Single-cell spatial transcriptome reveals cell-type organization in the macaque cortex

Chen, Ao; Sun, Yi; Lei, Ying; Li, Chao; Liao, Sha; Meng, Juan; Bai, Yiqin; Liu, Zhen; Zhang, Liang; Zhu, Zhiyong; Yuan, Naiming; Yang, Hao; Wu, Zihan; Lin, Feng; Wang, Kexin; Li, Mei; Zhang, Shuzhen; Yang, Meisong; Fei, Tianyi; Zhuang, Zhenkun; Huang, Yiming; Zhang, Yong; Xu, Yan; Cui, Luman; Zhang, Ruiyi; Han, Lei; Sun, Xing; Chen, Bichao; Li, Wenjiao; Huangfu, Baoqian; Ma, Kailong; Ma, Jianyun; Li, Zhao; Yikun, Lin; Wang, He; Zhong, Yan-Qing; Zhang, Huifang; Yu, Qian; Wang, Yaqian; Liu, Xing; Peng, Jian; Liu, Chuanyu; Chen, Wei; Pan, Wentao; An, Yingjie; Xia, Shihui; Lu, Yanbing; Wang, Mingli; Song, Xinxiang; Liu, Shuai; Wang, Zhifeng; Gong, Chun; Huang, Xin; Yuan, Yue; Zhao, Yun; Chai, Qinwen; Tan, Xing Haw Marvin; Liu, Jianfeng; Zheng, Mingyuan; Li, Shengkang; Huang, Yaling; Hong, Yan; Huang, Zirui; Li, Min; Jin, Mengmeng; Li, Yan; Zhang, Hui; Sun, Shuangwen; Gao, Li; Bai, Yinqi; Cheng, Mengnan; Hu, Guohai; Liu, Shiping; Wang, Bo; Xiang, Bin; Li, Shuting; Li, Huanhuan; Chen, Mengni; Wang, Shiwen; Li, Minglong; Liu, Weibin; Liu, Xin; Zhao, Qian; Lisby, Michael; Wang, Jing; Jiao, Fang; Lin, Yuanhua; Xie, Qing; He, Jie; Xu, Huatai; Wei, Huang; Mulder, Jan; Yang, Huanming; Sun, Yan-Gang; Uhlén, Mathias; Poo, Mu‐ming; Wang, Jian; Yao, Jianhua; Wu, Wei; Li, Yuxiang; Shen, Zhiming; Liu, Longqi; Liu, Zhiyong; Xu, Xun; Li, C.

doi:10.1016/j.cell.2023.06.009

Cited by 38 publications

(27 citation statements)

References 77 publications

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“…Starting with studies in rodents (Oh et al, 2014; Kim et al, 2017; Bjerke et al, 2020), the traditional approach of investigating areas and nuclei one or a few at a time is being complemented by projects involving larger datasets, and focused on unveiling organizational principles, often relying on multiple techniques. Such approaches have recently made their way to the brains of non-human primates, revealing new information based on single-neuron resolution connectivity (Majka et al, 2020; Skibbe et al, 2023) and transcriptomics (Krienen et al, 2020, 2023; Chen et al, 2023), sometimes combined with non-invasive imaging (Liu et al 2020; Tian et al, 2022). However, one missing link in these efforts has been their relation to the traditionally recognized cell types of the mammalian cortex, for which a wealth of cytological and physiological knowledge is available, and which are central to the generation of biophysically realistic models of brain function (e.g.…”

Section: Discussionmentioning

confidence: 99%

“…For example, to date, comprehensive spatial maps of classes of neurons defined by expression of calcium-binding proteins have only been obtained in the mouse brain (Kim et al, 2017; Bjerke et al, 2020). In comparison, our knowledge of this subject in the primate cortex remains less complete, despite recent progress in mapping the distribution of cells expressing different molecules based on transcriptomics (Chen et al, 2023; Krienen et al, 2023) and receptor radioautography (Froudist-Walsh et al, 2023). A comprehensive knowledge of the distribution of different neuronal types in non-human primates is particularly important given the marked elaboration of the cortex in primate evolution and their essential role in translational research (Mitchell et al, 2018; Lear et al, 2022).…”

Section: Introductionmentioning

confidence: 99%

“…CB + neurons in the primate cortex are, in vast majority, inhibitory (GABAergic) interneurons (Hendry et al, 1989; Condé et al, 1994; De Felipe 1997; De Felipe et al, 1999; Bourne et al, 2007), but also include, in some areas, a smaller and more variable population of pyramidal cells (Kondo et al, 1999). The CB marker gene (CALB1) is mainly expressed by the somatostatin (SST) and lysosome-associated membrane protein 5 (LAMP5) subclasses of GABAergic cells, which are among the five main categories of interneurons in the mammalian brain (Hodge et al, 2019; Bakken et al, 2021; Yao et al, 2021; Chen et al, 2023).…”

Section: Introductionmentioning

confidence: 99%

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Distribution of calbindin-positive neurons across areas and layers of the marmoset cerebral cortex

Atapour,

Rosa,

Bai

et al. 2024

Preprint

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SummaryThe calcium-binding protein calbindin is selectively expressed in specific neuronal populations of the cerebral cortex, including major classes of inhibitory interneurons. We have charted the distribution of calbindin-positive (CB+) neurons across areas and layers of the entire marmoset cortex using a combination of immunohistochemistry, AI-based image segmentation, 3-dimensional reconstruction, and cytoarchitecture-aware registration. CB+neurons formed 10-20% of the cortical neuronal population, occurring in higher proportions in areas corresponding to low hierarchical levels of processing, such as sensory cortices. Although CB+neurons concentrated in the supragranular layers, there were clear trends in laminar distribution: the relative density in infragranular layers increased with hierarchical level, and the density in layer 4 was lowest in areas involved in sensorimotor integration and action planning. These results reveal new aspects of the cytoarchitectural organization of the primate cortex and demonstrate an efficient approach to mapping the full distribution of neurochemically distinct cell types throughout the brain, readily applicable to most mammalian species and parts of the nervous system.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Distribution of calbindin-positive neurons across areas and layers of the marmoset cerebral cortex

Atapour,

Rosa,

Bai

et al. 2024

Preprint

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“…ISN can produce rich and naturalistic neural responses, similar to real neural firing rates. Our network comprised 150 excitatory and 50 inhibitory neurons (N=200 neurons) with a similar neuron proportion to that in the MC of non-human primates (Bakken et al, 2021; Chen et al, 2023).…”

Section: Methodsmentioning

confidence: 99%

Internal Dynamics Interact with Proprioceptive Feedback During Movement Execution in an RNN Model of Motor Cortex

Jiang,

Bu,

Zheng

et al. 2023

Preprint

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Neuronal population responses in motor cortex display low-dimensional rotational patterns, where neural state rotates consistently during movement execution. These patterns are thought to arise from the internal dynamics within motor cortex. However, external inputs such as proprioception also shape motor cortical activity. To investigate the roles of internal dynamics and proprioceptive feedback, we constructed an inhibitory stabilized network, with excitatory recurrence stabilized by inhibition, designed to control an arm model performing delayed reach task. The optimized network generated patterns similar to those observed in motor cortex data, demonstrating our model’s plausibility. We designed a disruption strategy to dissect the contribution of internal dynamics and proprioceptive feedback, and found that disrupting internal dynamics significantly diminished rotational dynamics, whereas disrupting proprioceptive feedback led to ceaseless movement. Thus, internal dynamics dominate, while proprioceptive feedback fine-turns cortical pattern generation. Analysis of the ablation experiment revealed that proprioceptive feedback improved the robustness against noisy initial conditions by decreasing tangling in neural activity. Finally, our network still exhibited rotational dynamics when the arm moved at a constant speed, suggesting that these rotations could be prominent features of motor cortical activity.

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“…Future studies will continue to refine our understanding of the insula, hopefully improving toward anatomically and functionally relatable and less ambiguous partition. Recent advanced enabling, for example, the combination of classical cytoarchitectonics or tract tracing with neurotransmitter receptor mapping (Froudist-Walsh et al, 2023) or high-density single-cell spatial mapping of the expression of hundreds of genes (Chen et al, 2023), could help support or instead simplify the dysgranular parcellations. High-resolution neuroimaging capturing the curved surface of the insula (Goense & Logothetis, 2006;Zhu & Vanduffel, 2019) and high-density electrode arrays implanted across different stripes of the insula could verify and reveal their functional implications.…”

Section: Limitations Of the Present Study And Future Perspectivesmentioning

confidence: 99%

Cytoarchitectonic and connection stripes in the dysgranular insular cortex in the macaque monkey

Krockenberger,

Saleh‐Mattesich,

Evrard

2023

J of Comparative Neurology

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The insula has been classically divided into broad granular, dysgranular, and agranular architectonic sectors. We previously proposed a novel partition, dividing each sector into four to seven sharply delimited architectonic areas, with the dysgranular areas being possibly further subdivided into subtle horizontal partitions or “stripes.” In architectonics, discrete subparcellations are prone to subjective variability and need being supported with additional neuroanatomical methods. Here, using a secondary analysis of indirect connectional data in the rhesus macaque monkey, we examined the spatial relationship between the dysgranular architectonic stripes and tract‐tracing labeling patterns produced in the insula with injections of neuronal tracers in other cortical regions. The injections consistently produced sharply delimited patches of anterograde and/or retrograde labeling, which formed stripes across consecutive coronal sections of the insula. While the overall pattern of labeling on individual coronal sections varied with the injection site, the boundaries of the patches consistently coincided with architectonic boundaries on an adjacent cyto‐ (Nissl) and/or myelo‐ (Gallyas) architectonic section. This overlap supports the existence of a fine dysgranular stripe‐like partition of the primate insula, with possibly major implications for interoceptive processing in primates including humans. The modular organization of the insula could underlie a serial stream of integration from a dorsal primary interoceptive cortex toward progressively more ventral egocentric “self‐agency” and allocentric “social” dysgranular processing units.

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Single-cell spatial transcriptome reveals cell-type organization in the macaque cortex

Cited by 38 publications

References 77 publications

Distribution of calbindin-positive neurons across areas and layers of the marmoset cerebral cortex

Distribution of calbindin-positive neurons across areas and layers of the marmoset cerebral cortex

Internal Dynamics Interact with Proprioceptive Feedback During Movement Execution in an RNN Model of Motor Cortex

Cytoarchitectonic and connection stripes in the dysgranular insular cortex in the macaque monkey

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