Hippocampal-prefrontal theta phase synchrony in planning of multi-step actions based on memory retrieval

Planning of multi-step actions based on the retrieval of acquired information is essential for efficient foraging. The hippocampus (HPC) and prefrontal cortex (PFC) may play critical roles in this process. However, in rodents, many studies investigating such roles utilized T-maze tasks that only require one-step actions (i. e., selection of one of two alternatives), in which memory retrieval and selection of an action based on the retrieval cannot be clearly differentiated. In monkeys, PFC has been suggested to be involved in planning of multi-step actions; however, the synchrony between HPC and PFC has not been evaluated. To address the combined role of the regions in planning of multi-step actions, we introduced a task in rats that required three successive nose-poke responses to three sequentially illuminated nose-poke holes. During the task, local field potentials (LFP) and spikes from hippocampal CA1 and medial PFC (mPFC) were simultaneously recorded. The position of the first hole indicated whether the following two holes would be presented in a predictable sequence or not. During the first nose-poke period, phase synchrony of LFPs in the theta range (4-10 Hz) between the regions was not different between predictable and unpredictable trials. However, only in trials of predictable sequences, the magnitude of theta phase synchrony during the first nose-poke period was negatively correlated with latency of the two-step ahead nose-poke response. Our findings point to the HPC-mPFC theta phase synchrony as a key mechanism underlying planning of multi-step actions based on memory retrieval rather than the retrieval itself.