Does Cell Lineage in the Developing Cerebral Cortex Contribute to its Columnar Organization?

Edmond and Lily Safra International Institute of Neuroscience of Natal, Natal, Rio Grande do Norte Brazil.
Frontiers in Neuroanatomy (Impact Factor: 4.18). 06/2010; 4:26. DOI: 10.3389/fnana.2010.00026
Source: PubMed

ABSTRACT Since the pioneer work of Lorente de Nó, Ramón y Cajal, Brodmann, Mountcastle, Hubel and Wiesel and others, the cerebral cortex has been seen as a jigsaw of anatomic and functional modules involved in the processing of different sets of information. In fact, a columnar distribution of neurons displaying similar functional properties throughout the cerebral cortex has been observed by many researchers. Although it has been suggested that much of the anatomical substrate for such organization would be already specified at early developmental stages, before activity-dependent mechanisms could take place, it is still unclear whether gene expression in the ventricular zone (VZ) could play a role in the development of discrete functional units, such as minicolumns or columns. Cell lineage experiments using replication-incompetent retroviral vectors have shown that the progeny of a single neuroepithelial/radial glial cell in the dorsal telencephalon is organized into discrete radial clusters of sibling excitatory neurons, which have a higher propensity for developing chemical synapses with each other rather than with neighboring non-siblings. Here, we will discuss the possibility that the cell lineage of single neuroepithelial/radial glia cells could contribute for the columnar organization of the neocortex by generating radial columns of sibling, interconnected neurons. Borrowing some concepts from the studies on cell-cell recognition and transcription factor networks, we will also touch upon the potential molecular mechanisms involved in the establishment of sibling-neuron circuits.

Download full-text


Available from: Cecilia Hedin-Pereira, Aug 22, 2015
  • Source
    • "Such functional columns are often termed " barrels " or " intracortical modules " by neurophysiologists, and the pattern of dendritic bundles and of thalamocortical projections may determine their integrity (Feldmeyer et al., 2013; Li et al., 2013; Rockland and Ichinohe, 2004). Nevertheless, some investigators remain reserved or skeptical of the importance of functional columns in the mature brain (da Costa and Martin, 2010; Horton and Adams, 2005). In FCD1a, some areas of dysplastic cortex show no architectural organization, the neurons seemingly disoriented and displaced without recognizable vertical or horizontal lamination. "
    [Show abstract] [Hide abstract]
    ABSTRACT: Cerebral malformations are best understood as abnormal tissue morphogenesis in the context of disorders of ontogenesis. In neuroembryology, the timing of onset and duration of abnormal genetic expression and neurodevelopmental processes are primordial and must always be assessed, regardless whether the dysgenesis is primarily genetic in origin or acquired in utero due to ischemia, fetal infarcts that interrupt cellular migration or exposure to teratogenic drugs or neurotoxins. Defective timing interferes with the synchrony between different developmental processes, such as synaptogenesis in relation to other aspects of neuronal maturation. Timing may be delay or arrest development at an immature stage or may be precocious but asynchronous with other developmental features. Focal cortical dysplasia (FCD) types 1 and 3 may be arrested maturation of the radial microcolumnar neocortical architecture that is normal in the first half of gestation, without the expected transition to a horizontal or tangential laminar cortical architecture in the second half. Lack of lamination in either the vertical or horizontal planes may be due to defective extracellular adhesion molecules that cause detachment of migratory neuroblasts from their radial glial guide fibers, to enable recently arriving neuroblasts to bypass those already in place within the cortical plate for the programmed inside-out neuronal arrangement. FCD type 2 has a different pathogenesis. The megalocytic and dysmorphic neurons may result from somatic mutations of some, but not all, neuronal precursors in the periventricular region. FCD2 and hemimegalencephaly (HME) may have the same pathogenesis, the principal difference being timing of onset within the 33 mitotic cycles of the periventricular neuroepithelium to exponentially produce the total neuronal population of the cerebral cortex: if the mutation occurs during the late mitotic cycles, FCD2 results as a small dysgenesis; if the mutation occurs in the early mitotic cycles, the distribution of abnormal neurons is more extensive and HME may result. Why some cerebral malformations are more epileptogenic than others, despite similar histological features, remains enigmatic but probably involves differences in synaptic circuitry among individual cases.
    Progress in brain research 01/2014; 213C:181-198. DOI:10.1016/B978-0-444-63326-2.00010-7 · 5.10 Impact Factor
  • Source
    • "Both in vivo and in vitro experiments assure that a single neocortical progenitor generates multiple layer-specific subtypes . For example, in cell lineage tracing, a single progenitor generates clonally-related neurons that are radially distributed across the neocortical layers (Luskin et al. 1988; Price & Thurlow 1988; Walsh & Cepko 1990; Kornack & Rakic 1995; Reid et al. 1997; Noctor et al. 2001; Costa & Hedin-Pereira 2010). Preferential synaptic connections among these clonally related neurons are suggested to be the developmental basis for constructing the radial columnar unit of neural circuits (Yu et al. 2009, 2012; Li et al. 2012; Ohtsuki et al. 2012). "
    [Show abstract] [Hide abstract]
    ABSTRACT: The neocortex facilitates mammalian adaptive radiation by conferring highly sophisticated cognitive and motor abilities. A unique feature of the mammalian neocortex is its laminar structure in which similar neuronal subtypes are arranged in tangential layers and construct columnar circuits via interlaminar connections. The neocortical layer structure is completely conserved among all mammalian species, including monotremes and marsupials. However, this structure is missing in non-mammalian sister groups, such as birds and reptiles. The evolutionary origins of neocortical layers and cytoarchitectural borders have been the subject of debate over the past century. Using the chicken embryos as a model of evolutionary developmental biology (evo-devo model), we recently provided evidence suggesting that the evolutionary origin of layer-specific neuron subtypes predates the emergence of laminar structures. Based on this finding, we review the evolutionary conservation and divergence of neocortical development between mammals and non-mammals and discuss how the layered cytoarchitecture of the mammalian neocortex originated during evolution.
    Development Growth and Regeneration 12/2012; DOI:10.1111/dgd.12020 · 2.18 Impact Factor
  • Source
    • "Regulates Multipolar Cell Phase Transitions dispersion at the multipolar cell phase may also be critical for establishing intercolumnar cortical connectivity (Costa and Hedin-Pereira, 2010). Our work adds to these findings by demonstrating that the timing and duration of the multipolar phase is precisely regulated by FoxG1 activity. "
    [Show abstract] [Hide abstract]
    ABSTRACT: Pyramidal cells of the cerebral cortex are born in the ventricular zone and migrate through the intermediate zone to enter into the cortical plate. In the intermediate zone, these migrating precursors move tangentially and initiate the extension of their axons by transiently adopting a characteristic multipolar morphology. We observe that expression of the forkhead transcription factor FoxG1 is dynamically regulated during this transitional period. By utilizing conditional genetic strategies, we show that the downregulation of FoxG1 at the beginning of the multipolar cell phase induces Unc5D expression, the timing of which ultimately determines the laminar identity of pyramidal neurons. In addition, we demonstrate that the re-expression of FoxG1 is required for cells to transit out of the multipolar cell phase and to enter into the cortical plate. Thus, the dynamic expression of FoxG1 during migration within the intermediate zone is essential for the proper assembly of the cerebral cortex.
    Neuron 06/2012; 74(6):1045-58. DOI:10.1016/j.neuron.2012.04.025 · 15.98 Impact Factor
Show more