Dentate gyrus population activity during immobility drives formation of precise memories

Martin Pofahl1, Negar Nikbakht1, Andre N. Haubrich1, Theresa Nguyen1, Nicola Masala1, Oliver Braganza1, Jakob H. Macke2, Laura A. Ewell1, Kurtulus Golcuk1, Heinz Beck1

1 Institute for Experimental Epileptology and Cognition Research, University of Bonn, Germany
2 Computational Neuroengineering, Department of Electrical and Computer Engineering, Technical University of Munich, Germany

All vertebrates are capable of generating dissimilar patterns of neuronal population activity from similar sensory-driven input patterns, a widely studied phenomenon called pattern separation 1–3. It is much less clear, however, how these separated patterns are transformed into lasting memory traces that retain the initial discrimination and make it relevant for ongoing behaviour. We describe a novel form of population activity in the hippocampal dentate gyrus, a region known to perform pattern separation in different species 1–3, that supports the formation of such precise memories. Using dual-color in-vivo two-photon Ca2+ imaging, we show that dentate gyrus granule cells exhibit extremely sparse, synchronized activity patterns during quiet immobility that are driven by perforant path activity. These population events are structured, incorporate place- and speed cells, are modified by changes in the environment and are similar to population patterns evoked during self-motion. Inhibiting only granule cell activity selectively during immobility impairs formation of pattern separated memories. These data demonstrate that the dentate gyrus exhibits a short time-scale, sparse form of population replay that is essential for precise memory formation.