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Comparative transcriptomics reveals emergent cortical architecture and plasticity at the metatherian-eutherian split [snRNA-Seq]

ABSTRACT: The neocortex supports mammalian cognition through a conserved columnar architecture, but variation in the transcriptomic organization of cortical columns across deep mammalian divergences has not been directly examined. We used single-nucleus RNA sequencing and spatial transcriptomics to compare primary visual cortex in marsupial (opossum) and placental (mouse) mammals. Major neuronal subclasses and laminar architecture were broadly conserved, but intratelencephalic (IT) neurons differed markedly. Opossum IT neurons exhibited more generalized, overlapping transcriptomic identities with a continuous spatio-transcriptomic gradient between superficial (L2/3) and deep (L5) IT populations, whereas mouse IT neurons showed sharper transcriptomic distinctions and greater spatial confinement, consistent with increased specialization. Mouse cortex also displayed reduced PV interneuron density and redistribution of perineuronal nets, suggesting altered constraints on cortical plasticity. These findings demonstrate that substantial variation in intracortical circuit organization exists across deeply diverged mammalian lineages, identifying IT neurons as a principal axis of evolutionary divergence in the neocortical column.

ORGANISM(S): Monodelphis domestica

PROVIDER: GSE299387 | GEO | 2026/03/31

REPOSITORIES: GEO

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Similar Datasets

Comparative transcriptomics reveals emergent cortical architecture and plasticity at the metatherian-eutherian split [Stereo-seq]

Project description:The neocortex supports mammalian cognition through a conserved columnar architecture, but variation in the transcriptomic organization of cortical columns across deep mammalian divergences has not been directly examined. We used single-nucleus RNA sequencing and spatial transcriptomics to compare primary visual cortex in marsupial (opossum) and placental (mouse) mammals. Major neuronal subclasses and laminar architecture were broadly conserved, but intratelencephalic (IT) neurons differed markedly. Opossum IT neurons exhibited more generalized, overlapping transcriptomic identities with a continuous spatio-transcriptomic gradient between superficial (L2/3) and deep (L5) IT populations, whereas mouse IT neurons showed sharper transcriptomic distinctions and greater spatial confinement, consistent with increased specialization. Mouse cortex also displayed reduced PV interneuron density and redistribution of perineuronal nets, suggesting altered constraints on cortical plasticity. These findings demonstrate that substantial variation in intracortical circuit organization exists across deeply diverged mammalian lineages, identifying IT neurons as a principal axis of evolutionary divergence in the neocortical column.

2026-03-31 | GSE299386 | GEO

Cortical layer 5 neuron-specific synaptic protein profiling suggests differential vulnerability to neurodevelopmental disorders

Project description:Pyramidal neurons in the cortex are embedded in distinct information processing pathways. Cortical layer 5 (L5) intratelencephalic (IT) and pyramidal tract (PT) neurons receive different input and project to distinct brain regions. The synaptic molecular signatures that define synaptic connectivity and function of L5 IT and PT neurons are largely unknown. Here, we use an optimized proximity biotinylation workflow to characterize the excitatory postsynaptic proteomes of L5 IT and PT neurons in intact somatosensory circuits. We find that differential expression of neurotransmitter receptors, ion channels and cell-surface proteins (CSPs), most prominently of the leucine-rich repeat (LRR) family, specifies L5 IT and PT neuron input connectivity and function. Our analysis further uncovers differential vulnerability to neurodevelopmental disorders for L5 IT and PT neurons, with a marked enrichment of autism risk genes in the postsynaptic excitatory proteome of IT, but not of PT, neurons. Together, cell type- and input type-specific synaptic proteome profiling implies that many of the proteins specifying connectivity and function of two closely related cortical pyramidal cell types also underlie their differential vulnerability to neurodevelopmental disorders.

2024-11-04 | PXD046812 | Pride

Single-cell genomics of the mouse olfactory cortex reveals contrasts with neocortex and ancestral signatures of cell type evolution

Project description:Understanding the molecular logic of cortical cell-type diversity can illuminate cortical circuit function and evolution. Here, we performed single-nucleus transcriptome and chromatin accessibility analyses to compare neurons across three- to six-layered cortical areas of adult mice and across tetrapod species. We found that, in contrast to the six-layered neocortex, glutamatergic neurons of the three-layered mouse olfactory (piriform) cortex displayed continuous rather than discrete variation in transcriptomic profiles. Subsets of piriform and neocortical glutamatergic cells with conserved transcriptomic profiles were distinguished by distinct, area-specific epigenetic states. Furthermore, we identified a prominent population of immature neurons in piriform cortex and observed that, in contrast to the neocortex, piriform cortex exhibited divergence between glutamatergic cells in lab versus wild-derived mice. Finally, we showed that piriform neurons displayed greater transcriptomic similarity to cortical neurons of turtles, lizards, and salamanders than to those of the neocortex. In summary, despite over 200 million years of co-evolution alongside the neocortex, olfactory cortex neurons retain molecular signatures of ancestral cortical identity.

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Neocortical layer 4 in adult mouse differs in major cell types and circuit organization between primary sensory areas

Project description:Layer 4 (L4) of mammalian neocortex plays a crucial role in cortical information processing, yet a complete census of its cell types and connectivity remains elusive. Using whole-cell recordings with morphological recovery, we identified one major excitatory and seven inhibitory types of neurons in L4 of adult mouse visual cortex (V1). Nearly all excitatory neurons were pyramidal and all somatostatin-positive (SOM+) non-fast-spiking interneurons were Martinotti cells. In contrast, in somatosensory cortex (S1), excitatory neurons were mostly stellate and SOM+ interneurons were non-Martinotti. These morphologically distinct SOM+ interneurons corresponded to different transcriptomic cell types and were differentially integrated into the local circuit with only S1 neurons receiving local excitatory input. We propose that cell type specific circuit motifs, such as the Martinotti/pyramidal and non-Martinotti/stellate pairs, are used across the cortex as building blocks to assemble cortical circuits.

2019-08-06 | GSE134378 | GEO

Pyramidal neurons proportionately alter the identity and survival of specific cortical interneuron subtypes

Project description:The mammalian cerebral cortex comprises a complex neuronal network that maintains a delicate balance between excitatory neurons and inhibitory interneurons. Previous studies, including our own research, have shown that specific interneuron subtypes are closely associated with particular pyramidal neuron types, forming stereotyped local inhibitory microcircuits. However, the developmental processes that establish these precise networks are not well understood. Here we show that pyramidal neuron types are instrumental in maintaining the terminal differentiation and survival of specific associated interneuron subtypes. In a wild-type cortex, the relative abundance of different interneuron subtypes aligns precisely with the pyramidal neuron types with which they synaptically target. In Fezf2 mutant cortex, characterized by the absence of layer 5 pyramidal tract neurons and an expansion of layer 6 intratelencephalic neurons, we observed a corresponding decrease in associated layer 5b interneurons and an increase in layer 6 subtypes. Interestingly, these shifts in composition are achieved through mechanisms that are specific to different interneuron types. While SST interneurons adjust their abundance to the change in pyramidal neuron prevalence through the regulation of programmed cell death, parvalbumin cells alter their identity. These findings illustrate two key strategies by which the dynamic interplay between pyramidal neurons and interneurons allows local microcircuits to be sculpted precisely. These insights underscored the precise roles of extrinsic signals from pyramidal cells in the establishment of interneuron diversity and their subsequent integration into local cortical microcircuits.

2024-08-15 | GSE272706 | GEO

Multiple parallel cell lineages in the developing mammalian cerebral cortex

Project description:Cortical neurogenesis follows a simple lineage: apical Radial Glia Cells (RGC) generate basal progenitors, and these produce neurons. How this occurs in species with expanded germinal zones and a folded cortex, like human, remains unclear. We used single-cell RNA sequencing from individual cortical germinal zones in ferret, and barcoded lineage tracking, to determine the molecular diversity of progenitor cells and their lineages. We identified multiple RGC classes that initiate parallel lineages, converging onto a common class of newborn neuron. Parallel RGC classes and transcriptomic trajectories were repeated across germinal zones and conserved in ferret and human, but not mouse. Neurons followed parallel differentiation trajectories in gyrus and sulcus, with different expression of human cortical malformation genes. Progenitor cell lineage multiplicity is conserved in the folded mammalian cerebral cortex. This SuperSeries is composed of the SubSeries listed below.

2024-03-27 | GSE234305 | GEO

Quantitative synaptic proteomics analysis reveal OTX1 regulates complement-dependent microglia-mediated synaptic pruning in the cerebral cortex of Otx1 mutant mouse

Project description:The mammalian cortex is the structural basis for learning, cognition, and movement coordination. Dysgenesis of axon dendrites and synapses in cortical neurons can hinder learning and cognitive development, leading to epilepsy. Transcription factor Otx1 plays an important role in the development of the morphology and electrophysiological activity of cortical neurons and is associated with the occurrence of epilepsy. Abnormal synaptic pruning has been proposed to be one of the molecular mechanisms underlying epilepsy. Otx1 mutant mice leads to defective axonal pruning and changes the excitability and synaptic connections of the cortical neurons. However, little is known about the molecular pathways through which the loss of Otx1 causes epilepsy. On this basis, we found that the density and morphology of dendritic spines and microglia in Otx1 mutant mice changed significantly. TMT analysis of synaptic proteins reveals that Otx1 regulates the structure and function of cortical neurons and synaptic characteristics by regulating microglia-mediated synaptic pruning through the complement system, which also has important theoretical significance and application value for effective prevention and treatment of epilepsy.

2023-04-15 | PXD041568 |

scRNA-seq of ferret cortical germinal zones from splenial gyrus and lateral sulcus (Borrell lab)

Project description:Diversity of cortical radial glia cells (RGCs) and their complex relationships to generate neurons in species with expanded germinal zones and a folded cortex, remains unclear. We used single-cell RNA sequencing (scRNA-seq) of microdissected cortical germinal layers (ventricular zone (VZ) and outer subventricular zone (OSVZ)), from two cortical regions (splenial gyrus (SG) and neighboring lateral sulcus (LS)) at two critical time points for ferret cortex development (embryonic day (E) 34 and postnatal day (P) 1) to distinguish the molecular diversity of progenitors and newborn neurons, and study their transcriptomic trajectories.

2024-03-27 | GSE219254 | GEO

A dynamic unfolded protein response contributes to the control of cortical neurogenesis

Project description:The cerebral cortex contains layers of neurons sequentially generated by distinct lineage-related progenitors. At the onset of corticogenesis, the first-born progenitors are apical progenitors (APs) whose asymmetric division give birth directly to neurons. Later, they switch to indirect neurogenesis by generating intermediate progenitors (IPs), which give rise to projection neurons of all cortical layers. While a direct lineage relationship between APs and IPs has been established, the molecular mechanism that controls their transition remains elusive. Our data suggest that interfering with codon translation speed triggers endoplasmic reticulum stress and the unfolded protein response (UPR), further impairing the generation of IPs and leading to microcephaly. Moreover, we demonstrate that a progressive downregulation of UPR in cortical progenitors acts as physiological signal to amplify IPs and promotes indirect neurogenesis. Thus, our findings reveal a hitherto unrecognized contribution of UPR to cell fate acquisition during mammalian brain development. Ribosome profiling and RNA-Seq of forebrains from E14.5 mouse embryos from wild type animals and mutants carrying a conditional knockout of ELP3 in cortical progenitors

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Project description:Increased cortical size is essential to the enhanced intellectual capacity of primates during mammalian evolution. The mechanisms that control cortical size are largely unknown. Here, we show that mammalian BAF170, a subunit of the chromatin remodeling complex mSWI/SNF, is an intrinsic factor that controls cortical size. We find that the conditional deletion of BAF170 promotes indirect neurogenesis by increasing the pool of intermediate progenitors (IPs) and results in an enlarged cortex, whereas cortex-specific BAF170 over-expression results an opposing phenotype. Mechanistically, BAF170 competes with BAF155 subunit in the BAF complex, affecting the euchromatin structure and thereby modulating the binding efficiency of Pax6/REST-corepressor complex to Pax6 target genes that regulate the generation of IPs and late cortical progenitors. Our findings reveal a molecular mechanism mediated by the mSWI/SNF chromatin-remodeling complex that controls cortical architecture. Cortical gene expression is compared between three E12.5 mouse embryos with cortex-specific loss of BAF170 function and three littermate control embryos.

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