Construction of a polarized neuron

Abstract

Aside from rare counterexamples (e.g. the starburst amacrine cell in retina), neurons are polarized into two compartments, dendrites and axon, which are linked at the cell body. This structural polarization carries an underlying molecular definition and maps into a general functional polarization whereby inputs are collected by the dendrites and cell body, and output is distributed via the axon. Explanations of how the polarized structure arises invariably coalesce around somatic polarity, defined by the roving location of the microtubule organizing centre, or centrosome, the Golgi apparatus, associated endosomes and the nucleus during early development. In some neurons, proper positioning of these structures can determine the sites for axon and dendrite elongation, and support processes that underlie cell migration. We briefly review these events as a basis to propose a new role for polarized arrangement of somatic organelles as a potential determinant for patterned innervation of the cell body membrane. We cite an example from preliminary studies of synaptogenesis at the calyx of Held, a large nerve terminal that selectively innervates the cell body of its postsynaptic partner, and suggest other neural systems in which polarity mechanisms may guide initial synapse formation onto the somatic surface.

Figure 1. Polarity of somatic organelles at multiple stages of neuron development

A, during mitosis, intra-somatic polarity is defined by centrosome (light blue) position at opposite poles of cells aligned with reforming Golgi apparatus (green) and nucleus (red). B, prior to radial migration, neurons enter a bipolar phase with extension of an axon from the region of the soma (red) nearest the centrosome and Golgi apparatus. Microtubules (black) in the nascent axon are extended from nucleation sites in either the centrosome or Golgi apparatus. The second process typically emits at the opposite pole of the cell (blue). Most neurons initially migrate from their site of origin prior to entering a bipolar state for radial migration. C, intra-somatic polarity in radially migrating neurons is typified by a leading centrosome, often an intervening Golgi apparatus and a following nucleus. In the cortex the leading process is a dendrite (blue bar), and an axon (red) extends behind the translocating nucleus. Radial migration occurs along a glial substrate (orange bar).

Figure 2. 3D reconstruction of MNTB principal cell

The nucleus (red) is eccentrically located within the cell body (tan contours) and lies opposite from the newly formed calyceal input (blue). The centroids of the nucleus and cell body (green spheres) are maximally separated given their cellular geometry. The polarization axis is indicated by a vector passing through the centroids of the nucleus and cell body. Scale bar: 2 μm.