Interaction of memory systems is controlled by context in both food-storing and non-storing birds.

Animals and humans have multiple memory systems. While both black-capped chickadees (Poecile atricapillus) and dark-eyed juncos (Junco hyemalis) are under selective pressure to remember reliable long-term spatial locations (habit memory), chickadees must additionally quickly form and rapidly update spatial memory for unique cache sites (one-trial memory). We conducted a series of three experiments in which we assessed the degree to which habit and one-trial memory were expressed in both species as a function of training context. In Experiment 1, birds failed to demonstrate habits on probe trials after being trained in the context of a biased Match-to-Sample task in which the same high-frequency target was always correct. In Experiment 2, habit strongly controlled performance when habits were learned as Discriminations, defining a specific training context. In Experiment 3, context no longer defined when to express habits and habit and one-trial memory competed for control of behavior. Across all experiments, birds preferentially used the memory system at test that was consistent with the context in which it was acquired. Although the memory adaptations that allow chickadees to successfully recover cached food might predispose them to favor one-trial memory, we found no species differences in the weighting of habit and one-trial memory. In the experiments here, context was a powerful factor controlling the interaction of memory systems.

Cognitive control of working memory but not familiarity in rhesus monkeys (Macaca mulatta).

Directed forgetting paradigms assess cognitive control by determining whether memory accuracy is superior in trials on which subjects were instructed to remember compared with accuracy in trials on which they were instructed to forget. We used a directed forgetting paradigm to compare the extent to which working memory and familiarity are subject to rehearsal-like cognitive control in rhesus monkeys. Monkeys studied a sample image, then saw one of two distinctive cues during a retention interval. The remember cue typically predicted a four-choice match to sample test, for which memory of the sample was critical. The forget cue typically predicted one of five perceptual discrimination tests, matched for accuracy to the memory tests, for which memory of the sample was irrelevant. On rare probe trials, the test type other than the type typically predicted by the cue was presented. When cognitive control of memory was possible, accuracy should have been higher on memory tests following the remember cue than on those following the forget cue. We found that accuracy was higher following the remember cue under conditions that favored working memory (small image set) but was not higher under conditions that favored matching on the basis of relative familiarity (large image set). Working memory, but not familiarity, is subject to cognitive control in rhesus monkeys.

Dissociation of memory signals for metamemory in rhesus monkeys (Macaca mulatta).

Some nonhuman species demonstrate metamemory, the ability to monitor and control memory. Here, we identify memory signals that control metamemory judgments in rhesus monkeys by directly comparing performance in two metamemory paradigms while holding the availability of one memory signal constant and manipulating another. Monkeys performed a four-choice match-to-sample memory task. In Experiment 1, monkeys could decline memory tests on some trials for a small, guaranteed reward. In Experiment 2, monkeys could review the sample on some trials. In both experiments, monkeys improved accuracy by selectively declining tests or reviewing samples when memory was poor. To assess the degree to which different memory signals made independent contributions to the metamemory judgement, we made the decline-test or review-sample response available either prospectively, before the test, or concurrently with test stimuli. Prospective metamemory judgements are likely controlled by the current contents of working memory, whereas concurrent metamemory judgements may also be controlled by additional relative familiarity signals evoked by the sight of the test stimuli. In both paradigms, metacognitive responding enhanced accuracy more on concurrent than on prospective tests, suggesting additive contributions of working memory and stimulus-evoked familiarity. Consistent with the hypothesis that working memory and stimulus-evoked familiarity both control metamemory judgments when available, metacognitive choice latencies were longer in the concurrent condition, when both were available. Together, these data demonstrate that multiple memory signals can additively control metacognitive judgements in monkeys and provide a framework for mapping the interaction of explicit memory signals in primate memory.

Automated cognitive testing of monkeys in social groups yields results comparable to individual laboratory-based testing.

Cognitive abilities likely evolved in response to specific environmental and social challenges and are therefore expected to be specialized for the life history of each species. Specialized cognitive abilities may be most readily engaged under conditions that approximate the natural environment of the species being studied. While naturalistic environments might therefore have advantages over laboratory settings for cognitive research, it is difficult to conduct certain types of cognitive tests in these settings. We implemented methods for automated cognitive testing of monkeys (Macaca mulatta) in large social groups (Field station) and compared the performance to that of laboratory-housed monkeys (Laboratory). The Field station animals shared access to four touch-screen computers in a large naturalistic social group. Each Field station subject had an RFID chip implanted in each arm for computerized identification and individualized assignment of cognitive tests. The Laboratory group was housed and tested in a typical laboratory setting, with individual access to testing computers in their home cages. Monkeys in both groups voluntarily participated at their own pace for food rewards. We evaluated performance in two visual psychophysics tests, a perceptual classification test, a transitive inference test, and a delayed matching-to-sample memory test. Despite the differences in housing, social environment, age, and sex, monkeys in the two groups performed similarly in all tests. Semi-free ranging monkeys living in complex social environments are therefore viable subjects for cognitive testing designed to take advantage of the unique affordances of naturalistic testing environments.

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.

An assessment of domain-general metacognitive responding in rhesus monkeys.

Metacognition is the ability to monitor and control one's cognition. Monitoring may involve either public cues or introspection of private cognitive states. We tested rhesus monkeys (Macaca mulatta) in a series of generalization tests to determine which type of cues control metacognition. In Experiment 1, monkeys learned a perceptual discrimination in which a "decline-test" response allowed them to avoid tests and receive a guaranteed small reward. Monkeys declined more difficult than easy tests. In Experiments 2-4, we evaluated whether monkeys generalized this metacognitive responding to new perceptual tests. Monkeys showed a trend toward generalization in Experiments 2 & 3, and reliable generalization in Experiment 4. In Experiments 5 & 6, we presented the decline-test response in a delayed matching-to-sample task. Memory tests differed from perceptual tests in that the appearance of the test display could not control metacognitive responding. In Experiment 6, monkeys made prospective metamemory judgments before seeing the tests. Generalization across perceptual tests with different visual properties and mixed generalization from perceptual to memory tests provide provisional evidence that domain-general, private cues controlled metacognition in some monkeys. We observed individual differences in generalization, suggesting that monkeys differ in use of public and private metacognitive cues.

Evaluation of seven hypotheses for metamemory performance in rhesus monkeys.

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.

An application of the active time model to multiple concurrent variable-interval schedules.

The current experiment investigates whether an active time model can account for anomalous results that have emerged from multiple schedule, concurrent variable-interval (VI) VI experiments. The model assumes that (1) during concurrent VI VI training pigeons learn a function that relates time since the most immediate response, i.e., active time, to changeover probabilities and (2) that molar preference is the result of an interaction between inter-response time frequencies and the learned active time changeover functions. Pigeons were trained under a concurrent VI 30-s VI 30-s schedule and a concurrent VI 60-s VI 60-s schedule. Probes were conducted in which VI 30-s and VI 60-s stimuli were paired. During these probes, birds allocated choices equally to the stimuli. The active time model accurately fit individual subject data. In contrast data were not fit by a variant of scalar expectancy theory proposed by Gibbon [Gibbon, J., 1995. Dynamics of time matching: arousal makes better seem worse. Psychon. Bull. Rev. 2, 208-215].