Dynamic interplay between thalamic activity and Cajal-Retzius cells regulates the wiring of cortical layer 1

Genescu, Ioana; Aníbal-Martínez, Mar; Kouskoff, Vladimir; Chenouard, Nicolas; Mailhes-Hamon, Caroline; Cartonnet, Hugues; Lokmane, Ludmilla; Rijli, Filippo M.; López‐Bendito, Guillermina; Gambino, Frédéric; Garel, Sonia

doi:10.1016/j.celrep.2022.110667

Cited by 11 publications

(7 citation statements)

References 112 publications

(228 reference statements)

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“…Their disappearance at early stages of postnatal development in the neocortex (Ma et al, 2014) had often led to neglecting their postnatal role. However, in the last years, studies focused on interventions targeting CR-cell densities in the neocortex have shown effects on spine density, dendritic complexity, excitatory/inhibitory balance and thalamic input integration (de Frutos et al, 2016; Genescu et al, 2022; Riva et al, 2019). These studies greatly highlighted the importance of CR cells during the development of neocortical regions.…”

Section: Discussionmentioning

confidence: 99%

Persistence of Cajal-Retzius cells in the postnatal hippocampus is required for development of dendritic spines of CA1 pyramidal cells

Glærum

Dunville

Montaldo

et al. 2022

Preprint

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SummaryCajal-Retzius (CR) cells are a transient type of neuron that populate the postnatal hippocampus. The role of transient cell types and circuits have been vastly addressed in neocortical regions, but poorly studied in the hippocampus. To understand how CR cells’ persistence influences the maturation of hippocampal circuits, we specifically ablated CR cells from the postnatal hippocampus. Our results highlighted layer-specific effects on dendritic spines and synaptic-related genes and revealed a critical role of CR cells in the establishment of the hippocampal network.

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Section: Discussionmentioning

confidence: 99%

Persistence of Cajal-Retzius cells in the postnatal hippocampus is required for development of dendritic spines of CA1 pyramidal cells

Glærum

Dunville

Montaldo

et al. 2022

Preprint

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“…Cortical in utero lesions were induced unilaterally using a 100 μm diameter glass capillary, by poking through the cortical plate up to the lateral ventricle, as usually done for in utero electroporation or viral infection. 104 Lesioned embryos were left to recover in the mother’s womb for 2.5 h after surgery, after which their brains were collected and fixed in 4% PFA at 4°C overnight.…”

Section: Methodsmentioning

confidence: 99%

Microglia maintain structural integrity during fetal brain morphogenesis

Lawrence,

Canzi,

Bridlance

et al. 2024

Cell

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“…Our study focuses on the Δ Np73-Cre line, because of its popularity in CR cell research ( Tissir et al, 2009 ; Ledonne et al, 2016 ; Riva et al, 2019 ; Anstötz et al, 2022 ; Genescu et al, 2022 ) and our data showing its high specificity compared with the Wnt3a-Cre line. However, the homozygous Δ Np73-Cre mouse model results in knockout of ΔNp73 and ablation of ΔNp73 -lineage CR cells in the brain ( Tissir et al, 2009 ).…”

Section: Discussionmentioning

confidence: 99%

“…In our study, we used only the hemizygous Δ Np73-Cre mice, which do not demonstrate CR cell loss ( Tissir et al, 2009 ) and present with similar CR cell densities in the hippocampus compared with wild-type mice. Moreover, while our study focuses only on the postnatal and adult hippocampus, we recognize that CR cells in the neocortex are also derived from the Δ Np73 lineage ( Ledonne et al, 2016 ; Riva et al, 2019 ; Genescu et al, 2022 ); therefore, our strategy will also transduce neocortical CRs. While very few neocortical CRs are present in the adult brain ( Fig.…”

Section: Discussionmentioning

confidence: 99%

“…Once in residence, CR cells control cortical neuron migration via secretion of the glycoprotein reelin ( Meyer et al, 2004 ; Yoshida et al, 2006 ; Tissir et al, 2009 ; Amelio et al, 2020 ; Vílchez-Acosta et al, 2022 ). They also regulate cortical and hippocampal circuits through their connectivity in local networks ( Anstötz et al, 2022 ; Genescu et al, 2022 ; Riva et al, 2023 ).…”

Section: Introductionmentioning

confidence: 99%

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A Versatile Strategy for Genetic Manipulation of Cajal–Retzius Cells in the Adult Mouse Hippocampus

van Bruggen,

Patel,

Wang

et al. 2023

eNeuro

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Cajal-Retzius (CR) cells are transient neurons with long-lasting effects on the architecture and circuitry of the neocortex and hippocampus. Contrary to the prevailing assumption that CR cells completely disappear in rodents shortly after birth, a substantial portion of these cells persist in the hippocampus throughout adulthood. The role of these surviving CR cells in the adult hippocampus is largely unknown, partly because of the paucity of suitable tools to dissect their functions in the adult versus the embryonic brain. Here, we show that genetic crosses of theΔNp73-Cremouse line, widely used to target CR cells, to reporter mice induce reporter expression not only in CR cells but also progressively in postnatal dentate gyrus granule neurons. Such a lack of specificity may confound studies of CR cell function in the adult hippocampus. To overcome this, we devise a method that not only leverages the temporary CR cell-targeting specificity of theΔNp73-Cremice before the first postnatal week, but also capitalizes on the simplicity and effectiveness of freehand neonatal intracerebroventricular injection of adeno-associated virus. We achieve robust Cre-mediated recombination that remains largely restricted to hippocampal CR cells from early postnatal age to adulthood. We further demonstrate the utility of this method to manipulate neuronal activity of CR cells in the adult hippocampus. This versatile and scalable strategy will facilitate experiments of CR cell-specific gene knockdown and/or overexpression, lineage tracing, and neural activity modulation in the postnatal and adult brain.Significance StatementHigh-throughput and specific tools for genetic manipulation of neuronal subtypesin vivoare desirable for scalable experiments and accurate data interpretation. However, limitations in available tools present a challenge for certain cell types, such as Cajal-Retzius cells, a class of transient neurons of which a portion persists in the adult brain. Highlighting the limitation of Cre-driver mouse lines because of loss of specificity in adulthood, we demonstrate the use of neonatal intracerebroventricular delivery of adeno-associated viral vectors to specifically manipulate Cajal-Retzius cells in the adult hippocampus. Our strategy offers a framework to address similar issues with experiment throughput and specificity of other neuronal subtypes.

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Dynamic interplay between thalamic activity and Cajal-Retzius cells regulates the wiring of cortical layer 1

Cited by 11 publications

References 112 publications

Persistence of Cajal-Retzius cells in the postnatal hippocampus is required for development of dendritic spines of CA1 pyramidal cells

Persistence of Cajal-Retzius cells in the postnatal hippocampus is required for development of dendritic spines of CA1 pyramidal cells

Microglia maintain structural integrity during fetal brain morphogenesis

A Versatile Strategy for Genetic Manipulation of Cajal–Retzius Cells in the Adult Mouse Hippocampus

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