Elsevier

Neuropsychologia

Volume 138, 17 February 2020, 107326
Neuropsychologia

Explicit memory and cognition in monkeys

https://doi.org/10.1016/j.neuropsychologia.2019.107326Get rights and content

Highlights

  • Monkeys monitor, or introspect about, some of their cognitions, including memories.

  • This capacity to monitor is consistent with explicit cognition and memory.

  • Current findings strongly encourage new comparative and neurobehavioral work.

  • New work will help characterize the distribution and function of explicit cognition.

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.

Section snippets

Metacognition and memory monitoring paradigms provide psychologically valid measures of explicit memory for drawing parallels in cognition among species

In humans, memory monitoring is associated with consciousness and is often identified on the basis of verbal reports of private experience (e.g., “I knew” versus “I guessed”). Because nonhuman species cannot provide verbal reports on their experience of memory, to determine whether nonhumans have explicit cognition, we need to establish other behavioral criteria that discriminate between explicit and implicit memories. Given that even complex cognitions, such as correct use of grammar (Knowlton

Rhesus monkeys monitor memory

In traditional tests of memory in nonhuman animals, subjects are given “forced-choice” tests in which they simply do the best they can with what information they have. There are no behavioral options analogous to asking a friend for the name of the acquaintance. But paradigms have been developed in several laboratories that do provide animals with such alternatives, thus more accurately modeling situations in which humans make adaptive choices based on memory monitoring. Most of this work has

Nonhumans have dissociable memory systems

Understanding how different memory systems act together or independently to control behavior is a major challenge in the study of the brain's multiple memory systems (Cohen and Eichenbaum, 1994; Eichenbaum et al., 2007; Fernandez-Ruiz et al., 2001; Kim and Baxter, 2001; McDonald and White, 1993; Packard, 1999; Packard and McGaugh, 1996; Poldrack and Packard, 2003; Schroeder et al., 2002; Sherry, 2006). Often more than one memory system participates even in “simple” memory tests. In a

Some dissociations of cognitive systems are suggestive of the explicit-implicit distinction in monkeys, but are not conclusive

Because both implicit and explicit memory may contribute to performance in a given cognitive task, it will be rare for there to be a one-to-one correspondence between specific memory tests and these types of memory. One approach that may distinguish the relative contributions of explicit and implicit memory systems is Process Dissociation Paradigm (PDP), which was specifically designed to quantify the contributions of multiple memory systems within a single cognitive test (Hay and Jacoby, 1996;

Behavioral dissociation of putative explicit and implicit memory systems by PDP is consistent with neurobiological evidence in nonhuman animals

Evidence from neurobiological studies in primates has identified the temporal lobe and striatum as distinct recipients of visual information. The primate ventral visual processing stream conveys highly processed visual information to both the medial temporal lobes (Suzuki, 1996) and tail of caudate and ventral putamen (Saintcyr et al., 1990; Webster et al., 1993). This is consistent with the idea that the temporal lobe and striatum support parallel visual memory systems, the former associated

Frontal brain regions are involved in metamemory in monkeys

While temporal lobe and basal ganglia structures have been identified as critical for memory, adaptive behavior results from activation of a larger network of brain areas, often including the frontal cortex (e.g. Burgess, Maguire, Spiers and O'Keefe, 2001). There are strong reciprocal connections between the temporal lobes and frontal cortices (e.g. Goldman-Rakic et al., 1984; Lavenex and Amaral, 2000; Rempel-Clower and Barbas, 2000), such that frontal cortices are positioned to monitor and

Evidence from perceptual tasks is consistent with a distinction between implicit and explicit cognition in monkeys

Much of this review has focused on work in metamemory, and the question of whether monkeys metacognitively monitor at least some of their memory processes. Memory is just one of many possible target cognitive processes for metacognition. Humans also have introspective access to some perceptual processes, evident in our ability to predict the accuracy of perceptual and other judgements (Shields et al., 2005; Shields et al., 1997). At the same time, it is well documented that vast portions of

Cognitive control is likely limited to explicit cognition and likely depends on metacognition

It is likely that much of the adaptive function of metacognitive monitoring manifests in the role monitoring fills-- providing feedback to regulate cognitive control. Knowing you don't know is not much use if there is nothing you can do about it. The establishment of metacognition in monkeys positions us to shift the focus of our studies from whether metacognition occurs at all to identification of the properties of the interplay between monitoring processes and the control of cognitive states.

Some speculations on how working memory and explicit cognition are intertwined

To a large extent, material processed in working memory is the material of which we are conscious. Working memory actively maintains information in a heightened state of accessibility using extremely limited cognitive resources (Baddeley, 2003; Baddeley and Hitch, 1974; Basile and Hampton, 2013; Cowan, 2008; Unsworth and Engle, 2007). In contrast to long term memory, which is capacious and apparently passive once established, when we fail to “attend” to working memory, information is rapidly

Summary and prospects for the future

The studies reviewed demonstrate that monkeys monitor some of their memories. They know when they remember. They avoid tests when they do not know the answer. They seek information when ignorant. Their behavior captures core functional properties of explicit memory, as conveyed to us by Tulving. Monkeys clearly have multiple memory systems, and these systems dissociate in patterns that parallel findings in humans, such as with process dissociation paradigm. It is reasonable to state that

Acknowledgment

Preparing this manuscript was support by National Science Foundation grant BCS-1632477 and by the National Institutes of Health’s Office of the Director, Office of Research Infrastructure Programs, P51OD011132.

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