Navigational strategy dictates hippocampal representation of space in an everyday memory task

Hippocampal activity provides a representation of the world around us, as well as our position within that world. However, it is not known if and to what extent the chosen navigational reference frame can influence hippocampal representations during memory-based tasks, including those focused on future activity. Here, we develop and employ two naturalistic, carefully controlled variants of the everyday memory task to model the use of egocentric and allocentric coordinates in the same arena.

By recording hippocampal neural activity through miniature microscopes in male rats performing each of the two tasks, we uncover differences in the representation of space, and in the features of memory-based action planning. By also deploying optogenetic inactivation during navigational decision making, we find that hippocampal representations observed during the planning phase are necessary for solving the allocentric, but not the egocentric version of the task. Overall, our findings reveal a functional link between non-local hippocampal representations and allocentric navigation.

We wish to thank the members of the Schnitzer group for their support and constructive suggestions, and especially Thomas Rogerson and Jessica Rosa Maxey for their help and insight. We wish to thank the former and current members of the Inscopix team for their constant help and in-depth discussion to solve problems. We are particularly grateful to Diane Damez-Werno, Mark Turnbull and Fabrizio Stizia of Inscopix for their assistance and constant support.

We wish to thank all the members of the Morris and Schultz lab and our colleagues at the University of Edinburgh for their support. Among them, Giuseppe Gava for help with code writing, and Emma Wood, Paul Dudchenko, Tara Spires-Jones and Nick Robinson for useful discussions. We wish to thank Hugo Spiers (University College London), Timothy Behrens, Francesca Pozzolo and the other members of the Behrens lab (University College London), Freyja Ólafsdóttir (Donders Institute, the Netherlands), Lisa Genzel (Donders Institute, the Netherlands), Sam McKenzie (University of New Mexico, USA) and Garrett Blair (New York University, USA) for their valuable insight and discussion.

Last, we wish to thank the Bioveterinary Science Staff at the University of Edinburgh for their support and expertise, and looking after our animals’ welfare; we thank wholeheartedly Lynn Morrison, Caroline Quigley and Montse Rigol-Muxart. The work was funded by the Wellcome Trust, Grant n.207481/Z/17/Z “The retention of memory and creation of knowledge” (1 October 2017 - 32 May 2023) to RGMM. We are grateful to Wellcome Trust for the financial support.

For the purpose of open access, the authors have applied a CC BY public copyright licence to any Author Accepted Manuscript version arising from this submission. These authors jointly supervised this work: Simon R. Institute for Neuroscience and Cardiovascular Research and Edinburgh Neuroscience, The University of Edinburgh, Edinburgh, UK Francesco Gobbo, Rufus Mitchell-Heggs, Dorothy Tse, Nuria Garcia-Font, Patrick A.