Cajal-Retzius (CR) cells are early generated neurons, involved in the assembly of developing neocortical and hippocampal circuits. However, their roles in networks of the postnatal brain remain poorly understood. In order to get insights into these latter functions, we have studied their morphological and synaptic properties in the postnatal hippocampus of the CXCR4-EGFP mouse, where CR cells are easily identifiable. Our data indicate that CR cells are nonuniformly distributed along different subfields of the hippocampal formation, and that their postnatal decline is regulated in a region-specific manner. In fact, CR cells persist in distinct areas of fully mature animals. Subclasses of CR cells project and target either local (molecular layers) or distant regions [subicular complex and entorhinal cortex (EC)] of the hippocampal formation, but have similar firing patterns. Lastly, CR cells are biased toward targeting dendritic shafts compared with spines, and produce large-amplitude glutamatergic unitary postsynaptic potentials on γ-aminobutyric acid (GABA) containing interneurons. Taken together, our results suggest that CR cells are involved in a novel excitatory loop of the postnatal hippocampal formation, which potentially contributes to shaping the flow of information between the hippocampus, parahippocampal regions and entorhinal cortex, and to the low seizure threshold of these brain areas.

/pdf/developmental-profile-morphology-and-synaptic-connectivity-1o1s1qf5jz.pdf

Developmental Profile, Morphology, and Synaptic Connectivity of Cajal–Retzius Cells in the Postnatal Mouse Hippocampus

During cortical development, Cajal-Retzius (CR) cells are among the earliest-born subclasses of neurons. These enigmatic neurons play an important role in cortical development through their expression of the extracellular protein, reelin. CR cells arise from discrete sources within the telencephalon, including the pallial-subpallial border and the medial (cortical hem) regions of the pallium. Combined evidence suggests that CR cells derived from distinct origins may have different distributions and functions. By tracing CR cells derived from the cortical hem using the inducible Cre transgenic mouse tool, Frizzled 10-CreER™, we examined the specific properties of hem-derived CR cells during cortical development. Our results show that the progenitor zone for later production of CR cells from the hem can be specifically marked as early as embryonic day 6.5 (E6.5), a pre-neural period. Moreover, using our Cre line, we found that some hem-derived CR cells migrated out along the fimbrial radial glial scaffold, which was also derived from the cortical hem, and preferentially settled in the hippocampal marginal zone, which indicated specific roles for hem-derived CR cells in hippocampal development.

https://escholarship.org/content/qt2c46f5xs/qt2c46f5xs.pdf?t=qafp2a

Inducible genetic lineage tracing of cortical hem derived Cajal-Retzius cells reveals novel properties

Segregation and coactivation of developing neocortical layer 1 neurons

The generation and differentiation of an appropriate number of neurons, as well as its distribution in different parts of the brain, is crucial for the proper establishment, maintenance and plasticity of neuronal circuitries. Newborn neurons travel along the brain, in a process called neuronal migration, to finalize their correct position in the nervous system. Defects in neuronal migration produce abnormalities in the brain that can generate neurodevelopmental pathologies, such as autism, schizophrenia and intellectual disability. In this review, we present an overview of the developmental origin of the different telencephalic subdivisions and a further description of migratory pathways taken by some neural populations that travel long distances before reaching their target position in the brain. In addition, we will discuss some of the molecules implicated in the guidance of these migratory paths and transcription factors that contribute to the correct migration and integration of these neurons.

/pdf/rostro-caudal-and-caudo-rostral-migrations-in-the-5rksgavuuk.pdf

Rostro-Caudal and Caudo-Rostral Migrations in the Telencephalon: Going Forward or Backward?

The superior colliculus (SC) in the mammalian midbrain is essential for multisensory integration and is composed of a rich diversity of excitatory and inhibitory neurons and glia. However, the developmental principles directing the generation of SC cell-type diversity are not understood. Here, we pursued systematic cell lineage tracing in silico and in vivo, preserving full spatial information, using genetic mosaic analysis with double markers (MADM)-based clonal analysis with single-cell sequencing (MADM-CloneSeq). The analysis of clonally related cell lineages revealed that radial glial progenitors (RGPs) in SC are exceptionally multipotent. Individual resident RGPs have the capacity to produce all excitatory and inhibitory SC neuron types, even at the stage of terminal division. While individual clonal units show no pre-defined cellular composition, the establishment of appropriate relative proportions of distinct neuronal types occurs in a PTEN-dependent manner. Collectively, our findings provide an inaugural framework at the single-RGP/-cell level of the mammalian SC ontogeny. 

Multipotent progenitors instruct ontogeny of the superior colliculus

Cajal-Retzius cells are an enigmatic class of neurons located in the most superficial layer of the cerebral cortex, and they play an important role in cortical development. Although many studies have indicated that CR cells are involved in regulating cell migration and cortical maturation, the function of these cells is still not fully understood. Here we describe an inducible Cre mouse line in which CreER is driven by the promoter for the Wnt receptor Frizzled10. Consistent with our previous studies on Frizzled10 expression and transgenic mouse lines using the Frizzled10 promoter, we found that in the developing telencephalon, Cre was mainly detected at the cortical hem, the largest source of CR cells. By crossing the Cre line to R26R reporter mice and injecting tamoxifen at different time points, we were able to detect via X-gal staining CR cells produced from the cortical hem at distinct stages during development. Thus, this transgenic Cre mouse line is a valuable tool for studying the molecular and cellular mechanisms of CR cell development.

/pdf/characterization-of-the-frizzled10-creer-transgenic-mouse-an-1dk5l20a18.pdf

Characterization of the Frizzled10‐CreER™ transgenic mouse: An inducible Cre line for the study of Cajal‐Retzius cell development

Gene targeting techniques have become highly developed to study gene function in mice However, in conventional gene knockouts, the function of a gene is often difficult to recognize because of embryonic lethality This is particularly difficult for the brain whose function is controlled by complex gene expression patterns and is made up of numerous distinct cell types These limitations can be overcome by transgenic expression of Cre recombinase, which catalyses the excision of DNA segments that are flanked by loxP sites (Sauer and Henderson, 1988) With the Cre/loxP recombinase system as a tool, scientists have gotten closer to the level of “no more practical limitations” in tailoring the mouse genome When Cre is expressed under the control of a tissue- or cell type-specific promoter in transgenic mice, precise spatial control of target gene disruption is straightforward (Branda and Dymecki, 2004)

To study the molecular mechanisms of cortical development or aspects of learning and memory, many mouse lines that express Cre in specific areas of the forebrain have been generated (Berger et al, 2004; Casanova et al, 2001; Iwasato et al, 2004; van den Bout et al, 2002) However, compared with the extreme complexity of the brain, the range and specificity of the existing Cre lines remains a significant limitation We have been taking advantage of the specific regional and temporal expression of members of the Wnt family and their receptors to generate a variety of useful mouse reagents (Kim et al, 2001; Zhao and Pleasure, 2004, 2005; Zhao et al, 2006)

The Wnt family of glycoproteins is involved in numerous developmental and disease processes in higher eukaryotes They signal by binding to at least two cell surface receptor families: the Frizzled family of receptors and their coreceptor “low density lipoprotein-related proteins” (Logan and Nusse, 2004) Frizzled proteins are cell surface receptors that participate in a wide variety of developmental processes, including cerebellar degeneration, esophageal distension and dysfunction loss of hair cells or other auditory neurons [Fzd4 (Wang et al, 2001)], macroscopic hair patterning [Fz6 (Guo et al, 2004)], hippocampal cell survival [Fz9 (Zhao et al, 2005)], and the development of major brain axon tracts [Fz3 (Lyuksyutova et al, 2003; Wang et al, 2002)] In our previous study, we generated a transgenic mouse line in which the TauLacZ reporter gene was expressed in the cortical hem, dorsal thalamus, and dorsal neural tube under the control of Frizzled10 promoter during embryonic life (Zhao et al, 2006) To take advantage of the regionally specific expression of the Frizzled10 promoter, we have generated a Cre transgenic mouse line using the same Frizzled 10 promoter In these mice, Cre was strongly expressed in the developing cortex and hippocampus, and there is very strong recombination activity in these regions Our transgenic Cre line has Cre expression with the following features:


expressed in cortex, hippocampus, dorsal thalamus, and caudate putamen (CPu)


strong activity in the developing dorsal telencephalon


dynamic expression at different development stages



The Cre expression shows prominent differences with that of our previously generated TauLacZ transgene mice, which expressed TauLacZ in a pattern closely resembling the native expression of Frizzled10 These differences are probably due to the different insertion site of the transgene Despite the unique expression pattern of Cre in this mouse line, we believe that this line will be quite useful for the study of brain development and conditional inactivation of target genes in cortex and hippocampus Additionally, we detected Cre expression in the specific patterns in the cerebellum, retina, and spinal cord

/pdf/generation-of-frizzled10-cre-transgenic-mouse-line-a-useful-37ic0ultvt.pdf

Generation of Frizzled10-Cre transgenic mouse line: a useful tool for the study of dorsal telencephalic development.

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Characterization of the Frizzled10‐CreER™ transgenic mouse: An inducible Cre line for the study of Cajal‐Retzius cell development

Generation of Frizzled10-Cre transgenic mouse line: a useful tool for the study of dorsal telencephalic development.