Vision-dependent specification of cell types and function in the developing cortex

Cheng, Skye Hongiun; Butrus, Salwan; Tan, Liming; Xu, Runzhe; Sagireddy, Srikant; Trachtenberg, Joshua T.; Shekhar, Karthik; Zipursky, S Lawrence

doi:10.1016/j.cell.2021.12.022

Cited by 63 publications

(74 citation statements)

References 74 publications

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“…described in vertebrate retinas. As with vertebrates, we anticipate that more extensive studies will subdivide these 26 cell types into subtypes based on function, connectivity and expression of marker genes (Cheng et al, 2021; Shekhar et al, 2016, 2021; Tran et al, 2019). In vertebrates, the ability to drive reporter gene expression and enrich for specific cell classes by cell sorting has been essential for detailed analysis; these tools are not yet available in cephalopods.…”

Section: Discussionmentioning

confidence: 99%

A single-cell atlas of bobtail squid visual and nervous system highlights molecular principles of convergent evolution

Gavriouchkina

Tan

Ziadi-Künzli

et al. 2022

Preprint

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Although the camera-type eyes of cephalopods and vertebrates are a canonical example of convergent morphological evolution, the cellular and molecular mechanisms underlying this convergence remain obscure. We used genomics and single cell transcriptomics to study these mechanisms in the visual system of the bobtail squid Euprymna berryi, an emerging cephalopod model. Analysis of 98,537 cellular transcriptomes from the squid visual and nervous system identified dozens of cell types that cannot be placed in simple correspondence with those of vertebrate or fly visual systems, as proposed by Ramón y Cajal and J.Z. Young. Instead, we find an unexpected diversity of neural types, dominated by dopamine, and previously uncharacterized glial cells. Surprisingly, we observe changes in cell populations and neurotransmitter usage during maturation and growth of the visual systems from hatchling to adult. Together these genomic and cellular findings shed new light on the parallel evolution of visual system complexity in cephalopods and vertebrates.

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Section: Discussionmentioning

confidence: 99%

A single-cell atlas of bobtail squid visual and nervous system highlights molecular principles of convergent evolution

Gavriouchkina

Tan

Ziadi-Künzli

et al. 2022

Preprint

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“…Unfortunately, although there are methods for disrupting the coherence of spontaneous activity among RGCs (Kirkby et al, 2013), it is currently not feasible to inhibit all action potentials in RGCs over a prolonged period. However, visual input has been shown to have clear effects on dendritic morphology of RGCs and refinement and maintenance of RGC axonal arbors in the superior colliculus (see Introduction ), and transcriptomic analyses have documented significant alterations in gene expression in the lateral geniculate nucleus and visual cortex following visual deprivation (Cheadle et al, 2018; Cheng et al, 2022; Hrvatin et al, 2018; Tropea et al, 2006).…”

Section: Discussionmentioning

confidence: 99%

Vision-dependent and -independent molecular maturation of mouse retinal ganglion cells

Whitney

Butrus

Dyer

et al. 2022

Preprint

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The development and connectivity of retinal ganglion cells (RGCs), the retina’s sole output neurons, are patterned by activity-independent transcriptional programs and activity-dependent remodeling. To inventory the molecular correlates of these influences, we applied high-throughput single-cell RNA sequencing (scRNA-seq) to mouse RGCs at six embryonic and postnatal ages. We identified temporally regulated modules of genes that correlate with, and likely regulate, multiple phases of RGC development, ranging from differentiation and axon guidance to synaptic recognition and refinement. Some of these genes are expressed broadly while others, including key transcription factors and recognition molecules, are selectively expressed by one or a few of the 45 transcriptomically distinct types defined previously in adult mice. Next, we used these results as a foundation to analyze the transcriptomes of RGCs in mice lacking visual experience due to dark rearing from birth or to mutations that ablate either bipolar or photoreceptor cells. 98.5% of visually deprived (VD) RGCs could be unequivocally assigned to a single RGC type based on their transcriptional profiles, demonstrating that visual activity is dispensable for acquisition and maintenance of RGC type identity. However, visual deprivation significantly reduced the transcriptomic distinctions among RGC types, implying that activity is required for complete RGC maturation or maintenance. Consistent with this notion, transcriptomic alternations in VD RGCs significantly overlapped with gene modules found in developing RGCs. Our results provide a resource for mechanistic analyses of RGC differentiation and maturation, and for investigating the role of activity in these processes.

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“…Other studies, have highlighted that the combination of a cell connectivity pattern and activity state are key to drive its transcriptional identity, as it is the case for layer 6 cortical neurons with different connectivity patterns ( Chevée et al, 2018 ), suggesting that sensory experience might fine-tune cellular differentiation in the late stages of development. Accordingly, in visual cortex, vision is required for the specification of intra-layer 2/3 cell subtypes and the dysregulation of an activity-dependent gene key for this process leads to disruptions in visual circuit function ( Cheng et al, 2022 ). While the sensory experience-dependent programs regulating the refinement and plasticity of neuronal connectivity in vivo are emerging ( Louros et al, 2014 ; Mardinly et al, 2016 ; Cheadle et al, 2018 ), those regulating the specification of cell identity remain to be characterized.…”

Section: Transcriptional and Chromatin Regulation Of Activity-regulat...mentioning

confidence: 99%

Epigenetic and Transcriptional Regulation of Spontaneous and Sensory Activity Dependent Programs During Neuronal Circuit Development

Pumo

Kitazawa

Rijli

2022

Front. Neural Circuits

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Spontaneous activity generated before the onset of sensory transduction has a key role in wiring developing sensory circuits. From axonal targeting, to synapse formation and elimination, to the balanced integration of neurons into developing circuits, this type of activity is implicated in a variety of cellular processes. However, little is known about its molecular mechanisms of action, especially at the level of genome regulation. Conversely, sensory experience-dependent activity implements well-characterized transcriptional and epigenetic chromatin programs that underlie heterogeneous but specific genomic responses that shape both postnatal circuit development and neuroplasticity in the adult. In this review, we focus on our knowledge of the developmental processes regulated by spontaneous activity and the underlying transcriptional mechanisms. We also review novel findings on how chromatin regulates the specificity and developmental induction of the experience-dependent program, and speculate their relevance for our understanding of how spontaneous activity may act at the genomic level to instruct circuit assembly and prepare developing neurons for sensory-dependent connectivity refinement and processing.

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Vision-dependent specification of cell types and function in the developing cortex

Cited by 63 publications

References 74 publications

A single-cell atlas of bobtail squid visual and nervous system highlights molecular principles of convergent evolution

A single-cell atlas of bobtail squid visual and nervous system highlights molecular principles of convergent evolution

Vision-dependent and -independent molecular maturation of mouse retinal ganglion cells

Epigenetic and Transcriptional Regulation of Spontaneous and Sensory Activity Dependent Programs During Neuronal Circuit Development

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