Victoria L. Templer

Rhesus monkeys (Macaca mulatta) show robust evidence for memory awareness across multiple generalization tests

The possibility that memory awareness occurs in nonhuman animals has been evaluated by providing opportunity to decline memory tests. Current evidence suggests that rhesus monkeys (Macaca mulatta) selectively decline tests when memory is weak (Hampton in Proc Natl Acad Sci USA 98:5359–5362, 2001; Smith et al. in Behav Brain Sci 26:317–374, 2003). However, much of the existing research in nonhuman metacognition is subject to the criticism that, after considerable training on one test type, subjects learn to decline difficult trials based on associative learning of external test-specific contingencies rather than by evaluating the private status of memory or other cognitive states. We evaluated whether such test-specific associations could account for performance by presenting monkeys with a series of generalization tests across which no single association with external stimuli was likely to adaptively control use of the decline response. Six monkeys performed a four alternative delayed matching to location task and were significantly more accurate on trials with a decline option available than on trials without it, indicating that subjects selectively declined tests when memory was weak. Monkeys transferred appropriate use of the decline response under three conditions that assessed generalization: two tests that weakened memory and one test that enhanced memory in a novel way. Bidirectional generalization indicates that use of the decline response by monkeys is not controlled by specific external stimuli but is rather a flexible behavior based on a private assessment of memory.

Cognitive mechanisms of memory for order in rhesus monkeys (Macaca mulatta).

One important aspect of episodic memory is the ability to remember the order in which events occurred. Memory for sequences in rats and has been shown to rely on the hippocampus and medial prefrontal cortex (DeVito and Eichenbaum (2011) J Neuro 31:3169‐3175; Fortin et al. (2002) Nat Neuro 5:458‐462). Rats with hippocampal lesions were impaired in selecting the odor that had appeared earlier in a sequence of five odors but were not impaired in recognition of previously sampled odors (Fortin et al., 2002; Kesner et al. (2002) Behav Neuro 116:286‐290). These results suggest that order is not represented by relative familiarity or memory strength. However, the cognitive mechanisms underlying memory for order have not been determined. We presented monkeys with lists of five images drawn randomly from a pool of 6,000 images. At test, two images were presented and monkeys were rewarded for selecting the image that had appeared earlier in the studied list. Monkeys learned to discriminate the order of the images, even those that were consecutive in the studied list. In subsequent experiments, we found that discrimination of order was not controlled by list position or relative memory strength. Instead, monkeys used temporal order, a mechanism that appears to encode order of occurrence relative to other events, rather than in absolute time. We found that number of intervening images, rather than passage of time per se, most strongly determined the discriminability of order of occurrence. Better specifying the cognitive mechanisms nonhuman primates use to remember the order of events enhances this animal model of episodic memory, and may further inform our understanding of the functions of the hippocampus.

Rats know when they remember: transfer of metacognitive responding across odor-based delayed match-to-sample tests

Metamemory entails cognitively assessing the strength of one’s memories. We tested the ability of nine Long-Evans rats to distinguish between remembering and forgetting by presenting a decline option that allowed a four-choice odor-based delayed match to sample (DMTS) tests to be by-passed. Rats performed significantly better on tests they chose to take than on tests they were forced to take, indicating metacognitive responding. However, rather than control by internal mnemonic cues, one alternative explanation is that decline use is based on external test-specific cues that become associated with increased rewards overtime. To examine this possibility, we tested rats on three generalization tests in which external contingencies were inconsistent and therefore could not serve as discriminative cues. Rats transferred adaptive use of the decline response in tests that eliminated memory by presenting no sample, increased memory by presenting multiple samples, and both weakened and strengthened memory by varying the retention interval. Further, subjects chose to take or decline the test before encountering the memory test, providing evidence that rats based their metacognitive responding on internal cues rather than external ones. To our knowledge, this is the first robust evidence for metamemory in rats using the DMTS decline-test paradigm in which several possible sources of external stimulus control can be ruled out.

Similar stimulus features control visual classification in orangutans and rhesus monkeys.

Many species classify images according to visual attributes. In pigeons, local features may disproportionately control classification, whereas in primates global features may exert greater control. In the absence of explicitly comparative studies, in which different species are tested with the same stimuli under similar conditions, it is not possible to determine how much of the variation in the control of classification is due to species differences and how much is due to differences in the stimuli, training, or testing conditions. We tested rhesus monkeys (Macaca mulatta) and orangutans (Pongo pygmaeus and Pongo abelii) in identical tests in which images were modified to determine which stimulus features controlled classification. Monkeys and orangutans were trained to classify full color images of birds, fish, flowers, and people; they were later given generalization tests in which images were novel, black and white, black and white line drawings, or scrambled. Classification in these primate species was controlled by multiple stimulus attributes, both global and local, and the species behaved similarly.

Rhesus monkeys metacognitively monitor memories of the order of events

Human working memory is a capacity- and duration-limited system in which retention and manipulation of information is subject to metacognitive monitoring and control. At least some nonhuman animals appear to also monitor and control the contents of working memory, but only relatively simple cases where animals monitor or control the presence or absence of single memories have been studied. Here we combine a comparatively complex order memory task with methodology that assesses the capacity to introspect about memory. Monkeys observed sequential presentations of five images, and at test, reported which of two images from the list had appeared first during study. Concurrently, they chose to complete or avoid these tests on a trial-by-trial basis. Monkeys “knew when they knew” the correct response. They were less accurate discriminating images that had appeared close in time to one another during study and were more likely to avoid these difficult tests than they were to avoid easier tests. These results indicate that monkeys can metacognitively monitor relatively complex properties of the contents of working memory, including the quality of representations of temporal relations among images.

Tools of engagement: Information seeking in chimpanzees

SummaryTwo widely studied and impressive cognitive feats in nonhuman animals, metacognition and tool use, both require the cognitive tools of monitoring and controlling knowledge states and adaptive actions toward desirable outcomes. In a recent study, Perdue, Evans, and Beran (PLoS ONE, 13(4), e0193229, 2018) found that some chimpanzees used tools to selectively acquire information and make inferences, indicating metacognitive awareness and appropriate use of tools depending on the content of those knowledge states.

Testing for Metacognitive Responding Using an Odor-based Delayed Match-to-Sample Test in Rats

Metamemory involves the cognitive ability to assess the strength of ones memories. To explore the possibility of metamemory in non-human animals, numerous behavioral tasks have been created, many of which utilize an option to decline memory tests. To assess metamemory in rats, we utilized this decline-test option paradigm by adapting previous visual delayed-match-to-sample tests (DMTS)12 developed for primate species to an odor-based test suitable for rodents. First, rats are given a sample to remember by digging in a cup of scented sand. After a delay, the rat is presented with four distinctly scented cups, one of which contains the identical scent experienced during the sample; if this matching cup is selected, then the rat obtains a preferred, larger reward. Selection of any of the other three non-matching sand-filled scented cups results in no reward. Retention intervals are individually titrated such that subjects perform between 40 and 70% correct, therefore ensuring rats sometimes remember and sometimes forget the sample. Here, the operational definition of metamemory is the ability to distinguish between the presence and absence of memory through behavioral responding. Towards this end, on two-thirds of trials, a decline option is presented in addition to the four choice cups (choice trials). If the decline-test option- an unscented colored sand cup, is selected, the subject receives a smaller less-preferred reward and avoids the memory test. On the remaining third of trials, the decline-test option is not available (forced trials), causing subjects to guess the correct cup when the sample is forgotten. On choice tests, subjects that know when they remember should select the decline option when memory is weak rather than take the test and choose incorrectly. Therefore, significantly higher performance on chosen tests as compared to forced memory tests is indicative of the adaptive use of the decline-test response and metacognitive responding.