Perirhinal cortex lesions uncover subsidiary systems in the rat for the detection of novel and familiar objects

Abstract

The present study compared the impact of perirhinal cortex lesions on tests of object recognition. Object recognition was tested directly by looking at the preferential exploration of novel objects over simultaneously presented familiar objects. Object recognition was also tested indirectly by presenting just novel objects or just familiar objects, and recording exploration levels. Rats with perirhinal cortex lesions were severely impaired at discriminating a novel object from a simultaneously presented familiar object (direct test), yet displayed normal levels of exploration to novel objects presented on their own and showed normal declines in exploration times for familiar objects that were repeatedly presented (indirect tests). This effective reduction in the exploration of familiar objects after perirhinal cortex lesions points to the sparing of some recognition mechanisms. This possibility led us to determine whether rats with perirhinal cortex lesions can overcome their preferential exploration deficits when given multiple object familiarisation trials prior to that same (familiar) object being paired with a novel object. It was found that after multiple familiarisation trials, objects could now successfully be recognised as familiar by rats with perirhinal cortex lesions, both following a 90-min delay (the longest delay tested) and when object recognition was tested in the dark after familiarisation trials in the light. These latter findings reveal: (i) the presumed recruitment of other regions to solve recognition memory problems in the absence of perirhinal cortex tissue; and (ii) that these additional recognition mechanisms require more familiarisation trials than perirhinal-based recognition mechanisms.

Fig. 1

(A) Schematic of the bow-tie maze. A central sliding door separates the two ends of the maze in which two objects are placed. (B) General procedure for the standard object recognition test showing the presentation order of the objects. All objects are rewarded (+). Arrows show direction of rat movements. Bold letters represent novel objects and grey letters represent familiar objects.

Fig. 2

Diagrammatic reconstructions of the PRh lesions showing the individual cases with the largest (grey) and smallest (black) lesions. The numbers refer to the distance (in millimetre) from bregma (adapted from Paxinos & Watson, 2005). The black arrows represent the borders of the perirhinal cortex. The PRh group comprised 12 rats.

Fig. 3

Experiment 1a: standard object recognition by rats with PRh lesions (black triangle) and their controls (white circle). One novel and one familiar object were presented at each trial. The diagram shows the recognition discrimination ratio D2, which was updated after every trial using cumulative data. Scores can range from −1 to +1. Data shown are mean ± standard error of the mean. Group differences ***P< 0.001. The dashed line is chance. In the schematic of the testing protocol (see Table 1) bold letters (upper) represent novel objects and lower letters represent familiar objects.

Fig. 4

Mean total exploration per trial in the novel + novel condition (two different objects were presented in each trial) in Experiment 1a (A) and Experiment 1b (B). The PRh group is represented by black triangles, the Control group by white circles. The inset graphs in grey show the cumulative exploration (s) across trials. Data shown are mean ± standard error of the mean. The dashed line is chance. In the schematic of the testing protocol (see Table 1) bold letters represent novel objects, i.e. all objects are novel.

Fig. 5

Overall total exploration in seconds of the novel + novel (two different objects were presented in each trial) and the familiar (identical copies of the same objects were presented across trials) conditions in Experiment 1a (A) and Experiment 1b (B). The PRh group is in black and Control group is in white. Data shown are mean ± standard error of the mean.

Fig. 6

Rates of habituation to repeated objects. Mean total exploration per trial in the familiar + familiar condition (identical copies of two objects were presented in each trial) in Experiment 1b (A) and in the familiar condition (identical copies of only one object were presented across trials) in Experiment 1c (B). The PRh group is represented by black symbols, the Control group by white symbols. Data shown are mean ± standard error of the mean. The dashed line is chance. In the schematic of the testing protocol (see Table 1) bold letters represent novel objects (Trial 1).

Fig. 7

(A) Experiment 1a: discrimination ratio (updated D2) when rats were presented with one novel object and one highly familiar object. (B) Experiment 1c: discrimination ratio (D2) on Trial 7 when rats explored one novel object and one highly familiar object after three retention delays: < 1, 15 or 90 min. The PRh group is represented by black triangles, the Control group by white circles. Scores can range from −1 to +1. Data shown are mean ± standard error of the mean. The dashed line is chance. In the schematic of the testing protocol (see Table 1) bold letters (upper) represent novel objects and lower letters represent familiar objects.

Fig. 8

Experiment 2: performance of rats with perirhinal cortex lesions (PRh, black triangles) and their controls (Controls, white circle). (A) The left graph shows the trial by trial discrimination ratio (D2) when a series of novel objects is paired with the same, repeated familiar object for four trials (Experiment 2a). (B) Experiment 2b is a replication of Experiment 2a, except that an additional trial was given with recognition testing for that trial in the dark. Scores can range from −1 to +1. Data shown are mean ± standard error of the mean. Group differences *P< 0.05, ***P< 0.001. The dashed line is chance. In the schematic of the testing protocol (see Table 1) bold letters (upper) represent novel objects and lower letters represent familiar objects.