Temporal coding and rate remapping: Representation of non-spatial information in the hippocampus.

Hippocampal place cells represent non-spatial information in addition to their more frequently studied spatial response properties. This encoding of non-spatial information by a process called rate remapping involves the increase or decrease in the firing rate of a place cell without changes in its spatial specificity. However, many hippocampal phenomena occur on very short time scales over which long-term average firing rates are not an appropriate description of activity. To understand how rate remapping relates to fine-scale temporal firing phenomena in the hippocampus, we studied place cell responses during two tasks that induce rate remapping. For those two tasks, we looked at how rate remapping affected burst firing, spike count distributions, and trial-to-trial variability. In addition, we looked at how rate remapping is expressed with respect to the theta-frequency oscillations of the hippocampus, which are thought to temporally organize firing on time scales faster than 100 ms. We found that, while rate remapping could increase the number of spikes in each theta cycle, it did not increase their temporal dispersion, thus preserving theta phase coding. Interestingly, rate remapping in CA1 in response to task demands preferentially occurred during the first half of theta oscillations. The other half of the theta cycle contained preferential expression of phase precession, a phenomenon associated with place cell sequences, in agreement with previous results. This difference of place cell coding during different halves of the theta cycle supports recent theoretical suggestions that different processes occur during the two halves of the theta cycle. The differentiation between the halves of the theta cycle was not clear in the recordings from CA3 during rate remapping induced by task-irrelevant sensory changes. These findings provide new insight into the way that temporal coding is utilized in the hippocampus and how rate remapping is expressed through that temporal code. This article is protected by copyright. All rights reserved.