Dynamic θ Frequency Coordination within and between the Prefrontal Cortex-Hippocampus Circuit during Learning of a Spatial Avoidance Task

θ-Scale coordination of prelimbic medial prefrontal cortex (mPFC) local field potentials (LFPs) and its influence via direct or indirect projections to the ventral hippocampus (vHC) and dorsal hippocampus (dHC) during spatial learning remains poorly understood. We hypothesized that θ frequency coordination dynamics within and between the mPFC, dHC, and vHC would be predetermined by the level of connectivity rather than reflecting differing circuit throughput relationships depending on cognitive demands. Moreover, we hypothesized that coherence levels would not change during learning of a complex spatial avoidance task. Adult male rats were bilaterally implanted with EEG electrodes and LFPs recorded in each structure. Contrary to predictions, θ coherence averaged across “Early” or “Late” training sessions in the mPFC-HC, mPFC-mPFC, and HC-HC increased as a function of task learning. Coherence levels were also highest between the indirectly connected mPFC-dHC circuit, particularly during early training. Although mPFC postacquisition coherence remained higher with dHC than vHC, dynamic mPFC coherence patterns with both hippocampal poles across avoidance epochs were similar. In the 3 s before avoidance, a regional temporal sequence of transitory coherence peaks emerged between the mPFC-mPFC, the mPFC-HC, and then dHC-dHC. During this sequence, coherence within θ bandwidth fluctuated between epochs at distinct subfrequencies, suggesting frequency-specific roles for the propagation of task-relevant processing. On a second timescale, coherence frequency within and between the mPFC and hippocampal septotemporal axis change as a function of avoidance learning and cognitive demand. The results support a role for θ coherence subbandwidths, and specifically an 8- to 9-Hz mPFC θ signal, for generating and processing qualitatively different types of information in the organization of spatial avoidance behavior in the mPFC-HC circuit.