Hippocampal principal neurons display both spatial tuning properties and memory features. Whether this distinction corresponds to separate neuron types or a context-dependent continuum has been debated. We report here that the task-context (“splitter”) feature is highly variable along both trial and spatial position axes. Neurons acquire or lose splitter features across trials even when place field features remain unaltered. Multiple place fields of the same neuron can individually encode both past or future run trajectories, implying that splitter fields are under the control of assembly activity. Place fields can be differentiated into subfields by the behavioral choice of the animal, and splitting within subfields evolves across trials. Interneurons also differentiate choices by integrating inputs from pyramidal cells. Finally, bilateral optogenetic inactivation of the medial entorhinal cortex reversibly decreases the fraction of splitter fields. Our findings suggest that place or splitter features are different manifestations of the same hippocampal computation.