Neuronal cell migration for the developmental formation of the mammalian striatum

Hamasaki, Tadashi; Goto, Satoshi; Nishikawa, Sadakatsu; Ushio, Yukitaka

doi:10.1016/s0165-0173(02)00216-3

Cited by 46 publications

(37 citation statements)

References 134 publications

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“…Development of the striatum, for example, is thought to involve three sequential steps: (1) production of different classes of projection neurons from the same common progenitor pool in the lateral ganglionic eminence (LGE); (2) radial migration of striatal projection neurons to form a distinct neuronal assemble in the telencephalic mantle; and (3) tangential migration of interneurons from a remote progenitor pool in the medial ganglionic eminence (MGE), which further increases cell diversity within the nucleus (Deacon et al, 1994;Olsson et al, 1995Olsson et al, , 1998Marín et al, 2000;Wichterle et al, 2001;Hamasaki et al, 2003). A similar process has been proposed recently for the generation of some nuclei in the amygdala ).…”

Section: Introductionmentioning

confidence: 99%

Origin and Molecular Specification of Globus Pallidus Neurons

Nóbrega-Pereira¹,

Gelman²,

Bartolini³

et al. 2010

J. Neurosci.

124

157

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The mechanisms controlling the assembly of brain nuclei are poorly understood. In the forebrain, it is typically assumed that the formation of nuclei follows a similar sequence of events that in the cortex. In this structure, projection neurons are generated sequentially from common progenitor cells and migrate radially to reach their final destination, whereas interneurons are generated remotely and arrive to the cortex through tangential migration. Using the globus pallidus as a model to study the formation of forebrain nuclei, we found that the development of this basal ganglia structure involves the generation of several distinct classes of projection neurons from relatively distant progenitor pools, which then assemble together through tangential migration. Our results thus suggest that tangential migration in the forebrain is not limited to interneurons, as previously thought, but also involves projection neurons and reveal that the assembly of forebrain nuclei is more complex than previously anticipated.

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Section: Introductionmentioning

confidence: 99%

Origin and Molecular Specification of Globus Pallidus Neurons

Nóbrega-Pereira¹,

Gelman²,

Bartolini³

et al. 2010

J. Neurosci.

124

157

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“…Despite the importance of this brain region, there is only scarce information concerning both the morphological and functional aspects of the normal striatal development [see [12][13][14][15][16][17][18], knowledge which is a prerequisite for the understanding of pathology-related changes.…”

Section: Introductionmentioning

confidence: 99%

A CD15-Immunoreactive Subpopulation of Radial Glial Cells in the Developing Human Lateral Ganglionic Eminence

et al. 2003

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There is evidence that precursor cells for the different derivatives of the ganglionic eminences arise from topographically different areas of the proliferative neuroepithelium, indicating a molecular specification for this histologically homogeneous region. We describe a regionally differentiated expression pattern within the lateral ganglionic eminence during human fetal development of a subpopulation of radial glial cells stained for CD15. These cells were first observed around 12–13 weeks of fertilization in the ventricular layer of the lateral ganglionic eminence at the corticostriatal sulcus. In the following weeks increasing numbers of cells and their positively stained processes concentrate along the lateral perimeter of the striatum, with processes continuing towards the pial surface defining the border between the olfactory tubercle medially and the piriform cortex laterally. The number of immunoreactive cells and processes increases until 24 weeks. At that time, these cells are found throughout the lateral ganglionic eminence, defining a border against the unstained medial ganglionic eminence. Concomitant with the rise in the number of fibres until 24 weeks of fertilization, there is also an increase in immunoreactivity in the dorsal striatum. According to the accepted role of radial glial cells as a guidance structure for migrating postmitotic neurones, these CD15-immunoreactive fibres may enable the registration between localized proliferation areas within the lateral ganglionic eminence and related differentiation areas, thereby helping to characterize the fundamental subdivisions of the brain.

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“…Approximately 95% of striatal neurons are medium-sized spiny neurons (MSNs) with the rest being interneurons (8). MSNs, which use γ-aminobutyric acid (GABA) as a transmitter, are born in the lateral ganglionic eminence (LGE) and migrate to the striatum during embryogenesis (9). They are divided into two populations based on their projection sites.…”

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confidence: 99%

TrkB receptor controls striatal formation by regulating the number of newborn striatal neurons

Baydyuk

Russell

Liao

et al. 2011

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

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In the peripheral nervous system, target tissues control the final size of innervating neuronal populations by producing limited amounts of survival-promoting neurotrophic factors during development. However, it remains largely unknown if the same principle works to regulate the size of neuronal populations in the developing brain. Here we show that neurotrophin signaling mediated by the TrkB receptor controls striatal size by promoting the survival of developing medium-sized spiny neurons (MSNs). Selective deletion of the gene for the TrkB receptor in striatal progenitors, using the Dlx5/6-Cre transgene, led to a hindpawclasping phenotype and a 50% loss of MSNs without affecting striatal interneurons. This loss resulted mainly from increased apoptosis of newborn MSNs within their birthplace, the lateral ganglionic eminence. Among MSNs, those expressing the dopamine receptor D2 (DRD2) were most affected, as indicated by a drastic loss of these neurons and specific down-regulation of the DRD2 and enkephalin. This specific phenotype of mutant animals is likely due to preferential TrkB expression in DRD2 MSNs. These findings suggest that neurotrophins can control the size of neuronal populations in the brain by promoting the survival of newborn neurons before they migrate to their final destinations.A neural circuit consists of several connected nodes that are composed of neurons or nonneuronal cells, and its proper function requires a correct number of cells at each node. Thus, it is important to understand the mechanism by which the size of neuronal populations is determined during development. In the peripheral nervous system (PNS), it has been well documented that developing neurons have to compete for a limited amount of neurotrophic factors produced by their target tissues, and that neurons unable to obtain sufficient amounts of trophic factors die through programmed cell death (1). In this way a peripheral target can control the final size of the innervating neuronal populations through neurotrophic factors. One important family of neurotrophic factors is called neurotrophins, which include nerve growth factor (NGF), brain-derived neurotrophic factor (BDNF), neurotrophin 3 (NT3), and neurotrophin 4/5 (NT4/5). Neurotrophins exert many biological effects by binding and activating specific Trk receptor tyrosine kinases: NGF activates TrkA; BDNF and NT4/5 activate TrkB; and NT3 activates TrkC (2). Deletion of neurotrophin genes causes a severe loss of sensory and sympathetic neurons (3). Although ablation of neurotrophic signaling increases programmed cell death in hippocampal dentate gyrus and cerebellar granular layer during the first two postnatal weeks (4, 5), no studies have identified a large population of developing brain neurons that are dependent on a single neurotrophic factor for survival. Therefore, it remains unknown whether neurotrophic factors can coordinate the size of two connected brain regions in the developing brain.The striatum is the largest component of the basal ganglia. It is responsible...

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Neuronal cell migration for the developmental formation of the mammalian striatum

Cited by 46 publications

References 134 publications

Origin and Molecular Specification of Globus Pallidus Neurons

Origin and Molecular Specification of Globus Pallidus Neurons

A CD15-Immunoreactive Subpopulation of Radial Glial Cells in the Developing Human Lateral Ganglionic Eminence

TrkB receptor controls striatal formation by regulating the number of newborn striatal neurons

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