Environmental novelty elicits a later theta phase of firing in CA1 but not subiculum

Abstract

The mechanism supporting the role of the hippocampal formation in novelty detection remains controversial. A comparator function has been variously ascribed to CA1 or subiculum, whereas the theta rhythm has been suggested to separate neural firing into encoding and retrieval phases. We investigated theta phase of firing in principal cells in subiculum and CA1 as rats foraged in familiar and novel environments. We found that the preferred theta phase of firing in CA1, but not subiculum, was shifted to a later phase of the theta cycle during environmental novelty. Furthermore, the amount of phase shift elicited by environmental change correlated with the extent of place cell remapping in CA1. Our results support a relationship between theta phase and novelty-induced plasticity in CA1.

Figure 1. Preferred theta phase of firing in CA1, but not subiculum, increases in novelty

(A) Laboratory recording setup. (B) Test trial series showing order of trials across and within days. Environment A was a square-walled box, Environment B a cylinder of different material to A (room cues visible), Environnment C was a raised platform, the ‘floor’ of Environments A and B. (C) Schematic diagram of main result. Preferred theta phase of firing in CA1 ensembles occurs later in the theta cycle in novelty than familiarity. Indication of absolute preferred phase for illustrative purposes only. (D) Preferred theta phase in CA1, but not subiculum, occurred later in the theta cycle in the first trial of the day in Environment A relative to subsequent trials in that same environment. * p ≤ 0.03 (see main text).(E) Preferred theta phase in CA1, but not subiculum, increased in trials in the novel environments B & C, relative to trials in the familiar environment A (first trial of day excluded). *** p = 0.004 (see main text). Note that 0° is defined for each ensemble as the preferred theta phase of the last trial of the day in the familiar environment, i.e. T4 in (D); T5 in (E). (F) Increase in theta phase preference is associated with remapping (ie. low spatial similarity score).

Figure 2. Novelty-elicited increase of preferred phase of firing in CA1 ensembles

Rose histograms show distribution of CA1 spikes over the theta cycle for each trial in 10°-bins. Representative spike ensembles show preferred phase is later in the theta cycle: (A) on the day’s first trial relative to later trials (Day 1, rat C and Day 2, rat A); (B) in novel environments compared to familiar environment (Day 1*, rat A). Phase of spiking normalised such that mean phase in Trial 4 (A) and Trial 5 (B) is 0°. μ is mean phase, κ is Von Mises’ κ (concentration), Z is Raleigh’s Z test statistic. κ is inversely related to the dispersion of the data, and is an index of the depth of theta modulation (Cacucci et al, 2004).