Hippocampal trace coding dominates and disrupts place coding

The hippocampus is widely viewed as a spatial mapping system because many CA1 neurons show location-specific activity during exploration. However, the hippocampus is also required for non-spatial learning, including trace eye-blink conditioning. Because most prior reports of non-spatial signals were obtained in immobile animals, it has been proposed that the hippocampus encodes space during locomotion and non-spatial variables during immobility. To test this directly, we used calcium imaging to record thousands of CA1 neurons while rats performed trace eye-blink conditioning during free exploration of an open field. Across more than 6,000 neurons from five rats, mean firing rates during trace-conditioning periods were [~]1.5-fold higher than during non-trial periods, and this difference persisted after controlling for locomotor speed. At the single-cell level, task-related modulation was widespread and strongly biased toward increased firing. Task-enhanced neurons outnumbered spatially selective neurons by more than threefold, indicating that trace coding predominated over place coding. Although trace-conditioning events occurred at random spatial locations and during continuous locomotion, trace-related activity remained robust at both single-cell and population levels. In contrast, spatial coding was reduced during trace periods, with lower spatial information and decreased similarity between task and non-task rate maps. These findings show that during active behavior, trace coding dominates and disrupts place coding, challenging the view that the hippocampus functions primarily as a stable spatial map.