Hippocampal place cells encode global location but not connectivity in a complex space

Éléonore Duvelle; Roddy M Grieves; Anyi Liu; Selim Jedidi-Ayoub; Joanna Holeniewska; Adam Harris; Nils Nyberg; Francesco Donnarumma; Julie M Lefort; Kate J Jeffery; Christopher Summerfield; Giovanni Pezzulo; Hugo J Spiers

doi:10.1016/j.cub.2021.01.005

Hippocampal place cells encode global location but not connectivity in a complex space

Curr Biol. 2021 Mar 22;31(6):1221-1233.e9. doi: 10.1016/j.cub.2021.01.005. Epub 2021 Feb 12.

Affiliations

¹ Department of Experimental Psychology, Institute of Behavioural Neuroscience, University College London, London, UK; Department of Psychological and Brain Sciences, Dartmouth College, Hanover, NH, USA. Electronic address: e.duvelle@ucl.ac.uk.
² Department of Experimental Psychology, Institute of Behavioural Neuroscience, University College London, London, UK; Department of Psychological and Brain Sciences, Dartmouth College, Hanover, NH, USA.
³ Department of Experimental Psychology, Institute of Behavioural Neuroscience, University College London, London, UK.
⁴ Department of Experimental Psychology, University of Oxford, OX2 6BW Oxford, UK.
⁵ Institute of Cognitive Sciences and Technologies, National Research Council, via S. Martino d. Battaglia 44, 00185 Rome, Italy.
⁶ University College London, Department of Cell and Developmental Biology, London, UK.
⁷ Department of Experimental Psychology, Institute of Behavioural Neuroscience, University College London, London, UK. Electronic address: h.spiers@ucl.ac.uk.

Abstract

Flexible navigation relies on a cognitive map of space, thought to be implemented by hippocampal place cells: neurons that exhibit location-specific firing. In connected environments, optimal navigation requires keeping track of one's location and of the available connections between subspaces. We examined whether the dorsal CA1 place cells of rats encode environmental connectivity in four geometrically identical boxes arranged in a square. Rats moved between boxes by pushing saloon-type doors that could be locked in one or both directions. Although rats demonstrated knowledge of environmental connectivity, their place cells did not respond to connectivity changes, nor did they represent doorways differently from other locations. Place cells coded location in a global reference frame, with a different map for each box and minimal repetitive fields despite the repetitive geometry. These results suggest that CA1 place cells provide a spatial map that does not explicitly include connectivity.

Keywords: detour; four-room maze; hippocampus; navigation; place cells; place field repetition; rat; spatial connectivity; topology; transitions.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Action Potentials
Animals
Hippocampus / cytology*
Place Cells* / cytology
Rats
Space Perception*

Grants and funding

WT_/Wellcome Trust/United Kingdom