Postnatal switch from synaptic to extrasynaptic transmission between interneurons and NG2 cells.
NG2 cells, oligodendrocyte precursors, play a critical role in myelination during postnatal brain maturation, but a pool of these precursors is maintained in the adult and recruited to lesions in demyelinating diseases. NG2 cells in immature animals have recently been shown to receive synaptic inputs from neurons, and these have been assumed to persist in the adult. Here, we investigated the GABAergic synaptic activity of NG2 cells in acute slices of the barrel cortex of NG2-DsRed transgenic mice during the first postnatal month, which corresponds to the period of active myelination in the neocortex. Our data demonstrated that the frequency of spontaneous and miniature GABAergic synaptic activity of cortical NG2 cells dramatically decreases after the second postnatal week, indicating a decrease in the number of synaptic inputs onto NG2 cells during development. However, NG2 cells still receive GABAergic inputs from interneurons in the adult cortex. These inputs do not rely on the presence of functional synapses but involve a form of GABA spillover. This GABA volume transmission allows interneurons to induce phasic responses in target NG2 cells through the activation of extrasynaptic GABA(A) receptors. Hence, after development is complete, volume transmission allows NG2 cells to integrate neuronal activity patterns at frequencies occurring during in vivo sensory stimulation.
Vélez-Fort
Mateo
M
Institut National de la Santé et de la Recherche Médicale Unité 603, Centre National de la Recherche Scientifique Unité Mixte de Recherche 8154, Université Paris Descartes, 75006 Paris, France.
Maldonado
Paloma P
PP
Butt
Arthur M
AM
Audinat
Etienne
E
Angulo
María Cecilia
MC
D000367:Age Factors; D000818:Animals; D000831:Animals, Newborn; D001703:Biophysics; D002118:Calcium / Q000378:metabolism; D002461:Cell Line, Transformed; D002540:Cerebral Cortex / Q000166:cytology* / Q000254:growth & development*; D004553:Electric Conductivity; D018691:Excitatory Amino Acid Antagonists / Q000494:pharmacology; D066298:In Vitro Techniques; D007395:Interneurons / Q000502:physiology*; D008164:Luminescent Proteins / Q000235:genetics; D008239:Lysine / Q000031:analogs & derivatives / Q000378:metabolism; D051379:Mice; D008822:Mice, Transgenic; D014179:Neurotransmitter Uptake Inhibitors / Q000494:pharmacology; D009557:Nipecotic Acids / Q000494:pharmacology; D009836:Oligodendroglia / Q000502:physiology*; D010091:Oximes / Q000494:pharmacology; D018408:Patch-Clamp Techniques / Q000379:methods; D010721:Phosphinic Acids / Q000494:pharmacology; D011724:Pyridazines / Q000494:pharmacology; D011725:Pyridines / Q000494:pharmacology; D011810:Quinoxalines / Q000494:pharmacology; D018709:Statistics, Nonparametric; D013234:Stem Cells; D013569:Synapses / Q000502:physiology*; D009435:Synaptic Transmission / Q000502:physiology*; D005680:gamma-Aminobutyric Acid / Q000378:metabolism
C101879:(1,2,5,6-tetrahydropyridin-4-yl)methylphosphinic acid; D018691:Excitatory Amino Acid Antagonists; D008164:Luminescent Proteins; D014179:Neurotransmitter Uptake Inhibitors; D009557:Nipecotic Acids; D010091:Oximes; D010721:Phosphinic Acids; D011724:Pyridazines; D011725:Pyridines; D011810:Quinoxalines; C413663:fluorescent protein 583; C062865:2,3-dioxo-6-nitro-7-sulfamoylbenzo(f)quinoxaline; C078793:NNC 711; D005680:gamma-Aminobutyric Acid; C049853:gabazine; C013411:biocytin; D008239:Lysine; D002118:Calcium