Representation of three-dimensional objects by the rat perirhinal cortex

Abstract

The perirhinal cortex (PRC) is known to play an important role in object recognition. Little is known, however, regarding the activity of PRC neurons during the presentation of stimuli that are commonly used for recognition memory tasks in rodents, that is, three-dimensional objects. Rats in the present study were exposed to three-dimensional objects while they traversed a circular track for food reward. Under some behavioral conditions, the track contained novel objects, familiar objects, or no objects. Approximately 38% of PRC neurons demonstrated "object fields" (a selective increase in firing at the location of one or more objects). Although the rats spent more time exploring the objects when they were novel compared to familiar, indicating successful recognition memory, the proportion of object fields and the firing rates of PRC neurons were not affected by the rats' previous experience with the objects. Together, these data indicate that the activity of PRC cells is powerfully affected by the presence of objects while animals navigate through an environment; but under these conditions, the firing patterns are not altered by the relative novelty of objects during successful object recognition.

Figure 1. Behavioral procedures used for electrophysiological recordings

The track used for behavior during all electrophysiological recordings. Rats were required to run 20 laps bi-directionally (10 counterclockwise, 10 clockwise) for a food reward. (A) During the No objects condition the track was empty during both epochs of track running. Rewards were given in two food dishes located on opposite sides of a barrier (indicated by squares), at the position where the rat was required to turn around. The “X” indicates the location of the pot that the rat was placed in during rest episodes. (B) Examples of behavioral procedures where objects were placed on the track. Numbers indicate the approximate positions of the different objects. In the ‘objects both epochs condition’, 8 novel objects were placed at discrete locations around the track for the first epoch of behavior (top panel), and the rat had to run past the objects to obtain the food reward. During the second epoch of behavior (bottom panel), 6 of the 8 objects used in epoch 1 were placed on the track at the same location as in epoch 1, while 2 of the 8 objects were removed and substituted with 2 novel objects (in this case objects 3 and 5 were replaced with objects 9 and 10 as indicated by the grey boxes). (C) Two of the eight rats participated in an additional ‘novel objects both epochs condition’. For this behavioral procedure, 6 novel objects were placed around the track for the first epoch of track running (top panel; objects 1–6). During the second epoch the objects from epoch 1 were replaced with 6 new objects (bottom panel objects 7–12).

Figure 2. PRC neuron activity patterns

(A) The activity of four representative PRC neurons under conditions with objects on the track. In the top panels, the black trace indicates the path of the rats and the red spots indicate the locations of spikes. The blue numbers represent the locations of objects. The bottom panels show the occupancy-normalized firing rate maps of the cells shown in A. (B) The raw spike data of four PRC neurons recorded when the track did not contain objects (top panels), and the associated occupancy-normalized firing rate maps (bottom panels).

Figure 3. The effect of objects on PRC neuron spatial information content

(A) The mean spatial information score of the PRC neurons that showed activity during track running for epoch 1 (white) and epoch 2 (light grey) during the different behavioral conditions. (B) The mean proportion of the PRC neurons that met the criteria for having at least one object field during track running for epoch 1 (white) and epoch 2 (light grey) for the different behavioral conditions. Error bars represent +/−1 SEM.

Figure 4. Example PRC neuron activity patterns for the Novel objects both epochs condition

The firing patterns for two representative PRC neurons during the condition in which the 6 novel objects on the track were changed between epoch 1 (top panels) and epoch two (bottom panels). The firing rate histogram by ‘linearized’ position during the first epoch (top panel) and the second epoch (bottom panel). The X axes are position on the track (cm) with zero indicating the position of the barrier. Positive numbers are for laps when the rat was running in the counterclockwise direction while negative numbers indicate the position when the rat was running in the clockwise direction. The Y axes are the occupancy normalized firing rates for each neuron. The associated raster plots by lap are also shown. Each horizontal line indicates a lap and blue lines are the laps in which the rat ran in the counterclockwise direction while red lines represent laps run in the clockwise direction. The black vertical lines indicate the position of the objects. (A) One neuron showed a low correlation value (r < 0.4) between the two epochs of track running while the other cell (B) had a similar firing field during both epochs even thought the objects were different (r > 0.8).

Figure 5. Activity pattern correlations between epochs 1 and 2

Frequency distributions of activity correlations (r) between epoch 1 and epoch 2 for PRC neurons in the (A) Objects both epochs, (B) Novel objects both epochs, and (C) No objects conditions. Each distribution was normalized by the number of neurons recorded during a given condition. The vertical dashed line indicates a correlation value of 0.8.

Figure 6. Running velocity during the different behavioral conditions

(A) The mean running velocity during epoch 1 (white) and epoch 2 (light grey) for the different behavioral conditions. Rats had significantly faster running velocities during epoch 2 relative to epoch 1 (F_[1,15] = 12.24, p < 0.01; repeated-measures ANOVA). Behavioral condition, however, did not significantly affect the running speed of the rats (F_[2,15] = 1.75, p = 0.21; repeated-measures ANOVA). (B) The mean running velocity during laps 1–2 compared laps 19–20 when the track contained novel objects (grey), familiar objects (grey dashed), or no objects (black). Rats ran slower during laps 1–2 relative to laps 19– 20 (F_[1,21] = 27.33, p < 0.001; repeated-measures ANOVA). Moreover, behavioral condition significantly affected the difference in running velocity between laps 1–2 and laps 19–20 (F_[2,21] = 8.25, p < 0.01; repeated-measures ANOVA), with the novel objects condition showing the greatest velocity change.

Figure 7. Firing rate by running velocity

Mean firing rate was not significantly modulated by velocity during (A) epoch 1 or (B) epoch 2 for any of the behavioral conditions. Error bars represent +/−1 SEM.

Figure 8. The effect of novelty on firing rate

(A) The difference in normalized firing rate between lap 1 and lap 10. There was no systematic change in firing rate between lap 1 and lap 10 during either epoch 1 or epoch 2. Moreover, there was no significant difference in normalized firing rate between lap 1 and lap 10 for the No objects (black), Objects both epochs (blue), or Novel objects both epochs conditions (red). (B) The proportion of cells that had a response decrement between of at least 2 standard deviations between laps 1 and 10 for the No objects (black), Objects both epochs (blue), and Novel objects both epochs conditions (red). Error bars represent +/−1 SEM.