Distinct directional couplings between slow and fast gamma power to the phase of theta oscillations in the rat hippocampus

It is well‐established that theta (~4–10 Hz) and gamma (~25–100 Hz) oscillations interact in the rat hippocampus. This cross‐frequency coupling might facilitate neuronal coordination both within and between brain areas. However, it remains unclear whether the phase of theta oscillations controls the power of slow and fast gamma activity or vice versa. We here applied spectral Granger causality, phase slope index and a newly developed cross‐frequency directionality (CFD) measure to investigate directional interactions between local field potentials recorded within and across hippocampal subregions of CA1 and CA3 of freely exploring rats. Given the well‐known CA3 to CA1 anatomical connection, we hypothesized that interregional directional interactions were constrained by anatomical connection, and within‐frequency and cross‐frequency directional interactions were always from CA3 to CA1. As expected, we found that CA3 drove CA1 in the theta band, and theta phase‐to‐gamma power coupling was prominent both within and between CA3 and CA1 regions. The CFD measure further demonstrated that distinct directional couplings with respect to theta phase was different between slow and fast gamma activity. Importantly, CA3 slow gamma power phase‐adjusted CA1 theta oscillations, suggesting that slow gamma activity in CA3 entrains theta oscillations in CA1. In contrast, CA3 theta phase controls CA1 fast gamma activity, indicating that communication at CA1 fast gamma is coordinated by CA3 theta phase. Overall, these findings demonstrate dynamic directional interactions between theta and slow/fast gamma oscillations in the hippocampal network, suggesting that anatomical connections constrain the directional interactions.