Dataset Information

Spatiotemporal Mapping and Molecular Basis of Whole-brain Circuit Maturation.

ABSTRACT: Brain development is highly dynamic and asynchronous, marked by the sequential maturation of functional circuits across the brain. The timing and mechanisms driving circuit maturation remain elusive due to an inability to identify and map maturing neuronal populations. Here we create DevATLAS (Developmental Activation Timing-based Longitudinal Acquisition System) to overcome this obstacle. We develop whole-brain mapping methods to construct the first longitudinal, spatiotemporal map of circuit maturation in early postnatal mouse brains. Moreover, we uncover dramatic impairments within the deep cortical layers in a neurodevelopmental disorders (NDDs) model, demonstrating the utility of this resource to pinpoint when and where circuit maturation is disrupted. Using DevATLAS, we reveal that early experiences accelerate the development of hippocampus-dependent learning by increasing the synaptically mature granule cell population in the dentate gyrus. Finally, DevATLAS enables the discovery of molecular mechanisms driving activity-dependent circuit maturation.

SUBMITTER: Xue J

PROVIDER: S-EPMC10802351 | biostudies-literature | 2024 Jan

REPOSITORIES: biostudies-literature

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Spatiotemporal Mapping and Molecular Basis of Whole-brain Circuit Maturation.

Xue Jian J Brawner Andrew T AT Thompson Jacqueline R JR Yelhekar Tushar D TD Newmaster Kyra T KT Qiu Qiang Q Cooper Yonatan A YA Yu C Ron CR Ahmed-Braima Yasir H YH Kim Yongsoo Y Lin Yingxi Y

bioRxiv : the preprint server for biology 20240104

Brain development is highly dynamic and asynchronous, marked by the sequential maturation of functional circuits across the brain. The timing and mechanisms driving circuit maturation remain elusive due to an inability to identify and map maturing neuronal populations. Here we create DevATLAS (Developmental Activation Timing-based Longitudinal Acquisition System) to overcome this obstacle. We develop whole-brain mapping methods to construct the first longitudinal, spatiotemporal map of circuit m ...[more]

PMID: 38260331

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Project description:ImportanceCreativity is important for problem solving, adaptation to a changing environment, and innovation. Neuroimaging studies seeking to map creativity have yielded conflicting results, and studies of patients with brain disease have reported both decreases and paradoxical increases in creativity, leaving the neural basis of creativity unclear.ObjectiveTo investigate the brain circuit underlying creativity and assess its association with brain injury and neurodegenerative disease.Design, setting, and participantsThis study examined neuroimaging coordinates from a meta-analysis of 36 studies published between 2004 and 2019 associated with increased activity during creative tasks in healthy participants. A validated method termed coordinate network mapping and a database of resting-state functional connectivity from 1000 healthy individuals were used to test whether these coordinates mapped to a common brain circuit. Specificity was assessed through comparison to random coordinates and coordinates from working memory tasks in healthy participants. Reproducibility was assessed using an independent dataset of coordinates from additional studies of creativity in healthy participants. Finally, alignment with effects of focal brain damage on creativity was tested using data from patients with brain lesions and coordinates of brain atrophy from 7 different neurodegenerative disorders.Main outcomes and measuresThe primary outcomes were creativity or no creativity and alignment with a creativity circuit or no alignment.ResultsCreativity tasks activated heterogenous locations, with coordinates scattered across many different brain regions (415 coordinates derived from 857 healthy participants; pooled mean [SD] age, 24.1 [6.91] years; 461 [54%] female). However, these activation coordinates were part of a common brain circuit, defined by negative connectivity to the right frontal pole. This result was consistent across creative domains, reproducible in an independent dataset (383 coordinates derived from 691 participants) and specific to creativity when compared with random gray matter coordinates (n = 415) or coordinates activated by working memory tasks (3072 coordinates derived from 2900 healthy participants). Damage to this creativity circuit by lesions (n = 56 patients) or neurodegenerative disease (2262 coordinates derived from 4804 patients) aligned with both decreases and increases in creativity observed in these disorders.Conclusions and relevanceFindings from this study suggest that brain regions activated by creativity tasks map to a brain circuit defined by negative functional connectivity to the right frontal pole. Damage to this circuit aligned with changes in creativity observed in individuals with certain brain diseases, including paradoxical creativity increases.

Dataset Information

Spatiotemporal Mapping and Molecular Basis of Whole-brain Circuit Maturation.

Publications

Spatiotemporal Mapping and Molecular Basis of Whole-brain Circuit Maturation.

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