Rhesus monkeys (Macaca mulatta) show robust evidence for memory awareness across multiple generalization tests

Abstract

The possibility that memory awareness occurs in nonhuman animals has been evaluated by providing opportunity to decline memory tests. Current evidence suggests that rhesus monkeys (Macaca mulatta) selectively decline tests when memory is weak (Hampton in Proc Natl Acad Sci USA 98:5359-5362, 2001; Smith et al. in Behav Brain Sci 26:317-374, 2003). However, much of the existing research in nonhuman metacognition is subject to the criticism that, after considerable training on one test type, subjects learn to decline difficult trials based on associative learning of external test-specific contingencies rather than by evaluating the private status of memory or other cognitive states. We evaluated whether such test-specific associations could account for performance by presenting monkeys with a series of generalization tests across which no single association with external stimuli was likely to adaptively control use of the decline response. Six monkeys performed a four alternative delayed matching to location task and were significantly more accurate on trials with a decline option available than on trials without it, indicating that subjects selectively declined tests when memory was weak. Monkeys transferred appropriate use of the decline response under three conditions that assessed generalization: two tests that weakened memory and one test that enhanced memory in a novel way. Bidirectional generalization indicates that use of the decline response by monkeys is not controlled by specific external stimuli but is rather a flexible behavior based on a private assessment of memory.

Figure 1

Photograph of the testing tray. The tray was pushed forward to the monkey's cage during the choice phase of trials. One of the four black choice cups normally contained two raisins. The flat green disk provided a decline-test option rewarded with a single raisin and was present only on choice trials. The opaque barrier visible in the top left of the photograph was used to obscure the monkeys’ view of the test tray between trials and during delay intervals.

Figure 2

Average accuracy on forced tests and chosen tests in Experiment 1. Chance, .25, is indicated by the dashed line. Error bars are standard errors of the means.

Figure 3

Probability of the decline response on normal trials, on which a choice cup was baited, and on no sample trials, on which no choice cup was baited in Experiment 2. Grey bars represent the first session only, consisting of 6 no sample probe trials and 12 normal trials per monkey. Black bars represent average performance across all 5 sessions, totaling 30 probes and 60 normal trials. Error bars are standard errors of the mean.

Figure 4

Performance on forced and chosen tests after a short delay (3 s), medium delay (6, 12, 24, 48 s depending on the monkey's criterion delay), and long delay (96 s) in Experiment 3. The proportion of correct trials for forced (filled squares) and chosen (open squares) tests corresponds with the left y-axis. Proportion of trials declined (filled circles) corresponds to the right y-axis. Error bars are standard errors of the means.

Figure 5

Average accuracy on forced and chosen trials beginning with either normal or double samples in Experiment 4. Accuracies correspond to the left y-axis while probability of the decline response is indexed on the right y-axis. Error bars are standard errors of the means.