Allothetic and idiothetic spatial cues control the multiplexed theta phase coding of place cells

Theta oscillation is considered a temporal scaffold for hippocampal computations that organizes the activity of spatially tuned cells known as place cells. Late phases of theta support prospective spatial representation via phase ‘precession’. In contrast, some studies have hypothesized that early phases of theta may subserve both retrospective spatial representation via phase ‘procession’ and the encoding of new associations. Here, combining virtual reality, electrophysiology and computational modeling, we provide experimental evidence for such a functionally multiplexed phase code and describe how distinct spatial inputs control its manifestation. Specifically, when rats continuously learned new associations between external landmark (allothetic) cues and self-motion (idiothetic) cues, phase ‘precession’ remained intact, allowing continuous prediction of future positions. Conversely, phase ‘procession’ was diminished, matching the putative role in encoding at the early theta phase. This multiplexed phase code may serve as a general circuit logic for alternating different computations at a sub-second scale. Using a virtual reality apparatus in rats that dissociates external landmarks from self-motion cues, the authors describe how the two modes of theta phase coding in the hippocampus during navigation are controlled via distinct computations.