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.
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.
Cellular Neurobiology Unit, Centre de recherche de l'Institut Universitaire en Santé Mentale de Québec, Quebec City, Quebec, Canada G1J 2G3, Centre for Optics, Photonics, and Lasers, Université Laval, Quebec City, Quebec, Canada G1K 7P4, and Department of Psychiatry and Neuroscience, Université Laval, Quebec City, Quebec, Canada G1K 7P4.
Vincent
V
Breton-Provencher
Daniel
D
Coté
Armen
A
Saghatelyan
D053687:Adult Stem Cells / Q000187:drug effects; D000818:Animals; D003712:Dendrites / Q000187:drug effects / Q000502:physiology*; D018690:Excitatory Amino Acid Agonists / Q000494:pharmacology; D018691:Excitatory Amino Acid Antagonists / Q000494:pharmacology; D019706:Excitatory Postsynaptic Potentials / Q000187:drug effects / Q000235:genetics; D018014:Gene Transfer Techniques; D049452:Green Fluorescent Proteins / Q000235:genetics; D007478:Iontophoresis; D008297:Male; D008564:Membrane Potentials / Q000187:drug effects / Q000235:genetics; D051379:Mice; D008810:Mice, Inbred C57BL; D016202:N-Methylaspartate / Q000494:pharmacology; D009474:Neurons / Q000166:cytology* / Q000187:drug effects / Q000502:physiology*; D009812:Odorants; D009830:Olfactory Bulb / Q000166:cytology*; D018408:Patch-Clamp Techniques; D011554:Pseudopodia / Q000187:drug effects / Q000502:physiology; D016194:Receptors, N-Methyl-D-Aspartate / Q000378:metabolism*; D018709:Statistics, Nonparametric; D013997:Time Factors; D059008:Time-Lapse Imaging
D018690:Excitatory Amino Acid Agonists; D018691:Excitatory Amino Acid Antagonists; D016194:Receptors, N-Methyl-D-Aspartate; D049452:Green Fluorescent Proteins; D016202:N-Methylaspartate
NMDA; adult neurogenesis; granule cells; maturation; olfactory bulb; two-photon imaging