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A neuronal code for space in hippocampal coactivity dynamics independent of place fields

Hippocampus is comprised of ∼20% place cells, discharging in cell-specific locations (“place fields”), standardly interpreted as a dedicated neuronal code for space. However, place cell discharge is temporally unreliable across seconds and days, and spatially multimodal, suggesting an alternative “ensemble cofiring” spatial code with manifold dynamics that does not require reliable spatial tuning. We evaluated these hypotheses using GCaMP6f and miniature microscopes to image mouse CA1 ensemble activity in two environments, across 3 weeks. Both place fields and ensemble coactivity relationships “remap,” being distinct between and (weakly) similar within environments. We find that decoding the environment from cell-pair coactivity relationships is effective and improves with experience, even after removing place tuning. Decoding from 1-s ensemble activity is indifferent to firing fields, relying crucially on the most anti-coactive cells because ensemble activity is internally-organized on a low-dimensional manifold of non-linear cofiring relationships that intermittently reregisters to environments according to anti-cofiring subpopulation activity.