The cellular kinetics of the developing mouse cerebellum. II. The function of the external granular layer in the process of gyrification

Maresˇ, V.; Lodin, Z

doi:10.1016/0006-8993(70)90061-2

Cited by 102 publications

(49 citation statements)

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“…Our discovery supports a previously proposed model that positioning of the fissures is determined by interactions between PCs and mossy fibers as well as GC parallel fibers (Altman and Bayer, 1997). Another theory for the mechanism of foliation is that differential rates of proliferation in the EGL (with a greater rate in the depths of the fissures) causes buckling forces to generate fissures (Mares and Lodin, 1970). Although we cannot exclude this model, as Shh signaling is even along the base and the crown of the lobules (Corrales et al, 2004), Shh does not appear to influence the complexity of foliation by regulating the rate of proliferation.…”

Section: Discussionmentioning

confidence: 92%

“…The foliation pattern elaborates for 2 weeks after birth in mouse and 3 weeks in rat. Although a number of theories have been proposed (Lauder et al, 1974;Mares and Lodin, 1970), it remains unknown how the conserved position of the fissures is determined, and what genetic mechanisms regulate the size and complexity of the lobes. It is also not known whether positioning of the folia and regulation of the number of fissures are independent or inter-related events.…”

Section: Introductionmentioning

confidence: 99%

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The level of sonic hedgehog signaling regulates the complexity of cerebellar foliation

et al. 2006

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Foliation of the mouse cerebellum occurs primarily during the first 2 weeks after birth and is accompanied by tremendous proliferation of granule cell precursors (GCPs). We have previously shown that sonic hedgehog (Shh) signaling correlates spatially and temporally with fissure formation, and that Gli2 is the main activator driving Shh induced proliferation of embryonic GCPs. Here, we have tested whether the level of Shh signaling regulates the extent of cerebellar foliation. By progressively lowering signaling by removing Gli1 and Gli2 or the Shh receptor smoothened, we found the extent of foliation is gradually reduced, and that this correlates with a decrease in the duration of GCP proliferation. Importantly, the pattern of the remaining fissures in the mutants corresponds to the first fissures that form during normal development. In a complementary manner, an increase in the level and length of Shh signaling results in formation of an extra fissure in a position conserved in rat. The complexity of cerebellar foliation varies greatly between vertebrate species. Our studies have uncovered a mechanism by which the level and length of Shh signaling could be integral to determining the distinct number of fissures in each species.

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Section: Discussionmentioning

confidence: 92%

Section: Introductionmentioning

confidence: 99%

The level of sonic hedgehog signaling regulates the complexity of cerebellar foliation

et al. 2006

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“…This shifted GCP proliferation period probably explains the abnormal cerebellar foliation observed in Plexin-B2 Ϫ/Ϫ mutants (Mares and Lodin, 1970;Millen et al, 1995). More importantly, proliferating cells that express markers of differentiated GCs are found in Plexin-B2 Ϫ/Ϫ mutants within the cerebellum parenchyma and around ectopic Purkinje cells.…”

Section: B2mentioning

confidence: 99%

Plexin-B2 Controls the Development of Cerebellar Granule Cells

Friedel¹,

Kerjan²,

Rayburn³

et al. 2007

J. Neurosci.

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Cerebellar granule cell progenitors proliferate postnatally in the upper part of the external granule cell layer (EGL) of the cerebellum. Postmitotic granule cells differentiate and migrate, tangentially in the EGL and then radially through the molecular and Purkinje cell layers. The molecular control of the transition between proliferation and differentiation in cerebellar granule cells is poorly understood. We show here that the transmembrane receptor Plexin-B2 is expressed by proliferating granule cell progenitors. To study Plexin-B2 function, we generated a targeted mutation of mouse Plexin-B2. Most Plexin-B2 Ϫ/Ϫ mutants die at birth as a result of neural tube closure defects. Some mutants survive but their cerebellum cytoarchitecture is profoundly altered. This is correlated with a disorganization of the timing of granule cell proliferation and differentiation in the EGL. Many differentiated granule cells migrate inside the cerebellum and keep proliferating. These results reveal that Plexin-B2 controls the balance between proliferation and differentiation in granule cells.

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“…In this hypothesis, the tangential expansion of cortical regions, which is driven by the local augmented proliferation of cells and changes in cell sizes and shapes, is assumed to be the driving force for cerebral convolutional development (Mares and Lodin, 1970; Caviness, 1975;Smart and McSherry, 1986;Ronan et al, 2013). Thus, forces driving brain folding are predominantly intracortical.…”

Section: Differential Expansion Hypothesismentioning

confidence: 99%

The mechanical control of nervous system development

2013

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The development of the nervous system has so far, to a large extent, been considered in the context of biochemistry, molecular biology and genetics. However, there is growing evidence that many biological systems also integrate mechanical information when making decisions during differentiation, growth, proliferation, migration and general function. Based on recent findings, I hypothesize that several steps during nervous system development, including neural progenitor cell differentiation, neuronal migration, axon extension and the folding of the brain, rely on or are even driven by mechanical cues and forces.Key words: Mechanics, Mechanosensitivity, Mechanotaxis, Mechanotransduction, Stiffness, Force, Tension, Brain folding Introduction Many processes in development involve growth and motion on different length and time scales. All of these processes are driven by forces; the development of organisms and organ systems would not proceed without mechanics. For example, during neuronal development, neurons migrate and extend immature processes (neurites), which become axons and dendrites. Axons then grow in two different phases, both of which are distinguished by the nature of the forces that drive the growth. In the first phase, growth cones at the tips of axonal processes actively exert forces on their environment (Betz et al., 2011), thus pulling on the processes (Lamoureux et al., 1989). In a second phase, after connecting with their target tissue, axons may be passively pulled by the increasing distance between target and nervous tissue, resulting in considerable growth in length, a process referred to as stretch growth (Weiss, 1941). Once the final connectivity is established, tension may develop along neuronal axons, which may be involved in neuronal network formation and the folding of the brain. Apart from this direct requirement of forces for developmental processes, which has been studied to some degree in the past, the mechanical interaction of cells with their environment may add an additional level of control to several processes in the developing nervous system, including progenitor cell differentiation and cellular guidance.The idea of an important contribution of mechanics to the development of the nervous system has been around for more than a century. However, recent decades have seen only little progress in this field compared with other (e.g. electrophysiology, molecular biology or genetics-based) areas of neuroscience. Progress often depends on the availability of appropriate methodology. Only recently has the increasing involvement of physical and engineering approaches in interdisciplinary studies of biological systems led to the development of new techniques and conceptual approaches that can be used to quantitatively probe and control relevant mechanical parameters, such as cell and tissue stiffness, cellular forces, and tension. In recent years, such tissue mechanics-based studies have resulted in an increasing awareness of the importance of physical parameters, particularly in developm...

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The cellular kinetics of the developing mouse cerebellum. II. The function of the external granular layer in the process of gyrification

Cited by 102 publications

References 5 publications

The level of sonic hedgehog signaling regulates the complexity of cerebellar foliation

The level of sonic hedgehog signaling regulates the complexity of cerebellar foliation

Plexin-B2 Controls the Development of Cerebellar Granule Cells

The mechanical control of nervous system development

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