Perirhinal cortex removal dissociates two memory systems in matching-to-sample performance in rhesus monkeys

Abstract

Dissociations of memory systems are typically made using independent cognitive tests. For example, in monkeys habits have been inferred from performance in object discrimination tests, while non-matching-to-sample tests are thought to measure familiarity resulting from single exposures. Such tests cannot measure individual memory processes accurately when more than one memory process contributes to performance. In process dissociation procedures (PDPs), two memory processes cooperate and compete in the performance of a single cognitive task, allowing quantitative estimates of the contributions of each process. We used PDP to measure the contributions of habits and one-trial memory to visual matching-to-sample performance. Sets of test images were shown only once in each daily testing session but were repeated day after day. To produce habits, high-frequency images were correct more frequently than other images across days. Habits were manifest in the extent to which choices in the test phase of matching-to-sample trials were made to the high-frequency images, regardless of which image had been presented as the sample. One-trial memory was measured by the extent to which choices at test were made to the image that had appeared as the sample on that trial, regardless of habit. Perirhinal cortex removal reduced the contribution of one-trial memory to matching performance, but left both habits and the ability to discriminate images intact. PDP can be applied in monkeys in a way that parallels its use in humans, providing a new tool for investigating the neurobiology of memory in nonhuman animals and for comparing memory across species.

Figure 1.

Each image quad appeared once in each daily testing session. Because one of the four images in each image quad was the sample more frequently than the others, there is opportunity for habits to select these high-frequency images to develop through repeated reinforcement. A total of 72 quads were used. Only one image quad is illustrated in the figure. The illustration shows a high-frequency image appearing as the sample on every single trial, as in Experiment 3. In Experiment 2, the three images in each image quad that were not the high-frequency image each appeared as the sample with a probability of 0.1.

Figure 2.

Location and extent of the perirhinal cortex lesion in PRh-E. The intended lesion of perirhinal cortex (shaded region) is shown on coronal sections from a standard rhesus monkey brain (left column). Postoperative MR images from matching levels (middle column) and plots of the lesion (shaded region) onto sections (right column) show the extent of the lesion in PRh-E. Numerals indicate distance in millimeters from the interaural plane. White arrows in the MR images show the boundaries of the lesion.

Figure 3.

Average matching-to-sample performance with different delays in control monkeys (n = 4; solid line) and monkeys from which perirhinal cortex was removed bilaterally, with all PRh monkeys (n = 6; dashed line) and with PRh-D excluded (n = 5; dotted line). Error bars indicate SEs.

Figure 4.

The contributions of one-trial memory and habit to matching-to-sample performance in control monkeys (black bars) and monkeys from which perirhinal cortex was removed bilaterally, including PRh-D (gray bars). Habits were produced over 25 sessions in which high-frequency images were rewarded on 70% of trials in Experiment 2. Error bars indicate SEs. See text for details of the process dissociation procedure analysis used to generate the values.

Figure 5.

The contribution of one-trial memory and habit to matching-to-sample performance in control monkeys (black bars) and monkeys from which perirhinal cortex was removed bilaterally, including PRh-D (gray bars). Habits were further developed over 15 sessions in which high-frequency images were rewarded on 100% of trials in Experiment 3. Error bars indicate SEs. See text for details of the process dissociation procedure analysis used to generate the values.