Rhesus monkeys show greater habituation to repeated computer-generated images than do orangutans.

Humans and several other species of animals have demonstrated the ability to use familiarity to recognize that they have seen images before. In prior experiments, orangutans failed to show use of familiarity in memory tasks, even when other solutions were not available. We tested for evidence of habituation, a decreased response to repeated stimuli, as a behavioral indicator that repeated images were familiar to subjects. Monkeys and orangutans selected the smallest target out of four while computerized images were presented as distractors. Latency to complete the target-finding task was compared between conditions in which the distractor image was a familiar, repeating image, a novel, never-before-seen image, or no distractor was present. Rhesus macaques showed significant habituation, and significantly more habituation than orangutans, in each of four experiments. Orangutans showed statistically reliable habituation in only one of the four experiments. These results are consistent with previous research in which orangutans failed to demonstrate familiarity. Because we expect that familiarity and habituation are evolutionarily ancient memory processes, we struggle to explain these surprising, but consistent findings. Future research is needed to determine why orangutans respond to computerized images in this peculiar way.

No evidence of real-world equivalence in chickens (Gallus gallus domesticus) categorizing visually diverse images of natural stimuli presented on LCD monitors.

Category learning is often tested with similar images that have no significance outside of the experiment for the subjects. By contrast, in nature animals often need to generalize a behavioral response like "eat" across visually distinct stimuli, such as spiders and seeds. Forming functional categories like "food" and "predator" may require conceptual rather than purely perceptual generalization. We trained free-range chickens to classify images assigned to one of four categories based on putative functional significance: inanimate objects, predators, food, and non-competing vertebrates. Images were visually diverse within each category, discouraging classification by perceptual similarity alone. In Experiment 1, chickens classified 80 images into four categories. Chickens then generalized to 80 new exemplars in each of three successive generalization tests. In Experiment 2, chickens saw new types of images to test whether their generalization was perceptual or functional. For example, chickens saw images of skunks for the predator category after training with images of hawks and snakes. Chickens used the "predator" response with these new images for both predators and non-threatening vertebrates, but not for objects or food, and did not successfully generalize any category other than predator. In Experiment 3, chickens categorized fractals as "food," and three of four chickens categorized a range of vertebrates they had not previously encountered as "predators," suggesting that chickens did not see the images as representing real world objects and animals. These results highlight constraints on the use of computer-generated images to assess categorization of natural stimuli in chickens.

Six adult male rhesus monkeys did not learn from the choices of a conspecific shown in videos.

There is substantial evidence of group-specific behaviors in wild animals that are thought to be socially transmitted. Yet experimental studies with monkeys have reported conflicting evidence on the extent to which monkeys learn by observing their conspecifics. In this study, we tested the feasibility of using pre-recorded video demonstrations to investigate social learning from conspecifics in rhesus monkeys. With training, monkeys gradually learned to respond correctly following videos of a demonstrator, however, follow-up experiments revealed that this was not due to learning from the demonstrator monkey. In generalization tests with videos that were horizontally reversed, monkeys continued responding to the location they had associated with each video, rather than matching the new choice location shown in the mirrored video. When the task was changed to make location irrelevant, such that monkeys could choose correctly only by selecting the same image selected by the demonstrator in the video, observer monkeys did not exceed chance in 12,000 training trials. Because monkeys readily learn to follow nonsocial visual cues presented on a monitor to guide image choice, their inability to learn from a demonstrator here indicates substantial limitations in the capacity for social learning from videos. Furthermore, these findings encourage deeper consideration of what monkeys perceive when presented with video stimuli on computer screens.

Rhesus monkeys manipulate mental images.

Humans form mental images and manipulate them in ways that mirror physical transformations of objects. Studies of nonhuman animals will inform our understanding of the evolution and distribution among species of mental imagery. Across three experiments, we found mostly converging evidence that rhesus monkeys formed and rotated mental images. In Experiment 1, monkeys discriminated rotations of sample images from mirror images, and showed longer response latencies with greater rotation as is characteristic of human mental rotation. In Experiment 2 monkeys used a rotation cue that indicated how far to mentally rotate sample images before tests, indicating a precision of better than 30° in discriminating rotations. Experiment 3 yielded mixed evidence on whether the rotation cue shortened decision times as has been found in humans. These results show that rhesus monkeys manipulate mental images.

Control of Attention in Rhesus Monkeys Measured Using a Flanker Task.

At least three processes determine whether information we encounter is attended to or ignored. First, attentional capture occurs when attention is drawn automatically by "bottom up" processes, to distinctive, salient, rewarding, or unexpected stimuli when they enter our sensory field. Second, "top down" attentional control can direct cognitive processing towards goal-relevant targets. Third, selection history, operates through repeated exposure to a stimulus, particularly when associated with reward. Attentional control is measured using tasks that require subjects to selectively attend to goal-relevant stimuli in the face of distractions. In the Eriksen flanker task, human participants report which direction a centrally placed arrow is facing, while ignoring "flanking" arrows that may point in the opposite direction. Attentional control is evident to the extent that performance reflects only the direction of the central arrow. We describe four experiments in which we systematically assessed attentional control in rhesus monkeys using a flanker task. In Experiment 1, monkeys responded according to the identity of a central target, and accuracy and latency varied systematically with manipulations of flanking stimuli, validating our adaptation of the Eriksen flanker task. We then tested for converging evidence of attentional control across three experiments in which flanker performance was modulated by the distance separating targets from flankers (Experiment 2), luminance differences (Experiment 3), and differences in associative value (Experiment 4). The approach described is a new and reliable measure of attentional control in rhesus monkeys that can be applied to a wide range of situations with freely behaving animals.

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.

Greater dependence on working memory and restricted familiarity in orangutans compared with rhesus monkeys.

The prefrontal cortex is larger than would be predicted by body size or visual cortex volume in great apes compared with monkeys. Because prefrontal cortex is critical for working memory, we hypothesized that recognition memory tests would engage working memory in orangutans more robustly than in rhesus monkeys. In contrast to working memory, the familiarity response that results from repetition of an image is less cognitively taxing and has been associated with nonfrontal brain regions. Across three experiments, we observed a striking species difference in the control of behavior by these two types of memory. First, we found that recognition memory performance in orangutans was controlled by working memory under conditions in which this memory system plays little role in rhesus monkeys. Second, we found that unlike the case in monkeys, familiarity was not involved in recognition memory performance in orangutans, shown by differences with monkeys across three different measures. Memory in orangutans was not improved by use of novel images, was always impaired by a concurrent cognitive load, and orangutans did not accurately identify images seen minutes ago. These results are surprising and puzzling, but do support the view that prefrontal expansion in great apes favored working memory. At least in orangutans, increased dependence on working memory may come at a cost in terms of the availability of familiarity.

Animal consciousness: Should a new behavioral correlate in monkeys persuade agnostics?

After human subjects learn to look away from visible cues, their attention can still be captured by cues so brief that they cause no conscious perception. A new study has found evidence that this behavior also occurs in monkeys. Is this further evidence for consciousness in a nonhuman animal?

Rhesus monkeys (Macaca mulatta) monitor evolving decisions to control adaptive information seeking.

Adaptive decision making in humans depends on feedback between monitoring, which assesses mental states, and control, by which cognitive processes are modified. We investigated the extent to which monitoring and control interact iteratively in monkeys. Monkeys classified images as birds, fish, flowers, or people. At the beginning of each trial, to-be-classified images were not visible. Monkeys touched the image area to incrementally brighten the image, referred to as the brighten response. The amount by which brightness increased with each brighten response was unpredictable, and the monkeys could choose to classify the images at any time during a trial. We hypothesized that if monkeys monitored the status of their classification decision then they would seek information depending on the amount of information available. In Experiment 1, monkeys rarely used the brighten response when images were bright initially, and they used the brighten response more when earlier uses in a given trial yielded smaller amounts of information. In Experiment 2, monkeys made more brighten responses when the presented image did not belong in any of the trained categories, suggesting monkeys were sensitive to the fact that they could not reach a classification decision despite the image brightening. In Experiment 3, we found that the probability that monkeys used the brighten response correlated with their ability to correctly classify when the brighten response was not available. These findings add to the literature documenting the metacognitive skills of nonhuman primates by demonstrating an iterative feedback loop between cognitive monitoring and cognitive control that allows for adaptive information-seeking behavior.

Designer receptor inhibition suggests mechanism for monkey Theory of Mind.

Theory of Mind (ToM) is a critical component of human social cognition that has not been found reliably in other primates, especially monkeys. Hayashi et al. (Cell Reports, 30, 4433-4444, 2020) used newly developed behavioral techniques to detect evidence for ToM in Japanese macaque monkeys and employed sophisticated neurobiological manipulations to implicate the medial prefrontal cortex is this capacity.

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.

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.

Explicit memory and cognition in monkeys.

Taxonomies of human memory, influenced heavily by Endel Tulving, make a fundamental distinction between explicit and implicit memory. Humans are aware of explicit memories, whereas implicit memories control behavior even though we are not aware of them. Efforts to understand the evolution of memory, and to use nonhuman animals to model human memory, will be facilitated by better understanding the extent to which this critical distinction exists in nonhuman animals. Work with metacognition paradigms in the past 20 years has produced a strong case for the existence of explicit memory in nonhuman primates and possibly other nonhuman animals. Clear dissociations of explicit and implicit memory by metacognition have yet to be demonstrated in nonhumans, although dissociations between memory systems by other behavioral techniques, and by brain manipulations, suggest that the explicit-implicit distinction applies to nonhumans. Neurobehavioral studies of metamemory are beginning to identify neural substrates for memory monitoring in the frontal cortex of monkeys. We have strong evidence that at least some memory systems are explicit in rhesus monkeys, but we need to learn more about the distribution of explicit processes across cognitive systems within monkeys, and across species.

Hippocampal damage attenuates habituation to videos in monkeys.

Monkeys with selective damage to the hippocampus are often unimpaired in matching-to-sample tests but are reportedly impaired in visual paired comparison. While both tests assess recognition of previously seen images, delayed matching-to-sample may engage active memory maintenance whereas visual paired comparison may not. Passive memory tests that are not rewarded with food and that do not require extensive training may provide more sensitive measures of hippocampal function. To test this hypothesis, we assessed memory in monkeys with hippocampal damage and matched controls by providing them the opportunity to repeatedly view small sets of videos. Monkeys pressed a button to play each video. The same 10 videos were used for six consecutive days, after which 10 new videos were introduced in each of seven cycles of testing. Our measure of memory was the extent to which monkeys habituated with repeated presentations, watching fewer videos per session over time. Monkeys with hippocampal lesions habituated more slowly than did control monkeys, indicating poorer memory for previous viewings. Both groups dishabituated each time new videos were introduced. These results, like those from preferential viewing, suggest that the hippocampus may be especially important for memory of incidentally encoded events.

Influences of demographic, seasonal, and social factors on automated touchscreen computer use by rhesus monkeys (Macaca mulatta) in a large naturalistic group.

Animals housed in naturalistic social groups with access to automated cognitive testing vary in whether and how much they participate in cognitive testing. Understanding how demographic, seasonal, and social factors relate to participation is essential to evaluating the usefulness of these systems for studying cognition and in assessing the data produced. We evaluated how sex, age, reproductive experience, seasonality, and rank related to patterns of participation in a naturalistic group of rhesus monkeys over a 4-year period. Females interacted with the touchscreen systems more than males and were more likely to complete initial training. Age was positively correlated with touchscreen activity through adolescence in females, at which point seasonality and reproductive experience were stronger associates of participation. While monkeys in different rank categories did not differ in how much they interacted with the touchscreen systems, monkeys of different ranks tended not to work at the same times, perhaps reflecting avoidance of high ranking animals by those of lower rank. Automated cognitive testing systems for naturalistic social groups of rhesus monkeys can yield quality cognitive data from individuals of all ages and ranks, but participation biases may make it difficult to study sex differences or seasonal variation in cognition.

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.

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.

Monkey Metacognition Could Generate More Insight.

Monkeys demonstrate metacognition by avoiding memory tests when they forget, seeking information when ignorant, and gambling sensibly after making judgments. Some of this metacognition appears to be based on introspection of private mental states. It is likely that nonhuman cognitive systems, like human systems, differ in accessibility to such introspective metacognition, and the extent to which differences in access map to explicit and implicit cognition will be an important topic for future work. It will be exciting to learn more about the distribution of metacognition among species, and the conditions under which metacognition evolves.

Nonnavigational spatial memory performance is unaffected by hippocampal damage in monkeys.

Evidence that the hippocampus is critical for spatial memory in nonnavigational tests is mixed. A recent study reported that temporary hippocampal inactivation impaired spatial memory in the nonnavigational Hamilton Search Task in monkeys. However, several studies have documented no impairment on other nonnavigational spatial memory tests following permanent hippocampal lesions. It was hypothesized that transient, but not permanent, hippocampal disruption produces deficits because monkeys undergoing transient inactivation continue to try to use a hippocampal-dependent strategy, whereas monkeys with permanent lesions use a nonhippocampal-dependent strategy. We evaluated this hypothesis by testing five rhesus monkeys with hippocampal lesions and five controls on a computerized analogue of the Hamilton Search Task. On each trial, monkeys saw an array of squares on a touchscreen, each of which "hid" one reward. Retrieving a reward depleted that location and monkeys continued selecting squares until they found all rewards. The optimal strategy is to remember chosen locations and choose each square once. Unlike the inactivation study, monkeys with hippocampal damage were as accurate as controls regardless of retention interval. Critically, we found no evidence that the groups used different strategies, as measured by learning rates, spatial search biases, perseverative win-stay errors, or inter-choice distance. This discrepancy between the effect of inactivations and lesions may result from off-target effects of inactivations or as-yet-unidentified differences between the physical and computerized tasks. Combined with previous evidence that hippocampal damage impairs navigational memory in monkeys, this evidence constrains the role of the hippocampus in spatial memory as being critical for navigational tests that likely involve allocentric spatial memory but not nonnavigational tests that likely involve egocentric spatial memory.