Properties of Doublecortin-(DCX)-Expressing Cells in the Piriform Cortex Compared to the Neurogenic Dentate Gyrus of Adult Mice

Friederike Klempin,Gerd Kempermann,Giselle Cheung,Golo Kronenberg,Helmut Kettenmann

doi:10.1371/journal.pone.0025760

Abstract

The piriform cortex receives input from the olfactory bulb and (via the entorhinal cortex) sends efferents to the hippocampus, thereby connecting the two canonical neurogenic regions of the adult rodent brain. Doublecortin (DCX) is a cytoskeleton-associated protein that is expressed transiently in the course of adult neurogenesis. Interestingly, the adult piriform cortex, which is usually considered non-neurogenic (even though some reports exist that state otherwise), also contains an abundant population of DCX-positive cells. We asked how similar these cells would be to DCX-positive cells in the course of adult hippocampal neurogenesis. Using BAC-generated transgenic mice that express GFP under the DCX promoter, we studied DCX-expression and electrophysiological properties of DCX-positive cells in the mouse piriform cortex in comparison with the dentate gyrus. While one class of cells in the piriform cortex indeed showed features similar to newly generated immature granule neurons, the majority of DCX cells in the piriform cortex was mature and revealed large Na+ currents and multiple action potentials. Furthermore, when proliferative activity was assessed, we found that all DCX-expressing cells in the piriform cortex were strictly postmitotic, suggesting that no DCX-positive “neuroblasts” exist here as they do in the dentate gyrus. We conclude that DCX in the piriform cortex marks a unique population of postmitotic neurons with a subpopulation that retains immature characteristics associated with synaptic plasticity. DCX is thus, per se, no marker of neurogenesis but might be associated more broadly with plasticity.

Highlights

Born granule cells in the adult dentate gyrus (DG) express a series of transient markers, such as the microtubule associated protein DCX, the polysialylated neural cell adhesion molecule PSA-NCAM, Tis21, and Calretinin [1,2,3,4,5]
In the adult mouse brain DCX-green fluorescent protein (GFP) was strongly expressed in the hippocampal dentate gyrus (Fig. 2A) and the subventricular zone (SVZ) of the lateral ventricle (Fig. 2B)
GFP expressing cells were not confined to the neurogenic regions only, but were, for example, detected in the stratum oriens of the hippocampal CA1 region (Fig. 2C), and in layers II and III of the non-neurogenic piriform cortex (Fig. 2D)

Summary

Introduction

Born granule cells in the adult dentate gyrus (DG) express a series of transient markers, such as the microtubule associated protein DCX, the polysialylated neural cell adhesion molecule PSA-NCAM, Tis, and Calretinin [1,2,3,4,5]. In adult hippocampal neurogenesis DCX marks the period between the committed progenitor cell stages (type-2b/3) and the early postmitotic maturation stage and is absent from the radial-glia-like stem cells (type-1), the non-committed progenitor cells (type-2a) and the mature neurons. DCX-positive (DCX+) cells in the dentate gyrus receive synaptic GABAergic input and migrate into the inner third of the granule cell layer [4,12,13,14]. The function of DCX in adult hippocampal neurogenesis is not known, but in many instances DCX-expression is used as surrogate marker of neurogenesis

Methods

Results

Conclusion