Thinking about order: a review of common processing of magnitude and learned orders in animals.

Rich behavioral and neurobiological evidence suggests cognitive and neural overlap in how quantitatively comparable dimensions such as quantity, time, and space are processed in humans and animals. While magnitude domains such as physical magnitude, time, and space represent information that can be quantitatively compared (4 "is half of" 8), they also represent information that can be organized ordinally (1→2→3→4). Recent evidence suggests that the common representations seen across physical magnitude, time, and space domains in humans may be due to their common ordinal features rather than their common quantitative features, as these common representations appear to extend beyond magnitude domains to include learned orders. In this review, we bring together separate lines of research on multiple ordinal domains including magnitude-based and learned orders in animals to explore the extent to which there is support for a common cognitive process underlying ordinal processing. Animals show similarities in performance patterns across natural quantitatively comparable ordered domains (physical magnitude, time, space, dominance) and learned orders (acquired through transitive inference or simultaneous chaining). Additionally, they show transfer and interference across tasks within and between ordinal domains that support the theory of a common ordinal representation across domains. This review provides some support for the development of a unified theory of ordinality and suggests areas for future research to better characterize the extent to which there are commonalities in cognitive processing of ordinal information generally.

Information seeking in western lowland gorillas (Gorilla gorilla gorilla).

Many animals will seek information when they do not know the answer to a problem, suggesting that they monitor their knowledge state. In the classic "tubes task," subjects are presented with a set of opaque tubes and either see (visible trials) or do not see (hidden trials) which tube holds a food reward on a given trial. Chimpanzees, bonobos, orangutans, and human children show information-seeking behavior on this task, looking into the tubes to find the reward more on hidden than on visible trials. However, evidence for information-seeking behavior in gorillas is limited. In Experiment 1, gorillas that were presented with a classic information-seeking tubes task showed performance patterns consistent with metacognitive behavior; they looked down tubes more on hidden than on visible trials, their accuracy on hidden trials on which they looked was higher than on hidden trials on which they did not look, and they primarily employed an appropriate search strategy when looking down the tubes. In Experiment 2, we decreased or increased the amount of effort required to look down the tubes by increasing or decreasing the height of the tubes, respectively. Gorillas were less likely to look in tubes on trials that required high effort, but continued to look more on hidden than on visible trials, indicating that their tendency to look was affected by both knowledge state and effort. Together these results provide strong evidence for logical, controlled information-seeking behavior by gorillas.

Geometrical representation of serial order in working memory.

Encoding a sequence relies on one's memory for ordinal succession of events and is critical for episodic memory, spatial navigation, language, and other cognitive functions. Investigating the neural mechanisms underlying sequence working memory in the macaque prefrontal cortex, Xie et al. (Science, 375, 632-639, 2022) uncovered a novel integrated representation of temporal and spatial information in different subspaces of a high-dimensional neural state space, offering broad implications across comparative cognition and neuroscience.

Social housing enhances acquisition of task set independently of environmental enrichment: A longitudinal study in the Barnes maze.

Human studies suggest that healthy social relationships benefit cognition, yet little is known about the underlying neural mechanisms of this protective effect. In rodents, studies on acute isolation and environmental enrichment (EE) confirm the importance of social exposure. Despite the widely recognized importance of sociality, however, rodent models have yet to explore the independent contributions of social housing divorced of other forms of enrichment. This study dissociates the effects of social and physical enrichment on spatial learning and memory from adulthood to old age. Rats were placed in either single or group housing, provided with ample enrichment, and tested at three time points on several phases/versions of the Barnes maze (BM) (standard, retention probes, variable location, and reversal). We found that sustained social housing enhanced cognitive flexibility, as evidenced by superior acquisition of task set (standard BM), adaptability to a new task set (variable BM), and improved reversal learning (reversal BM). Long-term retention (BM retention probes) of spatial memory was unaffected by housing conditions. Recent studies from our lab, including this report, are the first to show that social housing confers cognitive benefits beyond those of physical enrichment. Importantly, our experimental design is ideal for exploring the neural underpinnings of this socially induced cognitive protection. Understanding how sociality influences cognition will be invaluable to translational models of aging, neuropsychiatric disease, and neurological injury.

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.

Tools of engagement: Information seeking in chimpanzees.

Two 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.

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.

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.

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.

Preserved visual memory and relational cognition performance in monkeys with selective hippocampal lesions.

The theory that the hippocampus is critical for visual memory and relational cognition has been challenged by discovery of more spared hippocampal tissue than previously reported in H.M., previously unreported extra-hippocampal damage in developmental amnesiacs, and findings that the hippocampus is unnecessary for object-in-context memory in monkeys. These challenges highlight the need for causal tests of hippocampal function in nonhuman primate models. Here, we tested rhesus monkeys on a battery of cognitive tasks including transitive inference, temporal order memory, shape recall, source memory, and image recognition. Contrary to predictions, we observed no robust impairments in memory or relational cognition either within- or between-groups following hippocampal damage. These results caution against over-generalizing from human correlational studies or rodent experimental studies, compel a new generation of nonhuman primate studies, and indicate that we should reassess the relative contributions of the hippocampus proper compared to other regions in visual memory and relational cognition.

Slow Progress with the Most Widely Used Animal Model: Ten Years of Metacognition Research in Rats, 2009-2019.

Until recently, demonstrations of metacognition in primates have been frequent and robust, while in rodents they have been few and equivocal. However, the past few years have seen a change in this trend with the introduction of novel methods to determine whether metacognitive responding is governed by internal or external sources of stimulus control in rats. Such studies suggest that like primates, rats can indeed use internal assessment of memory strengths to guide metacognitive responding. Strong behavioral paradigms suitable for rodents support the development of easily-accessible animal models for the neurobiology of metamemory and translational studies on diseases of memory. They also allow for a more complete comparative study of the evolution of metacognition, as the presence of this ability in rodents would suggest that metacognition evolved ~80 rather than ~25 million years ago.

Co-operation of long-term and working memory representations in simultaneous chaining by rhesus monkeys (Macaca mulatta).

We studied the memory representations that control execution of action sequences by training rhesus monkeys (Macaca mulatta) to touch sets of five images in a predetermined arbitrary order (simultaneous chaining). In Experiment 1, we found that this training resulted in mental representations of ordinal position rather than learning associative chains, replicating the work of others. We conducted novel analyses of performance on probe tests consisting of two images "derived" from the full five-image lists (i.e., test B, D from list A→B→C→D→E). We found a "first item effect" such that monkeys responded most quickly to images that occurred early in the list in which they had been learned, indicating that monkeys covertly execute known lists mentally until an image on the screen matches the one stored in memory. Monkeys also made an ordinal comparison of the two images presented at test based on long-term memory of positional information, resulting in a "symbolic distance effect." Experiment 2 indicated that ordinal representations were based on absolute, rather than on relative, positional information because subjects did not link two lists into one large list after linking training, unlike what occurs in transitive inference. We further examined the contents of working memory during list execution in Experiments 3 and 4 and found evidence for a prospective, rather than a retrospective, coding of position in the lists. These results indicate that serial expertise in simultaneous chaining results in robust absolute ordinal coding in long-term memory, with rapidly updating prospective coding of position in working memory during list execution.

Social housing protects against age-related working memory decline independently of physical enrichment in rats.

Longitudinal human studies suggest that as we age, sociality provides protective benefits against cognitive decline. However, little is known about the underlying neural mechanisms. Rodent studies, which are ideal for studying cognition, fail to examine the independent effects of social housing while controlling for physical enrichment in all groups. In this study, rats were socially housed or nonsocially housed throughout their lifespan and tested in the radial arm maze to measure working memory (WM) and reference memory longitudinally at 3 ages. In old age, exclusively, socially housed rats made significantly less WM errors than nonsocially housed rats, while reference memory errors did not differ between groups at any age. Anxiety, as assessed behaviorally and physiologically, could not account for the observed differences in WM. These data provide the first evidence that social enrichment alone can prevent age-related WM deficits in spite of the effects of practice seen in longitudinal designs. Importantly, our model will facilitate future investigations into the mechanisms underlying the neuroprotective benefits of sociability in old age.

Social vs. Nonsocial Housing Differentially Affects Perseverative Behavior in Rats (Ratus norvegicus).

Perseverance, also commonly referred to as grit or industriousness, is the continued effort exerted to complete goal-directed tasks. Many factors, such as stress, can contribute to perseverative behavior, but the role of sociality on perseverance in animal models has not been studied. In this experiment, perseverance was measured in Long-Evans rats; half of which were socially housed (SH) and the other half were nonsocially housed (NSH). Rats were placed in a continuous T-maze; one arm of the maze contained an unobstructed low value reward and the other arm contained a high value reward blocked by a barrier that progressively increased in height across testing sessions. We will hereon refer to the low value reward and high value reward as the low reward and the high reward, respectively. Perseverative behavior was assessed by time spent interacting with the barrier and trials were characterized as either adaptive perseverative trials (high reward obtainment) and maladaptive perseverative trials (low reward obtainment after abandoning attempts to overcome the high reward barrier). SH and NSH rats were equally proficient at overcoming a physical barrier to obtain a higher-valued reward, but the NSH rats spent more time interacting with the barriers during maladaptive perseverative trials than SH rats. NSH rats thus exhibited prolonged efforts to overcome the barrier only to ultimately travel to the low reward option. In contrast, SH rats selected the low reward option earlier in the trial and did not maladaptively perseverate without obtaining the high reward. Putative evidence for increased perseverance in NSH rats is explained in the context of maladaptive perseverative behavior rather than perseverance per se. Increased adaptability and acquisition of task-set in SH rats suggests a role of social housing in advantageous decision making.

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.

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 one's 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)1,2 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.

Nonsocially housed rats (Ratus norvegicus) seek social interactions and social novelty more than socially housed counterparts.

Sociability is the act or quality of social interaction and can be quantified by determining the number and duration of interactions with conspecifics. The purpose of this study was to examine the extent to which sustained social contact, as achieved by constant social living conditions, influenced social behavior. Beginning in juvenility, 19 male Long-Evans rats were housed in enriched environments, with half living socially in a large group and half living individually. After several months in these housing conditions, rats were tested on a sociality test and a social novelty preference test. Nonsocially housed rats exhibited more social behavior than socially housed rats. In the sociality test, nonsocially housed rats engaged with an unfamiliar rat more than socially housed rats. Similarly, in the social novelty test, nonsocially housed rats visited a novel stranger more than the now-familiar rat (from the sociality test) as compared with the socially housed rats. It is unlikely that general anxiety factors can account for between-groups social effects, as there were no group differences in behavior on the elevated zero maze and open field test. Furthermore, socially and nonsocially housed rats were matched in spontaneous object exploration and novelty preference in a novel object recognition test, eliminating the possibility that general exploratory behavior or novelty preference accounted for group differences in the sociability tasks. These results suggest that lack of social interaction in nonsocially housed rats may be more powerful for social motivation than the consistent opportunity for social contact afforded by social living conditions. (PsycINFO Database Record

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.

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.

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.