Monkeys recall and reproduce simple shapes from memory

Abstract

If you draw from memory a picture of the front of your childhood home, you will have demonstrated recall. You could also recognize this house upon seeing it. Unlike recognition, recall demonstrates memory for things that are not present. Recall is necessary for planning and imagining, and it can increase the flexibility of navigation, social behavior, and other cognitive skills. Without recall, memory is more limited to recognition of the immediate environment. Amnesic patients are impaired on recall tests [1, 2], and recall performance often declines with aging [3]. Despite its importance, we know relatively little about nonhuman animals' ability to recall information; we lack suitable recall tests for them and depend instead on recognition tests to measure nonhuman memory. Here we report that rhesus monkeys can recall simple shapes from memory and reproduce them on a touchscreen. As in humans [4, 5], monkeys remembered less in recall than recognition tests, and their recall performance deteriorated more slowly. Transfer tests showed that monkeys used a flexible memory mechanism rather than memorizing specific actions for each shape. Observation of recall in Old World monkeys suggests that it has been adaptive for over 30 million years [6] and does not depend on language.

Figure 1

Schematic of the progression of a recall test (top) and matched recognition test (bottom). Monkeys started both tests by touching the green “start box” (FR=2 for all responses). An image then appeared and they had to touch the blue box, ensuring that they had seen the sample image. After a delay, the blue box appeared in a new location and the monkeys touched it to initiate the test phase. For the recalltests, monkeys earned food if they reproduced the studied shape by touching the appropriate grid location for the red box. For the recognition tests, monkeys earned food for touching the test stimulus if it was the same as that presented at study (depicted) or the non-match symbol if it was not. The small white crosses shown in the last panel of the recall test indicated to the monkeys which response locations were available. In the first phase of training, the white crosses were present in all the locations abutting the blue box. For the comparison with recognition, we reduced the response locations to two, which allowed us to equate the chance rate in the recall and recognition tests at 50%, permitting us to directly compare performance in the two types of test.

Figure 2

Under precisely matched testing conditions, monkeys showed greater accuracy and faster forgetting in the recognition test than in the recall test (two-factor within-subject ANOVA (test type X delay): main effect of test type (F_(1,4) = 6.66, p = .061), main effect of delay (F_(7,28) = 38.54, p < .001), and interaction (F_(7,28) = 3.96, p = .004)). Accuracy in both recall and recognition is reported as d′ [27], as a function of the delay in seconds between study and test. Error bars represent one standard error of the mean.

Figure 3

Monkeys successfully generalized to novel shapes. Accuracy was above chance on the first session both when monkeys had to reproduce one box of a three-box shape (middle bar; chance = .5; one-sample t-test: t₍₄₎ = 7.03, p = .002) and when they had to reproduce two boxes of a three-box shape (right bar; chance = .25; one-sample t-test: t₍₄₎ = 10.75, p < .001). Dashed lines represent accuracy expected by chance. Asterisks mark performance that is significantly above chance. Error bars are ± one standard error of the mean.