Subplate Neurons Pioneer the First Axon Pathway from the Cerebral Cortex

McConnell, Susan K.; Ghosh, Anirvan; Shatz, Carla J.

doi:10.1126/science.2475909

Cited by 621 publications

(421 citation statements)

References 27 publications

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“…Several studies have examined the early development of these projections and have identified pioneering axonal populations as well as potential intermediate targets and choice points for these axons (McConnell et al, 1989;De Carlos and O'Leary, 1992;Métin and Godement, 1996;Molnár et al, 1998;Braisted et al, 1999;Tuttle et al, 1999;Auladell et al, 2000;Ló pez-Bendito et al, 2006). In addition, multiple molecules that participate in the guidance of these connections have been identified, providing a comprehensive frame in which to understand their development (Serafini et al, 1996;Métin et al, 1997;Richards et al, 1997;Braisted et al, 2000;Leighton et al, 2001;Bagri et al, 2002;Ló pez-Bendito et al, 2006).…”

Section: Discussionmentioning

confidence: 99%

Robo1 and Robo2 Cooperate to Control the Guidance of Major Axonal Tracts in the Mammalian Forebrain

López‐Bendito¹,

Flames²,

Ma³

et al. 2007

J. Neurosci.

205

209

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The function of the nervous system depends on the precision of axon wiring during development. Previous studies have demonstrated that Slits, a family of secreted chemorepellent proteins, are crucial for the proper development of several major forebrain tracts. Mice deficient in Slit2 or, even more so, in both Slit1 and Slit2 have defects in multiple axonal pathways, including corticofugal, thalamocortical, and callosal connections. In the spinal cord, members of the Robo family of proteins help mediate the function of Slits, but the relative contribution of these receptors to the guidance of forebrain projections remains to be determined. In the present study, we addressed the function of Robo1 and Robo2 in the guidance of forebrain projections by analyzing Robo1-, Robo2-, and Robo1;Robo2-deficient mice. Mice deficient in Robo2 and, more dramatically, in both Robo1 and Robo2, display prominent axon guidance errors in the development of corticofugal, thalamocortical, and corticocortical callosal connections. Our results demonstrate that Robo1 and Robo2 mostly cooperate to mediate the function of Slit proteins in guiding the major forebrain projections.

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Section: Discussionmentioning

confidence: 99%

Robo1 and Robo2 Cooperate to Control the Guidance of Major Axonal Tracts in the Mammalian Forebrain

López‐Bendito¹,

Flames²,

Ma³

et al. 2007

J. Neurosci.

205

209

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“…There were two GABA-IR cell layers (the preplate and the lower I Z) in the early embryos (E14 -E15) and three layers (the marginal zone, the subplate, and the lower IZ) later, after the insertion of the cortical plate. The marginal zone contains different types of cells that have functions different from those of the subplate neurons (Shatz et al, 1988;McConnell et al, 1989McConnell et al, , 1990D'Arcangelo et al, 1995;Ogawa et al, 1995). Similarly, the subplate and the IZ were assumed to have different types of cells and different functions.…”

Section: Tangentially Migrating Map2-positive Cells Are a Distinct Pomentioning

confidence: 99%

Origin and Route of Tangentially Migrating Neurons in the Developing Neocortical Intermediate Zone

1997

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Neuroblasts produced in the ventricular zone of the neocortex migrate radially and form the cortical plate, settling in an insideout order. It is also well known that the tangential cell migration is not negligible in the embryonic neocortex. To have a better understanding of the tangential cell migration in the cortex, we disturbed the migration by making a cut in the neocortex, and we labeled the migrating cells with 1,1Ј-dioctodecyl-3,3,3Ј,3Ј-tetramethylindocarbocyanine perchlorate (DiI) in vivo and in vitro. We also determined the birth dates of the cells.Disturbance of tangential cell migration caused an accumulation and disappearance of microtubule-associated protein 2 immunoreactive (MAP2-IR) cells on the ventral and dorsal side of the cut, respectively, which indicated that most of the MAP2-IR cells in the intermediate zone (IZ) were migrating toward the dorsal cortex. The DiI injection study in vivo confirmed the tendency of the direction of cell migration and suggested the origin of the cells to be in the lateral ganglionic eminence (LGE). DiI injection into the LGE in vitro confirmed that the LGE cells cross the corticostriatal boundary and enter the IZ of the neocortex. The migrating cells acquired multipolar shape in the IZ of the dorsal cortex and seemed to reside there. A 5-bromo-deoxyuridine incorporation study revealed that the migrating MAP2-IR cells in the IZ were early-generated neurons. We concluded that the majority of tangentially migrating cells were generated in the LGE and identified as a distinct population that was assumed not to have joined the cortical plate.

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“…Layer 5 cells are born between E12 and E15.5 (Polleux et al, 1997) and migrate to the cortical plate until at least E18. It is believed that the first cell population to extend corticothalamic axons are the subplate neurons, followed shortly afterward by axons from the developing cortical plate (McConnell et al, 1989;De Carlos and O'Leary, 1992;Auladell et al, 2000). At E12, cortical axonal processes extend laterally and course in the intermediate zone parallel to the pial surface.…”

Section: Time Schedule For Development Of Thalamocortical and Corticomentioning

confidence: 99%

Connecting thalamus and cortex: The role of ephrins

et al. 2006

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The complex task of wiring up the brain during embryonic development is achieved by a multitude of guidance signals acting in complex combinations to drive growing axons to their proper targets. The somatosensory system provides an extensively studied model system featuring many universal mechanisms of neural development. In rodents, it constitutes an important model to study how precise topographic connections are achieved. Recent evidence suggests that the Eph/ephrin family of guidance molecules is of pivotal importance for the development of the somatosensory system. Members of Eph/ephrin family are thought to be involved in the global presorting of thalamic axons projecting to the cortex, in labeling specific cortical areas for innervation, in providing topographic cues within the target area, and in distinguishing cortical layers for intracortical wiring. The Eph/ephrin system also seems to contribute to the formation of specific corticothalamic feedback projections. So far, the functions of only a few members of the Eph/ephrin family have been examined, but expression analysis indicates complex combinatorial effects of these signaling molecules. Understanding the Eph/ephrin wiring code is expected to yield new insights into the development and plasticity of brain circuits involved in higher functions.

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Subplate Neurons Pioneer the First Axon Pathway from the Cerebral Cortex

Cited by 621 publications

References 27 publications

Robo1 and Robo2 Cooperate to Control the Guidance of Major Axonal Tracts in the Mammalian Forebrain

Robo1 and Robo2 Cooperate to Control the Guidance of Major Axonal Tracts in the Mammalian Forebrain

Origin and Route of Tangentially Migrating Neurons in the Developing Neocortical Intermediate Zone

Connecting thalamus and cortex: The role of ephrins

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