Fast Network Oscillations in the Newborn Rat HippocampusIn Vitro

Abstract

Spontaneous neural activity is crucial for the formation of the intricate patterns of cortical connectivity during development. In particular, temporal correlations in presynaptic and postsynaptic activity have been hypothesized to be a critical determinant in the selection of neurons that are to become wired together. To date, however, temporally correlated activity in the neonatal brain has been believed to take place with a precision of tens of milliseconds to seconds. Here we describe a novel type of a fast network oscillation associated with millisecond synchronization of pyramidal cell firing in newborn rat hippocampus in vitro. Individual pyramidal neurons fired mainly at lower gamma frequencies (20-40 Hz) but were synchronized into a high-frequency (100-400 Hz) population oscillation that was reflected in field potential spikes and intracellular AMPA-kainate receptor-mediated currents. The high-frequency population oscillation was patterned by a gamma-frequency modulatory oscillation. The gamma modulation was imposed by GABAergic currents, which exerted an inhibitory action on pyramidal neurons. Patterned activity based on GABAergic inhibition and glutamatergic excitation thus occurs already in newborn hippocampus. The network oscillations described here may be a mechanism for selective coincidence detection with a millisecond range temporal precision to shape the patterns of connectivity within the emerging hippocampal synaptic circuitry.