Trends in Neurosciences
Patterns of neuronal migration in the embryonic cortex
Section snippets
Dynamics of cortical assembly
The first postmitotic cortical neurons collect in an outside-in sequence to form a transient layer termed the preplate [8]. Subsequently-born neurons migrate into the preplate to form a new series of layers collectively known as the cortical plate, which thereby splits the preplate into a superficial layer, the marginal zone, and a deeper layer, the subplate. As additional waves of migrating neurons arrive in the cortical plate they bypass earlier-generated neurons to form the cortical layers
Non-cortical origin of cortical interneurons
Recent studies have demonstrated that many cortical interneurons originate in the basal ganglia primordia – the lateral, medial and caudal ganglionic eminences (LGE, MGE and CGE, respectively) – and migrate tangentially into the cerebral cortex. These include studies using dye labeling [18], retroviral lineage analysis or chimeric mice 19, 20, 21, as well as analysis of mutant mice lacking the transcription factors Dlx or Mash 1, which are normally expressed in the proliferative zone of the
Tangential migration of interneurons: distinct phases
Whereas all cortical interneurons arising in the MGE must migrate tangentially to reach the cortex, the migration pathways used by MGE cells change through development 25, 35. Early in rodent neurogenesis, GABA-expressing cells from the MGE migrate through the intermediate zone (IZ) of the ganglionic eminence and disperse to all cortical layers, whereas later-born cells migrate through the striatal VZ and SVZ to enter the cortex. Within the developing cortex, the initial bands of tangentially
Modes of radial migration in the developing neocortex
Cortical neurons that migrate radially into the cortical plate are thought to do so through one of two possible modes: translocation or locomotion. Translocating cells possess a relatively long pia-directed process that has a stable attachment with the pial surface or marginal zone 53, 54, 55, 56. The translocating cell moves its nucleus radially within this fixed process to reach an appropriate position in the cortex. By contrast, locomoting cells are freely migrating cells that have a
Pattern of radial migration in the cortex: distinct phases of locomotion
It has long been suspected that cortical pyramidal neurons arise from the proliferative zones of the dorsal telencephalon [75]. This has been confirmed in recent experiments including those based on cortical explants isolated from ventral telencephalon [13], fate-mapping studies of transgenic mice [14], and transcription factor expression in pyramidal neurons [15]. Recent studies using time-lapse imaging in slice cultures have demonstrated that neurons generated in the cortical proliferative
Transitions between phases of migration
Transitions between phases of migration might involve environmental signals and depend upon specific intracellular events. Moreover, specific neuronal migration disorders might involve failure of neurons to transition from one phase to another [7]. For example, the condition known as doublecortex (subcortical band heterotopia) could involve arrest of neurons in phase two of migration. Recent observations using in utero electroporation of VZ precursor cells with small-interfering RNA (siRNA) of
Birthdate-dependent laminar fate for both pyramidal neurons and interneurons
The cortex develops in an inside-out manner, with early-generated neurons occupying deep layers and late-generated neurons migrating beyond the early-generated neurons to occupy more superficial layers [9]. Birthdate labeling experiments confirm that cortical interneurons and pyramidal cells both follow the inside-out layering sequence 10, 11, 12. An exception appears to be the somatostatin-expressing interneurons that appear to be born early [82]. The realization that GABAergic neurons
Tangential dispersion of cortical-derived neurons could occur in phase two
Cortical neurons arise from radial glia 60, 61, 62, 63, 64 and daughter neurons often migrate along the parental fiber [60]. However, this is not the rule, and migrating neurons also travel along parallel adjacent paths, presumably using adjacent radial glial fiber guides 42, 88. In rodents, clonally related neurons become tangentially dispersed, particularly in the upper layers, as reflected by the conical appearance of columns of related cells in chimeric mouse models [20]. Using retroviral
Lower IZ–SVZ might favor tangential migration of both interneurons and pyramidal cells
Tangential migration occurs at all depths of the cortex, but particularly high percentages of tangentially migrating cells have been observed in the SVZ and lower IZ by most observers 19, 27, 29, 36, 45, 94. The neocortical SVZ and lower IZ have thus been proposed to serve as a main corridor for the tangential migration of cortical interneurons 27, 36. Interestingly, the lower IZ–SVZ also represents a decision point for radially migrating neurons, which pause in this region and either resume
Concluding remarks
Patterns of neuronal migration during cortical development appear more complicated than once thought. Cortical interneurons take a predominantly tangential path to reach the cortex and travel relatively long distances, whereas pyramidal cells take a predominantly radial path and reach the cortex more directly. Detailed studies of the dynamic movements of both cell types have revealed that cells undergo distinct phases in migration. The transitions between these phases might signal changes in
Acknowledgements
We thank Stewart Anderson and Tamily Weismann for helpful comments on the manuscript. This work was supported by the NIH and a grant from the Lieber Center (ARK).
References (94)
Cellular and molecular mechanisms of neuronal migration in neocortical development
Semin. Cell Dev. Biol.
(2003)- et al.
Neuronal migration disorders: from genetic diseases to developmental mechanisms
Trends Neurosci.
(2000) Cogeneration of retrogradely labeled corticocortical projection and GABA-immunoreactive local circuit neurons in cerebral cortex
Brain Res.
(1985)Separate progenitors for radial and tangential cell dispersion during development of the cerebral neocortex
Neuron
(1998)Correct coordination of neuronal differentiation events in ventral forebrain requires the bHLH factor MASH1
Mol. Cell. Neurosci.
(1999)Tangential migration in neocortical development
Dev. Biol.
(2002)- et al.
Cleavage orientation and the asymmetric inheritance of Notch1 immunoreactivity in mammalian neurogenesis
Cell
(1995) Cellular and molecular guidance of GABAergic neuronal migration from an extracortical origin to the neocortex
Neuron
(1999)Riding the glial monorail: a common mechanism for glial-guided neuronal migration in different regions of the developing mammalian brain
Trends Neurosci.
(1990)Asymmetric inheritance of radial glial fibers by cortical neurons
Neuron
(2001)
Radial glia is a progenitor of neocortical neurons in the developing cerebral cortex
Neurosci. Res.
The history of radial glia
Brain Res. Bull.
The earliest patterns of neuronal differentiation and migration in the mammalian central nervous system
Exp. Neurol.
The origin and migration of cortical neurones: new vistas
Trends Neurosci.
Doublecortin is a microtubule-associated protein and is expressed widely by migrating neurons
Neuron
Doublecortin is a developmentally regulated, microtubule-associated protein expressed in migrating and differentiating neurons
Neuron
Restriction of late cerebral cortical progenitors to an upper-layer fate
Neuron
Widespread tangential dispersion and extensive cell death during early neurogenesis in the mouse neocortex
Dev. Biol.
Systematic widespread clonal organization in cerebral cortex
Neuron
Developmental and evolutionary adaptations of cortical radial glia
Cereb. Cortex
New directions in neuronal migration
Science
Central nervous system neuronal migration
Annu. Rev. Neurosci.
Orchestration of neuronal migration by activity of ion channels, neurotransmitter receptors, and intracellular Ca2+ fluctuations
J. Neurobiol.
Human brain malformations and their lessons for neuronal migration
Annu. Rev. Neurosci.
Early prenatal ontogenesis of the cerebral cortex (neocortex) of the cat (Felis domestica). A Golgi study. I. The primordial neocortical organization
Z. Anat. Entwicklungsgesch.
Autoradiographic study of cell migration during histogenesis of cerebral cortex in the mouse
Nature
Times of generation of glutamic acid decarboxylase immunoreactive neurons in mouse somatosensory cortex
J. Comp. Neurol.
Genesis of GABA-immunoreactive neurons in the ferret visual cortex
J. Neurosci.
In vitro analysis of the origin, migratory behavior, and maturation of cortical pyramidal cells
J. Comp. Neurol.
Cortical excitatory neurons and glia, but not GABAergic neurons, are produced in the Emx1-expressing lineage
J. Neurosci.
Emx1 is a marker for pyramidal neurons of the cerebral cortex
Cereb. Cortex
Interneuron migration from basal forebrain to neocortex: dependence on dlx genes
Science
Origin and route of tangentially migrating neurons in the developing neocortical intermediate zone
J. Neurosci.
Dynamics of cell migration from the lateral ganglionic eminence in the rat
J. Neurosci.
The medial ganglionic eminence gives rise to a population of early neurons in the developing cerebral cortex
J. Neurosci.
Coexistence of widespread clones and large radial clones in early embryonic ferret cortex
Cereb. Cortex
Differential origins of neocortical projection and local circuit neurons: role of Dlx genes in neocortical interneuronogenesis
Cereb. Cortex
Mash1 regulates neurogenesis in the ventral telencephalon
Development
Distinct cortical migrations from the medial and lateral ganglionic eminences
Development
Control of cortical interneuron migration by neurotrophins and PI3-kinase signaling
Development
In utero fate mapping reveals distinct migratory pathways and fates of neurons born in the mammalian basal forebrain
Development
Young neurons from medial ganglionic eminence disperse in adult and embryonic brain
Nat. Neurosci.
The caudal ganglionic eminence is a source of distinct cortical and subcortical cell populations
Nat. Neurosci.
Different origins and developmental histories of transient neurons in the marginal zone of the fetal and neonatal rat cortex
J. Comp. Neurol.
Cortical interneuron fate determination: diverse sources for distinct subtypes?
Cereb. Cortex
Origin of GABAergic neurons in the human neocortex
Nature
Emerging complexity of layer I in human cerebral cortex
Cereb. Cortex
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