Experience-dependent, asymmetric expansion of hippocampal place fields

Abstract

Theories of sequence learning based on temporally asymmetric, Hebbian long-term potentiation predict that during route learning the spatial firing distributions of hippocampal neurons should enlarge in a direction opposite to the animal's movement. On a route AB, increased synaptic drive from cells representing A would cause cells representing B to fire earlier and more robustly. These effects appeared within a few laps in rats running on closed tracks. This provides indirect evidence for Hebbian synaptic plasticity and a functional explanation for why place cells become directionally selective during route following, namely, to preserve the synaptic asymmetry necessary to encode the sequence direction.

Figure 1

The location of each spike (measured relative to the respective average place field center) during the first (A) and the seventeenth (B) laps, is shown for all the 186 fields recorded from seven rats in 10 sessions. The size of each circle is proportional to the log of the instantaneous firing rate at that location during the lap. (C) The histograms of the total firing rate at each location during the first and the last laps are also shown (light curve, lap 1; solid curve, lap 17. Bin width = 0.41 cm, which corresponds to the resolution of the position tracking camera). The center of mass of the firing rate distribution (indicated by arrows in A and B, and by vertical lines in C) of all the spikes in the last lap is shifted backwards (by ≈1.4 cm) compared with that during the first lap. There was a 66% increase in the total firing rate. Thus, with experience, the location of the place fields shifted backwards and the place cells fired more spikes.

Figure 2

(A) The relative place field size (mean ± SE) of the 186 place fields increased significantly and asymptotically over the 17 laps on the track (P < 0.0001). (B) The location of each place field on each lap (for which there was at least one spike) was calculated relative to the center of mass of the corresponding average place field for all 17 trials. The place field location (mean ± SE) for 186 place fields is shown as a function of lap number. There was a significant, asymptotic backward shift in the relative field locations over the 17 laps on the track (P < 0.0001). The location parameter was significantly inversely correlated (r = −0.9) with field size.

Figure 3

(A) Relative place field size (mean ± SE) in the second environment, for 43 place cells that had a place cells in the first environment. The place field size again increased asymptotically by 124% in 17 laps (P < 0.0001) and (B) the place field location (mean ± SE) again shifted backwards by 2.5 cm (P < 0.001), thus indicating that the effect is environment specific and could not be attributed to general excitability changes.