Animal Cognition https://doi.org/10.1007/s10071-019-01246-5 ORIGINAL PAPER Dissociation of memory signals for metamemory in rhesus monkeys (Macaca mulatta) Emily Kathryn Brown1 · Benjamin M. Basile2 · Victoria L. Templer3 · Robert R. Hampton1 Received: 19 August 2018 / Revised: 28 January 2019 / Accepted: 31 January 2019 © Springer-Verlag GmbH Germany, part of Springer Nature 2019 Abstract 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 meta- memory 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. Keywords Metacognition · Information seeking · Monitoring · Working memory · Familiarity Introduction answer and a vague sense of which choice feels most famil- iar. The memory systems giving rise to these signals dif- Performance on memory tasks is supported by a variety fer in flexibility, robustness against interference, and the of memory systems, each characterized by distinct func- conditions under which they are available for introspective tional properties and underlying neural substrates (Sherry monitoring. Monitorable memory signals have gained par- and Schacter 1987; Squire and Zola-Morgan 1991; Yoneli- ticular attention because they afford subjects the opportu- nas 2002). For example, a contestant on a trivia show may nity to control their cognition, such as by seeking additional answer based on a combination of retrieval of the correct information or altering response strategy. The way in which subjects monitor and control different memory signals can be assessed using metamemory paradigms. * Emily Kathryn Brown [email protected] Metamemory is the ability to monitor memory processes and adapt behavior or cognition in accord with monitored 1 Department of Psychology, Yerkes National Primate memory signals. Metamemory is exemplified by the game Research Center, Emory University, 36 Eagle Row, Atlanta, show “Who wants to be a millionaire?” wherein contest- GA 30322, USA ants must answer trivia questions and make judgments about 2 Laboratory of Neuropsychology, NIMH, NIH, Bethesda, whether they have answered correctly. Contestants are given MD, USA the opportunity to reconsider their answers after reflection, 3 Department of Psychology, Providence College, Providence, or to collect additional information by contacting a friend. RI, USA Vol.:(0123456789)1 3 Animal Cognition The metamemory judgments made by contestants can be manipulated. Prospective metamemory judgments are made controlled by whether a memory was successfully retrieved, before the test options have been seen and thus favor moni- has been successfully held in working memory, or evokes toring of working memory because information about the strong relative familiarity compared to other test options relative familiarity of the test options is not yet available. (Flavell 1979; Kornell 2013; Nelson 1996). Just as memory Concurrent metamemory judgments are made in the pres- performance often reflects a combination of memory signals, ence of the memory test. Monkeys can still monitor work- so too do metamemory judgements. ing memory in concurrent metamemory judgments, and A substantial body of work with nonhuman primate spe- additional information about the relative familiarity of the cies indicates that they can monitor memory, as indicated sample and distractors is also available. by their ability to selectively decline difficult tests, review Here, we assessed both prospective and concurrent meta- previously studied but forgotten information, seek informa- memory judgments. In Experiment 1, we used a decline- tion when ignorant, or adaptively wager rewards based on test paradigm, in which monkeys chose to avoid some tests recent test choices (Basile et al. 2015; Brown et al. 2017; for a small, but guaranteed, reward (Fujita 2009; Hampton Hampton 2001; Kornell et al. 2007; Templer and Hampton 2001; Suda-King 2008; Suda-King et al. 2013; Templer and 2012; Washburn et al. 2010). Only recently has experimental Hampton 2012; Templer et al. 2017; Washburn et al. 2010). work been directed at determining which specific memory In Experiment 2, we used an information-seeking paradigm, systems are subject to memory monitoring and how different in which monkeys chose to review the sample on some trials memory signals interact to control metamemory judgments (Basile et al. 2009, 2015; Beran and Smith 2011; Call and in nonhumans (e.g., Coutinho et al. 2015; Smith et al. 2013; Carpenter 2001; Castro and Wasserman 2013; Iwasaki et al. Takagi and Fujita 2018). 2013; Kirk et al. 2014; Kornell et al. 2007; Marsh 2014; Because memory systems provide different types of infor- Marsh and MacDonald 2012; McMahon et al. 2010; Vining mation, and multiple systems contribute to performance on and Marsh 2015; Watanabe and Clayton 2016). Using these memory tasks, metamemory is likely controlled by a com- two paradigms to assess metacognition, presented both pro- bination of memory signals. The way that these signals are spectively and concurrently, provides a powerful test of the weighted in metamemory decisions in monkeys is unknown. generalizability of our findings. One possibility is that in the presence of multiple memory To compare the contributions of working memory and signals, metacognitive choice may be guided by only one, familiarity in both decline-test and information-seeking such as the strongest signal. A second possibility is that mul- paradigms, we required a common metric. In prior work tiple memory signals contribute additively to metamemory with the decline-test paradigm, monkeys showed a perfor- judgments, such that congruent positive signals strengthen mance advantage on chosen tests compared to performance the likelihood of a high-confidence metamemory judgment. on forced tests when there was no option to decline the To evaluate the degree to which monkey metamemory is memory test (Brown et al. 2017; Hampton 2001; Templer controlled by multiple memory signals, we compared meta- and Hampton 2012). When monkeys monitored memory memory judgments under conditions that always allowed for to choose when to use the decline-test response, they dis- the use of one memory signal but systematically manipulated proportionately chose to take trials when memory was the availability of a second memory signal. In nonhuman strong and selectively avoided tests on which memory was primates, there is strong evidence that recognition memory weak, resulting in higher accuracy on tests they chose to performance is supported by at least two types of memory: take. Forced trials included both trials on which memory working memory and relative familiarity (Basile and Hamp- was strong, which would have been chosen had that option ton 2013; Wittig et al. 2016; Wittig and Richmond 2014). been available, and trials on which memory was weak, Working memory is a limited-capacity system that allows which may have been declined, had the option been avail- the active, relatively short-term maintenance and manipula- able. This accuracy benefit can be applied equivalently to tion of information (Baddeley 2000, 2003). Familiarity is a both decline-test and information-seeking paradigms. On passive signal evoked by the re-presentation of a stimulus choice trials in the information-seeking paradigm, subjects that has been seen previously (Yonelinas 2002; Yonelinas can either choose to take the test immediately, if memory is et al. 2010). In matching to sample memory tests, the image strong, or first review the sample, if memory is weak. Forced seen as a sample on the current trial can potentially be held trials, when the option to review the sample is omitted, will in working memory during the delay. The sample image is include some tests that would have been taken immediately also expected to be relatively more familiar than the distrac- and some tests when subjects would have first reviewed the tors presented with it at test, because