Theta phase precession beyond the hippocampus

Abstract

The spike timing of spatially tuned cells throughout the rodent hippocampal formation displays a strikingly robust and precise organization. In individual place cells, spikes precess relative to the theta local field potential (6-10 Hz) as an animal traverses a place field. At the population level, theta cycles shape repeated, compressed place cell sequences that correspond to coherent paths. The theta phase precession phenomenon not only has afforded insights into how multiple processing elements in the hippocampal formation interact, but is also believed to facilitate hippocampal contributions to rapid learning, navigation, and lookahead. However, theta phase precession is not unique to the hippocampus, suggesting that insights derived from hippocampal phase precession could elucidate processing in other structures. In this review, we consider the implications of extrahippocampal phase precession in terms of mechanisms and functional relevance. We focus on phase precession in the ventral striatum (vStr), a prominent output structure of the hippocampus in which phase precession systematically appears in the firing of reward-anticipatory 'ramp' neurons. We outline how ventral striatal phase precession can advance our understanding of behaviors thought to depend on interactions between the hippocampus and the vStr, such as conditioned place preference and context-dependent reinstatement. More generally, we argue that phase precession can be a useful experimental tool in dissecting the functional connectivity between the hippocampus and its outputs.