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Activity map of a cortico-cerebellar loop underlying motor planning.

ABSTRACT: The neocortex and cerebellum interact to mediate cognitive functions. It remains unknown how the two structures organize into functional networks to mediate specific behaviors. Here we delineate activity supporting motor planning in relation to the mesoscale cortico-cerebellar connectome. In mice planning directional licking based on short-term memory, preparatory activity instructing future movement depends on the anterior lateral motor cortex (ALM) and the cerebellum. Transneuronal tracing revealed divergent and largely open-loop connectivity between the ALM and distributed regions of the cerebellum. A cerebellum-wide survey of neuronal activity revealed enriched preparatory activity in hotspot regions with conjunctive input-output connectivity to the ALM. Perturbation experiments show that the conjunction regions were required for maintaining preparatory activity and correct subsequent movement. Other cerebellar regions contributed little to motor planning despite input or output connectivity to the ALM. These results identify a functional cortico-cerebellar loop and suggest the cerebellar cortex selectively establishes reciprocal cortico-cerebellar communications to orchestrate motor planning.

SUBMITTER: Zhu J

PROVIDER: S-EPMC10620095 | biostudies-literature | 2023 Nov

REPOSITORIES: biostudies-literature

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Activity map of a cortico-cerebellar loop underlying motor planning.

Zhu Jia J Hasanbegović Hana H Liu Liu D LD Gao Zhenyu Z Li Nuo N

Nature neuroscience 20231009 11

The neocortex and cerebellum interact to mediate cognitive functions. It remains unknown how the two structures organize into functional networks to mediate specific behaviors. Here we delineate activity supporting motor planning in relation to the mesoscale cortico-cerebellar connectome. In mice planning directional licking based on short-term memory, preparatory activity instructing future movement depends on the anterior lateral motor cortex (ALM) and the cerebellum. Transneuronal tracing rev ...[more]

PMID: 37814026

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Project description:The robust, reciprocal anatomical connections between the cerebellum and contralateral sensorimotor cerebral hemisphere underscores the strong physiological interdependence between these two regions in relation to human behavior. Previous studies have shown that damage to sensorimotor cortex can result in a lasting reduction of cerebellar metabolism, the magnitude of which has been linked to poor rehabilitative outcomes. A better understanding of movement-related cerebellar physiology as well as cortico-cerebellar coherence (CCC) in the chronic, post-stroke state may be key to developing novel neuromodulatory techniques that promote upper limb motor rehabilitation. As a part of the first in-human phase-I trial investigating the effects of deep brain stimulation of the cerebellar dentate nucleus (DN) on chronic, post-stroke motor rehabilitation, we collected invasive recordings from DN and scalp EEG in subjects (both sexes) with middle cerebral artery stroke during a visuo-motor tracking task. We investigated the excitability of ipsilesional cortex, DN and the their interaction as a function of motor impairment and performance. Our results indicate that 1) event-related oscillations in the ipsilesional cortex and DN were significantly correlated at movement onset in the low-β band, with moderately and severely impaired subjects showing desynchronization and synchronization, respectively. 2) Significant CCC was observed during isometric 'hold' period in the low-β band, which was critical for maintaining task accuracy. Our findings support a strong coupling between ipsilesional cortex and DN in the low-β band during motor control across all impairment levels which encourages the exploitation of the cerebello-thalamo-cortical pathway as a neuromodulation target to promote rehabilitation.Significance Statement:Cerebral infarct due to stroke can lead to lasting reduction in cerebellar metabolism resulting in poor rehabilitative outcomes. Thorough investigation of the cerebellar electrophysiology as well as cortico-cerebellar connectivity in humans that could provide key insights to facilitate development of novel neuromodulatory technologies, has been lacking. As a part of the first in-human phase-I trial investigating deep brain stimulation of the cerebellar dentate nucleus (DN) for chronic, post-stroke motor rehabilitation, we collected invasive recordings from DN and scalp EEG while stroke patients performed a motor task. Our data indicate strong coupling between ipsilesional sensorimotor cortex and DN in the low-β band across all impairment levels encouraging the exploration of electrical stimulation of the DN.

Dataset Information

Activity map of a cortico-cerebellar loop underlying motor planning.

Publications

Activity map of a cortico-cerebellar loop underlying motor planning.

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