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The theory that the hippocampus is critical for visual memory and relational cognition has been challenged by discovery of more spared hippocampal tissue than previously reported in H.M., previously unreported extra-hippocampal damage in developmental amnesiacs, and findings that the hippocampus is unnecessary for object-in-context memory in monkeys. These challenges highlight the need for causal tests of hippocampal function in nonhuman primate models. Here, we tested rhesus monkeys on a battery of cognitive tasks including transitive inference, temporal order memory, shape recall, source memory, and image recognition. Contrary to predictions, we observed no robust impairments in memory or relational cognition either within- or between-groups following hippocampal damage. These results caution against over-generalizing from human correlational studies or rodent experimental studies, compel a new generation of nonhuman primate studies, and indicate that we should reassess the relative contributions of the hippocampus proper compared to other regions in visual memory and relational cognition. 

Abstract Human working memory is a capacity- and duration-limited system in which retention and manipulation of information is subject to metacognitive monitoring and control. At least some nonhuman animals appear to also monitor and control the contents of working memory, but only relatively simple cases where animals monitor or control the presence or absence of single memories have been studied. Here we combine a comparatively complex order memory task with methodology that assesses the capacity to introspect about memory. Monkeys observed sequential presentations of five images, and at test, reported which of two images from the list had appeared first during study. Concurrently, they chose to complete or avoid these tests on a trial-by-trial basis. Monkeys “knew when they knew” the correct response. They were less accurate discriminating images that had appeared close in time to one another during study and were more likely to avoid these difficult tests than they were to avoid easier tests. These results indicate that monkeys can metacognitively monitor relatively complex properties of the contents of working memory, including the quality of representations of temporal relations among images. 

We studied the memory representations that control execution of action sequences by training rhesus monkeys ( Macaca mulatta) to touch sets of five images in a predetermined arbitrary order (simultaneous chaining). In Experiment 1, we found that this training resulted in mental representations of ordinal position rather than learning associative chains, replicating the work of others. We conducted novel analyses of performance on probe tests consisting of two images “derived” from the full five-image lists (i.e., test B, D from list A→B→C→D→E). We found a “first item effect” such that monkeys responded most quickly to images that occurred early in the list in which they had been learned, indicating that monkeys covertly execute known lists mentally until an image on the screen matches the one stored in memory. Monkeys also made an ordinal comparison of the two images presented at test based on long-term memory of positional information, resulting in a “symbolic distance effect.” Experiment 2 indicated that ordinal representations were based on absolute, rather than on relative, positional information because subjects did not link two lists into one large list after linking training, unlike what occurs in transitive inference. We further examined the contents of working memory during list execution in Experiments 3 and 4 and found evidence for a prospective, rather than a retrospective, coding of position in the lists. These results indicate that serial expertise in simultaneous chaining results in robust absolute ordinal coding in long-term memory, with rapidly updating prospective coding of position in working memory during list execution.