Riding the Glial Monorail:a Common Mechanism for Glial-Guided Migration in Different Regions of the Developing Brain

Department of Pathology, College of Physicians and Surgeons of Columbia University, New York, NY 10032.
Trends in Neurosciences (Impact Factor: 13.56). 06/1990; 13(5):179-84. DOI: 10.1016/0166-2236(90)90044-B
Source: PubMed


In vitro studies from our laboratory indicate that granule neurons, purified from early postnatal mouse cerebellum, migrate on astroglial fibers by forming a 'migration junction' with the glial fiber along the length of the neuronal soma and extending a motile 'leading process' in the direction of migration. Similar dynamics are seen for hippocampal neurons migrating along hippocampal astroglial fibers in vitro. In heterotypic recombinations of neurons and glia from mouse cerebellum and rat hippocampus, neurons migrate on astroglial processes with a cytology and neuron-glia relationship identical to that of homotypic neuronal migration in vitro. In all four cases, the migrating neuron presents a stereotyped posture, speed and mode of movement, suggesting that glial fibers provide a generic pathway for neuronal migration in developing brain. Studies on the molecular basis of glial-guided migration suggest that astrotactin, a neuronal antigen that functions as a neuron-glia ligand, is likely to play a crucial role in the locomotion of the neuron along glial fibers. The navigation of neurons from glial fibers into cortical layers, in turn, is likely to involve neuron-neuron adhesion ligands.

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    • "During the embryogenesis of Amniota, magnocellular neurons possibly migrate along radial glia from the 3rd ventricle into ventro-lateral direction; the association of radial glia and magnocellular neurons was reported in the wallaby, the representative of marsupial mammals (Cheng et al., 2002). Similar migrations are known for the radial development of spinal cord, cerebellum and cortex (Hatten, 1999; Nadarajah and Parnavelas, 2002; McDermott et al., 2005) and are also observable in cell culture studies where neuroblasts migrate back and forth until finding their destination (Hatten, 1990). The bidirectional movement of magnocellular neurons might have been physically blocked by the growing fibers of the solid medial forebrain bundle (phylogenetically evolving in amphibians and reptiles; Herrick, 1910; Nieuwenhuys et al., 1982), thereby hindering neuronal migration from the supraoptic region back to the 3rd ventricle and entrapping cells (i.e., SON) latero-dorsally to the optic tract. "
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    ABSTRACT: The central oxytocin system transformed tremendously during the evolution, thereby adapting to the expanding properties of species. In more basal vertebrates (paraphyletic taxon Anamnia, which includes agnathans, fish and amphibians), magnocellular neurosecretory neurons producing homologs of oxytocin reside in the wall of the third ventricle of the hypothalamus composing a single hypothalamic structure, the preoptic nucleus. This nucleus further diverged in advanced vertebrates (monophyletic taxon Amniota, which includes reptiles, birds, and mammals) into the paraventricular and supraoptic nuclei with accessory nuclei (AN) between them. The individual magnocellular neurons underwent a process of transformation from primitive uni- or bipolar neurons into highly differentiated neurons. Due to these microanatomical and cytological changes, the ancient release modes of oxytocin into the cerebrospinal fluid were largely replaced by vascular release. However, the most fascinating feature of the progressive transformations of the oxytocin system has been the expansion of oxytocin axonal projections to forebrain regions. In the present review we provide a background on these evolutionary advancements. Furthermore, we draw attention to the non-synaptic axonal release in small and defined brain regions with the aim to clearly distinguish this way of oxytocin action from the classical synaptic transmission on one side and from dendritic release followed by a global diffusion on the other side. Finally, we will summarize the effects of oxytocin and its homologs on pro-social reproductive behaviors in representatives of the phylogenetic tree and will propose anatomically plausible pathways of oxytocin release contributing to these behaviors in basal vertebrates and amniots.
    Frontiers in Behavioral Neuroscience 02/2014; 8:31. DOI:10.3389/fnbeh.2014.00031 · 3.27 Impact Factor
    • "), with subsequent development involving rapid cell proliferation and differentiation into various brain cell types. Once neurons are formed, glial cells guide their migration into the developing cortex (Hatten 1990). It has been suggested that these processes of neuron production and migration are roughly completed by midgestation (~20 weeks) (Stiles and Jernigan 2010). "
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    ABSTRACT: The human brain comprises distributed cortical regions that are structurally and functionally connected into a network that is known as the human connectome. Elaborate developmental processes starting in utero herald connectome genesis, with dynamic changes in its architecture continuing throughout life. Connectome changes during development, maturation, and aging may be governed by a set of biological rules or algorithms, forming and shaping the macroscopic architecture of the brain's wiring network. To explore the presence of developmental patterns indicative of such rules, this review considers insights from studies on the cellular and the systems level into macroscopic connectome genesis and dynamics across the life span. We observe that in parallel with synaptogenesis, macroscopic connectome formation and transformation is characterized by an initial overgrowth and subsequent elimination of cortico-cortical axonal projections. Furthermore, dynamic changes in connectome organization throughout the life span are suggested to follow an inverted U-shaped pattern, with an increasingly integrated topology during development, a plateau lasting for the majority of adulthood and an increasingly localized topology in late life. Elucidating developmental patterns in brain connectivity is crucial for our understanding of the human connectome and how it may give rise to brain function, including the occurrence of brain network disorders across the life span.
    The Neuroscientist 09/2013; 19(6). DOI:10.1177/1073858413503712 · 6.84 Impact Factor
    • "NPCs migrate long distances (3–5 mm in rodents) from the SVZ to the olfactory cell layers. Unlike neuronal migration during development (Hatten, 1990, 1993, 1999), NPCs of the adult SVZ and RMS migrate without guidance of glial or axonal processes (Alvarez-Buylla et al., 1987; Jankovski and Sotelo, 1996; Lois et al., 1996; Doetsch et al., 1997). Chains of NPCs line the wall of the entire rostrocaudal axis of the lateral ventricles (Doetsch and Alvarez-Buylla, 1996; Doetsch et al., 1997), migrating tangentially, parallel to the walls of brain ventricles (O'Rourke et al., 1992) and merge to migrate as chains along the RMS through the brain parenchyma (Rousselot et al., 1995; Jankovski and Sotelo, 1996; Lois et al., 1996; Peretto et al., 1997). "
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    ABSTRACT: Adult neural precursor cells (NPCs) are predominantly located in the subventricular zone (SVZ) of the lateral ventricles or in the subgranular zone of the dentate gyrus. These NPCs produce neuroblasts that normally migrate and integrate into the olfactory bulb and hippocampus, respectively. Following CNS damage due to disease or injury, NPCs can also migrate to the site of damage. Enhancement of NPC migration to sites of neural damage may increase their potential for repair but requires an understanding of processes that regulate basal and injury-induced migration so we can harness this potential. This review highlights the extrinsic factors and major intrinsic signalling pathways that regulate endogenous basal NPC migration to the olfactory bulb and the role of inflammatory mediators and chemokines in disease and injury-induced NPC migration.
    Neurochemistry International 09/2011; 59(3):382-93. DOI:10.1016/j.neuint.2010.12.024 · 3.09 Impact Factor
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