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Back to the Future: Preserved Hippocampal Network Activity during Reverse Ambulation

During movement, there is a transition of activity across the population, such that place-field centers ahead of the rat are sequentially activated in the order that they will be encountered. Although the mechanisms responsible for this sequence updating are unknown, two classes of models can be considered. The first class involves head-direction information for activating neurons in the order that their place fields will be traversed. An alternative model contends that motion and turn-related information from the posterior parietal cortex shift the subset of active hippocampal cells across the population. To explicitly test these two models, rodents were trained to run backward on a linear track, placing movement in opposition with head orientation. Although head-direction did not change between running conditions, place-field activity remapped and there was an increase in place-field size during backward running compared with forward. The population activity, however, could still be used to reconstruct the location of the rat accurately. Moreover, theta phase precession was maintained in both running conditions, indicating preservation of place-field sequences on short-time scales. The observation that sequence encoding persists even when the animal is orientated away from the direction of movement favors the concept that posterior parietal cortical mechanisms may be partially responsible for updating hippocampal activity patterns.