Spatial transcriptomics reveals human cortical layer and area specification
The human cerebral cortex is composed of six layers and dozens of areas that are molecularly and structurally distinct 1 , 2 , 3 – 4 . Although single-cell transcriptomic studies have advanced the molecular characterization of human cortical development, a substantial gap exists owing to the loss of...
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| Published in | Nature (London) Vol. 644; no. 8075; pp. 153 - 163 |
|---|---|
| Main Authors | , , , , , , , , , , , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
London
Nature Publishing Group UK
07.08.2025
Nature Publishing Group |
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| Online Access | Get full text |
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| Abstract | The human cerebral cortex is composed of six layers and dozens of areas that are molecularly and structurally distinct
1
,
2
,
3
–
4
. Although single-cell transcriptomic studies have advanced the molecular characterization of human cortical development, a substantial gap exists owing to the loss of spatial context during cell dissociation
5
,
6
,
7
–
8
. Here we used multiplexed error-robust fluorescence in situ hybridization (MERFISH)
9
, augmented with deep-learning-based nucleus segmentation, to examine the molecular, cellular and cytoarchitectural development of the human fetal cortex with spatially resolved single-cell resolution. Our extensive spatial atlas, encompassing more than 18 million single cells, spans eight cortical areas across seven developmental time points. We uncovered the early establishment of the six-layer structure, identifiable by the laminar distribution of excitatory neuron subtypes, 3 months before the emergence of cytoarchitectural layers. Notably, we discovered two distinct modes of cortical areal specification during mid-gestation: (1) a continuous, gradual transition observed across most cortical areas along the anterior–posterior axis and (2) a discrete, abrupt boundary specifically identified between the primary (V1) and secondary (V2) visual cortices as early as gestational week 20. This sharp binary transition in V1–V2 neuronal subtypes challenges the notion that mid-gestation cortical arealization involves only gradient-like transitions
6
,
10
. Furthermore, integrating single-nucleus RNA sequencing with MERFISH revealed an early upregulation of synaptogenesis in V1-specific layer 4 neurons. Collectively, our findings underscore the crucial role of spatial relationships in determining the molecular specification of cortical layers and areas. This study establishes a spatially resolved single-cell analysis paradigm and paves the way for the construction of a comprehensive developmental atlas of the human brain.
Multiplexed error-robust fluorescence in situ hybridization (MERFISH) together with deep-learning-based nucleus segmentation enabled the construction of a highly detailed and informative spatially resolved single-cell atlas of human fetal cortical development. |
|---|---|
| AbstractList | The human cerebral cortex is composed of six layers and dozens of areas that are molecularly and structurally distinct
. Although single-cell transcriptomic studies have advanced the molecular characterization of human cortical development, a substantial gap exists owing to the loss of spatial context during cell dissociation
. Here we used multiplexed error-robust fluorescence in situ hybridization (MERFISH)
, augmented with deep-learning-based nucleus segmentation, to examine the molecular, cellular and cytoarchitectural development of the human fetal cortex with spatially resolved single-cell resolution. Our extensive spatial atlas, encompassing more than 18 million single cells, spans eight cortical areas across seven developmental time points. We uncovered the early establishment of the six-layer structure, identifiable by the laminar distribution of excitatory neuron subtypes, 3 months before the emergence of cytoarchitectural layers. Notably, we discovered two distinct modes of cortical areal specification during mid-gestation: (1) a continuous, gradual transition observed across most cortical areas along the anterior-posterior axis and (2) a discrete, abrupt boundary specifically identified between the primary (V1) and secondary (V2) visual cortices as early as gestational week 20. This sharp binary transition in V1-V2 neuronal subtypes challenges the notion that mid-gestation cortical arealization involves only gradient-like transitions
. Furthermore, integrating single-nucleus RNA sequencing with MERFISH revealed an early upregulation of synaptogenesis in V1-specific layer 4 neurons. Collectively, our findings underscore the crucial role of spatial relationships in determining the molecular specification of cortical layers and areas. This study establishes a spatially resolved single-cell analysis paradigm and paves the way for the construction of a comprehensive developmental atlas of the human brain. The human cerebral cortex is composed of six layers and dozens of areas that are molecularly and structurally distinct 1 , 2 , 3 – 4 . Although single-cell transcriptomic studies have advanced the molecular characterization of human cortical development, a substantial gap exists owing to the loss of spatial context during cell dissociation 5 , 6 , 7 – 8 . Here we used multiplexed error-robust fluorescence in situ hybridization (MERFISH) 9 , augmented with deep-learning-based nucleus segmentation, to examine the molecular, cellular and cytoarchitectural development of the human fetal cortex with spatially resolved single-cell resolution. Our extensive spatial atlas, encompassing more than 18 million single cells, spans eight cortical areas across seven developmental time points. We uncovered the early establishment of the six-layer structure, identifiable by the laminar distribution of excitatory neuron subtypes, 3 months before the emergence of cytoarchitectural layers. Notably, we discovered two distinct modes of cortical areal specification during mid-gestation: (1) a continuous, gradual transition observed across most cortical areas along the anterior–posterior axis and (2) a discrete, abrupt boundary specifically identified between the primary (V1) and secondary (V2) visual cortices as early as gestational week 20. This sharp binary transition in V1–V2 neuronal subtypes challenges the notion that mid-gestation cortical arealization involves only gradient-like transitions 6 , 10 . Furthermore, integrating single-nucleus RNA sequencing with MERFISH revealed an early upregulation of synaptogenesis in V1-specific layer 4 neurons. Collectively, our findings underscore the crucial role of spatial relationships in determining the molecular specification of cortical layers and areas. This study establishes a spatially resolved single-cell analysis paradigm and paves the way for the construction of a comprehensive developmental atlas of the human brain. Multiplexed error-robust fluorescence in situ hybridization (MERFISH) together with deep-learning-based nucleus segmentation enabled the construction of a highly detailed and informative spatially resolved single-cell atlas of human fetal cortical development. The human cerebral cortex is composed of six layers and dozens of areas that are molecularly and structurally distinct 1 – 4 . Although single-cell transcriptomic studies have advanced the molecular characterization of human cortical development, a substantial gap exists owing to the loss of spatial context during cell dissociation 5 – 8 . Here we used multiplexed error-robust fluorescence in situ hybridization (MERFISH) 9 , augmented with deep-learning-based nucleus segmentation, to examine the molecular, cellular and cytoarchitectural development of the human fetal cortex with spatially resolved single-cell resolution. Our extensive spatial atlas, encompassing more than 18 million single cells, spans eight cortical areas across seven developmental time points. We uncovered the early establishment of the six-layer structure, identifiable by the laminar distribution of excitatory neuron subtypes, 3 months before the emergence of cytoarchitectural layers. Notably, we discovered two distinct modes of cortical areal specification during mid-gestation: (1) a continuous, gradual transition observed across most cortical areas along the anterior–posterior axis and (2) a discrete, abrupt boundary specifically identified between the primary (V1) and secondary (V2) visual cortices as early as gestational week 20. This sharp binary transition in V1–V2 neuronal subtypes challenges the notion that mid-gestation cortical arealization involves only gradient-like transitions 6 , 10 . Furthermore, integrating single-nucleus RNA sequencing with MERFISH revealed an early upregulation of synaptogenesis in V1-specific layer 4 neurons. Collectively, our findings underscore the crucial role of spatial relationships in determining the molecular specification of cortical layers and areas. This study establishes a spatially resolved single-cell analysis paradigm and paves the way for the construction of a comprehensive developmental atlas of the human brain. Multiplexed error-robust fluorescence in situ hybridization (MERFISH) together with deep-learning-based nucleus segmentation enabled the construction of a highly detailed and informative spatially resolved single-cell atlas of human fetal cortical development. The human cerebral cortex is composed of six layers and dozens of areas that are molecularly and structurally distinct1-4. Although single-cell transcriptomic studies have advanced the molecular characterization of human cortical development, a substantial gap exists owing to the loss of spatial context during cell dissociation5-8. Here we used multiplexed error-robust fluorescence in situ hybridization (MERFISH)9, augmented with deep-learning-based nucleus segmentation, to examine the molecular, cellular and cytoarchitectural development of the human fetal cortex with spatially resolved single-cell resolution. Our extensive spatial atlas, encompassing more than 18 million single cells, spans eight cortical areas across seven developmental time points. We uncovered the early establishment of the six-layer structure, identifiable by the laminar distribution of excitatory neuron subtypes, 3 months before the emergence of cytoarchitectural layers. Notably, we discovered two distinct modes of cortical areal specification during mid-gestation: (1) a continuous, gradual transition observed across most cortical areas along the anterior-posterior axis and (2) a discrete, abrupt boundary specifically identified between the primary (V1) and secondary (V2) visual cortices as early as gestational week 20. This sharp binary transition in V1-V2 neuronal subtypes challenges the notion that mid-gestation cortical arealization involves only gradient-like transitions6,10. Furthermore, integrating single-nucleus RNA sequencing with MERFISH revealed an early upregulation of synaptogenesis in V1-specific layer 4 neurons. Collectively, our findings underscore the crucial role of spatial relationships in determining the molecular specification of cortical layers and areas. This study establishes a spatially resolved single-cell analysis paradigm and paves the way for the construction of a comprehensive developmental atlas of the human brain.The human cerebral cortex is composed of six layers and dozens of areas that are molecularly and structurally distinct1-4. Although single-cell transcriptomic studies have advanced the molecular characterization of human cortical development, a substantial gap exists owing to the loss of spatial context during cell dissociation5-8. Here we used multiplexed error-robust fluorescence in situ hybridization (MERFISH)9, augmented with deep-learning-based nucleus segmentation, to examine the molecular, cellular and cytoarchitectural development of the human fetal cortex with spatially resolved single-cell resolution. Our extensive spatial atlas, encompassing more than 18 million single cells, spans eight cortical areas across seven developmental time points. We uncovered the early establishment of the six-layer structure, identifiable by the laminar distribution of excitatory neuron subtypes, 3 months before the emergence of cytoarchitectural layers. Notably, we discovered two distinct modes of cortical areal specification during mid-gestation: (1) a continuous, gradual transition observed across most cortical areas along the anterior-posterior axis and (2) a discrete, abrupt boundary specifically identified between the primary (V1) and secondary (V2) visual cortices as early as gestational week 20. This sharp binary transition in V1-V2 neuronal subtypes challenges the notion that mid-gestation cortical arealization involves only gradient-like transitions6,10. Furthermore, integrating single-nucleus RNA sequencing with MERFISH revealed an early upregulation of synaptogenesis in V1-specific layer 4 neurons. Collectively, our findings underscore the crucial role of spatial relationships in determining the molecular specification of cortical layers and areas. This study establishes a spatially resolved single-cell analysis paradigm and paves the way for the construction of a comprehensive developmental atlas of the human brain. The human cerebral cortex is composed of six layers and dozens of areas that are molecularly and structurally distinct 1–4 . Although single-cell transcriptomic studies have advanced the molecular characterization of human cortical development, a substantial gap exists owing to the loss of spatial context during cell dissociation 5–8 . Here we used multiplexed error-robust fluorescence in situ hybridization (MERFISH) 9 , augmented with deep-learning-based nucleus segmentation, to examine the molecular, cellular and cytoarchitectural development of the human fetal cortex with spatially resolved single-cell resolution. Our extensive spatial atlas, encompassing more than 18 million single cells, spans eight cortical areas across seven developmental time points. We uncovered the early establishment of the six-layer structure, identifiable by the laminar distribution of excitatory neuron subtypes, 3 months before the emergence of cytoarchitectural layers. Notably, we discovered two distinct modes of cortical areal specification during mid-gestation: (1) a continuous, gradual transition observed across most cortical areas along the anterior–posterior axis and (2) a discrete, abrupt boundary specifically identified between the primary (V1) and secondary (V2) visual cortices as early as gestational week 20. This sharp binary transition in V1–V2 neuronal subtypes challenges the notion that mid-gestation cortical arealization involves only gradient-like transitions 6,10 . Furthermore, integrating single-nucleus RNA sequencing with MERFISH revealed an early upregulation of synaptogenesis in V1-specific layer 4 neurons. Collectively, our findings underscore the crucial role of spatial relationships in determining the molecular specification of cortical layers and areas. This study establishes a spatially resolved single-cell analysis paradigm and paves the way for the construction of a comprehensive developmental atlas of the human brain. The human cerebral cortex is composed of six layers and dozens of areas that are molecularly and structurally distinct1, 2, 3–4. Although single-cell transcriptomic studies have advanced the molecular characterization of human cortical development, a substantial gap exists owing to the loss of spatial context during cell dissociation5, 6, 7–8. Here we used multiplexed error-robust fluorescence in situ hybridization (MERFISH)9, augmented with deep-learning-based nucleus segmentation, to examine the molecular, cellular and cytoarchitectural development of the human fetal cortex with spatially resolved single-cell resolution. Our extensive spatial atlas, encompassing more than 18 million single cells, spans eight cortical areas across seven developmental time points. We uncovered the early establishment of the six-layer structure, identifiable by the laminar distribution of excitatory neuron subtypes, 3 months before the emergence of cytoarchitectural layers. Notably, we discovered two distinct modes of cortical areal specification during mid-gestation: (1) a continuous, gradual transition observed across most cortical areas along the anterior–posterior axis and (2) a discrete, abrupt boundary specifically identified between the primary (V1) and secondary (V2) visual cortices as early as gestational week 20. This sharp binary transition in V1–V2 neuronal subtypes challenges the notion that mid-gestation cortical arealization involves only gradient-like transitions6,10. Furthermore, integrating single-nucleus RNA sequencing with MERFISH revealed an early upregulation of synaptogenesis in V1-specific layer 4 neurons. Collectively, our findings underscore the crucial role of spatial relationships in determining the molecular specification of cortical layers and areas. This study establishes a spatially resolved single-cell analysis paradigm and paves the way for the construction of a comprehensive developmental atlas of the human brain.Multiplexed error-robust fluorescence in situ hybridization (MERFISH) together with deep-learning-based nucleus segmentation enabled the construction of a highly detailed and informative spatially resolved single-cell atlas of human fetal cortical development. |
| Author | Walsh, Christopher A. Otani, Aoi Kriz, Andrea J. Johnson, Robert Sestan, Nenad Manam, Monica Devi Hecht, Jonathan L. Marciano, Jack H. Cai, Chunhui Andersen, Rebecca E. Coleman, Kyle Sun, Liang Stringer, Carsen Qian, Xuyu Neil, Jennifer E. Micali, Nicola Lai, Abbe Shao, Diane D. Miller, Michael B. Ghosh, Urmi Exposito-Alonso, David LeFevre, Alexandra Rakic, Pasko Jiang, Shunzhou Luo, Chunyu Li, Mingyao Caglayan, Emre |
| Author_xml | – sequence: 1 givenname: Xuyu orcidid: 0000-0001-5944-3816 surname: Qian fullname: Qian, Xuyu email: qianxuyu@gmail.com organization: Division of Genetics and Genomics, Department of Pediatrics, Boston Children’s Hospital, Harvard Medical School, Howard Hughes Medical Institute, Boston Children’s Hospital, Harvard Medical School – sequence: 2 givenname: Kyle surname: Coleman fullname: Coleman, Kyle organization: Statistical Center for Single-Cell and Spatial Genomics, Department of Biostatistics, Epidemiology and Informatics, Perelman School of Medicine, University of Pennsylvania – sequence: 3 givenname: Shunzhou orcidid: 0009-0000-7309-2389 surname: Jiang fullname: Jiang, Shunzhou organization: Statistical Center for Single-Cell and Spatial Genomics, Department of Biostatistics, Epidemiology and Informatics, Perelman School of Medicine, University of Pennsylvania – sequence: 4 givenname: Andrea J. surname: Kriz fullname: Kriz, Andrea J. organization: Division of Genetics and Genomics, Department of Pediatrics, Boston Children’s Hospital, Harvard Medical School, Howard Hughes Medical Institute, Boston Children’s Hospital, Harvard Medical School – sequence: 5 givenname: Jack H. orcidid: 0000-0002-0238-9916 surname: Marciano fullname: Marciano, Jack H. organization: Division of Genetics and Genomics, Department of Pediatrics, Boston Children’s Hospital, Harvard Medical School, Howard Hughes Medical Institute, Boston Children’s Hospital, Harvard Medical School – sequence: 6 givenname: Chunyu orcidid: 0009-0004-7047-0857 surname: Luo fullname: Luo, Chunyu organization: Statistical Center for Single-Cell and Spatial Genomics, Department of Biostatistics, Epidemiology and Informatics, Perelman School of Medicine, University of Pennsylvania – sequence: 7 givenname: Chunhui surname: Cai fullname: Cai, Chunhui organization: Research Computing, Department of Information Technology, Boston Children’s Hospital – sequence: 8 givenname: Monica Devi surname: Manam fullname: Manam, Monica Devi organization: Division of Genetics and Genomics, Department of Pediatrics, Boston Children’s Hospital, Harvard Medical School, Howard Hughes Medical Institute, Boston Children’s Hospital, Harvard Medical School – sequence: 9 givenname: Emre orcidid: 0000-0001-5340-8614 surname: Caglayan fullname: Caglayan, Emre organization: Division of Genetics and Genomics, Department of Pediatrics, Boston Children’s Hospital, Harvard Medical School, Howard Hughes Medical Institute, Boston Children’s Hospital, Harvard Medical School – sequence: 10 givenname: Abbe surname: Lai fullname: Lai, Abbe organization: Division of Genetics and Genomics, Department of Pediatrics, Boston Children’s Hospital, Harvard Medical School, Howard Hughes Medical Institute, Boston Children’s Hospital, Harvard Medical School – sequence: 11 givenname: David orcidid: 0000-0002-4950-2744 surname: Exposito-Alonso fullname: Exposito-Alonso, David organization: Division of Genetics and Genomics, Department of Pediatrics, Boston Children’s Hospital, Harvard Medical School, Howard Hughes Medical Institute, Boston Children’s Hospital, Harvard Medical School – sequence: 12 givenname: Aoi surname: Otani fullname: Otani, Aoi organization: Division of Genetics and Genomics, Department of Pediatrics, Boston Children’s Hospital, Harvard Medical School, Howard Hughes Medical Institute, Boston Children’s Hospital, Harvard Medical School – sequence: 13 givenname: Urmi surname: Ghosh fullname: Ghosh, Urmi organization: Division of Genetics and Genomics, Department of Pediatrics, Boston Children’s Hospital, Harvard Medical School, Howard Hughes Medical Institute, Boston Children’s Hospital, Harvard Medical School – sequence: 14 givenname: Diane D. orcidid: 0000-0003-2087-4082 surname: Shao fullname: Shao, Diane D. organization: Division of Genetics and Genomics, Department of Pediatrics, Boston Children’s Hospital, Harvard Medical School, Howard Hughes Medical Institute, Boston Children’s Hospital, Harvard Medical School, Department of Neurology, Boston Children’s Hospital, Broad Institute of MIT and Harvard – sequence: 15 givenname: Rebecca E. orcidid: 0000-0002-0702-3120 surname: Andersen fullname: Andersen, Rebecca E. organization: Division of Genetics and Genomics, Department of Pediatrics, Boston Children’s Hospital, Harvard Medical School, Howard Hughes Medical Institute, Boston Children’s Hospital, Harvard Medical School, Broad Institute of MIT and Harvard – sequence: 16 givenname: Jennifer E. surname: Neil fullname: Neil, Jennifer E. organization: Division of Genetics and Genomics, Department of Pediatrics, Boston Children’s Hospital, Harvard Medical School, Howard Hughes Medical Institute, Boston Children’s Hospital, Harvard Medical School – sequence: 17 givenname: Robert surname: Johnson fullname: Johnson, Robert organization: University of Maryland Brain and Tissue Bank, Department of Pediatrics, University of Maryland School of Medicine – 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Department of Biostatistics, Epidemiology and Informatics, Perelman School of Medicine, University of Pennsylvania, Department of Pathology and Laboratory Medicine, Perelman School of Medicine, University of Pennsylvania – sequence: 27 givenname: Christopher A. orcidid: 0000-0002-0156-2238 surname: Walsh fullname: Walsh, Christopher A. email: christopher.walsh@childrens.harvard.edu organization: Division of Genetics and Genomics, Department of Pediatrics, Boston Children’s Hospital, Harvard Medical School, Howard Hughes Medical Institute, Boston Children’s Hospital, Harvard Medical School, Department of Neurology, Boston Children’s Hospital, Broad Institute of MIT and Harvard, Departments of Pediatrics and Neurology, Harvard Medical School |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/40369074$$D View this record in MEDLINE/PubMed |
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| DOI | 10.1038/s41586-025-09010-1 |
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| Snippet | The human cerebral cortex is composed of six layers and dozens of areas that are molecularly and structurally distinct
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. Although single-cell... The human cerebral cortex is composed of six layers and dozens of areas that are molecularly and structurally distinct 1–4 . Although single-cell... The human cerebral cortex is composed of six layers and dozens of areas that are molecularly and structurally distinct . Although single-cell transcriptomic... The human cerebral cortex is composed of six layers and dozens of areas that are molecularly and structurally distinct1, 2, 3–4. Although single-cell... The human cerebral cortex is composed of six layers and dozens of areas that are molecularly and structurally distinct1-4. Although single-cell transcriptomic... The human cerebral cortex is composed of six layers and dozens of areas that are molecularly and structurally distinct 1 – 4 . Although single-cell... |
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| SubjectTerms | 13 14 38 38/32 38/39 45 631/136/368/2430 631/378/2571/1696 631/378/368/2430 82 82/51 Brain architecture Cells Cerebral cortex Cerebral Cortex - cytology Cerebral Cortex - embryology Cerebral Cortex - metabolism Deep Learning Female Fetus - cytology Fetus - embryology Fetuses Fluorescence Fluorescence in situ hybridization Gene Expression Profiling Gene sequencing Genes Gestation Humanities and Social Sciences Humans Hybridization Hypotheses In Situ Hybridization, Fluorescence Integrated approach Localization Male multidisciplinary Multiplexing Neurons Neurons - cytology Neurons - metabolism Nuclei (cytology) Robustness Science Science (multidisciplinary) Segmentation Single-Cell Analysis Specifications Synaptogenesis Transcriptome - genetics Transcriptomics Visual cortex Visual Cortex - cytology Visual Cortex - embryology |
| Title | Spatial transcriptomics reveals human cortical layer and area specification |
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