Interaction of perirhinal cortex with the fornix-fimbria: memory for objects and "object-in-place" memory

Abstract

Four monkeys (Macaca mulatta) were trained preoperatively in an automated object-in-place memory task in which they learned 20 new scenes in each daily session. In the object-in-place memory task, the correct, rewarded response in each scene is to a particular object of a pair, which always occupies a particular position in a unique background that has been generated using randomly chosen colors and shapes. Each animal then underwent two surgeries, with a period of testing after each. In the first, control surgery, each animal had either a unilateral lesion of the perirhinal cortex or unilateral fornixfimbria transection, combined with section of the body and splenium of the corpus callosum and the anterior commissure (to prevent interhemispheric transfer of visual information). The disconnection was completed in the second surgery, after which all animals had a unilateral perirhinal cortex ablation in one hemisphere, unilateral fornix-fimbria transection in the contralateral hemisphere, and partial forebrain commissurotomy. The monkeys performance was compared for the learning of 200 scenes, preoperatively and after each surgery. After control surgery, the animals were mildly impaired on the object-in-place task. After disconnection, the animals showed a severe impairment in object-in-place memory. We conclude from this that, in episodic memory, the perirhinal cortex provides input of visual object information to the subiculum, hippocampus, and fornix.

Fig. 1.

Five sections from each animal to illustrate the unilateral perirhinal cortex lesion. The entire hemisphere is shown in the top row, for orientation, and the temporal lobe is shown at greater magnification in the four lower rows. The sections, running from anterior at the left to posterior at the right, are from S3 (rows 1 and 2), S1 (row 3), S2 (row 4), and S4 (row 5). Sections are ∼2.5 mm apart in the fixed tissue. See text for description of ablations. Sections from animals S1, S2, and S3 are from the right hemisphere. The sections from animal S4 are from the left hemisphere and have been mirror-image-reversed for ease of comparison with the other animals.

Fig. 2.

Three sections from one animal (S3) to illustrate the method of unilateral fornix transection. The sections are 1.5 mm apart in the fixed tissue and run from anterior on theleft to posterior on the right. Sections from the other animals were similar to these.

Fig. 3.

Results from the three phases of the experiment.Left, Average trial-by-trial learning in 10 lists of 20 scenes. Each list was presented for eight trials. Open square, Preoperative; filled triangle, postoperation 1; filled circle, postoperation 2. Right, Average percentage error score for all four animals in each phase of the experiment. Subject 1, triangle; Subject 2, square; Subject 3, inverted triangle; Subject 4, circle.