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Cerebellar connectivity maps embody individual adaptive behavior in mice.

ABSTRACT: The cerebellar cortex encodes sensorimotor adaptation during skilled locomotor behaviors, however the precise relationship between synaptic connectivity and behavior is unclear. We studied synaptic connectivity between granule cells (GCs) and Purkinje cells (PCs) in murine acute cerebellar slices using photostimulation of caged glutamate combined with patch-clamp in developing or after mice adapted to different locomotor contexts. By translating individual maps into graph network entities, we found that synaptic maps in juvenile animals undergo critical period characterized by dissolution of their structure followed by the re-establishment of a patchy functional organization in adults. Although, in adapted mice, subdivisions in anatomical microzones do not fully account for the observed spatial map organization in relation to behavior, we can discriminate locomotor contexts with high accuracy. We also demonstrate that the variability observed in connectivity maps directly accounts for motor behavior traits at the individual level. Our findings suggest that, beyond general motor contexts, GC-PC networks also encode internal models underlying individual-specific motor adaptation.

SUBMITTER: Spaeth L

PROVIDER: S-EPMC8803868 | biostudies-literature | 2022 Jan

REPOSITORIES: biostudies-literature

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Cerebellar connectivity maps embody individual adaptive behavior in mice.

Spaeth Ludovic L Bahuguna Jyotika J Gagneux Theo T Dorgans Kevin K Sugihara Izumi I Poulain Bernard B Battaglia Demian D Isope Philippe P

Nature communications 20220131 1

The cerebellar cortex encodes sensorimotor adaptation during skilled locomotor behaviors, however the precise relationship between synaptic connectivity and behavior is unclear. We studied synaptic connectivity between granule cells (GCs) and Purkinje cells (PCs) in murine acute cerebellar slices using photostimulation of caged glutamate combined with patch-clamp in developing or after mice adapted to different locomotor contexts. By translating individual maps into graph network entities, we fo ...[more]

PMID: 35102165

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Project description:IntroductionPremutation carriers of the FMR1 gene are at risk of developing fragile X-associated tremor/ataxia syndrome (FXTAS), a neurodegenerative disease characterized by motor, cognitive, and psychiatric decline as well as cerebellar and cerebral white matter pathology. Several studies have documented preclinical sensorimotor issues in aging premutation carriers, but the extent to which sensorimotor brain systems are affected and may represent early indicators of atypical neurodegeneration has not been determined.Materials and methodsEighteen healthy controls and 16 FMR1 premutation carriers (including five with possible, probable, or definite FXTAS) group-matched on age, sex, and handedness completed a visually guided precision gripping task with their right hand during fMRI. During the test, they used a modified pinch grip to press at 60% of their maximum force against a custom fiber-optic transducer. Participants viewed a horizontal white force bar that moved upward with increased force and downward with decreased force and a static target bar that was red during rest and turned green to cue the participant to begin pressing at the beginning of each trial. Participants were instructed to press so that the white force bar stayed as steady as possible at the level of the green target bar. Trials were 2-sec in duration and alternated with 2-sec rest periods. Five 24-sec blocks consisting of six trials were presented. Participants' reaction time, the accuracy of their force relative to the target force, and the variability of their force accuracy across trials were examined. BOLD signal change and task-based functional connectivity (FC) were examined during force vs. rest.ResultsRelative to healthy controls, premutation carriers showed increased trial-to-trial variability of force output, though this was specific to younger premutation carriers in our sample. Relative to healthy controls, premutation carriers also showed reduced extrastriate activation during force relative to rest. FC between ipsilateral cerebellar Crus I and extrastriate cortex was reduced in premutation carriers compared to controls. Reduced Crus I-extrastriate FC was related to increased force accuracy variability in premutation carriers. Increased reaction time was associated with more severe clinically rated neurological abnormalities.ConclusionsFindings of reduced activation in extrastriate cortex and reduced Crus I-extrastriate FC implicate deficient visual feedback processing and reduced cerebellar modulation of corrective motor commands. Our results are consistent with documented cerebellar pathology and visual-spatial processing in FXTAS and pre-symptomatic premutation carriers, and suggest FC alterations of cerebellar-cortical networks during sensorimotor behavior may represent a "prodromal" feature associated with FXTAS degeneration.

Dataset Information

Cerebellar connectivity maps embody individual adaptive behavior in mice.

Publications

Cerebellar connectivity maps embody individual adaptive behavior in mice.

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