Activity of the principal cells of the olfactory bulb promotes a structural dynamic on the distal dendrites of immature adult-born granule cells via activation of NMDA receptors.

Publication Type:

Journal Article

Authors:

Breton-Provencher, Vincent; Daniel C Côté; Armen Saghatelyan

Source:

J Neurosci, Volume 34, Issue 5, p.1748-59 (2014)

Keywords:

Adult Stem Cells, Animals, Dendrites, Excitatory Amino Acid Agonists, Excitatory Amino Acid Antagonists, Excitatory Postsynaptic Potentials, Gene Transfer Techniques, Green Fluorescent Proteins, Iontophoresis, Male, Membrane Potentials, Mice, Mice, Inbred C57BL, N-Methylaspartate, Neurons, Odorants, Olfactory Bulb, Patch-Clamp Techniques, Pseudopodia, Receptors, N-Methyl-D-Aspartate, Statistics, Nonparametric, Time Factors, Time-Lapse Imaging

Abstract:

<p>The adult olfactory bulb is continuously supplied with neuronal precursors that differentiate into granule and periglomerular cells. Little is known about the structural dynamic of adult-born granule cells (GCs) at their different maturational stages, the mechanisms controlling the integration of new neurons into the pre-existing neuronal circuitry, or the role of principal cell activity in these processes. We used two-photon time-lapse imaging to reveal a high level of filopodia formation and retraction on the distal dendrites of adult-born GCs at their early maturational stages. This dynamic decreased as the adult-born interneurons matured. Filopodia formation/retraction on the dendrites of adult-born GCs at the early maturational stages depended on the activation of NMDA receptors (NMDARs). The stimulation of mitral cells using a pattern that mimics activity of these principal neurons to odor presentation promotes the NMDAR-dependent filopodia dynamic of adult-born GCs during their early but not late maturational stages. Moreover, NMDA iontophoresis was sufficient to induce the formation of new filopodia on the distal dendrites of immature adult-born GCs. The maturation of adult-born interneurons was accompanied by a progressive hyperpolarization of the membrane potential and an increased Mg(2+) block of NMDARs. Decreasing the extracellular Mg(2+) concentration led to filopodia formation on the dendrites of mature adult-born GCs following NMDA iontophoresis. Our findings reveal an increased structural dynamic of adult-born GCs during the early stages of their integration into the mouse bulbar circuitry and highlight a critical period during which the principal cells' activity influences filopodia formation/retraction on the dendrites of interneurons.</p>