Knowing the extent to which nonhumans and humans share mechanisms for metacognition will advance our understanding of cognitive evolution and will improve selection of model systems for biomedical research. Some nonhuman species avoid difficult cognitive tests, seek information when ignorant, or otherwise behave in ways consistent with metacognition. There is agreement that some nonhuman animals “succeed” in these metacognitive tasks, but little consensus about the cognitive mechanisms underlying performance. In one paradigm, rhesus monkeys visually searched for hidden food when ignorant of the location of the food, but acted immediately when knowledgeable. This result has been interpreted as evidence that monkeys introspectively monitored their memory to adaptively control information seeking. However, convincing alternative hypotheses have been advanced that might also account for the adaptive pattern of visual searching. We evaluated seven hypotheses using a computerized task in which monkeys chose either to take memory tests immediately or to see the answer again before proceeding to the test. We found no evidence to support the hypotheses of behavioral cue association, rote response learning, expectancy violation, response competition, generalized search strategy, or postural mediation. In contrast, we repeatedly found evidence to support the memory monitoring hypothesis. Monkeys chose to see the answer when memory was poor, either from natural variation or experimental manipulation. We found limited evidence that monkeys also monitored the fluency of memory access. Overall, the evidence indicates that rhesus monkeys can use memory strength as a discriminative cue for information seeking, consistent with introspective monitoring of explicit memory.

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, 2001; Smith, Shields, & Washburn, 2003). (R.R. Hampton, 2001; Smith, Shields, & Washburn, 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.

Summary Episodic memories differ from other types of memory because they represent aspects of the past not present in other memories, such as the time, place, or social context in which the memories were formed. Focus on phenomenal experience in human memory, such as the sense of “having been there” has resulted in conceptualizations of episodic memory that are difficult or impossible to apply to nonhumans. It is therefore a significant challenge for investigators to agree on objective behavioral criteria that can be applied in nonhumans and still capture features of memory thought to be critical in humans. Some investigators have attempted to use neurobiological parallels to bridge this gap. However, defining memory types on the basis of the brain structures involved rather than on identified cognitive mechanisms risks missing the most crucial functional aspects of episodic memory, which are ultimately behavioral. The most productive way forward is likely a combination of neurobiology and sophisticated cognitive testing that identifies the mental representations present in episodic memory. Investigators that have refined their approach from asking the naïve question “do nonhuman animals have episodic memory” to instead asking “what aspects of episodic memory are shared by humans and nonhumans” are making progress.

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.

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, J Neuro 2011; 31: 3169–3175; Fortin et al., Nat Neuro 2002; 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., Behav Neuro 2002; 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.