Corticohippocampal contributions to spatial and contextual learning

Abstract

Spatial and contextual learning are considered to be dependent on the hippocampus, but the extent to which other structures in the medial temporal lobe memory system support these functions is not well understood. This study examined the effects of individual and combined lesions of the perirhinal, postrhinal, and entorhinal cortices on spatial and contextual learning. Lesioned subjects were consistently impaired on measures of contextual fear learning and consistently unimpaired on spatial learning in the Morris water maze. Neurotoxic lesions of perirhinal or postrhinal cortex that were previously shown to impair contextual fear conditioning (Bucci et al., 2000) or contextual discrimination (Bucci et al., 2002) caused little or no impairment in place learning and incidental learning in the water maze. Combined lesions of perirhinal plus lateral entorhinal or postrhinal plus medial entorhinal cortices resulted in deficits in acquisition of contextual discrimination but had no effect on place learning in the water maze. Finally, a parahippocampal lesion comprising combined neurotoxic damage to perirhinal, postrhinal, and entorhinal cortices resulted in profound impairment in acquisition of a standard passive avoidance task but failed to impair place learning. In the same experiment, rats with hippocampal lesions were impaired in spatial navigation. These results indicate that tasks requiring the association between context and an aversive stimulus depend on corticohippocampal circuitry, whereas place learning in the water maze can be accomplished without the full complement of highly processed information from the cortical regions surrounding the hippocampus. The evidence that different brain systems underlie spatial navigation and contextual learning has implications for research on memory when parahippocampal regions are involved.

Figure 1.

Effects of damage to PER or POR in experiment 1. A, Latency to find the hidden platform during training trials. B, Average proximity to the platform during probe trials. Average proximity to the platform during probe trials was comparable across blocks for CTL and POR groups, but the PER group was mildly impaired. C, Relationship between mean contextual freezing in the first four 64 sec blocks of extinction (Bucci et al., 2000) and performance on the water maze (present study) as indicated by a learning index. Percentage of freezing during extinction in the contextual fear conditioning task was significantly correlated with performance on the water maze task overall, but not within groups. CTL, Control group; PER, perirhinal-lesioned group; POR, postrhinal-lesioned group. Data are mean ± SEM.

Figure 2.

Effects of damage to PER or POR on two water maze tasks in experiment 2. Place learning is shown in A and B, and incidental learning is shown in C and D. A, Latency to find the hidden platform during training trials. B, Average proximity to the platform during probe trials. C, Latency to swim to the visible platform during training trials. D, Time spent in each quadrant of the water maze during the final (probe) trial during incidental learning in the water maze. There were no group differences on either task. CTL, Control group; PER, perirhinal-lesioned group; POR, postrhinal-lesioned group. Data are mean ± SEM.

Figure 3.

PER/LEA and POR/MEA lesions. A, Schematic of the largest (gray) and smallest (black) PER/LEA neurotoxic lesions. B, Schematic of the largest (gray) and smallest (black) POR/MEA neurotoxic lesions. LEA, Lateral entorhinal cortex; MEA, medial entorhinal cortex; PaSub, parasubiculum; PER, perirhinal cortex; POR, postrhinal cortex.

Figure 4.

Effects of damage to PER/LEA or POR/MEA on contextual fear discrimination and place learning in the Morris water maze in experiment 3. A, Control rats successfully discriminated between the two contexts. Discrimination was impaired for lesioned rats.B, Latency to find the hidden platform during training trials.C, Average proximity to the platform during probe trials. Similar to findings for the PER and POR lesions, latency to find the platform decreased during training but did not differ between lesion groups. Probe trial performance during place training was also comparable for control and lesioned groups. CTL, Control group; PER/LEA, perirhinal plus lateral entorhinal-lesioned group; POR/MEA, postrhinal plus medial entorhinal-lesioned group. Data are mean ± SEM.

Figure 5.

Parahippocampal and hippocampal lesions. A, Schematic of the largest (gray) and smallest (black) parahippocampal neurotoxic lesions. B, Schematic of the largest (gray) and smallest (black) hippocampal neurotoxic lesions. LEA, Lateral entorhinal cortex; MEA, medial entorhinal cortex; PER, perirhinal cortex; POR, postrhinal cortex.

Figure 6.

Effects of damage to PH- or HC-lesioned rats on the Morris water maze task and on passive avoidance in experiment 4. A, Latency to find the hidden platform during training trials. B, Average proximity to the platform during probe trials. Similar to findings for the smaller lesions, latency to find the platform decreased during training but did not differ between the PH and CTL groups. Likewise, proximity to the platform location during probe trial performance was comparable for the PH and CTL groups. In contrast, the HC-lesioned rats were significantly impaired during training and on probe trials. C, Latency to enter the dark chamber on retention day of passive avoidance testing for CTL, PH, and HC lesion groups. Data are mean ± SEM. D, Relationship between log latency to enter the dark chamber in passive avoidance and performance on the water maze as indicated by a spatial learning index (see Results for details). Performance on the two tasks was not significantly correlated. CTL, Control group; HC, hippocampal-lesioned group; PH, combined perirhinal, postrhinal, lateral entorhinal, and medial entorhinal-lesioned group.