Double dissociation between the effects of peri-postrhinal cortex and hippocampal lesions on tests of object recognition and spatial memory: heterogeneity of function within the temporal lobe

Abstract

It is widely believed that declarative memory is mediated by a medial temporal lobe memory system consisting of several distinct structures, including the hippocampus and perirhinal cortex. The strong version of this view assumes a high degree of functional homogeneity and serial organization within the medial temporal lobe, such that double dissociations between individual structures should not be possible. In the present study, we tested for a functional double dissociation between the hippocampus and peri-postrhinal cortex in a single experiment. Rats with bilateral excitotoxic lesions of either the hippocampus or peri-postrhinal cortex were assessed in tests of spatial memory (radial maze) and object recognition memory. For the latter, the spontaneous object recognition task was conducted in a modified apparatus designed to minimize the potentially confounding influence of spatial and contextual factors. A clear functional double dissociation was observed: rats with hippocampal lesions were impaired relative to controls and those with peripostrhinal cortex lesions on the spatial memory task, whereas rats with peri-postrhinal lesions were impaired relative to the hippocampal and control groups in object recognition. These results provide strong evidence in favor of heterogeneity and independence of function within the temporal lobe.

Figure 1.

Illustration of the phases of the spontaneous object recognition task as run in the Y-shaped apparatus. The nearest wall of the apparatus appears transparent for illustrative purposes. The guillotine door is shown raised. At the beginning of each phase, the rat is released from the start box when the experimenter manually raises the guillotine door. In the sample phase, the rat is exposed to identical versions of the same object, one at the end of each exploration arm. At the end of the sample phase, a variable retention delay is imposed. After the retention delay, the rat is reintroduced to the apparatus, which now contains an identical copy of the sample object at the end of one exploration arm and a novel object at the end of the other arm. Normal rats spend more time exploring the novel object.

Figure 2.

a-d, Photomicrographs illustrating lesions from the PPRH (a, b) and HPC (c, d) groups. a, Typical perirhinal cortex damage, shown here at ∼4.8 mm posterior to bregma (Paxinos and Watson, 1997). b, Postrhinal cortex lesion at ∼8.0 mm posterior to bregma. The damage observed here was typically seen throughout the rostrocaudal extent of the perirhinal and postrhinal cortex. c, Dorsal hippocampus lesion shown at ∼2.8 mm posterior to bregma. d, More posterior (approximately bregma -5.8 mm) damage in the hippocampus from the one HPC rat with any hippocampal sparing. Typically, damage was complete throughout the dorsal and ventral hippocampus. See Results for additional details.

Figure 3.

Coronal sections illustrating the extent of the largest (gray) and smallest (black) lesions of the perirhinal and postrhinal cortex, from 3.14 to 8.72 mm posterior to bregma (Paxinos and Watson, 1997).

Figure 4.

Coronal sections illustrating the extent of the largest (gray) and smallest (black) lesions of the hippocampus from 2.12 to 7.64 mm posterior to bregma (Paxinos and Watson, 1997).

Figure 5.

Spontaneous object recognition performance by control, HPC, and PPRH animals at each of four different retention interval lengths. Data are presented as average discrimination ratio ±SEM.

Figure 6.

Spatial working memory performance of control, HPC, and PPRH animals in the radial maze. a, Number of errors made in collecting all eight rewards averaged across the initial six sessions of radial maze testing. b, Number of errors made in collecting the four rewards available postdelay averaged across the two probe sessions. Data are presented as average numbers of errors ±SEM.

Figure 7.

Figure illustrating the functional double dissociation between the effects of peri-postrhinal cortex and hippocampal lesions on object recognition and spatial memory. Mean difference scores were calculated for each lesion group by subtracting performance on each task from the mean control group performance levels on that task. See Results for additional details.