Extensive branching of radially‐migrating neurons in the mammalian cerebral cortex

Self Cite

The evolution of the mammalian cerebral cortex leading to humans involved a remarkable sophistication of developmental mechanisms. Specific adaptations of progenitor cell proliferation and neuronal migration mechanisms have been proposed to play major roles in this evolution of neocortical development. One of the central elements influencing neocortex development is the extracellular matrix (ECM). The ECM provides both a structural framework during tissue formation and to present signaling molecules to cells, which directly influences cell behavior and movement. Here we review recent advances in the understanding of the role of ECM molecules on progenitor cell proliferation and neuronal migration, and how these contribute to cerebral cortex expansion and folding. We discuss how transcriptomic studies in human, ferret and mouse identify components of ECM as being candidate key players in cortex expansion during development and evolution. Then we focus on recent functional studies showing that ECM components regulate cortical progenitor cell proliferation, neuron migration and the mechanical properties of the developing cortex. Finally, we discuss how these features differ between lissencephalic and gyrencephalic species, and how the molecular evolution of ECM components and their expression profiles may have been fundamental in the emergence and evolution of cortex folding across mammalian phylogeny.

Section: Evolution Of Ecm Components and The Evolution Of Cortical Fomentioning

confidence: 89%

The Extracellular Matrix in the Evolution of Cortical Development and Folding

Amin

Borrell

2020

Self Cite

“…The morphology of the leading process varies in different migrating neuronal types, which is considered to reflect an adaptation to the local migratory requirements ( Marin et al, 2010 ; Valiente and Marin, 2010 ). While the majority of radially migrating pyramidal neurons exhibit a simple single leading process ( Martínez-Martínez et al, 2019 ), fast tangentially migrating neurons display a more complex leading process with branched morphologies ( Bellion et al, 2005 ). One cannot exclude the possibility that the differences in the morphodynamics of radial migration is partly correlated to changes in geometry and/or adhesive properties of the extracellular environment in the SP.…”

Section: Discussionmentioning

confidence: 99%

Radial Migration Dynamics Is Modulated in a Laminar and Area-Specific Manner During Primate Corticogenesis

Cortay

Delaunay

Patti

et al. 2020

The orderly radial migration of cortical neurons from their birthplace in the germinal zones to their final destination in the cortical plate is a prerequisite for the functional assembly of microcircuits in the neocortex. Rodent and primate corticogenesis differ both quantitatively and qualitatively, particularly with respect to the generation of neurons of the supragranular layers. Marked area differences in the outer subventricular zone progenitor cell density impact the radial glia scaffold compactness which is likely to induce area differences in radial migration strategy. Here, we describe specific features of radial migration in the non-human primate, including the absence of the premigratory multipolar stage found in rodents. Ex vivo approaches in the embryonic macaque monkey visual cortex, show that migrating neurons destined for supragranular and infragranular layers exhibit significant differences in morphology and velocity. Migrating neurons destined for the supragranular layers show a more complex bipolar morphology and higher motility rates than do infragranular neurons. There are area differences in the gross morphology and membrane growth behavior of the tip of the leading process. In the subplate compartment migrating neurons destined for the supragranular layers of presumptive area 17 exhibit radial constrained trajectories and leading processes with filopodia, which contrast with the meandering trajectories and leading processes capped by lamellipodia observed in the migrating neurons destined for presumptive area 18. Together these results present evidence that migrating neurons may exhibit autonomy and in addition show marked area-specific differences. We hypothesize that the low motility and high radial trajectory of area 17 migrating neurons contribute to the unique structural features of this area.

“…Moreover, a recent study has shown that most of the bipolar neurons exhibit a branched leading process in the ferret, and to a lesser extent in the mouse. These branched processes are less parallel to radial fibers, do not affect radial migration, and importantly, seem to be involved in the remarkable lateral dispersion that occurs in folded cortices (Martínez-Martínez et al, 2019). Indeed, both the dynamic branching and filopodia formation that are observed in the leading process are similar features to those found in neurons exploring their environment during axon guidance (Dent et al, 2011).…”

Section: Tangential Distributionmentioning

confidence: 83%

FLRTing Neurons in Cortical Migration During Cerebral Cortex Development

Peregrina

Toro

2020

During development, two coordinated events shape the morphology of the mammalian cerebral cortex, leading to the cortex's columnar and layered structure: the proliferation of neuronal progenitors and cortical migration. Pyramidal neurons originating from germinal zones migrate along radial glial fibers to their final position in the cortical plate by both radial migration and tangential dispersion. These processes rely on the delicate balance of intercellular adhesive and repulsive signaling that takes place between neurons interacting with different substrates and guidance cues. Here, we focus on the function of the cell adhesion molecules fibronectin leucine-rich repeat transmembrane proteins (FLRTs) in regulating both the radial migration of neurons, as well as their tangential spread, and the impact these processes have on cortex morphogenesis. In combining structural and functional analysis, recent studies have begun to reveal how FLRT-mediated responses are precisely tuned-from forming different protein complexes to modulate either cell adhesion or repulsion in neurons. These approaches provide a deeper understanding of the context-dependent interactions of FLRTs with multiple receptors involved in axon guidance and synapse formation that contribute to finely regulated neuronal migration.