1. Department of Anatomy and Developmental Biology, University College London, Gower Street, London WC1E 6BT, UK
2. Institute of Cognitive Neuroscience, University College London, Gower Street, London WC1E 6BT, UK
3. Present address: Department of Anatomy, University of Bristol, Bristol BS8 1TD, UK

Correspondence to: John O'Keefe^1,2 Email: j.okeefe@ucl.ac.uk

Abstract

In the brain, hippocampal pyramidal cells use temporal¹ as well as rate² coding to signal spatial aspects of the animal's environment or behaviour. The temporal code takes the form of a phase relationship to the concurrent cycle of the hippocampal electroencephalogram theta rhythm¹. These two codes could each represent a different variable^{3, 4}. However, this requires the rate and phase to vary independently, in contrast to recent suggestions^{5, 6} that they are tightly coupled, both reflecting the amplitude of the cell's input. Here we show that the time of firing and firing rate are dissociable, and can represent two independent variables: respectively the animal's location within the place field, and its speed of movement through the field. Independent encoding of location together with actions and stimuli occurring there may help to explain the dual roles of the hippocampus in spatial and episodic memory^{7, 8}, or may indicate a more general role of the hippocampus in relational/declarative memory^{9, 10}.