Neuronal migration in the developing cerebral cortex: observations based on real-time imaging.

We have used time-lapse imaging of acute cortical slices to study the migration of neurons from their sites of origin to their positions in the developing neocortex. We found that two distinct modes of cell movement, somal translocation and glia-guided locomotion, are responsible for the radial migration of neurons generated in the cortical ventricular zone. The former is the prevalent form of radial movement of the early-born cortical neurons, while the latter is adopted by those generated later in corticogenesis. Interneurons, found to originate in the ganglionic eminence, follow tangential migratory paths to reach the developing cortex. Upon reaching the cortex, these cells seek the ventricular zone using a mode of movement that we have termed 'ventricle-directed migration', before they migrate to their positions in the cortical plate. In addition to these forms of movement, we report here a unique morphological and migratory behavior for a population of cortical neurons. These cells are multipolar in form, and are highly motile in the formation and retraction of their processes. Based on these morphological features, we refer to this type of cells as 'branching cells' and attribute the phenotype to a subset of cortical interneurons.

[1]  P. Rakić.  Mode of cell migration to the superficial layers of fetal monkey neocortex , 1972, The Journal of comparative neurology.

[2]  V. Caviness,et al.  The alignment of migrating neural cells in relation to the murine neopallial radial glial fiber system. , 1991, Cerebral cortex.

[3]  John G. Parnavelas,et al.  Modes of neuronal migration in the developing cerebral cortex , 2002, Nature Reviews Neuroscience.

[4]  L. Tsai,et al.  Mice Lacking p35, a Neuronal Specific Activator of Cdk5, Display Cortical Lamination Defects, Seizures, and Adult Lethality , 1997, Neuron.

[5]  Leyuan Shi,et al.  Interneuron migration from basal forebrain to neocortex: dependence on Dlx genes. , 1997, Science.

[6]  M. Mione,et al.  Cell Fate Specification and Symmetrical/Asymmetrical Divisions in the Developing Cerebral Cortex , 1997, The Journal of Neuroscience.

[7]  M. Marín‐padilla.  Dual origin of the mammalian neocortex and evolution of the cortical plate , 1978, Anatomy and Embryology.

[8]  A. Lavdas,et al.  The Medial Ganglionic Eminence Gives Rise to a Population of Early Neurons in the Developing Cerebral Cortex , 1999, The Journal of Neuroscience.

[9]  S. Mcconnell,et al.  Distinct origins of neocortical projection neurons and interneurons in vivo. , 2002, Cerebral cortex.

[10]  B. Reese,et al.  Cell dispersion patterns in different cortical regions studied with an X-inactivated transgenic marker. , 1995, Development.

[11]  G. Fishell,et al.  In utero fate mapping reveals distinct migratory pathways and fates of neurons born in the mammalian basal forebrain. , 2001, Development.

[12]  P. Rakic,et al.  Origin of GABAergic neurons in the human neocortex , 2002, Nature.

[13]  M. Gulisano,et al.  Emx1 is a marker for pyramidal neurons of the cerebral cortex. , 2001, Cerebral cortex.

[14]  A. W. Rogers,et al.  The migration of neuroblasts in the developing cerebral cortex. , 1965, Journal of anatomy.

[15]  C. Cepko,et al.  Clonal dispersion in proliferative layers of developing cerebral cortex , 1993, Nature.

[16]  S. Mcconnell,et al.  Diverse migratory pathways in the developing cerebral cortex. , 1992, Science.

[17]  Jaime Grutzendler,et al.  Two modes of radial migration in early development of the cerebral cortex , 2001, Nature Neuroscience.

[18]  J. Silver,et al.  The Earliest Patterns of Neuronal Differentiation and Migration in the Mammalian Central Nervous System , 1995, Experimental Neurology.

[19]  P. Rakić.  Neurons in Rhesus Monkey Visual Cortex: Systematic Relation between Time of Origin and Eventual Disposition , 1974, Science.

[20]  K. Herrup,et al.  Cyclin-Dependent Kinase 5-Deficient Mice Demonstrate Novel Developmental Arrest in Cerebral Cortex , 1998, The Journal of Neuroscience.

[21]  O. Marín,et al.  Loss of Nkx2.1 homeobox gene function results in a ventral to dorsal molecular respecification within the basal telencephalon: evidence for a transformation of the pallidum into the striatum. , 1999, Development.

[22]  M. Jacobson,et al.  Embryonic vertebrate central nervous system: Revised terminology , 1970 .

[23]  G. Shoukimas,et al.  The development of the cerebral cortex in the embryonic mouse: An electron microscopic serial section analysis , 1978, The Journal of comparative neurology.

[24]  B. Reese,et al.  Separate Progenitors for Radial and Tangential Cell Dispersion during Development of the Cerebral Neocortex , 1998, Neuron.

[25]  P. C. Murphy,et al.  Cerebral Cortex , 2017, Cerebral Cortex.

[26]  D. Morest.  A study of neurogenesis in the forebrain of opossum pouch young , 2004, Zeitschrift für Anatomie und Entwicklungsgeschichte.

[27]  R. Wong,et al.  Ventricle-directed migration in the developing cerebral cortex , 2002, Nature Neuroscience.

[28]  P. Rakic,et al.  Principles of neural cell migration , 1990, Experientia.

[29]  John G. Parnavelas,et al.  The origin and migration of cortical neurones: new vistas , 2000, Trends in Neurosciences.

[30]  A. Goffinet.  The embryonic development of the cortical plate in reptiles: A comparative study in Emys orbicularis and Lacerta agilis , 1983, The Journal of comparative neurology.