Dissociated effects of perirhinal cortex ablation, fornix transection and amygdalectomy: evidence for multiple memory systems in the primate temporal lobe

Four experiments were performed with macaque monkeys (rhesus, Macaca mulatta, and cynomolgus, M.fascicularis). In experiment 1 six rhesus monkeys learned pre-operatively to perform delayed matching-to-sample, with complex naturalistic scenes as the stimulus material. Three of these monkeys then received bilateral ablations of the perirhinal cortex, while the other three received fornix transection. Both groups showed an impairment postoperatively, but the effect of perirhinal cortex ablation was significantly more severe than the effect of fornix transection. In experiment 2 the same animals, together with three normal, control rhesus monkeys,which had a similar training history, performed simple, spatial discrimination learning in a Wisconsin General Test Apparatus. The animals with fornix transection were impaired, but the animals with ablations of perirhinal cortex were not. In experiment 3 the nine animals from experiment 2 were tested for the acquisition of systematic preferences among four novel foods (apple, lemon, olive, meat). Their results were compared with those from a previously published experiment with normal and amygdalectomized cynomolgus monkeys which had been given the same food preference test. Amygdalectomy produced a significant disruption of food preference learning but the other two lesions (fornix transection and perirhinal cortex ablation) did not. In experiment 4, 16 rhesus monkeys (9 normal controls, 4 with perirhinal cortex ablation, and 3 with fornix transection) learned to discriminate among complex naturalistic scenes, in a task in which each scene was presented only once per day in the main part of the experiment. The two operated groups were impaired, and there was no significant difference between the severity of the impairments. Thus, the effects of perirhinal cortex ablation can be doubly dissociated from the effects of fornix transection (experiments 1 and 2) and both can be dissociated from the effects of amygdalectomy (experiment 3). Furthermore, the results of experiment 4 show that the effects of perirhinal cortex ablation are not limited to tasks of memory over short retention intervals. On the basis of the presently reported data and other known effects of perirhinal cortex ablation, it is suggested that this ablation produces an impairment in knowledge (semantic memory) about objects.