Continuous and Discrete Neuron Types of the Adult Murine Striatum

Stanley, Geoffrey; Gokce, Ozgun; Malenka, Robert C.; Südhof, Thomas C.; Quake, Stephen R.

doi:10.1016/j.neuron.2019.11.004

Cited by 158Single-cell and spatial transcriptomicsNeuroscience and Neuropharmacology ResearchNeurogenesis and neuroplasticity mechanisms

Continuous and Discrete Neuron Types of the Adult Murine Striatum

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Stanley, Geoffrey, Gokce, Ozgun, Malenka, Robert C., Südhof, Thomas C., Quake, Stephen R.·2020·Neuron

DOI 10.1016/j.neuron.2019.11.004

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Abstract

The mammalian striatum is involved in many complex behaviors and yet is composed largely of a single neuron class: the spiny projection neuron (SPN). It is unclear to what extent the functional specialization of the striatum is due to the molecular specialization of SPN subtypes. We sought to define the molecular and anatomical diversity of adult SPNs using single-cell RNA sequencing (scRNA-seq) and quantitative RNA in situ hybridization (ISH). We computationally distinguished discrete versus continuous heterogeneity in scRNA-seq data and found that SPNs in the striatum can be classified into four major discrete types with no implied spatial relationship between them. Within these discrete types, we find continuous heterogeneity encoding spatial gradients of gene expression and defining anatomical location in a combinatorial mechanism. Our results suggest that neuronal circuitry has a substructure at far higher resolution than is typically interrogated, which is defined by the precise identity and location of a neuron.

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Recent transcriptomic and anatomical studies have argued that neurons in hippocampus, striatum, and cerebellum can be better described as forming partially continuous manifolds.
“Consistent with our interpretation, recent transcriptomic and anatomical studies have argued that neurons in hippocampus, striatum, and cerebellum can be better described as forming partially continuous manifolds27,37–39.”
From Phenotypic variation of transcriptomic cell types in mouse motor cortex (2021) · cites this paper as [38]
Continuous variation has frequently been observed even in transcriptomic data from isolated cells.
“Even in transcriptomic data from isolated cells, continuous variations were frequently observed (Stanley et al., 2020; Harris et al., 2018; Tasic et al., 2018).”
From Integrated Morphoelectric and Transcriptomic Classification of Cortical GABAergic Cells (2020) · cites this paper as Stanley et al., 2020
There is coexistence of discrete and continuous variations of cell features across modalities at the lower branch level.
“In this context, another important finding, consistent with and building on multiple other studies9,11,68,69, is the coexistence of discrete and continuous variations of cell features across modalities at the lower branch level.”
From A multimodal cell census and atlas of the mammalian primary motor cortex (2021) · cites this paper as [69]

STAR: ultrafast universal RNA-seq aligner
Dobin, A., Davis, C. A., Schlesinger, F., Drenkow, J., Zaleski, C., Jha, S., Batut, P., Chaisson, M., & Gingeras, T. R. (2013) · Bioinformatics · doi:10.1093/bioinformatics/bts635 · Cited by 51,709 · see citing works
HTSeq—a Python framework to work with high-throughput sequencing data
Anders, S., Pyl, P. T., & Huber, W. (2015) · Bioinformatics · doi:10.1093/bioinformatics/btu638 · Cited by 21,464 · see citing works
Integrative genomics viewer
Robinson, J. T., Thorvaldsdóttir, H., Winckler, W., Guttman, M., Lander, E. S., Getz, G., & Mesirov, J. P. (2011) · Nature Biotechnology · doi:10.1038/nbt.1754 · Cited by 15,390 · see citing works
SCANPY: large-scale single-cell gene expression data analysis
Wolf, F. A., Angerer, P., & Theis, F. J. (2018) · Genome Biology · doi:10.1186/s13059-017-1382-0 · Cited by 8,881 · see citing works
Spatial reconstruction of single-cell gene expression data
Satija, R., Farrell, J. A., Gennert, D., Schier, A. F., & Regev, A. (2015) · Nature Biotechnology · doi:10.1038/nbt.3192 · Cited by 7,055 · see citing works
Full-length RNA-seq from single cells using Smart-seq2
Picelli, S., Faridani, O. R., Björklund, Å. K., Winberg, G., Sagasser, S., & Sandberg, R. (2014) · Nature Protocols · doi:10.1038/nprot.2014.006 · Cited by 4,137 · see citing works
Cell types in the mouse cortex and hippocampus revealed by single-cell RNA-seq
Zeisel, A., Muñoz-Manchado, A. B., Codeluppi, S., Lönnerberg, P., La Manno, G., Juréus, A., Marques, S., Munguba, H., He, L., Betsholtz, C., et al. (2015) · Science · doi:10.1126/science.aaa1934 · Cited by 3,124 · see citing works
Molecular Architecture of the Mouse Nervous System
Zeisel, A., Hochgerner, H., Lönnerberg, P., Johnsson, A., Memic, F., van der Zwan, J., Häring, M., Braun, E., Borm, L. E., La Manno, G., et al. (2018) · Cell · doi:10.1016/j.cell.2018.06.021 · Cited by 2,995 · see citing works
A molecular atlas of cell types and zonation in the brain vasculature
Vanlandewijck, M., He, L., Mäe, M. A., Andrae, J., Ando, K., Del Gaudio, F., Nahar, K., Lebouvier, T., Laviña, B., Gouveia, L., et al. (2018) · Nature · doi:10.1038/nature25739 · Cited by 2,074 · see citing works
Molecular diversity and specializations among the cells of the adult mouse brain
Saunders, A., Macosko, E. Z., Wysoker, A., Goldman, M., Krienen, F. M., de Rivera, H., Bien, E., Baum, M., Bortolin, L., Wang, S., et al. (2018) · Cell · doi:10.1016/j.cell.2018.07.028 · Cited by 1,847 · see citing works
Adult mouse cortical cell taxonomy revealed by single cell transcriptomics
Tasic, B., Menon, V., Nguyen, T. N., Kim, T. K., Jarsky, T., Yao, Z., Levi, B., Gray, L. T., Sorensen, S. A., Dolbeare, T., et al. (2016) · Nature Neuroscience · doi:10.1038/nn.4216 · Cited by 1,714 · see citing works
PAGA: graph abstraction reconciles clustering with trajectory inference through a topology preserving map of single cells
Wolf, F. A., Hamey, F. K., Plass, M., Solana, J., Dahlin, J. S., Göttgens, B., Rajewsky, N., Simon, L., & Theis, F. J. (2019) · Genome Biology · doi:10.1186/s13059-019-1663-x · Cited by 1,698 · see citing works
Molecular evolution of FOXP2, a gene involved in speech and language
Enard, W., Przeworski, M., Fisher, S. E., Lai, C. S. L., Wiebe, V., Kitano, T., Monaco, A. P., & Pääbo, S. (2002) · Nature · doi:10.1038/nature01025 · Cited by 1,603 · see citing works
A survey of human brain transcriptome diversity at the single cell level
Darmanis, S., Sloan, S. A., Zhang, Y., Enge, M., Caneda, C., Shuer, L. M., Hayden Gephart, M. G., Barres, B. A., & Quake, S. R. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1507125112 · Cited by 1,401 · see citing works
Self-citation
Putting a spin on the dorsal-ventral divide of the striatum
Voorn, P., Vanderschuren, L. J. M. J., Groenewegen, H. J., Robbins, T. W., & Pennartz, C. M. A. (2004) · Trends in Neurosciences · doi:10.1016/j.tins.2004.06.006 · Cited by 1,188 · see citing works
Single-cell spatial reconstruction reveals global division of labour in the mammalian liver
Halpern, K. B., Shenhav, R., Matcovitch-Natan, O., Tóth, B., Lemze, D., Golan, M., Massasa, E. E., Baydatch, S., Landen, S., Moor, A. E., et al. (2017) · Nature · doi:10.1038/nature21065 · Cited by 1,059 · see citing works
Neuronal subtypes and diversity revealed by single-nucleus RNA sequencing of the human brain
Lake, B. B., Ai, R., Kaeser, G. E., Salathia, N. S., Yung, Y. C., Liu, R., Wildberg, A., Gao, D., Fung, H.-L., Chen, S., et al. (2016) · Science · doi:10.1126/science.aaf1204 · Cited by 957 · see citing works
CellProfiler™: Free, Versatile Software for Automated Biological Image Analysis
Lamprecht, M. R., Sabatini, D. M., & Carpenter, A. E. (2007) · BioTechniques · doi:10.2144/000112257 · Cited by 880 · see citing works
Neuronal cell-type classification: challenges, opportunities and the path forward
Zeng, H., & Sanes, J. R. (2017) · Nature Reviews Neuroscience · doi:10.1038/nrn.2017.85 · Cited by 841 · see citing works
Distinct functions of the two isoforms of dopamine D2 receptors
Usiello, A., Baik, J.-H., Rougé-Pont, F., Picetti, R., Dierich, A., LeMeur, M., Piazza, P. V., & Borrelli, E. (2000) · Nature · doi:10.1038/35041572 · Cited by 717 · see citing works
In Situ Transcription Profiling of Single Cells Reveals Spatial Organization of Cells in the Mouse Hippocampus
Shah, S., Lubeck, E., Zhou, W., & Cai, L. (2016) · Neuron · doi:10.1016/j.neuron.2016.10.001 · Cited by 671 · see citing works
The mouse cortico-striatal projectome
Hintiryan, H., Foster, N. N., Bowman, I., Bay, M., Song, M. Y., Gou, L., Yamashita, S., Bienkowski, M. S., Zingg, B., Zhu, M., et al. (2016) · Nature Neuroscience · doi:10.1038/nn.4332 · Cited by 541 · see citing works
FOXP2 as a molecular window into speech and language
Fisher, S. E., & Scharff, C. (2009) · Trends in Genetics · doi:10.1016/j.tig.2009.03.002 · Cited by 541 · see citing works
A comprehensive excitatory input map of the striatum reveals novel functional organization
Hunnicutt, B. J., Jongbloets, B. C., Birdsong, W. T., Gertz, K. J., Zhong, H., & Mao, T. (2016) · eLife · doi:10.7554/elife.19103 · Cited by 536 · see citing works
Basal Ganglia Disorders Associated with Imbalances in the Striatal Striosome and Matrix Compartments
Crittenden, J. R., & Graybiel, A. M. (2011) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2011.00059 · Cited by 470 · see citing works
Cellular Taxonomy of the Mouse Striatum as Revealed by Single-Cell RNA-Seq
Gokce, O., Stanley, G. M., Treutlein, B., Neff, N. F., Camp, J. G., Malenka, R. C., Rothwell, P. E., Fuccillo, M. V., Südhof, T. C., & Quake, S. R. (2016) · Cell Reports · doi:10.1016/j.celrep.2016.06.059 · Cited by 430 · see citing works
Self-citation
Mapping projections of molecularly defined dopamine neuron subtypes using intersectional genetic approaches
Poulin, J.-F., Caronia, G., Hofer, C., Cui, Q., Helm, B., Ramakrishnan, C., Chan, C. S., Dombeck, D. A., Deisseroth, K., & Awatramani, R. (2018) · Nature Neuroscience · doi:10.1038/s41593-018-0203-4 · Cited by 423 · see citing works
Spatial Gene-Expression Gradients Underlie Prominent Heterogeneity of CA1 Pyramidal Neurons
Cembrowski, M. S., Bachman, J. L., Wang, L., Sugino, K., Shields, B. C., & Spruston, N. (2016) · Neuron · doi:10.1016/j.neuron.2015.12.013 · Cited by 328 · see citing works
High-performance multiplexed fluorescence in situ hybridization in culture and tissue with matrix imprinting and clearing
Moffitt, J. R., Hao, J., Bambah-Mukku, D., Lu, T., Dulac, C., & Zhuang, X. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1617699113 · Cited by 308 · see citing works
Classes and continua of hippocampal CA1 inhibitory neurons revealed by single-cell transcriptomics
Harris, K. D., Hochgerner, H., Skene, N. G., Magno, L., Katona, L., Bengtsson Gonzales, C., Somogyi, P., Kessaris, N., Linnarsson, S., & Hjerling-Leffler, J. (2018) · PLoS Biology · doi:10.1371/journal.pbio.2006387 · Cited by 276 · see citing works
Spatial Autocorrelation: A Review of Existing and New Measures with Applications
Cliff, A. D., & Ord, K. (1970) · Economic Geography · doi:10.2307/143144 · Cited by 259 · see citing works
Classifying Drosophila Olfactory Projection Neuron Subtypes by Single-Cell RNA Sequencing
Li, H., Horns, F., Wu, B., Xie, Q., Li, J., Li, T., Luginbuhl, D. J., Quake, S. R., & Luo, L. (2017) · Cell · doi:10.1016/j.cell.2017.10.019 · Cited by 256 · see citing works
Self-citation
Cell clusters in the nucleus accumbens of the rat, and the mosaic relationship of opiate receptors, acetylcholinesterase and subcortical afferent terminations
Herkenham, M. A., Edley, S. M., & Stuart, J. (1984) · Neuroscience · doi:10.1016/0306-4522(84)90045-9 · Cited by 236 · see citing works
Single-cell analysis of early progenitor cells that build coronary arteries
Su, T., Stanley, G., Sinha, R., D’Amato, G., Das, S., Rhee, S., Chang, A. H., Poduri, A., Raftrey, B. C., Dinh, T. T., et al. (2018) · Nature · doi:10.1038/s41586-018-0288-7 · Cited by 230 · see citing works
Self-citation
Diversity of Interneurons in the Dorsal Striatum Revealed by Single-Cell RNA Sequencing and PatchSeq
Muñoz-Manchado, A. B., Bengtsson Gonzales, C., Zeisel, A., Munguba, H., Bekkouche, B., Skene, N. G., Lönnerberg, P., Ryge, J., Harris, K. D., Linnarsson, S., et al. (2018) · Cell Reports · doi:10.1016/j.celrep.2018.07.053 · Cited by 229 · see citing works
Quantitative visualization of alternative exon expression from RNA-seq data
Yarden Katz, A., Wang, E. T., Silterra, J., Schwartz, S., Wong, B., Thorvaldsdóttir, H., Robinson, J. T., Mesirov, J. P., Airoldi, E. M., & Burge, C. B. (2015) · Bioinformatics · doi:10.1093/bioinformatics/btv034 · Cited by 220 · see citing works
Getting specialized: presynaptic and postsynaptic dopamine D2 receptors
Mei, C. D., Ramos, M., Iitaka, C., & Borrelli, E. (2009) · Current Opinion in Pharmacology · doi:10.1016/j.coph.2008.12.002 · Cited by 220 · see citing works
Dissociable Structural and Functional Hippocampal Outputs via Distinct Subiculum Cell Classes
Cembrowski, M. S., Phillips, M. G., DiLisio, S. F., Shields, B. C., Winnubst, J., Chandrashekar, J. V., Bas, E., & Spruston, N. (2018) · Cell · doi:10.1016/j.cell.2018.03.031 · Cited by 195 · see citing works
Single-Cell RNA-Seq of Mouse Olfactory Bulb Reveals Cellular Heterogeneity and Activity-Dependent Molecular Census of Adult-Born Neurons
Tepe, B., Hill, M. C., Pekarek, B. T., Hunt, P. J., Martin, T. J., Martin, J. F., & Arenkiel, B. R. (2018) · Cell Reports · doi:10.1016/j.celrep.2018.11.034 · Cited by 183 · see citing works
Reconstruction of the Mouse Otocyst and Early Neuroblast Lineage at Single-Cell Resolution
Durruthy-Durruthy, R., Gottlieb, A., Hartman, B. H., Waldhaus, J., Laske, R. D., Altman, R., & Heller, S. (2014) · Cell · doi:10.1016/j.cell.2014.03.036 · Cited by 148 · see citing works
Comprehensive Identification and Spatial Mapping of Habenular Neuronal Types Using Single-Cell RNA-Seq
Pandey, S., Shekhar, K., Regev, A., & Schier, A. F. (2018) · Current Biology · doi:10.1016/j.cub.2018.02.040 · Cited by 144 · see citing works
The Dopamine D1–D2 Receptor Heteromer in Striatal Medium Spiny Neurons: Evidence for a Third Distinct Neuronal Pathway in Basal Ganglia
Perreault, M. L., Hasbi, A., O’Dowd, B. F., & George, S. R. (2011) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2011.00031 · Cited by 129 · see citing works
Diminished FoxP2 Levels Affect Dopaminergic Modulation of Corticostriatal Signaling Important to Song Variability
Murugan, M., Harward, S. C., Scharff, C., & MOONEY, R. D. (2013) · Neuron · doi:10.1016/j.neuron.2013.09.021 · Cited by 124 · see citing works
Single cell transcriptomics in neuroscience: cell classification and beyond
Tasic, B. (2018) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2018.04.021 · Cited by 83 · see citing works
The LIM homeobox gene <i>Isl1</i> is required for the correct development of the striatonigral pathway in the mouse
Ehrman, L. A., Mu, X., Waclaw, R. R., Yoshida, Y., Vorhees, C. V., Klein, W. H., & Campbell, K. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1308275110 · Cited by 79 · see citing works
Dual role for Islet-1 in promoting striatonigral and repressing striatopallidal genetic programs to specify striatonigral cell identity
Lu, K.-M., Evans, S. Μ., Hirano, S., & Liu, F.-C. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1319138111 · Cited by 69 · see citing works
The Zinc Finger Transcription Factor Sp9 Is Required for the Development of Striatopallidal Projection Neurons
Zhang, Q., Zhang, Y., Wang, C., Xu, Z., Liang, Q., An, L., Li, J., Liu, Z., You, Y., He, M., et al. (2016) · Cell Reports · doi:10.1016/j.celrep.2016.06.090 · Cited by 68 · see citing works
Single-cell transcriptomics of the developing lateral geniculate nucleus reveals insights into circuit assembly and refinement
Kalish, B. T., Cheadle, L., Hrvatin, S., Nagy, M. A., Rivera, S. A., Crow, M., Gillis, J. A., Kirchner, R. D., & Greenberg, M. E. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1717871115 · Cited by 68 · see citing works
Granule cells of the olfactory tubercle and the question of the islands of calleja
Millhouse, O. E. (1987) · The Journal of Comparative Neurology · doi:10.1002/cne.902650102 · Cited by 67 · see citing works
Neurokinin B‐producing projection neurons in the lateral stripe of the striatum and cell clusters of the accumbens nucleus in the rat
Zhou, L., Furuta, T., & Kaneko, T. (2004) · The Journal of Comparative Neurology · doi:10.1002/cne.20331 · Cited by 18 · see citing works

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Integrated Morphoelectric and Transcriptomic Classification of Cortical GABAergic Cells
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“Even in transcriptomic data from isolated cells, continuous variations were frequently observed (Stanley et al., 2020; Harris et al., 2018; Tasic et al., 2018).”
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Spatially resolved cell atlas of the mouse primary motor cortex by MERFISH
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Patch-seq: Past, Present, and Future
Lipovsek, M., Bardy, C., Cadwell, C. R., Hadley, K., Kobak, D., & Tripathy, S. J. (2021) · Journal of Neuroscience · doi:10.1523/jneurosci.1653-20.2020 · Cited by 98 · see citing works
The microcircuits of striatum in silico
Hjorth, J. J. J., Kozlov, A., Carannante, I., Nylén, J. F., Lindroos, R., Johansson, Y., Tokarska, A., Dorst, M. C., Suryanarayana, S. M., Silberberg, G., et al. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2000671117 · Cited by 96 · see citing works
A Molecular Calcium Integrator Reveals a Striatal Cell Type Driving Aversion
Kim, C. K., Sánchez, M. I., Hoerbelt, P., Fenno, L. E., Malenka, R. C., Deisseroth, K. A., & Ting, A. Y. (2020) · Cell · doi:10.1016/j.cell.2020.11.015 · Cited by 96 · see citing works
Self-citation
Transcriptional and anatomical diversity of medium spiny neurons in the primate striatum
He, J., Kleyman, M., Chen, J., Alikaya, A., Rothenhoefer, K. M., Öztürk, B. E., Wirthlin, M. E., Bostan, A. C., Fish, K. N., Byrne, L. C., et al. (2021) · Current Biology · doi:10.1016/j.cub.2021.10.015 · Cited by 96 · see citing works
The Tail of the Striatum: From Anatomy to Connectivity and Function
Valjent, E., & Gangarossa, G. (2020) · Trends in Neurosciences · doi:10.1016/j.tins.2020.10.016 · Cited by 95 · see citing works
Neural heterogeneity controls computations in spiking neural networks
Gast, R., Solla, S. A., & Kennedy, A. (2024) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2311885121 · Cited by 95 · see citing works
Bayesian model selection reveals biological origins of zero inflation in single-cell transcriptomics
Choi, K., Chen, Y., Skelly, D. A., & Churchill, G. A. (2020) · Genome biology · doi:10.1186/s13059-020-02103-2 · Cited by 77 · see citing works
Extensive and spatially variable within-cell-type heterogeneity across the basolateral amygdala
O’Leary, T. P., Sullivan, K. E., Wang, L., Clements, J., Lemire, A. L., & Cembrowski, M. S. (2020) · eLife · doi:10.7554/elife.59003 · Cited by 75 · see citing works
Loss of primary cilia and dopaminergic neuroprotection in pathogenic LRRK2-driven and idiopathic Parkinson’s disease
Khan, S. S., Jaimon, E., Lin, Y.-E., Nikoloff, J., Tonelli, F., Alessi, D. R., & Pfeffer, S. R. (2024) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2402206121 · Cited by 61 · see citing works
Crym-positive striatal astrocytes gate perseverative behaviour
Ollivier, M., Soto, J. S., Linker, K. E., Moye, S. L., Jami‐Alahmadi, Y., Jones, A. E., Divakaruni, A. S., Kawaguchi, R., Wohlschlegel, J. A., & Khakh, B. S. (2024) · Nature · doi:10.1038/s41586-024-07138-0 · Cited by 60 · see citing works
A multimodal cell census and atlas of the mammalian primary motor cortexPreprint
BRAIN Initiative Cell Census Network (BICCN), Adkins, R. S., Aldridge, A. I., Allen, S. W., Ament, S. A., An, X., Armand, E. J., Ascoli, G. A., Bakken, T. E., Bandrowski, A. E., et al. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.10.19.343129 · Cited by 60 · see citing works
Single nuclei transcriptomics in human and non-human primate striatum in opioid use disorder
Phan, B. N., Ray, M. H., Xue, X., Fu, C., Fenster, R. J., Kohut, S. J., Bergman, J., Haber, S. N., McCullough, K. M., Fish, M. K., et al. (2024) · Nature Communications · doi:10.1038/s41467-024-45165-7 · Cited by 56 · see citing works
Opponent control of reinforcement by striatal dopamine and serotonin
Pinto, D. F. C., Pomrenze, M. B., Guo, M. Y., Touponse, G. C., Chen, A. P. F., Bentzley, B. S., Eshel, N., & Malenka, R. C. (2024) · Nature · doi:10.1038/s41586-024-08412-x · Cited by 54 · see citing works
Self-citation
SWCNTs/PEDOT:PSS-Modified Microelectrode Arrays for Dual-Mode Detection of Electrophysiological Signals and Dopamine Concentration in the Striatum under Isoflurane Anesthesia
He, E., Xu, S., Dai, Y., Wang, Y., Xiao, G., Xie, J., Xu, S., Fan, P., Mo, F., Wang, M., et al. (2021) · ACS Sensors · doi:10.1021/acssensors.1c01241 · Cited by 52 · see citing works
Striatal projection neurons coexpressing dopamine D1 and D2 receptors modulate the motor function of D1- and D2-SPNs
Bonnavion, P., Varin, C., Fakhfouri, G., Olondo, P. M., Groote, A. D., Cornil, A., Lopez, R. L., Fernández, E. P., Isingrini, E., Rainer, Q., et al. (2024) · Nature Neuroscience · doi:10.1038/s41593-024-01694-4 · Cited by 51 · see citing works
Graded heterogeneity of metabotropic signaling underlies a continuum of cell-intrinsic temporal responses in unipolar brush cells
Guo, C., Huson, V., Macosko, E. Z., & Regehr, W. G. (2021) · Nature Communications · doi:10.1038/s41467-021-22893-8 · Cited by 50 · see citing works
Generating and Using Transcriptomically Based Retinal Cell Atlases
Shekhar, K., & Sanes, J. R. (2021) · Annual Review of Vision Science · doi:10.1146/annurev-vision-032621-075200 · Cited by 50 · see citing works
Molecular, spatial and projection diversity of neurons in primary motor cortex revealed by in situ single-cell transcriptomics
Zhang, M., Eichhorn, S. W., Zingg, B., Yao, Z., Zeng, H., Dong, H., & Zhuang, X. (2020) · doi:10.1101/2020.06.04.105700 · Cited by 44 · see citing works
Interneuron diversity in the human dorsal striatum
Garma, L. D., Harder, L., Barba-Reyes, J. M., Salas, S. M., Díez-Salguero, M., Nilsson, M. F., Serrano‐Pozo, A., Hyman, B. T., & Muñoz‐Manchado, A. B. (2024) · Nature Communications · doi:10.1038/s41467-024-50414-w · Cited by 48 · see citing works
From Progenitors to Progeny: Shaping Striatal Circuit Development and Function
Knowles, R., Dehorter, N., & Ellender, T. J. (2021) · Journal of Neuroscience · doi:10.1523/jneurosci.0620-21.2021 · Cited by 45 · see citing works
A molecularly defined D1 medium spiny neuron subtype negatively regulates cocaine addiction
Zhao, Z., Han, X., Chen, R., Liu, Y., Bhattacherjee, A., Chen, W., & Zhang, Y. (2022) · Science Advances · doi:10.1126/sciadv.abn3552 · Cited by 44 · see citing works
Predictive and robust gene selection for spatial transcriptomics
Covert, I., Gala, R., Wang, T., Svoboda, K., Sümbül, U., & Lee, S. (2023) · Nature Communications · doi:10.1038/s41467-023-37392-1 · Cited by 40 · see citing works
The nucleus accumbens shell: a neural hub at the interface of homeostatic and hedonic feeding
Marinescu, A., & Labouesse, M. A. (2024) · Frontiers in Neuroscience · doi:10.3389/fnins.2024.1437210 · Cited by 40 · see citing works
Dlx1/2- dependent expression of Meis2 promotes neuronal fate determination in the mammalian striatum
Su, Z., Wang, Z., Lindtner, S., Yang, L., Shang, Z., Tian, Y., Guo, R., You, Y., Zhou, W., Rubenstein, J. L. R., et al. (2022) · Development · doi:10.1242/dev.200035 · Cited by 40 · see citing works
Opportunities and challenges of single-cell and spatially resolved genomics methods for neuroscience discovery
Bonev, B., Castelo‐Branco, G., Chen, F., Codeluppi, S., Corces, M. R., Fan, J., Heiman, M., Harris, K., Inoue, F., Kellis, M., et al. (2024) · Nature Neuroscience · doi:10.1038/s41593-024-01806-0 · Cited by 39 · see citing works
Neuronal cell types, projections, and spatial organization of the central amygdala
O’Leary, T. P., Kendrick, R. M., Bristow, B. N., Sullivan, K. E., Wang, L., Clements, J., Lemire, A. L., & Cembrowski, M. S. (2022) · iScience · doi:10.1016/j.isci.2022.105497 · Cited by 38 · see citing works
Dopamine D1-D2 receptor heteromer expression in key brain regions of rat and higher species: Upregulation in rat striatum after cocaine administration
Hasbi, A., Sivasubramanian, M., Milenkovic, M., Komarek, K., Madras, B. K., & George, S. R. (2020) · Neurobiology of Disease · doi:10.1016/j.nbd.2020.105017 · Cited by 37 · see citing works
The cell as a bag of RNA
Quake, S. R. (2021) · Trends in Genetics · doi:10.1016/j.tig.2021.08.003 · Cited by 33 · see citing works
Self-citation
Morphological pseudotime ordering and fate mapping reveal diversification of cerebellar inhibitory interneurons
Wang, W. X., & Lefebvre, J. L. (2022) · Nature Communications · doi:10.1038/s41467-022-30977-2 · Cited by 32 · see citing works
Distinctiveness and continuity in transcriptome and connectivity in the anterior-posterior axis of the paraventricular nucleus of the thalamus
Shima, Y., Skibbe, H., Sasagawa, Y., Fujimori, N., Iwayama, Y., Isomura-Matoba, A., Yano, M., Ichikawa, T., Nikaido, I., Hattori, N., et al. (2023) · Cell Reports · doi:10.1016/j.celrep.2023.113309 · Cited by 31 · see citing works
Parallel and hierarchical neural mechanisms for adaptive and predictive behavioral control
Macpherson, T., Matsumoto, M., Gomi, H., Morimoto, J., Uchibe, E., & Hikida, T. (2021) · Neural Networks · doi:10.1016/j.neunet.2021.09.009 · Cited by 30 · see citing works
Transcriptomic and spatial organization of telencephalic GABAergic neurons
van Velthoven, C. T. J., Gao, Y., Kunst, M., Lee, C., McMillen, D., Chakka, A. B., Casper, T., Clark, M., Chakrabarty, R., Daniel, S. F., et al. (2025) · Nature · doi:10.1038/s41586-025-09296-1 · Cited by 30 · see citing works
Basal Ganglia—A Motion Perspective
Grillner, S. E., Robertson, B., & Kotaleski, J. H. (2020) · Comprehensive physiology · doi:10.1002/cphy.c190045 · Cited by 29 · see citing works
Applying single-cell and single-nucleus genomics to studies of cellular heterogeneity and cell fate transitions in the nervous system
Adameyko, I. I., Bakken, T. E., Bhaduri, A., Chhatbar, C., Filbin, M. G., Gate, D., Hochgerner, H., Kim, C. N., Krull, J. E., Manno, G. L., et al. (2024) · Nature Neuroscience · doi:10.1038/s41593-024-01827-9 · Cited by 25 · see citing works
Self-citation
An unsupervised map of excitatory neuron dendritic morphology in the mouse visual cortex
Weis, M. A., Papadopoulos, S., Hansel, L., Lüddecke, T., Celii, B., Fahey, P. G., Wang, E. Y., Bae, J. A., Bodor, A. L., Brittain, D., et al. (2025) · Nature Communications · doi:10.1038/s41467-025-58763-w · Cited by 24 · see citing works
Homeobox Gene Six3 is Required for the Differentiation of D2-Type Medium Spiny Neurons
Song, X., Chen, H., Shang, Z., Du, H., Li, Z., Wen, Y. F., Liu, G., Qi, D., You, Y., Yang, Z., et al. (2021) · Neuroscience Bulletin · doi:10.1007/s12264-021-00698-5 · Cited by 24 · see citing works
Excessive firing of dyskinesia-associated striatal direct pathway neurons is gated by dopamine and excitatory synaptic input
Ryan, M., Girasole, A. E., Flores, A. J., Twedell, E. L., McGregor, M. M., Brakaj, R. J., Paletzki, R. F., Hnasko, T. S., Gerfen, C. R., & Nelson, A. (2024) · Cell Reports · doi:10.1016/j.celrep.2024.114483 · Cited by 23 · see citing works
Development and function of the medial amygdala
Prakash, N., Irqeba, A. A., & Corbin, J. G. (2024) · Trends in Neurosciences · doi:10.1016/j.tins.2024.11.004 · Cited by 22 · see citing works
Lateral olivocochlear neurons modulate cochlear responses to noise exposure
Sitko, A. A., Frank, M. M., Romero, G. E., Hunt, M., & Goodrich, L. V. (2025) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2404558122 · Cited by 22 · see citing works
Molecular, anatomical, and functional organization of lung interoceptorsPreprint
Liu, Y., Kinsey, L., de Arce, A. D., & Krasnow, M. A. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.11.10.468116 · Cited by 22 · see citing works
Striatal Control of Movement: A Role for New Neuronal (Sub-) Populations?
Fieblinger, T. (2021) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2021.697284 · Cited by 21 · see citing works
TREX1 is required for microglial cholesterol homeostasis and oligodendrocyte terminal differentiation in human neural assembloids
Goldberg, G., Coelho, L. B. V., Mo, G., Adang, L. A., Patne, M., Chen, Z., García-Bassets, I., Mesci, P., & Muotri, A. R. (2023) · Molecular Psychiatry · doi:10.1038/s41380-023-02348-w · Cited by 20 · see citing works
The single-cell opioid responses in the context of HIV (SCORCH) consortium
Ament, S. A., Campbell, R. R., Lobo, M. K., Receveur, J. P., Agrawal, K., Borjabad, A., Byrareddy, S. N., Chang, L., Clarke, D., Emani, P. S., et al. (2024) · Molecular Psychiatry · doi:10.1038/s41380-024-02620-7 · Cited by 20 · see citing works
Unbiased identification of novel transcription factors in striatal compartmentation and striosome maturation
Cirnaru, M., Song, S., Tshilenge, K., Corwin, C., Mleczko, J., Aguirre, C. G., Benlhabib, H., Bendl, J. M., Apontes, P., Fullard, J. F., et al. (2021) · eLife · doi:10.7554/elife.65979 · Cited by 18 · see citing works
Intrinsic electrophysiological properties predict variability in morphology and connectivity among striatal Parvalbumin-expressing Pthlh-cells
Gonzales, C. B., Hunt, S., Muñoz‐Manchado, A. B., McBain, C. J., & Hjerling‐Leffler, J. (2020) · Scientific Reports · doi:10.1038/s41598-020-72588-1 · Cited by 17 · see citing works
Pathogenic <i>LRRK2</i> mutations cause loss of primary cilia and Neurturin in striatal parvalbumin interneurons
Lin, Y.-E., Jaimon, E., Tonelli, F., & Pfeffer, S. R. (2025) · Life Science Alliance · doi:10.26508/lsa.202402922 · Cited by 16 · see citing works
Integrating single-cell transcriptomics with cellular phenotypes: cell morphology, Ca2+ imaging and electrophysiology
Camuñas-Soler, J. (2023) · Biophysical Reviews · doi:10.1007/s12551-023-01174-2 · Cited by 16 · see citing works
Cross-species consensus atlas of the primate basal gangliaPreprint
Johansen, N., Fu, Y., Schmitz, M. T., Dubuc, A., Kempynck, N., Wirthlin, M. E., Garcia, A. D., Hewitt, M. N., Turner, M. A., Seeman, S. C., et al. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2025.12.15.694496 · Cited by 17 · see citing works
Highly sensitive spatial transcriptomics using FISHnCHIPs of multiple co-expressed genes
Zhou, X., Seow, W. Y., Ha, N., Cheng, T. H., Jiang, L., Boonruangkan, J., Goh, J. J. L., Prabhakar, S., Chou, N., & Chen, K. H. (2024) · Nature Communications · doi:10.1038/s41467-024-46669-y · Cited by 15 · see citing works
How dopamine enables learning from aversion
Lopez, G. C., & Lerner, T. N. (2024) · Current Opinion in Behavioral Sciences · doi:10.1016/j.cobeha.2024.101476 · Cited by 16 · see citing works
Integrative multi-dimensional characterization of striatal projection neuron heterogeneity in adult brainPreprint
Gayden, J. D., Puig, S., Srinivasan, C., Phan, B. N., Abdelhady, G., Buck, S. A., Gamble, M. C., Tejeda, H. A., Dong, Y., Pfenning, A. R., et al. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.05.04.539488 · Cited by 14 · see citing works
A global molecular code for birth order and neuronal identity in Drosophila
Cachero, S., Mitletton, M., Beckett, I. R., Marin, E. C., Capdevila, L. S., Gkantia, M., Soffers, J. H., Lacin, H., Jefferis, G. S. X. E., & Doná, E. (2026) · Nature · doi:10.1038/s41586-026-10797-w · Cited by 13 · see citing works
The transcription factor Zfp503 promotes the D1 MSN identity and represses the D2 MSN identity
Shang, Z., Shang, Z., Wang, Z., Wang, Z., Tian, Y., Gao, Y., Su, Z., Guo, R., Liu, G., Li, X., et al. (2022) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2022.948331 · Cited by 12 · see citing works
PQBP1 regulates striatum development through balancing striatal progenitor proliferation and differentiation
Liu, W., Xie, H., Liu, X., Xu, S., Cheng, S., Wang, Z., Xie, T., Zhang, Z. C., & Han, J. (2023) · Cell Reports · doi:10.1016/j.celrep.2023.112277 · Cited by 12 · see citing works
Spiny projection neurons exhibit transcriptional signatures within subregions of the dorsal striatum
Roman, K. M., Dinasarapu, A. R., VanSchoiack, A., Ross, P. M., Kroeppler, D., Jinnah, H. A., & Hess, E. J. (2023) · Cell Reports · doi:10.1016/j.celrep.2023.113435 · Cited by 12 · see citing works
Dynamic FoxP2 levels in male zebra finches are linked to morphology of adult-born Area X medium spiny neurons
Kosubek-Langer, J., & Scharff, C. (2020) · Scientific Reports · doi:10.1038/s41598-020-61740-6 · Cited by 11 · see citing works
Dopaminergic specializations for flexible behavioral control: linking levels of analysis and functional architectures
Hamid, A. (2021) · Current Opinion in Behavioral Sciences · doi:10.1016/j.cobeha.2021.07.005 · Cited by 11 · see citing works
Accurate inference of genome-wide spatial expression with iSpatial
Zhang, C., Chen, R., & Zhang, Y. (2022) · Science Advances · doi:10.1126/sciadv.abq0990 · Cited by 11 · see citing works
Spatial profiling of the interplay between cell type- and vision-dependent transcriptomic programs in the visual cortex
Xie, F., Jain, S., Xu, R., Butrus, S., Tan, Z., Xu, X., Shekhar, K., & Zipursky, S. L. (2025) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2421022122 · Cited by 10 · see citing works
Amygdalostriatal transition zone neurons encode sustained cue responses to guide defensive behaviors
Mills, F., Lee, C. R., Howe, J. R., Li, H., Keisler, M. N., Shao, S., Taschbach, F., Lemieux, M., Aloboudi, F., White, J., et al. (2026) · Neuron · doi:10.1016/j.neuron.2026.08.012 · Cited by 10 · see citing works
High-Content Single-Cell Förster Resonance Energy Transfer Imaging of Cultured Striatal Neurons Reveals Novel Cross-Talk in the Regulation of Nuclear Signaling by Protein Kinase A and Extracellular Signal-Regulated Kinase 1/2
Jones-Tabah, J., Martin, R., Tanny, J. C., Clarke, P. B. S., & Hébert, T. E. (2021) · Molecular Pharmacology · doi:10.1124/molpharm.121.000290 · Cited by 10 · see citing works
A cross-species spatial transcriptomic atlas of the human and non-human primate basal gangliaPreprint
Hewitt, M. N., Turner, M. A., Johansen, N., McMillen, D., Dan, S., DeBerardine, M., Ruiz, A., Huang, M., Quon, J. S., Fu, Y., et al. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.11.22.688128 · Cited by 10 · see citing works
A single-cell trajectory atlas of striatal development
Anderson, A. G., Kulkarni, A., & Konopka, G. (2023) · Scientific Reports · doi:10.1038/s41598-023-36255-5 · Cited by 9 · see citing works
SMDB: a Spatial Multimodal Data Browser
Cao, R., Ling, Y., Meng, J., Jiang, A., Luo, R., He, Q., Li, A., Chen, Y., Zhang, Z., Liu, F., et al. (2023) · Nucleic Acids Research · doi:10.1093/nar/gkad413 · Cited by 9 · see citing works
Cell types as species: Exploring a metaphor
Doyle, J. J. (2022) · Frontiers in Plant Science · doi:10.3389/fpls.2022.868565 · Cited by 8 · see citing works
Differential Activation States of Direct Pathway Striatal Output Neurons during l-DOPA-Induced Dyskinesia Development
Figge, D. A., Amaral, H. D. O., Crim, J., Cowell, R. M., Standaert, D. G., & Jaunarajs, K. L. E. (2024) · Journal of Neuroscience · doi:10.1523/jneurosci.0050-24.2024 · Cited by 7 · see citing works
High-throughput analysis of dendrite and axonal arbors reveals transcriptomic correlates of neuroanatomy
Gliko, O., Mallory, M., Dalley, R. A., Gala, R., Gornet, J., Zeng, H., Sorensen, S. A., & Sümbül, U. (2024) · Nature Communications · doi:10.1038/s41467-024-50728-9 · Cited by 7 · see citing works
Joint inference of discrete cell types and continuous type-specific variability in single-cell datasets with MMIDAS
Marghi, Y. M., Gala, R., Baftizadeh, F., & Sümbül, U. (2024) · Nature Computational Science · doi:10.1038/s43588-024-00683-8 · Cited by 6 · see citing works
Epigenomic profiling of mouse nucleus accumbens at single-cell resolution
Bhatia, P., Yang, L., Luo, J. X. J., Xu, M., & Renthal, W. (2023) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2023.103857 · Cited by 5 · see citing works
Spatiomolecular mapping reveals anatomical organization of heterogeneous cell types in the human nucleus accumbens
Ravichandran, P., Bach, S. V., Phillips, R. A., Valentine, M. R., Eagles, N. J., Du, Y., Rosario, I. D., AlGrain, H. A., Maguire, S. E., Miller, R. A., et al. (2026) · Neuron · doi:10.1016/j.neuron.2026.06.002 · Cited by 5 · see citing works
Topographic structure and function of locus coeruleus noradrenaline neurons
Su, Z., Kosillo, P., Jung, K., Chen, S., Summers, M. T., Piet, A. T., Hou, H., Hagihara, K. M., Friedmann, D., Ho-Shing, O., et al. (2026) · Nature · doi:10.1038/s41586-026-11026-0 · Cited by 5 · see citing works
Harmaline toxicity on dorsal striatal neurons and its role in tremor
Zhan, X., Do, L. V., Zou, L. B., Zhan, R. S., Jones, M., Nawaz, S., & Manaye, K. F. (2023) · NeuroToxicology · doi:10.1016/j.neuro.2023.10.005 · Cited by 5 · see citing works
INSTINCT: Multi-sample integration of spatial chromatin accessibility sequencing data via stochastic domain translation
Liu, Y., Li, Z., Chen, X., Cui, X., Gao, Z., & Jiang, R. (2025) · Nature Communications · doi:10.1038/s41467-025-56535-0 · Cited by 5 · see citing works
Δ9-Tetrahydrocannabinol does not upregulate an aversive dopamine receptor mechanism in adolescent brain unlike in adults
Raddo, M.-E. D., Milenkovic, M., Sivasubramanian, M., Hasbi, A., Bergman, J., Withey, S. L., Madras, B. K., & George, S. R. (2023) · Current Research in Neurobiology · doi:10.1016/j.crneur.2023.100107 · Cited by 5 · see citing works
Response mechanism of the auditory FitzHugh–Nagumo neuron
Zhao, Y., Wang, L., & Duan, S. (2025) · Chaos Solitons & Fractals · doi:10.1016/j.chaos.2025.117422 · Cited by 4 · see citing works
Dopamine and serotonin inversely modulate D2 medium spiny neurons to regulate cocaine reward
Pinto, D. F. C., Guo, M. Y., Pomrenze, M. B., Morishita, W., Li, M. X., Zweifel, L. S., Eshel, N., & Malenka, R. C. (2026) · Nature Communications · doi:10.1038/s41467-026-70519-8 · Cited by 4 · see citing works
Self-citation
Cross-species single-cell atlas of the striatum defines cell-type and subregion disease vulnerabilities
Linville, R. M., James, B. T., Galani, K., Ho, L., Shin, J. H., Oliver, E., Fass, S. B., Cameron, J. C., Fitzwalter, B. E., Bock, R., et al. (2026) · Cell · doi:10.1016/j.cell.2026.08.006 · Cited by 4 · see citing works
Cell‐Type Specific Circuits in the Mammillary Body for Place and Object Recognition Memory
Li, L., Guo, Y., Jing, W., Tang, X., Zeng, J., Hou, Z., Song, Y., He, A., Li, H., Zhu, L., et al. (2025) · Advanced Science · doi:10.1002/advs.202409397 · Cited by 4 · see citing works

Cellular Taxonomy of the Mouse Striatum as Revealed by Single Cell RNA Sequencing
Stanley, G., Gökçe, Ö., Treutlein, B., Südhof, T. C., & Quake, S. R. (2016) · Biophysical Journal · doi:10.1016/j.bpj.2015.11.1723 · Cited by 3 · see citing works
Self-citation
Integrative multi-dimensional characterization of striatal projection neuron heterogeneity in adult brainPreprint
Gayden, J. D., Puig, S., Srinivasan, C., Phan, B. N., Abdelhady, G., Buck, S. A., Gamble, M. C., Tejeda, H. A., Dong, Y., Pfenning, A. R., et al. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.05.04.539488 · Cited by 14 · see citing works
Cellular Taxonomy of the Mouse Striatum as Revealed by Single-Cell RNA-Seq
Gokce, O., Stanley, G. M., Treutlein, B., Neff, N. F., Camp, J. G., Malenka, R. C., Rothwell, P. E., Fuccillo, M. V., Südhof, T. C., & Quake, S. R. (2016) · Cell Reports · doi:10.1016/j.celrep.2016.06.059 · Cited by 430 · see citing works
Self-citation
A Multimodal Atlas Reveals the Anatomical Distribution of Medium Spiny Neuron Subtypes and a Novel RGS6+ Population in the Primate StriatumPreprint
Abdelhady, G., Brull, O. R., He, J., Lin, M. K., Galván, A., Pfenning, A. R., Bostan, A. C., & Stauffer, W. R. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.11.16.688724 · Cited by 2 · see citing works
A Spatiomolecular Map of the Striatum
Märtin, A., Calvigioni, D., Tzortzi, O., Fuzik, J., Wärnberg, E., & Meletis, K. (2019) · Cell Reports · doi:10.1016/j.celrep.2019.11.096 · Cited by 127 · see citing works

Authors: Stanley, G., Gokce, O., Malenka, R. C., Südhof, T. C., & Quake, S. R.
Affiliations: Stanford Medicine (US)
Howard Hughes Medical Institute (US)
Chan Zuckerberg Biohub San Francisco (US)
Corresponding author: Südhof, Thomas C.
Quake, Stephen R.
ORCID: Malenka, Robert C.
Südhof, Thomas C.
Quake, Stephen R.
Venue: Neuron
Publisher: Elsevier BV
Published: 2020-02
Volume: 105
Issue: 4
Pages: 688-699.e8
ISSN: 0896-6273 (ISSN-L)
DOI: 10.1016/j.neuron.2019.11.004
OpenAlex: W2991860444
Cited by: 158
References: 50
Citations by year: 2026: 24 · 2025: 27 · 2024: 28 · 2023: 17 · 2022: 13 · 2021: 27 · 2020: 22
FWCI: 5.13
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/legal/tdmrep-license (tdm)
www.elsevier.com/open-access/userlicense/1.0/ (vor, 384 d)
Locations: Neuron (publishedVersion)
bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by)
PubMed (publishedVersion)
Funders: National Institutes of Health
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Single-cell and spatial transcriptomics
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
Keywords: striatum, medium spiny neurons, neuronal heterogeneity, neuronal cell types, molecular subtypes, neural circuits, adult mice, single-cell RNA sequencing, spatial transcriptomics
MeSH terms: Animals, Corpus Striatum, Male, Mice, Inbred C57BL, Mice, Transgenic, Nerve Net, Neurons, Mice

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