Novelty-Induced Phase-Locked Firing to Slow Gamma Oscillations in the Hippocampus: Requirement of Synaptic Plasticity

Temporally precise neuronal firing phase-locked to gamma oscillations is thought to mediate the dynamic interaction of neuronal populations, which is essential for information processing underlying higher-order functions such as learning and memory. However, the cellular mechanisms determining phase locking remain unclear. By devising a virus-mediated approach to perform multi-tetrode recording from genetically manipulated neurons, we demonstrated that synaptic plasticity dependent on the GluR1 subunit of AMPA (α-amino-3-hydroxy-5-methyl-4-isoxazole propionate) receptor mediates two dynamic changes in neuronal firing in the hippocampal CA1 area during novel experiences: the establishment of phase-locked firing to slow gamma oscillations and the rapid formation of the spatial firing pattern of place cells. The results suggest a series of events potentially underlying the acquisition of new spatial information: slow gamma oscillations, originating from the CA3 area, induce the two GluR1-dependent changes of CA1 neuronal firing, which in turn determine information flow in the hippocampal-entorhinal system. •Microgenetic manipulation reveals cellular mechanisms determining firing patterns•Synaptic plasticity strengthens phase-locked firing along slow gamma oscillations•Slow gamma phase locking is associated with rapid formation of place cell activity•Synaptic plasticity may regulate information flow in hippocampal-entorhinal circuit Kitanishi et al. identify GluR1-dependent synaptic plasticity as a key cellular mechanism that strengthens phase-locked firing along slow, but not fast, gamma oscillations, which is associated with the rapid formation of place cell activity in the hippocampus during novel experiences.