The effects of selective hippocampal damage on tests of oddity in rhesus macaques

Abstract

The oddity task (e.g., A-, A-, B+) is classified as a conjunctive or relational task in which accurate performance depends upon learning to attend to stimulus relationships, not stimulus identity, and has no retention component as stimuli are presented simultaneously. It has been suggested that the hippocampus may play a particular role in learning this type of task in humans and animals. To test this, we trained adult rhesus macaques with selective neurotoxic damage to the hippocampal formation on their ability to learn and apply an oddity rule. The results suggest that the monkeys were able to adapt simple strategies to solve variations of the oddity task, however as the opportunity for such strategies was reduced, monkeys with hippocampal damage were increasingly impaired.

Figure 1

Oddity Training. A) “One-part” oddity: One member of an identical pair is presented behind the central food well. Monkeys are given a choice between the other member of the pair and an “odd” object. Displacing the odd object reveals a reward. B) “Two-part” oddity: One member of the identical pair is presented alone, covering a baited well. The monkey displaces the object to reveal a food reward. The tray is shielded from view and after a 5-sec delay, the displaced object is positioned behind the central well, and its identical pair and an odd object are placed over the lateral wells, in the same manner as for one-part oddity. The animal must select the odd (i.e. “nonmatching”) object. Two-part oddity differs from delayed nonmatching-to-sample in that the monkey is not required to retain the sample in memory. That is, the sample is present at the time of choice.

Figure 2

Performance Tasks. A) Task 1: Identical to one-part oddity, except each object covers a food well and the odd object can appear over the central well as well as either lateral well. Training Set of objects was used. B) Task 2: 19-well tray, objects can appear at any position during testing. Training Set of objects was used. C) Task3: Same as Task 2, however Probe Set of 10 identical pairs is used. On any trial there is an equal chance for an object to be presented with its pair or as an odd item (e.g. A A B, or A E E), all objects appear equally as pairs and odds within a session, and each object (as a pair or an “odd” item) is presented equally with the other 9.

Figure 3

Lesion extents for H-Ibo-7-9. Left panel is a presurgical, T1-weighted structural MR image at three levels through the hippocampus. Remaining Panels: one-week post-surgical FLAIR (fluid attenuated inversion recovery) images at the same three levels depicting lesion extent for H-Ibo-7, H-Ibo-8 & H-Ibo-9. Hypersignal indcates edema resulting from targeted ibotenic acid injections. Arrows indicate areas of hypersignal (less obvious at this resolution) indicating damage limited to CA1 and CA2 in the left hippocampus for H-Ibo-7.

Figure 4

Trials to criterion for One-part, Two-part, and One-part Repeated oddity training. Solid bars are Group N, open bars are Group H-Ibo. Error bars are standard error of the mean.

Figure 5

Trials to criterion for performance Tasks 1, 2 and 3. Conventions as in Figure 4. * indicates significant Group difference, p < 0.05. See text for discussion.