Neuronal Migration Dynamics in the Developing Ferret Cortex. Gertz, C. C & Kriegstein, A. R J Neurosci, 35(42):14307–14315, October, 2015.
abstract   bibtex   
During mammalian neocortical development, newborn excitatory and inhibitory neurons must migrate over long distances to reach their final positions within the cortical plate. In the lissencephalic rodent brain, pyramidal neurons are born in the ventricular and subventricular zones of the pallium and migrate along radial glia fibers to reach the appropriate cortical layer. Although much less is known about neuronal migration in species with a gyrencephalic cortex, retroviral studies in the ferret and primate suggest that, unlike the rodent, pyramidal neurons do not follow strict radial pathways and instead can disperse horizontally. However, the means by which pyramidal neurons laterally disperse remain unknown. In this study, we identified a viral labeling technique for visualizing neuronal migration in the ferret, a gyrencephalic carnivore, and found that migration was predominantly radial at early postnatal ages. In contrast, neurons displayed more tortuous migration routes with a decreased frequency of cortical plate-directed migration at later stages of neurogenesis concomitant with the start of brain folding. This was accompanied by neurons migrating sequentially along several different radial glial fibers, suggesting a mode by which pyramidal neurons may laterally disperse in a folded cortex. These findings provide insight into the migratory behavior of neurons in gyrencephalic species and provide a framework for using nonrodent model systems for studying neuronal migration disorders. SIGNIFICANCE STATEMENT: Elucidating neuronal migration dynamics in the gyrencephalic, or folded, cortex is important for understanding neurodevelopmental disorders. Similar to the rodent, we found that neuronal migration was predominantly radial at early postnatal ages in the gyrencephalic ferret cortex. Interestingly, ferret neurons displayed more tortuous migration routes and a decreased frequency of radial migration at later ages coincident with the start of cortical folding. We found that ferret neurons use several different radial glial fibers as migratory guides, including those belonging to the recently described outer radial glia, suggesting a mechanism by which ferret neurons disperse laterally. It is likely that excitatory neurons horizontally disperse in other gyrencephalic mammals, including the primate, suggesting an important modification to the current model deduced primarily from the rodent.
@ARTICLE{Gertz2015-pp,
  title    = "Neuronal Migration Dynamics in the Developing Ferret Cortex",
  author   = "Gertz, Caitlyn C and Kriegstein, Arnold R",
  abstract = "During mammalian neocortical development, newborn excitatory and
              inhibitory neurons must migrate over long distances to reach
              their final positions within the cortical plate. In the
              lissencephalic rodent brain, pyramidal neurons are born in the
              ventricular and subventricular zones of the pallium and migrate
              along radial glia fibers to reach the appropriate cortical layer.
              Although much less is known about neuronal migration in species
              with a gyrencephalic cortex, retroviral studies in the ferret and
              primate suggest that, unlike the rodent, pyramidal neurons do not
              follow strict radial pathways and instead can disperse
              horizontally. However, the means by which pyramidal neurons
              laterally disperse remain unknown. In this study, we identified a
              viral labeling technique for visualizing neuronal migration in
              the ferret, a gyrencephalic carnivore, and found that migration
              was predominantly radial at early postnatal ages. In contrast,
              neurons displayed more tortuous migration routes with a decreased
              frequency of cortical plate-directed migration at later stages of
              neurogenesis concomitant with the start of brain folding. This
              was accompanied by neurons migrating sequentially along several
              different radial glial fibers, suggesting a mode by which
              pyramidal neurons may laterally disperse in a folded cortex.
              These findings provide insight into the migratory behavior of
              neurons in gyrencephalic species and provide a framework for
              using nonrodent model systems for studying neuronal migration
              disorders. SIGNIFICANCE STATEMENT: Elucidating neuronal migration
              dynamics in the gyrencephalic, or folded, cortex is important for
              understanding neurodevelopmental disorders. Similar to the
              rodent, we found that neuronal migration was predominantly radial
              at early postnatal ages in the gyrencephalic ferret cortex.
              Interestingly, ferret neurons displayed more tortuous migration
              routes and a decreased frequency of radial migration at later
              ages coincident with the start of cortical folding. We found that
              ferret neurons use several different radial glial fibers as
              migratory guides, including those belonging to the recently
              described outer radial glia, suggesting a mechanism by which
              ferret neurons disperse laterally. It is likely that excitatory
              neurons horizontally disperse in other gyrencephalic mammals,
              including the primate, suggesting an important modification to
              the current model deduced primarily from the rodent.",
  journal  = "J Neurosci",
  volume   =  35,
  number   =  42,
  pages    = "14307--14315",
  month    =  oct,
  year     =  2015,
  keywords = "ferret; gyrencephaly; neuronal migration",
  language = "en"
}
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