PMCID
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PMC10914349
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High-throughput mapping of single-neuron projection and molecular features by retrograde barcoded labeling.
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Scale bars: 500 μm.
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PMC10914349
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High-throughput mapping of single-neuron projection and molecular features by retrograde barcoded labeling.
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AI-1, agranular insular cortex, anterior; AI-2, agranular insular cortex, posterior. (
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PMC10914349
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High-throughput mapping of single-neuron projection and molecular features by retrograde barcoded labeling.
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B) Frequency of hamming distance (HD) of five reference barcode sequences. (
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PMC10914349
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High-throughput mapping of single-neuron projection and molecular features by retrograde barcoded labeling.
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C) Density distribution of HD of best and second-best hit when comparing barcode sequences form reads to and five barcode references.
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PMC10914349
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High-throughput mapping of single-neuron projection and molecular features by retrograde barcoded labeling.
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The distance to the best hit (identified barcode) is 0 across four samples as we used perfect match for the identification.
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PMC10914349
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High-throughput mapping of single-neuron projection and molecular features by retrograde barcoded labeling.
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And the distance of the second best hit is ~10, showing that there are sufficient sequence difference to identify the right barcode among five references during sequencing. (
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PMC10914349
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High-throughput mapping of single-neuron projection and molecular features by retrograde barcoded labeling.
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D) Boxplot displaying the count distribution of UMIs for neurons with projections identified by different barcodes and a sum of all five barcodes across projectome and scRNA-seq libraries. (
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PMC10914349
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High-throughput mapping of single-neuron projection and molecular features by retrograde barcoded labeling.
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E) Density plots contrasting the distribution of UMIs for each target region between non-neuronal cells (green), EGFP-negative cells (blue), and FAC-sorted cells (red).
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PMC10914349
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High-throughput mapping of single-neuron projection and molecular features by retrograde barcoded labeling.
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The dashed line indicates a threshold for UMI counts of a barcoded neuron.
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PMC10914349
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High-throughput mapping of single-neuron projection and molecular features by retrograde barcoded labeling.
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Note that EGFP-negative cells are subset of FAC-sorted group and determined as nUMI of EFGP RNA = 0. (
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PMC10914349
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High-throughput mapping of single-neuron projection and molecular features by retrograde barcoded labeling.
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F) Violin plots of Log10 normalized projection index barcode counts.
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PMC10914349
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High-throughput mapping of single-neuron projection and molecular features by retrograde barcoded labeling.
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Note that after choosing the UMI counts threshold, UMI counts below threshold were dropped to zero. (
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PMC10914349
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High-throughput mapping of single-neuron projection and molecular features by retrograde barcoded labeling.
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G) Stacked bar plot showing barcoded and non-barcoded cell ratio in FAC-sorted group or unsorted group as determined by stringent UMI threshold. (
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PMC10914349
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High-throughput mapping of single-neuron projection and molecular features by retrograde barcoded labeling.
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H) Stacked bar plot showing EGFP-positive (nUMI of EFGP RNA >0) and EGFP-negative cells (nUMI of EFGP RNA = 0) ratio in FAC-sorted group or unsorted group as determined by scRNA-seq. (
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PMC10914349
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High-throughput mapping of single-neuron projection and molecular features by retrograde barcoded labeling.
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A) The position of injection sites (AI-1, AI-2, DMS, LH, MD, BLA) to deliver rAAV2-retro-EGFP plotted on coronal section diagrams (top).
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PMC10914349
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High-throughput mapping of single-neuron projection and molecular features by retrograde barcoded labeling.
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The left corner values indicate the anteroposterior distance of the section from bregma.
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PMC10914349
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High-throughput mapping of single-neuron projection and molecular features by retrograde barcoded labeling.
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Representative immunohistochemistry images showing rAAV2-retro-EGFP injection sites in coronal sections (bottom).
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PMC10914349
|
High-throughput mapping of single-neuron projection and molecular features by retrograde barcoded labeling.
|
Scale bars: 500 μm.
|
PMC10914349
|
High-throughput mapping of single-neuron projection and molecular features by retrograde barcoded labeling.
|
AI-1, agranular insular cortex, anterior; AI-2, agranular insular cortex, posterior. (
|
PMC10914349
|
High-throughput mapping of single-neuron projection and molecular features by retrograde barcoded labeling.
|
B) Frequency of hamming distance (HD) of five reference barcode sequences. (
|
PMC10914349
|
High-throughput mapping of single-neuron projection and molecular features by retrograde barcoded labeling.
|
C) Density distribution of HD of best and second-best hit when comparing barcode sequences form reads to and five barcode references.
|
PMC10914349
|
High-throughput mapping of single-neuron projection and molecular features by retrograde barcoded labeling.
|
The distance to the best hit (identified barcode) is 0 across four samples as we used perfect match for the identification.
|
PMC10914349
|
High-throughput mapping of single-neuron projection and molecular features by retrograde barcoded labeling.
|
And the distance of the second best hit is ~10, showing that there are sufficient sequence difference to identify the right barcode among five references during sequencing. (
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PMC10914349
|
High-throughput mapping of single-neuron projection and molecular features by retrograde barcoded labeling.
|
D) Boxplot displaying the count distribution of UMIs for neurons with projections identified by different barcodes and a sum of all five barcodes across projectome and scRNA-seq libraries. (
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PMC10914349
|
High-throughput mapping of single-neuron projection and molecular features by retrograde barcoded labeling.
|
E) Density plots contrasting the distribution of UMIs for each target region between non-neuronal cells (green), EGFP-negative cells (blue), and FAC-sorted cells (red).
|
PMC10914349
|
High-throughput mapping of single-neuron projection and molecular features by retrograde barcoded labeling.
|
The dashed line indicates a threshold for UMI counts of a barcoded neuron.
|
PMC10914349
|
High-throughput mapping of single-neuron projection and molecular features by retrograde barcoded labeling.
|
Note that EGFP-negative cells are subset of FAC-sorted group and determined as nUMI of EFGP RNA = 0. (
|
PMC10914349
|
High-throughput mapping of single-neuron projection and molecular features by retrograde barcoded labeling.
|
F) Violin plots of Log10 normalized projection index barcode counts.
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PMC10914349
|
High-throughput mapping of single-neuron projection and molecular features by retrograde barcoded labeling.
|
Note that after choosing the UMI counts threshold, UMI counts below threshold were dropped to zero. (
|
PMC10914349
|
High-throughput mapping of single-neuron projection and molecular features by retrograde barcoded labeling.
|
G) Stacked bar plot showing barcoded and non-barcoded cell ratio in FAC-sorted group or unsorted group as determined by stringent UMI threshold. (
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PMC10914349
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High-throughput mapping of single-neuron projection and molecular features by retrograde barcoded labeling.
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H) Stacked bar plot showing EGFP-positive (nUMI of EFGP RNA >0) and EGFP-negative cells (nUMI of EFGP RNA = 0) ratio in FAC-sorted group or unsorted group as determined by scRNA-seq.
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PMC10914349
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High-throughput mapping of single-neuron projection and molecular features by retrograde barcoded labeling.
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First, we validated that each target region was labeled and effectively covered by the rAAV2-retro-EGFP (Figure 1—figure supplement 1A).
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PMC10914349
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High-throughput mapping of single-neuron projection and molecular features by retrograde barcoded labeling.
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Next, we showed that there were sufficient sequence differences to distinguish one barcode from others and sufficient sequences difference to identify the right barcode among five references during sequencing (Figure 1—figure supplement 1B, C).
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PMC10914349
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High-throughput mapping of single-neuron projection and molecular features by retrograde barcoded labeling.
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Since each downstream brain region of vmPFC received a unique and predetermined barcoded virus, each virus barcode identified in a vmPFC neuron represents the specific corresponding downstream brain region that the neuron projects to.
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PMC10914349
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High-throughput mapping of single-neuron projection and molecular features by retrograde barcoded labeling.
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We found abundant zero counts for projection barcodes in scRNA-seq libraries, contrasting robust detection in projectome libraries generated by targeted amplification from full-length cDNA (Figure 1—figure supplement 1D).
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PMC10914349
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High-throughput mapping of single-neuron projection and molecular features by retrograde barcoded labeling.
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To determine validly barcoded cells, we first calculated the 95th nUMI percentile across all barcodes and removed outlier cells with exceptionally high nUMI (see Materials and methods).
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PMC10914349
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High-throughput mapping of single-neuron projection and molecular features by retrograde barcoded labeling.
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We used ‘EGFP-negative’ FAC-sorted cells (defined by nUMI EGFP = 0) and non-neuronal cells from scRNA-seq as negative controls to calculate 99.9th percentile UMI thresholds per barcode using empirical cumulative distribution functions (ECDF; Figure 1—figure supplement 1E).
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PMC10914349
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High-throughput mapping of single-neuron projection and molecular features by retrograde barcoded labeling.
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By taking the higher threshold for each barcode from these two negative control analyses, we classified cells exceeding these values as validly barcoded.
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PMC10914349
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High-throughput mapping of single-neuron projection and molecular features by retrograde barcoded labeling.
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It is worth mentioning that the UMI threshold differs for different targets due to different magnitude of barcode expression of each projection target (Figure 1—figure supplement 1F).
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PMC10914349
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High-throughput mapping of single-neuron projection and molecular features by retrograde barcoded labeling.
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Across all detected cell types, barcoded cells were primarily excitatory neurons rather than inhibitory neurons or non-neuronal cell types (2116 validly barcoded in 8805 excitatory neurons, and 5 validly barcoded in 2738 endothelial cells, 3 validly barcoded in 1780 oligodendrocyte progenitor cells, 7 validly barcoded in 1773 oligodendrocytes, and 17 in 1420 inhibitory neurons, Figure 1F and G).
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PMC10914349
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High-throughput mapping of single-neuron projection and molecular features by retrograde barcoded labeling.
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This is consistent with the finding that mPFC projection neurons are excitatory (Gabbott et al., 2005).
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PMC10914349
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High-throughput mapping of single-neuron projection and molecular features by retrograde barcoded labeling.
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Using this stringent threshold, 49.0% of FAC-sorted and 18.7% of unsorted cells were classified as barcoded (Figure 1—figure supplement 1G).
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PMC10914349
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High-throughput mapping of single-neuron projection and molecular features by retrograde barcoded labeling.
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In parallel, we calculated EGFP ratios (nUMI of EGFP RNA >0) as 81% for FAC-sorted and 26% on average for unsorted cells (Figure 1—figure supplement 1H).
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PMC10914349
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High-throughput mapping of single-neuron projection and molecular features by retrograde barcoded labeling.
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The lower fraction of barcoded versus EGFP cells suggests our conservative threshold increases false negatives, classifying some low UMI cells as non-barcoded.
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PMC10914349
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High-throughput mapping of single-neuron projection and molecular features by retrograde barcoded labeling.
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Therefore, we focused analyses on reliably barcoded cells, though conclusions may not capture the full heterogeneous projection repertoire.
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PMC10914349
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High-throughput mapping of single-neuron projection and molecular features by retrograde barcoded labeling.
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Together, these results demonstrate that MERGE-seq can record single neuron transcriptome and projectome simultaneously.
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PMC10914349
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High-throughput mapping of single-neuron projection and molecular features by retrograde barcoded labeling.
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Previous studies have shown that vmPFC neurons project to multiple brain regions including AI, DMS, BLA, LH, and MD; however, the cell type composition of these projection neurons remains largely unknown (Le Merre et al., 2021).
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PMC10914349
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High-throughput mapping of single-neuron projection and molecular features by retrograde barcoded labeling.
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Combining with single neuron transcriptome, we explored the transcriptome and subtype composition of vmPFC neurons projecting to different downstream brain regions.
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PMC10914349
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High-throughput mapping of single-neuron projection and molecular features by retrograde barcoded labeling.
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We first re-clustered excitatory projection neurons expressing Slc17a7 (also known as vesicular glutamate transporter, Vglut1).
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PMC10914349
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High-throughput mapping of single-neuron projection and molecular features by retrograde barcoded labeling.
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Clusters with low gene/UMI counts and high mitochondrial gene expression were filtered out as low-quality (Ilicic et al., 2016).
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PMC10914349
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High-throughput mapping of single-neuron projection and molecular features by retrograde barcoded labeling.
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Some clusters exhibited non-neuronal cell markers like microglial genes (C1qa, C1qb), oligodendrocyte genes (Olig1, Olig2), and endothelial cell genes (Flt1, Cldn5) despite small cluster size, indicating contamination from other cell types incorrectly grouped within excitatory neurons after initial clustering.
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PMC10914349
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High-throughput mapping of single-neuron projection and molecular features by retrograde barcoded labeling.
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In total, we filtered out 637 cells that were identified as either low-quality or contaminated with non-neuronal cell types and recovered 9368 excitatory neurons (see Materials and methods, Figure 2—figure supplement 1A, Supplementary file 1).
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PMC10914349
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High-throughput mapping of single-neuron projection and molecular features by retrograde barcoded labeling.
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We generated seven excitatory neuron clusters, which were annotated based on typical markers of cortical layers (Bhattacherjee et al., 2019; Sorensen et al., 2015; layer 2/3, Cux2; layer 5, Etv1; layer 6, Sulf1) and differentially expressed genes (DEGs; Supplementary file 2).
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PMC10914349
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High-throughput mapping of single-neuron projection and molecular features by retrograde barcoded labeling.
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These neuron clusters include L2/3-Calb1 (4.1%), L2/3-Rorb (5.9%), L5-Bcl6 (3.3%), L5-Htr2c (3.9%), L5-S100b (11.6%), L6-Npy (12.6%), and L6-Syt6 (58.7%; Figure 2A).
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PMC10914349
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High-throughput mapping of single-neuron projection and molecular features by retrograde barcoded labeling.
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The layer and subtype marker genes of these clusters were confirmed to be expressed in corresponding layers in the vmPFC, as revealed by in situ hybridization results of the Allen Mouse Brain Atlas (Figure 2A, Figure 2—figure supplement 1A–C).
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PMC10914349
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High-throughput mapping of single-neuron projection and molecular features by retrograde barcoded labeling.
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Of note, we captured more layer 6 neurons than superficial layer neurons (12.6% L6-Npy and 58.7% L6-Syt6, Figure 2B), which is different from a previous report (Bhattacherjee et al., 2019).
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PMC10914349
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High-throughput mapping of single-neuron projection and molecular features by retrograde barcoded labeling.
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We speculate that different dissociation protocols may cause biased neuron capture. (
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PMC10914349
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High-throughput mapping of single-neuron projection and molecular features by retrograde barcoded labeling.
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A) Umap embedding of excitatory neuron subtype annotation. (
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PMC10914349
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High-throughput mapping of single-neuron projection and molecular features by retrograde barcoded labeling.
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B) Bar plot showing frequency of barcoded (blue) and non-barcoded (grey) neurons in distinct neuron subtypes. (
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PMC10914349
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High-throughput mapping of single-neuron projection and molecular features by retrograde barcoded labeling.
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C) Stacked violin plot showing the expression of markers for each neuronal subtype. (
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PMC10914349
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High-throughput mapping of single-neuron projection and molecular features by retrograde barcoded labeling.
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D) Heatmap showing the gene-expression correlation between excitatory subtypes defined by Multiplexed Error-Robust Fluorescence in situ Hybridization (MERFISH) and scRNA-seq.
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PMC10914349
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High-throughput mapping of single-neuron projection and molecular features by retrograde barcoded labeling.
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MERFISH data were downloaded from Bhattacherjee et al., 2023. (
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PMC10914349
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High-throughput mapping of single-neuron projection and molecular features by retrograde barcoded labeling.
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E) Umap embeddings of barcoded (blue) neurons projecting to each target.
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PMC10914349
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High-throughput mapping of single-neuron projection and molecular features by retrograde barcoded labeling.
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Number indicates the number of barcoded cells for each target. (
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PMC10914349
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High-throughput mapping of single-neuron projection and molecular features by retrograde barcoded labeling.
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F) Bar plot describing the distribution of neuronal subtypes for barcoded neurons associated with each projection target.
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PMC10914349
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High-throughput mapping of single-neuron projection and molecular features by retrograde barcoded labeling.
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Neuronal subtype color codes are the same as in (A), number of barcoded cells are same as the number indicated in (E) for each target. (
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PMC10914349
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High-throughput mapping of single-neuron projection and molecular features by retrograde barcoded labeling.
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G) Bar plot describing the distribution of projection targets for barcoded neurons associated with each neuronal type.
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PMC10914349
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High-throughput mapping of single-neuron projection and molecular features by retrograde barcoded labeling.
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In (A, C, D), 9368 cells in total were represented.
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PMC10914349
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High-throughput mapping of single-neuron projection and molecular features by retrograde barcoded labeling.
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In (B, E, F), 8210 cells in total were represented.
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PMC10914349
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High-throughput mapping of single-neuron projection and molecular features by retrograde barcoded labeling.
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In (G), cell numbers represented are as follows: L2/3-Calb1=72 cells, L2/3-Rorb=331 cells, L5-Bcl6=145 cells, L5-S100b=766 cells, L6-Npy=526 cells, L6-Syt6=1264 cells.
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PMC10914349
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High-throughput mapping of single-neuron projection and molecular features by retrograde barcoded labeling.
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Figure 2—figure supplement 1.Layer and cluster annotation using the mouse brain atlas and published scRNA-seq transcriptomes, and projection patterns per mouse.(A) Normalized Slc17a7 (vGlut1) expression for all extracted excitatory neurons. (
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PMC10914349
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High-throughput mapping of single-neuron projection and molecular features by retrograde barcoded labeling.
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B) In situ hybridization of typical layer-specific markers within the vmPFC region from the Adult Mouse Brain Atlas.
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PMC10914349
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High-throughput mapping of single-neuron projection and molecular features by retrograde barcoded labeling.
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Cux2 is layer 2/3-specific; Etv1 is layer 5-specific; Sulf1 is layer 6-specific (left).
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PMC10914349
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High-throughput mapping of single-neuron projection and molecular features by retrograde barcoded labeling.
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Normalized expression of Cux2, Etv1, and Sulf1 at umap embedding (right). (
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PMC10914349
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High-throughput mapping of single-neuron projection and molecular features by retrograde barcoded labeling.
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C) In situ hybridization of typical neuronal subtype markers in the vmPFC from the Adult Mouse Brain Atlas.
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PMC10914349
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High-throughput mapping of single-neuron projection and molecular features by retrograde barcoded labeling.
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Calb1 and Rorb are layer 2/3-specific; Htr2c and S100b are layer 5-specific; Bcl6 is around the transition of layer 2/3 and layer 5.
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PMC10914349
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High-throughput mapping of single-neuron projection and molecular features by retrograde barcoded labeling.
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Syt6 and Npy are layer 6-specific, though Npy is distributed sporadically.
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PMC10914349
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High-throughput mapping of single-neuron projection and molecular features by retrograde barcoded labeling.
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Corresponding normalized gene expression embedded in umap is plotted in the right panel. (
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PMC10914349
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High-throughput mapping of single-neuron projection and molecular features by retrograde barcoded labeling.
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D) Heatmap showing the gene-expression correlation between excitatory subtypes defined by scRNA-seq of this study and (Lui et al., 2021), (left) or (Yao et al., 2021), (middle) or (Bhattacherjee et al., 2019), (right). (
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PMC10914349
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High-throughput mapping of single-neuron projection and molecular features by retrograde barcoded labeling.
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E) Stacked bar plots showing neuronal subtype composition of pooled unsorted mice and pooled FAC-sorted mice for each projection target.
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PMC10914349
|
High-throughput mapping of single-neuron projection and molecular features by retrograde barcoded labeling.
|
Statistical approach was not applied due to the limitations of having a single observation per cluster per group. (
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PMC10914349
|
High-throughput mapping of single-neuron projection and molecular features by retrograde barcoded labeling.
|
A) Normalized Slc17a7 (vGlut1) expression for all extracted excitatory neurons. (
|
PMC10914349
|
High-throughput mapping of single-neuron projection and molecular features by retrograde barcoded labeling.
|
B) In situ hybridization of typical layer-specific markers within the vmPFC region from the Adult Mouse Brain Atlas.
|
PMC10914349
|
High-throughput mapping of single-neuron projection and molecular features by retrograde barcoded labeling.
|
Cux2 is layer 2/3-specific; Etv1 is layer 5-specific; Sulf1 is layer 6-specific (left).
|
PMC10914349
|
High-throughput mapping of single-neuron projection and molecular features by retrograde barcoded labeling.
|
Normalized expression of Cux2, Etv1, and Sulf1 at umap embedding (right). (
|
PMC10914349
|
High-throughput mapping of single-neuron projection and molecular features by retrograde barcoded labeling.
|
C) In situ hybridization of typical neuronal subtype markers in the vmPFC from the Adult Mouse Brain Atlas.
|
PMC10914349
|
High-throughput mapping of single-neuron projection and molecular features by retrograde barcoded labeling.
|
Calb1 and Rorb are layer 2/3-specific; Htr2c and S100b are layer 5-specific; Bcl6 is around the transition of layer 2/3 and layer 5.
|
PMC10914349
|
High-throughput mapping of single-neuron projection and molecular features by retrograde barcoded labeling.
|
Syt6 and Npy are layer 6-specific, though Npy is distributed sporadically.
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PMC10914349
|
High-throughput mapping of single-neuron projection and molecular features by retrograde barcoded labeling.
|
Corresponding normalized gene expression embedded in umap is plotted in the right panel. (
|
PMC10914349
|
High-throughput mapping of single-neuron projection and molecular features by retrograde barcoded labeling.
|
D) Heatmap showing the gene-expression correlation between excitatory subtypes defined by scRNA-seq of this study and (Lui et al., 2021), (left) or (Yao et al., 2021), (middle) or (Bhattacherjee et al., 2019), (right). (
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PMC10914349
|
High-throughput mapping of single-neuron projection and molecular features by retrograde barcoded labeling.
|
E) Stacked bar plots showing neuronal subtype composition of pooled unsorted mice and pooled FAC-sorted mice for each projection target.
|
PMC10914349
|
High-throughput mapping of single-neuron projection and molecular features by retrograde barcoded labeling.
|
Statistical approach was not applied due to the limitations of having a single observation per cluster per group.
|
PMC10914349
|
High-throughput mapping of single-neuron projection and molecular features by retrograde barcoded labeling.
|
Cells that were retrogradely barcoded spanned all layers of the vmPFC (layer 2/3, 5, and 6) and included all seven neuronal subtypes (Figure 2A–C).
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PMC10914349
|
High-throughput mapping of single-neuron projection and molecular features by retrograde barcoded labeling.
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These subtypes were highly corresponding to the spatially resolved PFC excitatory neuronal subtypes (Bhattacherjee et al., 2023; see Materials and methods, Figure 2D).
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PMC10914349
|
High-throughput mapping of single-neuron projection and molecular features by retrograde barcoded labeling.
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High correlation allows us to infer the spatial localization of our annotated subtypes detected in scRNA-seq data.
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PMC10914349
|
High-throughput mapping of single-neuron projection and molecular features by retrograde barcoded labeling.
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We also found that excitatory neuronal subtypes are transcriptionally similar to those previously reported (Figure 2—figure supplement 1D; Bhattacherjee et al., 2019; Lui et al., 2021; Yao et al., 2021).
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PMC10914349
|
High-throughput mapping of single-neuron projection and molecular features by retrograde barcoded labeling.
|
All these integrated analyses suggest that multiple viral infections will not significantly affect the transcriptional state of these retrogradely labeled vmPFC neurons.
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PMC10914349
|
High-throughput mapping of single-neuron projection and molecular features by retrograde barcoded labeling.
|
For the L5-Htr2c subtype, only nine neurons were recovered with valid barcodes, possibly due to cell loss during single-cell dissociation or tropism of AAV2-retro, or these neurons may intrinsically not project to any target we chose (Figure 2B).
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PMC10914349
|
High-throughput mapping of single-neuron projection and molecular features by retrograde barcoded labeling.
|
Neurons projecting to DMS were abundant (n=1242), whereas neurons projecting to BLA were rare (n=163; Figure 2E).
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PMC10914349
|
High-throughput mapping of single-neuron projection and molecular features by retrograde barcoded labeling.
|
These results are consistent with data acquired via conventional fluorescence-based retrograde tracing in the prefrontal cortex of rats (Gabbott et al., 2005).
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