Evaluation of seven hypotheses for metamemory performance in rhesus monkeys

Abstract

Knowing the extent to which nonhumans and humans share mechanisms for metacognition will advance our understanding of cognitive evolution and will improve selection of model systems for biomedical research. Some nonhuman species avoid difficult cognitive tests, seek information when ignorant, or otherwise behave in ways consistent with metacognition. There is agreement that some nonhuman animals "succeed" in these metacognitive tasks, but little consensus about the cognitive mechanisms underlying performance. In one paradigm, rhesus monkeys visually searched for hidden food when ignorant of the location of the food, but acted immediately when knowledgeable. This result has been interpreted as evidence that monkeys introspectively monitored their memory to adaptively control information seeking. However, convincing alternative hypotheses have been advanced that might also account for the adaptive pattern of visual searching. We evaluated seven hypotheses using a computerized task in which monkeys chose either to take memory tests immediately or to see the answer again before proceeding to the test. We found no evidence to support the hypotheses of behavioral cue association, rote response learning, expectancy violation, response competition, generalized search strategy, or postural mediation. In contrast, we repeatedly found evidence to support the memory monitoring hypothesis. Monkeys chose to see the answer when memory was poor, either from natural variation or experimental manipulation. We found limited evidence that monkeys also monitored the fluency of memory access. Overall, the evidence indicates that rhesus monkeys can use memory strength as a discriminative cue for information seeking, consistent with introspective monitoring of explicit memory.

Figure 1

Trial progression of the computerized information-seeking task as presented during the final test phase. Monkeys initiated each trial by touching a green square (top). At study, monkeys either saw a blank screen (Unseen trials) or a sample in one of four screen locations (Seen trials). After an unfilled memory delay, four dim blue boxes appeared to mark the possible locations, but were not yet responsive to touches. Two symbols also appeared to mark the metacognitive response options. Touching the green recycle symbol extinguished all symbols, caused the red dot to appear as in the sample phase of Seen trials, and then proceeded to the memory test. Touching the blue arrow extinguished the metacognitive symbols and initiated the memory test. At the memory test, four bright blue boxes marked the possible locations. If the monkey touched the box marking the correct location, the box disappeared, revealing the red dot, and touching the red dot produced a food reward and a positive audio reinforcement (“Excellent!”). If the monkey touched one of the three incorrect boxes, that box disappeared, revealing nothing, followed by a negative audio stimulus (“D’oh!”) and an unfilled two-second timeout. Trials were separated by an unfilled 10-second interval. To prevent accidental choices, all responses required two consecutive touches to the same response location. Touches to the correct location during the memory delay aborted the trial.

Figure 2

Diagram of screen displays used to test metamemory in monkeys. Each panel represents an example display as monkeys saw it. The first row represents the study phases of trials, and the second row represents what monkeys saw at the time of metacognitive choice. If monkeys chose to see the answer, they then saw what is depicted in the third row, followed by a test like that depicted in the fourth row. If monkeys chose to proceed to the test, what is depicted in the third row was skipped and they proceeded directly to the test depicted in the fourth row. From left to right, columns represent displays from the concurrent metacognitive judgment of memory for a spatial location in Experiments 1 and 2, the Forced Answer and Forced Test trials as used in the spatial experiments, the missing-location probe trials in Experiment 3, the high-value probe trials in Experiment 4, the prospective metacognitive judgment of memory for a spatial location in Experiment 5, and the prospective metacognitive judgment of memory for an image in Experiment 6. For Forced Answer and Forced Test trials in Experiments 5 and 6, the single available metacognitive option was presented alone on the screen. The progression of trials in all experiments followed the pattern shown in Figure 1.

Figure 3

Proportion (SEM) of Seen and Unseen trials on which monkeys chose to see the answer in Experiment 1.

Figure 4

Proportion correct (SEM) on Seen and Unseen trials in Experiment 1. Light bars represent trials on which the monkeys chose to see the answer. Dark bars represent trials on which monkeys chose to take the test. The horizontal dashed line represents accuracy expected by chance.

Figure 5

Accuracy and choice to see the answer as a function of memory delay in Experiment 2. The solid green line depicts the proportion (SEM) of Forced Test trials at each delay on which the monkey was correct. The dashed blue line depicts the proportion (SEM) of Seen trials at each delay on which the monkey chose to see the answer. The horizontal dashed gray line represents the proportion correct expected by chance.

Figure 6

Individual change in accuracy as a function of individual change in choice to see the answer in Experiment 2. Each dot represents one monkey. Individual changes are the values at the longest delay subtracted from the values at the trained one-second delay. For example, the most upper-left point represents a monkey for which proportion correct was 1 at the 1s delay and .25 at the 4s delay, and for which proportion of trials on which he chose to see the answer was .3 at the 1s delay and 1 at the 4s delay.

Figure 7

Choice to see the answer as a function of whether the correct location was present at test in Experiment 3. Bars depict the proportion (SEM) of Seen trials on which the monkey chose to see the answer.

Figure 8

Accuracy and choices to see the answer as a function of stimulus value in Experiment 4. The solid green line depicts the proportion (SEM) of Forced Test trials on which the monkey was correct. The dashed blue line depicts the proportion (SEM) of Seen trials on which the monkey chose to see the answer. The horizontal dashed gray line represents the proportion correct expected by chance. The left panel depicts performance at the trained 1s memory delay, whereas the right panel depicts performance at a longer 4s memory delay.

Figure 9

Individual change in accuracy as a function of the individual change in choice to see the answer in Experiment 4. Each dot represents one monkey. Individual changes are the values with the high-value target subtracted from the values with the normal-value target. The left panel depicts performance at the trained 1s memory delay, whereas the right panel depicts performance at a longer 4s memory delay.

Figure 10

Proportion (SEM) of Seen and Unseen trials on which monkeys prospectively chose to see the answer in Experiment 5.

Figure 11

Proportion (SEM) of Seen and Unseen trials on which monkeys prospectively chose to see the answer prior to the image-memory test in Experiment 6.