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Cerebro-cerebellar interactions in nonhuman primates examined by optogenetic functional magnetic resonance imaging.

ABSTRACT: Functional magnetic resonance imaging (fMRI) is a promising approach for the simultaneous and extensive scanning of whole-brain activities. Optogenetics is free from electrical and magnetic artifacts and is an ideal stimulation method for combined use with fMRI. However, the application of optogenetics in nonhuman primates (NHPs) remains limited. Recently, we developed an efficient optogenetic intracortical microstimulation method of the primary motor cortex (M1), which successfully induced forelimb movements in macaque monkeys. Here, we aimed to investigate how optogenetic M1 stimulation causes neural modulation in the local and remote brain regions in anesthetized monkeys using 7-tesla fMRI. We demonstrated that optogenetic stimulation of the M1 forelimb and hindlimb regions successfully evoked robust direct and remote fMRI activities. Prominent remote activities were detected in the anterior and posterior lobes in the contralateral cerebellum, which receive projections polysynaptically from the M1. We further demonstrated that the cerebro-cerebellar projections from these M1 regions were topographically organized, which is concordant with the somatotopic map in the cerebellar cortex previously reported in macaques and humans. The present study significantly enhances optogenetic fMRI in NHPs, resulting in profound understanding of the brain network, thereby accelerating the translation of findings from animal models to humans.

SUBMITTER: Goda N

PROVIDER: S-EPMC9233902 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Pre-clinical animal models are important to study the fundamental biological and functional mechanisms involved in the longitudinal evolution of heart failure (HF). Particularly, large animal models, like nonhuman primates (NHPs), that possess greater physiological, biochemical, and phylogenetic similarity to humans are gaining interest. To assess the translatability of these models into human diseases, imaging biomarkers play a significant role in non-invasive phenotyping, prediction of downstream remodeling, and evaluation of novel experimental therapeutics. This paper sheds insight into NHP cardiac function through the quantification of magnetic resonance (MR) imaging biomarkers that comprehensively characterize the spatiotemporal dynamics of left ventricular (LV) systolic pumping and LV diastolic relaxation. MR tagging and phase contrast (PC) imaging were used to quantify NHP cardiac strain and flow. Temporal inter-relationships between rotational mechanics, myocardial strain and LV chamber flow are presented, and functional biomarkers are evaluated through test-retest repeatability and inter subject variability analyses. The temporal trends observed in strain and flow was similar to published data in humans. Our results indicate a dominant dimension based pumping during early systole, followed by a torsion dominant pumping action during late systole. Early diastole is characterized by close to 65% of untwist, the remainder of which likely contributes to efficient filling during atrial kick. Our data reveal that moderate to good intra-subject repeatability was observed for peak strain, strain-rates, E/circumferential strain-rate (CSR) ratio, E/longitudinal strain-rate (LSR) ratio, and deceleration time. The inter-subject variability was high for strain dyssynchrony, diastolic strain-rates, peak torsion and peak untwist rate. We have successfully characterized cardiac function in NHPs using MR imaging. Peak strain, average systolic strain-rate, diastolic E/CSR and E/LSR ratios, and deceleration time were identified as robust biomarkers that could potentially be applied to future pre-clinical drug studies.

Project description:BackgroundThe cerebellum and cerebral cortex form the most important cortico-cerebellar system in the brain. However, diffusion magnetic resonance imaging (MRI)-based tractography of the connecting white matter between the cerebellum and cerebral cortex, which support language function, has not been extensively reported on. This work aims to serve as a guideline for facilitating the analysis of white matter tracts along the language-related cerebro-cerebellar pathway (LRCCP), which includes the corticopontine, pontocerebellar, corticorubral, rubroolivary, olivocerebellar, and dentatorubrothalamic tracts.MethodsThe LRCCP templates were developed via processing the high-resolution, population-averaged atlas available in the Human Connectome Project (HCP)-1065 dataset (2017 Q4, 1,200-subject release) in DSI Studio. The deterministic tracking was performed with the manually selected regions of interest (ROIs) on this atlas according to prior anatomic knowledge. Templates were then applied to the MRI datasets of 30 health participants acquired from a single hospital to verify the practicability of the tracking. The diffusion tensor and shape analysis metrics were calculated for all LRCCP tracts. Differences in the tracking metrics between the left and right hemispheres were compared, and the related white matter asymmetry was discussed.ResultsThe LRCCP templates were successfully created and applied to healthy participants for quantitative analysis. Significantly higher mean fractional anisotropy (FA) values were discovered on the left (L) corticorubral tract [L, 0.43±0.02 vs. right (R), 0.41±0.02; P<0.01] and left dentatorubrothalamic tract (L, 0.47±0.02 vs. R, 0.46±0.02; P<0.01). Significant differences in tract volume and streamline number were observed between the corticopontine, corticorubral, and dentatorubrothalamic tracts. The size of the right corticopontine and corticorubral tracts were smaller, and both had smaller streamline numbers and innervation areas when compared with the contralateral sides. The R dentatorubrothalamic tract showed a larger volume (R, 23,582.47±4,160.71 mm3 vs. L, 19,821.27±2,983.91 mm3; P<0.01) and innervation area (R, 2,117.37±433.98 mm2 vs. L, 1,610.00±356.19 mm2; P<0.01) than did the L side. No significant differences were observed in the rubroolivary tracts.ConclusionsThis work suggests the feasibility of applying tractography templates of the LRCCP to quantitatively evaluate white matter properties associated with language function. Lateralized diffusion metrics were observed in preliminary experiments. LRCCP tractography-based research may provide a potential quantitative method to better understanding neuroplasticity.

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Cerebro-cerebellar interactions in nonhuman primates examined by optogenetic functional magnetic resonance imaging.

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