Abstract
Place cells and concept neurons are defined by a rise in firing rate at a particular location or for a particular person or object. Neurons without such a rise remain unlabeled, although they keep firing during the task. Such neurons could still carry information in the timing of their spikes. Hippocampal theta provides a reference for this timing.
We therefore asked whether the theta phase of a neuron's spikes depends on location or on the viewed image, even when its firing rate does not. We analysed hippocampal neurons in humans navigating a virtual city, rats running on a linear track, and humans viewing images of anima ls, faces, and places.
In both navigation datasets, more neurons than expected by chance fired at a consistent theta phase at particular locations. This phase tuning remained after we excluded neurons whose firing rate depended on location. In human navigation, the spike phases of these remaining neurons improved location decoding beyond the firing rates of all neurons. More phase-tuned neurons than expected by chance also fired at progressively earlier theta phases as participants passed each neuron's preferred location. This pattern resembles phase precession, which classically occurs as an animal crosses the firing-rate field of a place cell. The neurons that showed it had no firing-rate field, so their phase shift was anchored to the location defined by phase tuning alone.
During image viewing, more neurons than expected by chance changed the theta phase of their spikes after a particular image appeared. This effect remained after we removed, for each neuron, the images that changed its firing rate. Spike phases alone also predicted the image category above chance.
Theta-relative spike timing therefore carries in formation about location and images that firing rate alone misses. We propose that weak input changes when a neuron fires with in the theta cycle, whereas strong input also raises its firing rate.