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A marmoset brain cell census reveals regional specialization of cellular identities.

ABSTRACT: The mammalian brain is composed of many brain structures, each with its own ontogenetic and developmental history. We used single-nucleus RNA sequencing to sample over 2.4 million brain cells across 18 locations in the common marmoset, a New World monkey primed for genetic engineering, and examined gene expression patterns of cell types within and across brain structures. The adult transcriptomic identity of most neuronal types is shaped more by developmental origin than by neurotransmitter signaling repertoire. Quantitative mapping of GABAergic types with single-molecule FISH (smFISH) reveals that interneurons in the striatum and neocortex follow distinct spatial principles, and that lateral prefrontal and other higher-order cortical association areas are distinguished by high proportions of VIP⁺ neurons. We use cell type-specific enhancers to drive AAV-GFP and reconstruct the morphologies of molecularly resolved interneuron types in neocortex and striatum. Our analyses highlight how lineage, local context, and functional class contribute to the transcriptional identity and biodistribution of primate brain cell types.

SUBMITTER: Krienen FM

PROVIDER: S-EPMC10569717 | biostudies-literature | 2023 Oct

REPOSITORIES: biostudies-literature

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A marmoset brain cell census reveals regional specialization of cellular identities.

Krienen Fenna M FM Levandowski Kirsten M KM Zaniewski Heather H Del Rosario Ricardo C H RCH Schroeder Margaret E ME Goldman Melissa M Wienisch Martin M Lutservitz Alyssa A Beja-Glasser Victoria F VF Chen Cindy C Zhang Qiangge Q Chan Ken Y KY Li Katelyn X KX Sharma Jitendra J McCormack Dana D Shin Tay Won TW Harrahill Andrew A Nyase Eric E Mudhar Gagandeep G Mauermann Abigail A Wysoker Alec A Nemesh James J Kashin Seva S Vergara Josselyn J Chelini Gabriele G Dimidschstein Jordane J Berretta Sabina S Deverman Benjamin E BE Boyden Ed E McCarroll Steven A SA Feng Guoping G

Science advances 20231012 41

The mammalian brain is composed of many brain structures, each with its own ontogenetic and developmental history. We used single-nucleus RNA sequencing to sample over 2.4 million brain cells across 18 locations in the common marmoset, a New World monkey primed for genetic engineering, and examined gene expression patterns of cell types within and across brain structures. The adult transcriptomic identity of most neuronal types is shaped more by developmental origin than by neurotransmitter sign ...[more]

PMID: 37824615

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Project description:BackgroundThe mammalian brain is organized into regions with specific biological functions and properties. These regions have distinct transcriptomes, but little is known whether they may also differ in their metabolome. The metabolome, a collection of small molecules or metabolites, is at the intersection of the genetic background of a given cell or tissue and the environmental influences that affect it. Thus, the metabolome directly reflects information about the physiologic state of a biological system under a particular condition. The objective of this study was to investigate whether various brain regions have diverse metabolome profiles, similarly to their genetic diversity. The answer to this question would suggest that not only the genome but also the metabolome may contribute to the functional diversity of brain regions.MethodsWe investigated the metabolome of four regions of the mouse brain that have very distinct functions: frontal cortex, hippocampus, cerebellum, and olfactory bulb. We utilized gas- and liquid- chromatography mass spectrometry platforms and identified 215 metabolites.ResultsPrincipal component analysis, an unsupervised multivariate analysis, clustered each brain region based on its metabolome content, thus providing the unique metabolic profile of each region. A pathway-centric analysis indicated that olfactory bulb and cerebellum had most distinct metabolic profiles, while the cortical parenchyma and hippocampus were more similar in their metabolome content. Among the notable differences were distinct oxidative-anti-oxidative status and region-specific lipid profiles. Finally, a global metabolic connectivity analysis using the weighted correlation network analysis identified five hub metabolites that organized a unique metabolic network architecture within each examined brain region. These data indicate the diversity of global metabolome corresponding to specialized regional brain function and provide a new perspective on the underlying properties of brain regions.ConclusionIn summary, we observed many differences in the metabolome among the various brain regions investigated. All four brain regions in our study had a unique metabolic signature, but the metabolites came from all categories and were not pathway-centric.

Dataset Information

A marmoset brain cell census reveals regional specialization of cellular identities.

Publications

A marmoset brain cell census reveals regional specialization of cellular identities.

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