Correlated neuronal activity is instrumental in the formation of networks, but its emergence during maturation is poorly understood. We have used multibeam two-photon calcium microscopy combined with targeted electrophysiological recordings in order to determine the development of population coherence from embryonic to postnatal stages in the hippocampus. At embryonic stages (E16-E19), synchronized activity is absent, and neurons are intrinsically active and generate L-type channel-mediated calcium spikes. At birth, small cell assemblies coupled by gap junctions spontaneously generate synchronous nonsynaptic calcium plateaus associated to recurrent burst discharges. The emergence of coherent calcium plateaus at birth is controlled by oxytocin, a maternal hormone initiating labour, and progressively shut down a few days later by the synapse-driven giant depolarizing potentials (GDPs) that synchronize the entire network. Therefore, in the developing hippocampus, delivery is an important signal that triggers the first coherent activity pattern, which is silenced by the emergence of synaptic transmission.
We have shown previously that a selective metabotropic glutamate receptor (mGluR) agonist, 1S,3R-1-aminocyclopentane-1,3-dicarboxylate (1S,3R-ACPD), evokes an inward current in CA1 pyramidal neurons of rat hippocampal slices in the presence of K ϩ channel blockers (Cré pel et al., 1994). This current has been characterized as a Ca 2ϩ -activated nonselective cationic (CAN) current. Using whole-cell patch-clamp recordings and intracellular dialysis, we now have identified the mGluR subtype and the mechanisms underlying the CAN current (I CAN ) and report for the first time the presence of a synaptic I CAN in the mammalian CNS. First, we have shown pharmacologically that activation of I CAN by 1S,3R-ACPD involves the group I mGluRs (and not the groups II and III) and a G-protein-dependent process. We also report that I CAN is modulated by the divalent cations (Mg 2ϩ , Cd 2ϩ , and Zn 2ϩ ). Second, we have isolated a slow synaptic inward current evoked by a high-frequency stimulation in the presence of K ϩ channel blockers, ionotropic glutamate, and GABA A receptor antagonists. This current shows similar properties to the exogenously evoked I CAN : its reversal potential is close to the reversal potential of the 1S,3R-ACPD-evoked I CAN , and it is G-protein-and Ca 2ϩ -dependent. Because the amplitude and duration of I CAN increased in the presence of a glutamate uptake blocker, we suggest that this synaptic current is generated via the activation of mGluRs. We propose that the synaptic I CAN , activated by a brief tetanic stimulation and leading to a long-lasting inward current, may be involved in neuronal plasticity and synchronized network-driven oscillations.
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