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On the development of non-pyramidal neurons and axons outside the cortical plate: The early marginal zone as a pallial anlage

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The development of non-pyramidal neurons was studied in the pallium of albino rats using autoradiography after thymidine labelling (determination of “birth dates”), Golgi impregnations (differentiation of dendrites and axons) and electron microscopy including 3D-reconstructions (cytoplasmic differentiation and early synaptogenesis).

The marginal zone appears between E13 and E14 and contains glial cells, axons and preneurons from the beginning. The latter can be identified by structural criteria (contacts, cytoplasm, nuclei). The first vertically oriented pyramidal neurons (cortical plate) appear within the marginal zone not before E16, separating its contents into a superficial (lamina I) and a deep portion (intermediate and subventricular zone). Since this old neuronal population of lamina I and the subcortical pallial region can be followed until adulthood, it is proposed to call the early marginal zone a “pallial anlage”. It can be demonstrated that during the whole period of neuron production (until E21) non-pyramidal neurons are added to all parts of the “pallial anlage”.

The structural differentiation of non-plate neurons is described. Neurons form specific, desmosome-like contacts with axonal growth cones already on E14. Typical synapses (vesicle aggregations) have been observed two days later. In lamina I two types of neurons develop: horizontal neurons (Cajal-Retzius cells) and multipolar neurons (small spiny stellate cells). Subcortical pallial neurons retain mostly their clear horizontal orientation. Only neurons situated very close to the lower border of the cortex show dendritic branches extending into lamina VI. Axons appearing early in the neocortex originate not only from subcortical regions, but also from neurons of the paleopallium, the archicortex, the limbic cortex and the neighbouring neocortex. The tangential growth of the neocortex, as estimated from E14 onwards causes a strong dilution of the elements of the “pallial anlage” until adulthood.

The classification of neurons outside the cortical plate and the fate of the total “pallial anlage” are discussed. As a consequence of these observations some modifications of the terminology of the Boulder Committee are proposed.

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Rickmann, M., Chronwall, B.M. & Wolff, J.R. On the development of non-pyramidal neurons and axons outside the cortical plate: The early marginal zone as a pallial anlage. Anat Embryol 151, 285–307 (1977). https://doi.org/10.1007/BF00318931

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