Explicit memory and cognition in monkeys

Abstract

Taxonomies of human memory, influenced heavily by Endel Tulving, make a fundamental distinction between explicit and implicit memory. Humans are aware of explicit memories, whereas implicit memories control behavior even though we are not aware of them. Efforts to understand the evolution of memory, and to use nonhuman animals to model human memory, will be facilitated by better understanding the extent to which this critical distinction exists in nonhuman animals. Work with metacognition paradigms in the past 20 years has produced a strong case for the existence of explicit memory in nonhuman primates and possibly other nonhuman animals. Clear dissociations of explicit and implicit memory by metacognition have yet to be demonstrated in nonhumans, although dissociations between memory systems by other behavioral techniques, and by brain manipulations, suggest that the explicit-implicit distinction applies to nonhumans. Neurobehavioral studies of metamemory are beginning to identify neural substrates for memory monitoring in the frontal cortex of monkeys. We have strong evidence that at least some memory systems are explicit in rhesus monkeys, but we need to learn more about the distribution of explicit processes across cognitive systems within monkeys, and across species.

Keywords: Implicit; Memory monitoring; Memory systems; Metacognition; Monkey; Primate; Tulving.

Fig. 1.. Taxonomy of human memory systems (Squire and Zola-Morgan, 1991).

Implicit memory affects behavior without awareness. In contrast, humans are consciously aware of explicit memories. In other words, explicit memories and accessible to cognitive monitoring, but implicit memories are not. We use this difference in accessibility to metacognitive monitoring to classify nonhuman primate cognitive systems.

Fig. 2.. A memory monitoring paradigm for detecting explicit memory in monkeys.

Each panel depicts what the monkey saw on a touch-sensitive computer monitor at different stages in a trial.

Fig. 3.. Process Dissociation Paradigm for monkeys.

Each row represents one trial with one of the image quads that was shown to monkeys each day. The leftmost images represent the to-be-remembered sample image monkeys saw at the beginning of a trial. The four images to the right represent the choice images displayed at test (these images were randomly assigned to the four corners of the touch screen; the box indicates which image was correct and was not shown to the monkeys). Unlike in a normal recognition memory test procedure, here the selection of the sample image was parametrically biased toward the high frequency image (the blimp in this one case). After many days of training, monkeys were given probe trials of two types. On congruent probes, a high frequency image was the to-be-remembered sample, just as in training. On incongruent probes, a different image was selected as the sample, and the same choice stimuli appeared at test. Monkeys tended to make errors by selecting the high frequency image on incongruent trials (the blimp in this case). A double dissociation was revealed both by manipulating the strength of habits by varying the bias used with samples, and by manipulating memory by varying the memory interval between study and test. Habit and memory varied independently.

Fig. 4.. Memory, but not habit, was impaired by perirhinal cortex lesions (Tu et al., 2011).

Lesions impaired intra-trial memory (“memory”) but left extra-trial memory (“habits”) intact. Bars represent the scores resulting from the analysis of congruent and incongruent trials in the PDP paradigm.

Fig. 5.. Test of dynamic cognitive monitoring of decision-making.

Monkeys touched the green square to start the trial. When the grey plaque appeared, monkeys could touch the purple button to gradually reveal the image. They were free to identify the image as a bird, fish, person, or flower at any time by contacting the choice stimuli in the corners of the screen. Monkeys regulated how much of the image they revealed, pressing the button more times when each button press revealed only a small part of the image, and pressing fewer times when each press revealed a large part of the image (Tu et al., 2015).