Spatial Firing Properties of Hippocampal CA1 Populations in an Environment Containing Two Visually Identical Regions

Spatial firing plots for 25 simultaneously recorded CA1 pyramidal cells from rat 1, during the first and second sessions. The two boxes were interchanged between sessions. Light gray represents the rat’s trajectory; black pointsrepresent the rat’s location at moments when the cell spiked. For this rat, the majority of cells showed distinct firing patterns in the N and S boxes, but there were a significantly above-chance number of cases of similar firing patterns (e.g., cells 2, 4, 12, 15, 19, 24, and 25). There were occasional instances of fields appearing or disappearing between sessions (e.g., cell 1), but no cases of fields switching sides when the boxes were interchanged. This implies that the different firing fields in N and S were not caused by differences in the physical features of the two boxes.

Spatial firing plots for 25 simultaneously recorded CA1 pyramidal cells from rat 2, during the first and second sessions. For this rat, the majority of cells showed similar firing patterns in the N and S boxes, but there were several instances of clearly distinct firing patterns on the two sides. In most cases these differences were maintained across sessions (e.g., cells 4, 7, 10, 20, and 25), although there were a few exceptions (e.g., cell 17). The reliable maintenance of robust differences indicates that the differences in this rat were not merely attributable to idiosyncracies of sampling. The N–S firing patterns for rats 3 and 4 resembled those for rat 2, albeit with a slightly higher level of differential N–S activity.

Relations between firing fields in the N and S boxes. A, For each rat, the top plot shows the distribution of N–S correlations across all cells recorded during a single session on one of the later days. As a control, the distribution obtained by taking N and S firing rate maps from different, randomly chosen cells is shown below, reflecting the distribution that would be expected if the N and S firing fields of a cell were unrelated. For each rat, the observed distribution of N–S correlations differed significantly from the mixed-cell control (p < 0.005; Kolmogorov–Smirnov test). B, Distribution of N–S correlations for the first recording session of every day, from each of the four rats. Each point shows the N–S correlation of one cell, and each vertical streak shows values from one session. The horizontal coordinates are randomized slightly to make the points easier to distinguish. For rat 1, the distributions from different sessions were statistically indistinguishable. For rats 2, 3, and 4, in contrast, there was significant variability across sessions, as shown by ANOVAs (p < 0.01 for each; F test).C, Mean levels of N–S correlation for the first and last available recording sessions for each rat. For rats 1, 2, and 4, the first session came from day 1 in the apparatus; for rat 3, it came from day 5. The last session for each rat was session 1 of the day of the probe session. There was no apparent tendency for the level of N–S correlation to increase or decrease as a function of experience.

Evidence for map shifting during the probe session. A, Two examples of the behavior of individual cells from rat 1. For each cell, spatial firing plots are shown for sessions 1, 2a, and 2b. In both cases (and this was typical), the plot for session 2a resembles the N portion of the plot for session 1 much better than the S portion, whereas the plot for session 2b closely matches the plot for session 1. B, Trajectory reconstructions for the first 5 min of the probe session, for rats 1, 2, and 3. In each plot, the horizontal coordinate represents time, and the vertical coordinate represents the Y coordinate of the rat’s position, with the light gray line at the level of the wall between the two boxes. The solid line represents the rat’s actual position, and the small rectangles represent positions reconstructed from 1 sec samples of population activity, using firing rate maps from the previous session as the basis for reconstruction. For rats 1 and 3, the reconstructed locations during the initial stay in the S box fell mostly into the N box, but as soon as the rat passed through the corridor, the reconstructions reverted to mostly match the rat’s actual position. For rat 2, the reconstructions were at all times distributed almost evenly between the N and S boxes, regardless of the rat’s actual position. Trajectory reconstruction was not performed for rat 4 because of the small number of cells available.C, Correlation plots of firing rate maps derived from the S2a and S2b subsessions with maps for the same cells from the N and S boxes in session 1. Each point represents one cell. The horizontal coordinate is the correlation of the cell’s N1 firing rate map with the S2a map (top panel) or S2b map (bottom panel). The vertical coordinate is the correlation of the S1 map with the S2a map or S2b map. Thus, points lying below the diagonal indicate greater resemblance to N1 than to S1. For all four rats, the majority of points in the top plots lie below the diagonal, indicating that the population representation during S2a aligned better with N1 than with S1; however, the difference was statistically significant only for rat 1 (p < 0.00001;t test). Again for all four rats, the majority of points in the bottom plots lie above the diagonal, indicating that the population representation during S2b aligned better with S1 than with N1 (p < 0.01 for each; t test).

Data relating to the question of multiple interfering maps. A, Left, Spatial firing plots for three simultaneously recorded cells from rat 1, two having asymmetric firing fields (cells 1 and 3) and one having a symmetric field (cell 2). Right, Temporal cross-correlation plots for each pair of these three cells. Horizontal axis: seconds. Vertical axis: counts. This example illustrates the general observation that when symmetric and asymmetric fields overlapped spatially, the spike trains of the cells also overlapped temporally, indicating that the cells were unlikely to belong to separate, mutually exclusive maps.B, Trajectory reconstructions for 10 min periods from rats 1, 2, and 3. See legend of Figure 5 for explanation. In this plot, the times when the rat was inside the corridor are not shown. The reconstructions are based on populations of 38, 32, and 31 cells, respectively.