Rhesus monkeys know when they remember

Abstract

Humans are consciously aware of some memories and can make verbal reports about these memories. Other memories cannot be brought to consciousness, even though they influence behavior. This conspicuous difference in access to memories is central in taxonomies of human memory systems but has been difficult to document in animal studies, suggesting that some forms of memory may be unique to humans. Here I show that rhesus macaque monkeys can report the presence or absence of memory. Although it is probably impossible to document subjective, conscious properties of memory in nonverbal animals, this result objectively demonstrates an important functional parallel with human conscious memory. Animals able to discern the presence and absence of memory should improve accuracy if allowed to decline memory tests when they have forgotten, and should decline tests most frequently when memory is attenuated experimentally. One of two monkeys examined unequivocally met these criteria under all test conditions, whereas the second monkey met them in all but one case. Probe tests were used to rule out "cueing" by a wide variety of environmental and behavioral stimuli, leaving detection of the absence of memory per se as the most likely mechanism underlying the monkeys' abilities to selectively decline memory tests when they had forgotten.

Figure 1

Method for assessing whether monkeys know when they remember. Each colored panel represents what monkeys saw on a touch-sensitive computer monitor at a given stage in a trial. At the start of each trial, monkeys studied a randomly selected image. A delay period followed over which monkeys often forgot the studied image. In two-thirds of trials, animals chose between taking a memory test (Right, left-hand stimulus) and declining the test (Right, right-hand stimulus). In one-third of trials, monkeys were forced to take the test (Left). Better accuracy on chosen than on forced tests indicates that monkeys know when they remember and decline tests when they have forgotten, if given the option.

Figure 2

Accuracy on freely chosen and forced tests. Dark bars represent accuracy on tests the monkeys chose to take. Light bars represent performance on trials where the animals were not given the choice of declining tests. Scores for the two monkeys are the means of 10 daily sessions. Error bars are standard errors. Subjects would be correct 25% of the time if guessing.

Figure 3

Probability of declining tests on normal trials and on probe trials lacking an image to study. Dark bars show the proportion of normal trials in which monkeys declined tests; the light bars represent this proportion in probe trials. Error bars are standard errors. Inset in each bar is the percent of each test type declined only in the first session of testing. These results indicate that it is the absence of a memory that causes the monkeys to decline tests. If some factor other than the absence of memory per se, such as distracting noises, variation in motivation, or fatigue, controlled the decision to decline tests, normal and probe trials would be affected equally.

Figure 4

Accuracy and the probability of declining tests after variable delay intervals. Filled squares depict the probability of declining tests. Open circles represent accuracy on freely chosen tests and filled circles represent accuracy on forced tests. Error bars are standard errors.