here, we report on low-frequency oscillatory (LFO) activity that emerges in cortico-cerebellar networks with learning the reach-to-grasp motor skill. We chronically recorded the motor and the cerebellar cortices in rats which revealed the emergence of coordinated movement-related activity in the local-field potentials (LFPs) as the reaching skill consolidated. We found that the local and cross-area spiking activity was coordinated with LFOs. Finally, we also found that these neural dynamics were more prominently expressed during accurate behavior. This work furthers our understanding on emergent dynamics in the cortico-cerebellar loop that underlie learning and execution of precise skilled movement.

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“…This may be due to the fact that the structure of the middle cerebral artery in SD rats highly varies from one rat to another [ 21 , 32 ]. Nevertheless, previous studies on the FCI model using Long–Evans (LE) rats do not show any deviation or variability related to this rat strain [ 33 , 34 , 35 , 36 , 37 , 38 ]. We therefore chose to induce the ischemic stroke specifically in LE rats.…”

Section: Discussionmentioning

confidence: 81%

A Novel Improved Thromboembolism-Based Rat Stroke Model That Meets the Latest Standards in Preclinical Studies

Pawletko

¹

,

Jędrzejowska–Szypułka

²

,

Bogus

³

et al. 2022

Brain Sciences

3

0

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The animal thromboembolic model of ischemia perfectly mimics human ischemic stroke which remains the leading cause of disability and mortality in humans. The development of new treatment strategies was therefore imperative. The purpose of this study is to improve the thromboembolic stroke model in rats in order to design experiments that use motor tests, and are in accordance with the 3R principles to prevent complications and maintain the same size of the infarct repeatedly. Tail vein dye application, a protective skull mask and a stress minimization protocol were used as additional modifications to the animal stroke model. These modifications significantly minimized the pain and stress severity of the procedures in this model. In our experimental group of Long-Evans rats, a photo-induced stroke was caused by the application of a photosensitive dye (Rose Bengal) activated with white-light irradiation, thus eliminating the need to perform a craniotomy. The animals’ neurological status was evaluated using a runway elevated test. Histological examination of the brain tissue was performed at 12, 24 and 48 h, and seven days post-stroke. Tissue examination revealed necrotic foci in the cortex and the subcortical regions of the ipsilateral hemisphere in all experimental groups. Changes in the area, width and depth of the necrotic focus were observed over time. All the experimental groups showed motor disturbances after stroke survival. In the proposed model, photochemically-induced stroke caused long-term motor deficits, showed high reproducibility and low mortality rates. Consequently, the animals could participate in motor tests which are particularly suitable for assessing the efficacy of neuro-regenerative therapies, while remaining in line with the latest trends in animal experimental design.

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Epidural cerebellar stimulation drives widespread neural synchrony in the intact and stroke perilesional cortex

Cited by 14 publications

References 82 publications

Emergent Low-Frequency Activity in Cortico-Cerebellar Networks with Motor Skill Learning

Emergent Low-Frequency Activity in Cortico-Cerebellar Networks with Motor Skill Learning

Emergent low-frequency activity in cortico-cerebellar networks with motor skill learning

A Novel Improved Thromboembolism-Based Rat Stroke Model That Meets the Latest Standards in Preclinical Studies

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