Segregation and Coactivation of Developing Neocortical Layer 1 Neurons

Soda, Takeshi; Nakashima, Ryoichi; Watanabe, Dai; Nakajima, Kazunori; Pastan, Ira; Nakanishi, Shigetada

doi:10.1523/jneurosci.23-15-06272.2003

Cited by 85 publications

(116 citation statements)

References 49 publications

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“…However, it is not known when and how CR cells can detect serotonergic signals and whether CR cells express serotonin receptors. CR cells express an array of receptors for other neurotransmitters, such as glutamate, GABA, glycine, and norepinephrine (Schwartz et al, 1998;Lu et al, 2001;Radnikow et al, 2002, Luhmann et al, 2003Soda et al, 2003). The absence of published reports on serotonin receptors on CR cells appears to be attributable to the availability of adequate serotonin receptor antibodies.…”

Section: Discussionmentioning

confidence: 99%

Early Serotonergic Projections to Cajal-Retzius Cells: Relevance for Cortical Development

Janušonis¹,

Glunčić²,

Rakić³

2004

J. Neurosci.

135

123

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Although the serotonergic system plays an important role in various neurological disorders, the role of early serotonergic projections to the developing cerebral cortex is not well understood. Because serotonergic fibers enter the marginal zone (MZ) before birth, it has been suggested that they may influence cortical development through synaptic contacts with Cajal-Retzius (CR) cells. We used immunohistochemistry combined with confocal and electron microscopy to show that the earliest serotonergic projections to the MZ form synaptic contacts with the somata and proximal dendrites of CR cells as early as embryonic day 17. To elucidate the functional significance of these early serotonergic contacts with CR cells, we perturbed their normal development by injecting pregnant mice with 5-methoxytryptamine. Lower reelin levels were detected in the brains of newborn pups from the exposed animals. Because reelin plays an important role in the cortical laminar and columnar organization during development, we killed some pups from the same litters on postnatal day 7 and analyzed their presubicular cortex. We found that the supragranular layers of the presubicular cortex (which normally display a visible columnar deployment of neurons) were altered in the treated animals. Our results suggest a mechanism of how serotonergic abnormalities during cortical development may disturb the normal cortical organization; and, therefore, may be relevant for understanding neurological disorders in which abnormalities of the serotonergic system are accompanied by cortical pathology (such as autism).

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Section: Discussionmentioning

confidence: 99%

Early Serotonergic Projections to Cajal-Retzius Cells: Relevance for Cortical Development

Janušonis¹,

Glunčić²,

Rakić³

2004

J. Neurosci.

135

123

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“…The University of California, San Diego Institutional Animal Care and Use Committee approved all procedures. Newborn rats (Sprague Dawley; P1-P7), mice (C57B6/J; P0 -P7), and transgenic mice [C57BL/6J-TgN(grm2-IL2RA/GFP)1; P5-P7] in which the fusion protein interleukin 2␣ subunit (IL2RA)-green fluorescent protein (GFP) is expressed under the metabotropic glutamate receptor subtype 2 (mGluR2) promoter were used (Watanabe et al, 1998;Soda et al, 2003). For these studies, we do not take advantage of the IL2RA, which allows for immunotoxin-mediated selective ablation of starburst amacrine cells (Yoshida et al, 2001).…”

Section: Methodsmentioning

confidence: 99%

GABA_AReceptor-Mediated Signaling Alters the Structure of Spontaneous Activity in the Developing Retina

Wang

Blankenship²,

Anishchenko³

et al. 2007

J. Neurosci.

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Ambient GABA modulates firing patterns in adult neural circuits by tonically activating extrasynaptic GABA A receptors. Here, we demonstrate that during a developmental period when activation of GABA A receptors causes membrane depolarization, tonic activation of GABA A receptors blocks all spontaneous activity recorded in retinal ganglion cells (RGCs) and starburst amacrine cells (SACs). Bath application of the GABA A receptor agonist muscimol blocked spontaneous correlated increases in intracellular calcium concentration and compound postsynaptic currents in RGCs associated with retinal waves. In addition, GABA A receptor agonists activated a tonic current in RGCs that significantly reduced their excitability. Using a transgenic mouse in which green fluorescent protein is expressed under the metabotropic glutamate receptor subtype 2 promoter to target recordings from SACs, we found that GABA A receptor agonists blocked compound postsynaptic currents and also activated a tonic current. GABA A receptor antagonists reduced the holding current in SACs but not RGCs, indicating that ambient levels of GABA tonically activate GABA A receptors in SACs. GABA A receptor antagonists did not block retinal waves but did alter the frequency and correlation structure of spontaneous RGC firing. Interestingly, the drug aminophylline, a general adenosine receptor antagonist used to block retinal waves, induced a tonic GABA A receptor antagonist-sensitive current in outside-out patches excised from RGCs, indicating that aminophylline exerts its action on retinal waves by direct activation of GABA A receptors. These findings have implications for how various neuroactive drugs and neurohormones known to modulate extrasynaptic GABA A receptors may influence spontaneous firing patterns that are critical for the establishment of adult neural circuits.

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“…We focused on CR cells at E13.5 and P2, because the expression of the GFP transgene is not only specific to CR cells within the developing neocortex but also sufficiently appears at both stages (7,9). The neocortices were prepared from the brains of E13.5 and P2 transgenic mice, and cells were dissociated into single cells by papain treatment.…”

Section: Purification Of Cr Cells By Facsmentioning

confidence: 99%

“…Reelin is defective in the reeler mouse mutant and human congenital lissencephaly, both of which show altered cortical cell migration and an abnormal cortical layer formation (4,5). CR cells also form synaptic connections with migrating cortical neurons, thus serving as a physiological scaffolding of cortical synaptic circuits during neocortical development (3,6,7). Despite great advances in the characterization of CR cells in neocortical development, neither the molecular entities that govern the CR cell identity nor the molecular mechanisms in which CR cells participate in the control of cortical organization were well understood.…”

mentioning

confidence: 99%

“…In our previous studies, we reported that the membraneanchored GFP transgene, when driven by the promoter function of metabotropic glutamate receptor subtype 2 (8), is specifically expressed by CR cells both in the MZ during the embryonic stage and in layer 1 during the postnatal period (7,9). This specific expression of GFP in CR cells provided a unique opportunity to purify CR cells to homogeneity by fluorescence-activated cell sorting (FACS) and to investigate a genomewide expression profile of CR cells during neocortical development with microarray techniques.…”

mentioning

confidence: 99%

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Distinct ontogenic and regional expressions of newly identified Cajal-Retzius cell-specific genes during neocorticogenesis

Yamazaki

Sekiguchi

Takamatsu

et al. 2004

Proc. Natl. Acad. Sci. U.S.A.

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Cajal-Retzius (CR) cells are early-generated transient neurons and are important in the regulation of cortical neuronal migration and cortical laminar formation. Molecular entities characterizing the CR cell identity, however, remain largely elusive. We purified mouse cortical CR cells expressing GFP to homogeneity by fluorescenceactivated cell sorting and examined a genomewide expression profile of cortical CR cells at embryonic and postnatal periods. We identified 49 genes that exceeded hybridization signals by >10-fold in CR cells compared with non-CR cells at embryonic day 13.5, postnatal day 2, or both. Among these CR cell-specific genes, 25 genes, including the CR cell marker genes such as the reelin and calretinin genes, are selectively and highly expressed in both embryonic and postnatal CR cells. These genes, which encode generic properties of CR cell specificity, are eminently characterized as modulatory composites of voltage-dependent calcium channels and sets of functionally related cellular components involved in cell migration, adhesion, and neurite extension. Five genes are highly expressed in CR cells at the early embryonic period and are rapidly down-regulated thereafter. Furthermore, some of these genes have been shown to mark two distinctly different focal regions corresponding to the CR cell origins. At the late prenatal and postnatal periods, 19 genes are selectively up-regulated in CR cells. These genes include functional molecules implicated in synaptic transmission and modulation. CR cells thus strikingly change their cellular phenotypes during cortical development and play a pivotal role in both corticogenesis and cortical circuit maturation.

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Segregation and Coactivation of Developing Neocortical Layer 1 Neurons

Cited by 85 publications

References 49 publications

Early Serotonergic Projections to Cajal-Retzius Cells: Relevance for Cortical Development

Early Serotonergic Projections to Cajal-Retzius Cells: Relevance for Cortical Development

GABA_AReceptor-Mediated Signaling Alters the Structure of Spontaneous Activity in the Developing Retina

Distinct ontogenic and regional expressions of newly identified Cajal-Retzius cell-specific genes during neocorticogenesis

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Segregation and Coactivation of Developing Neocortical Layer 1 Neurons

Cited by 85 publications

References 49 publications

Early Serotonergic Projections to Cajal-Retzius Cells: Relevance for Cortical Development

Early Serotonergic Projections to Cajal-Retzius Cells: Relevance for Cortical Development

GABAAReceptor-Mediated Signaling Alters the Structure of Spontaneous Activity in the Developing Retina

Distinct ontogenic and regional expressions of newly identified Cajal-Retzius cell-specific genes during neocorticogenesis

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GABA_AReceptor-Mediated Signaling Alters the Structure of Spontaneous Activity in the Developing Retina