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: 4.06). 01/2010; 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.

  • Source
    [Show abstract] [Hide abstract]
    ABSTRACT: In various species and areas of the cerebral cortex, apical dendrites of pyramidal neurons form clusters which extend through several layers of the cortex also known as dendritic bundles. Previously, it has been shown that 5-HT(3A) receptor knockout mice show hypercomplex apical dendrites of cortical layer 2/3 pyramidal neurons, together with a reduction in reelin levels, a glycoprotein involved in cortical development. Other studies showed that in the mouse presubicular cortex, reelin is involved in the formation of modular structures. Here, we compare apical dendrite bundling in the somatosensory cortex of wildtype and 5-HT(3A) receptor knockout mice. Using a microtubule associated protein-2 immunostaining to visualize apical dendrites of pyramidal neurons, we compared dendritic bundle properties of wildtype and 5-HT(3A) receptor knockout mice in tangential sections of the somatosensory cortex. A Voronoi tessellation was performed on immunostained tangential sections to determine the spatial organization of dendrites and to define dendritic bundles. In 5-HT(3A) receptor knockout mice, dendritic bundle surface was larger compared to wildtype mice, while the number and distribution of reelin-secreting Cajal-Retzius cells was similar for both groups. Together with previously observed differences in dendritic complexity of cortical layer 2/3 pyramidal neurons and cortical reelin levels, these results suggest an important role for the 5-HT(3) receptor in determining the spatial organization of cortical connectivity in the mouse somatosensory cortex.
    Frontiers in Neuroanatomy 01/2011; 5:64. · 4.06 Impact Factor
  • Source
    [Show abstract] [Hide abstract]
    ABSTRACT: The mature neocortex contains many different classes of GABAergic inhibitory interneurons, distributed, with some degree of selectivity, through six layers, and through many different regions. Some of the events in the early lives of these neurones that may determine their ultimate destination, their maturation and their selective innervation of targets appropriate for each subtype, are discussed. Both time and place of birth influence the class of interneuron that an early post-mitotic interneuronal precursor will become, driven by the selective expression of different combinations of transcription factors in different regions of their birth places in the ganglionic eminence and ventricular zone. The long distance migration of these precursors along tangential routes in marginal, subventricular, and intermediate zones and their final radial movement, into the developing cortex, is regulated by chemical cues, both attractant and repellent. Once they arrive at their final destination, they must integrate into the developing circuitry. As they mature within the cortex, their axons grow and branch in highly specific patterns that may be partially determined by the genetic blueprint for each interneuronal class and partly by the environment in which they find themselves. Finally, as each interneuron class begins to form synapses with only certain postsynaptic targets, cell-cell recognition, most probably via protein-protein interactions across the synaptic cleft, facilitate the formation of appropriate synapses.
    Frontiers in Cellular Neuroscience 01/2011; 5:14. · 4.47 Impact Factor
  • Source
    [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.
    Embryologia 12/2012; · 2.21 Impact Factor

Full-text (2 Sources)

Available from
May 20, 2014