Layer Positioning of Late-Born Cortical Interneurons Is Dependent on Reelin But Not p35 Signaling

Hammond, Vicki E.; So, Eva; Gunnersen, Jenny M.; Valcanis, Helen; Kalloniatis, Michael; Tan, Seong‐Seng

doi:10.1523/jneurosci.3651-05.2006

Cited by 53 publications

(47 citation statements)

References 50 publications

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“…These results suggest that the distribution of projection neurons and/or a normal radial glia organization is required for interneurons to distribute appropriately in the cortex. These findings challenge recent experiments in which wild-type interneurons were found to distribute normally when transplanted into the lateral ventricle of Dab1 mutant embryos (Hammond et al, 2006). Other than the obvious methodological differences that exist between both experiments (transplantation in the MGE versus transplantation in the lateral ventricle), we cannot explain the origin of this discrepancy.…”

Section: Layer Acquisition By Cortical Interneurons Does Not Directlycontrasting

confidence: 93%

Layer Acquisition by Cortical GABAergic Interneurons Is Independent of Reelin Signaling

et al. 2006

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Functioning of the cerebral cortex requires the coordinated assembly of circuits involving glutamatergic projection neurons and GABAergic interneurons. Despite their segregated origin in different regions of the telencephalon, projection neurons and interneurons born synchronically end up adopting the same cortical layer, suggesting that layer acquisition is highly coordinated for both neuronal types. The radial migration and laminar arrangement of projection neurons depends on Reelin, a secreted glycoprotein expressed near the pial surface during embryogenesis. In contrast, the mechanisms controlling layer acquisition by cortical interneurons remain essentially unknown. Here, we have used an ultrasound-guided transplantation approach to analyze the mechanisms underlying the acquisition of laminar locations by cortical interneurons. We found that layer acquisition by cortical GABAergic interneurons does not directly depend on Reelin signaling. Moreover, interneurons invade their target layers well after synchronically generated projection neurons reach their final destination. These results suggest a model in which cues provided by projection neurons guide cortical interneurons to their appropriate layer, and reveal that, at least for some neuronal types, long-range radial migration does not directly require Reelin.

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Section: Layer Acquisition By Cortical Interneurons Does Not Directlycontrasting

confidence: 93%

Layer Acquisition by Cortical GABAergic Interneurons Is Independent of Reelin Signaling

et al. 2006

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“…Previous studies have suggested differences between the migratory properties of murine MGE cells born at different developmental stages (29)(30)(31). Because chicken E6.5, the time when the donor MGE cells were dissected out, is in the middle of the neurogenic period in the chicken dorsal telencephalon (E5-8) (32), chicken MGE cells born earlier or later than E6.5 may behave differently from E6.5 chicken MGE cells.…”

Section: Resultsmentioning

confidence: 99%

Changes in cortical interneuron migration contribute to the evolution of the neocortex

Tanaka

Oiwa

Sasaki

et al. 2011

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

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The establishment of the mammalian neocortex is often explained phylogenetically by an evolutionary change in the pallial neuronal progenitors of excitatory projection neurons. It remains unclear, however, whether and how the evolutionary change in inhibitory interneurons, which originate outside the neocortex, has been involved in the establishment of the neocortex. In this study, we transplanted chicken, turtle, mouse, and marmoset medial ganglionic eminence (MGE) cells into the embryonic mouse MGE in utero and compared their migratory behaviors. We found that the MGE cells from all of the species were able to migrate through the mouse neocortical subventricular zone and that both the mouse and marmoset cells subsequently invaded the neocortical cortical plate (CP). However, regardless of their birthdates and interneuron subtypes, most of the chicken and turtle cells ignored the neocortical CP and passed beneath it, although they were able to invade the archicortex and paleocortex, suggesting that the proper responsiveness of MGE cells to guidance cues to enter the neocortical CP is unique to mammals. When chicken MGE cells were transplanted directly into the neocortical CP, they were able to survive and mature, suggesting that the neocortical CP itself is essentially permissive for postmigratory development of chicken MGE cells. These results suggest that an evolutionary change in the migratory ability of inhibitory interneurons, which originate outside the neocortex, was involved in the establishment of the neocortex by supplying inhibitory components to the network.dorsal pallium | GABAergic interneurons | tangential migration | mammalian evolution | interspecies transplantation D uring neocortical development, the projection neurons are generated in proliferative zones lying along the ventricle within the neocortex, namely the ventricular zone (VZ) and the subventricular zone (SVZ), and migrate radially to the brain surface (1-3) to form a cortical plate (CP) (4). Newly generated projection neurons migrate past the earlier-born neurons to settle just beneath the marginal zone (MZ), thereby constructing the neocortical CP in a birth date-dependent inside-out fashion (5). Although many (∼65% in humans) interneurons also seem to originate within the neocortical VZ/SVZ in primates (6, 7), most interneurons in most mammals (almost all interneurons in mice) seem to originate in the medial ganglionic eminence (MGE), caudal ganglionic eminence, and preoptic area located in the subpallium and migrate tangentially to the neocortex (8-11). After entering the neocortex, many MGE-derived interneurons, which constitute the majority of the interneurons in mice (9), continue to migrate tangentially through the neocortical SVZ and intermediate zone (IZ), and then, they change their trajectory and migrate to the brain surface so that they enter the CP and the MZ (12, 13).Phylogenetically, the neocortex is observed only in mammals, and because it evolved from the dorsal pallium of the ancestor of amniotes (mammals and saurop...

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“…None of the differentially expressed genes were previously shown to play a specific role in SST interneuron differentiation, though a number of them play a role in interneuron migration or differentiation in general. Disabled-1 (DAB1), has been implicated in interneuron migration, though it may not be required for this process (Hammond et al, 2006;Pla et al, 2006). Deletion of contactin-associated proteinlike 2 (CNTNAP2) disrupts interneuron migration, results in a loss of interneurons, and mutations in CNTNAP2 are associated with epilepsy and autism in humans (Penagarikano et al, 2011).…”

Section: Discussionmentioning

confidence: 99%

Single-Cell Profiling of an In Vitro Model of Human Interneuron Development Reveals Temporal Dynamics of Cell Type Production and Maturation

Close¹,

Yao²,

Miller³

et al. 2017

Neuron

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SummaryGABAergic interneurons are essential for neural circuit function and their loss or dysfunction is implicated in human neuropsychiatric disease. In vitro methods for interneuron generation hold promise for studying human cellular and functional properties and ultimately therapeutic cell replacement. We describe here a protocol for generating cortical interneurons from hESCs and analyze the properties and maturation timecourse of cell types using single-cell RNAseq. We find that the cell types produced mimic in vivo temporal patterns of neuron and glial production, with immature progenitors and neurons observed early and mature cortical neurons and glial cell types produced late. By comparing the transcriptomes of immature interneurons to more mature neurons, we identified genes important for human interneuron differentiation. Many of these genes were previously implicated in neurodevelopmental and neuropsychiatric disorders. Publisher's Disclaimer: This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final citable form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. HHS Public Access

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Layer Positioning of Late-Born Cortical Interneurons Is Dependent on Reelin But Not p35 Signaling

Cited by 53 publications

References 50 publications

Layer Acquisition by Cortical GABAergic Interneurons Is Independent of Reelin Signaling

Layer Acquisition by Cortical GABAergic Interneurons Is Independent of Reelin Signaling

Changes in cortical interneuron migration contribute to the evolution of the neocortex

Single-Cell Profiling of an In Vitro Model of Human Interneuron Development Reveals Temporal Dynamics of Cell Type Production and Maturation

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