Pallial origin of basal forebrain cholinergic neurons in the nucleus basalis of Meynert and horizontal limb of the diagonal band nucleus

Pombero, Ana; Bueno, Carlos; Saglietti, Laura; Rodenas, Monica; Guimerà, Jordi; Bulfone, Alexandro

doi:10.1242/dev.069534

Cited by 29 publications

(20 citation statements)

References 82 publications

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“…We found that CB ϩ /ChAT There are four groups of cholinergic neurons in the ventral telencephalon that originate from both subpallium and pallium (22,58,59). Ch1 neurons in the medial septum and Ch2 neurons in the vertical limb of the diagonal band project to the hippocampus.…”

Section: Discussionmentioning

confidence: 84%

Regulation of the Protocadherin Celsr3 Gene and Its Role in Globus Pallidus Development and Connectivity

Jia

Guo

Tang

et al. 2014

Molecular and Cellular Biology

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The globus pallidus (GP) is a central component of basal ganglia whose malfunctions cause a variety of neuropsychiatric disorders as well as cognitive impairments in neurodegenerative diseases such as Parkinson's disease. Here we report that the protocadherin gene Celsr3 is regulated by the insulator CCCTC-binding factor (CTCF) and the repressor neuron-restrictive silencer factor (NRSF, also known as REST) and is required for the development and connectivity of GP. Specifically, CTCF/cohesin and NRSF inhibit the expression of Celsr3 through specific binding to its promoter. In addition, we found that the Celsr3 promoter interacts with CTCF/cohesin-occupied neighboring promoters. In Celsr3 knockout mice, we found that the ventral GP is occupied by aberrant calbindin-positive cholinergic neurons ectopic from the nucleus basalis of Meynert. Furthermore, the guidepost cells for thalamocortical axonal development are missing in the caudal GP. Finally, axonal connections of GP with striatum, subthalamic nucleus, substantia nigra, and raphe are compromised. These data reveal the essential role of Celsr3 in GP development in the basal forebrain and shed light on the mechanisms of the axonal defects caused by the Celsr3 deletion. The genes Celsr1, Celsr2, and Celsr3 are members of the mammalian nonclustered protocadherin (Pcdh) family that are homologous to the fly flamingo gene (1). The flamingo gene plays important roles in dendrite development and self-avoidance, axonal projection, and planar cell polarity (PCP) in Drosophila (2-7). The mammalian Celsr genes are the so-called core PCP genes that have conserved as well as newly diversified functions. In particular, the vertebrate Celsr3 gene has been shown to regulate axonal projections, dendrite development, neuronal migration, ciliogenesis, and retina circuit development (8-16). However, very little is known about Celsr gene regulation.The globus pallidus (GP) is a central nucleus of the basal ganglia (BG) (17,18). Malfunctions of GP lead to several neuropathological conditions, such as Parkinson's disease, as well as many neuropsychiatric diseases (19). The mouse GP, which corresponds to the GPe in primates, contains approximately 44% of parvalbumin-positive (PV ϩ ) neurons and 1% of calretinin-positive (CR ϩ ) interneurons, but calbindin-positive (CB ϩ ) cells are rare (20,21). The GP is traditionally thought to be derived from the medial ganglionic eminence (MGE) (22); however, recent studies have revealed that, in addition to MGE, subpopulations of GP cells are also generated from the lateral ganglionic eminence (LGE) and preoptic area (POA) (21, 23). The molecular requirements for GP development are not known, but specific transcription factors appear to be essential. For example, Nkx2-1 is required for the generation of most GP neurons except the Npas1 ϩ type from LGE (23). In addition, Lhx6/8 double-mutant mice do not have a well-defined GP (24).The GP functions through extensive axonal connections with other brain nuclei. For example, GP receives GABAergic ax...

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Section: Discussionmentioning

confidence: 84%

Regulation of the Protocadherin Celsr3 Gene and Its Role in Globus Pallidus Development and Connectivity

Jia

Guo

Tang

et al. 2014

Molecular and Cellular Biology

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“…The newborn neurons migrate radially, and organize into distinct clusters along the rostral-caudal axis of the forebrain (Marin et al, 2000). An alternative path for a sub population of cholinergic neurons in Ch3 (hDB) and Ch4 (NB/SI) that appear to originate in the ventral pallium has also been described (Pombero et al, 2011). BFCN identity is determined by the sequential expression of distinct combinations of transcription factors.…”

Section: Cholinergic Neurons and Cholinergic Signaling Mechanisms mentioning

confidence: 99%

Basal Forebrain Cholinergic Circuits and Signaling in Cognition and Cognitive Decline

Ballinger

Ananth

Talmage

et al. 2016

Neuron

603

517

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Recent work continues to place cholinergic circuits at center stage for normal executive and mnemonic functioning, and provides compelling evidence that the loss of cholinergic signaling and cognitive decline are inextricably linked. This review focuses on the last few years of studies on the mechanisms by which cholinergic signaling contributes to circuit activity related to cognition. We attempt to identify areas of controversy, as well as consensus, on what is and is not yet known about how cholinergic signaling in the CNS contributes to normal cognitive processes. In addition, we delineate the findings from recent work on the extent to which dysfunction of cholinergic circuits contributes to cognitive decline associated with neurodegenerative disorders.

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“…Developmental signals in fact still persist in specific areas of the postnatal brain and can also participate as guidance cues by stimulating the intrinsic capacity of newly generated neurons to migrate (Balordi and Fishell, ; Angot et al, ). Among many guiding molecules implicated in tangential migration such as the classical factors Slits, Netrins, and integrins (Murase and Horwitz, ; Nguyen‐Ba‐Charvet et al, ; Belvindrah et al, ; Hakanen et al, ), we have tested whether FGF signaling, already known for its guidance ability of neural precursors during early embryonic development (Kuhn et al, ; Smith et al, ; Pombero et al, ), could maintain these functions during postnatal stages.…”

Section: Introductionmentioning

confidence: 99%

Attractive action of FGF‐signaling contributes to the postnatal developing hippocampus

et al. 2014

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During brain development neural cell migration is a crucial, well-orchestrated, process, which leads to the proper whole brain structural organization. As development proceeds, new neurons are continuously produced, and this protracted neurogenesis is maintained throughout life in specialized germinative areas inside the telencephalon: the subventricular zone (SVZ) and the dentate gyrus (DG) of the hippocampus. In the anterior SVZ, newly generated neurons migrate through long distances, along the rostral migratory stream (RMS), before reaching their final destinations in the olfactory bulb (OB). Intriguingly, recent observations pointed out the existence of other postnatal tangential routes of migration alternative to the RMS but still starting from the SVZ. The presence of such dynamic and heterogeneous cell movements contributes to important features in the postnatal brain such as neural cell replacement and plasticity in cortical regions. In this work, we asked whether a caudal migratory pathway starting from the caudal SVZ continues through life. Strikingly, in vivo analysis of this caudal migration revealed the presence of a postnatal contribution of SVZ to the hippocampus. In vitro studies of the caudal migratory stream revealed the role of FGF signaling in attracting caudally the migrating neuroblasts during postnatal stages. Our findings demonstrate a postnatal neuronal contribution from the caudal ganglionic eminence (CGE) CGE-SVZ to the hippocampus through an FGF-dependent migrating mechanism. All together our data emphasizes the emerging idea that a developmental program is still operating in discrete domains of the postnatal brain and may contribute to the regulation of neural cell replacement processes in physiological plasticity and/or pathological circumstances.

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Pallial origin of basal forebrain cholinergic neurons in the nucleus basalis of Meynert and horizontal limb of the diagonal band nucleus

Cited by 29 publications

References 82 publications

Regulation of the Protocadherin Celsr3 Gene and Its Role in Globus Pallidus Development and Connectivity

Regulation of the Protocadherin Celsr3 Gene and Its Role in Globus Pallidus Development and Connectivity

Basal Forebrain Cholinergic Circuits and Signaling in Cognition and Cognitive Decline

Attractive action of FGF‐signaling contributes to the postnatal developing hippocampus

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