Benjamin M. Basile

An assessment of memory awareness in tufted capuchin monkeys (Cebus apella)

Humans, apes, and rhesus monkeys demonstrate memory awareness by collecting information when ignorant and acting immediately when informed. In this study, five capuchin monkeys searched for food after either watching the experimenter bait one of four opaque tubes (seen trials), or not watching (unseen trials). Monkeys with memory awareness should look into the tubes before making a selection only on unseen trials because on seen trials they already know the location of the food. In Experiment 1, one of the five capuchins looked significantly more often on unseen trials. In Experiment 2, we ensured that the monkeys attended to the baiting by interleaving training and test sessions. Three of the five monkeys looked more often on unseen trials. Because monkeys looked more often than not on both trial types, potentially creating a ceiling effect, we increased the effort required to look in Experiment 3, and predicted a larger difference in the probability of looking between seen and unseen trials. None of the five monkeys looked more often on unseen trials. These findings provide equivocal evidence for memory awareness in capuchin monkeys using tests that have yielded clear evidence in humans, apes, and rhesus monkeys.

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 (Macaca mulatta) rapidly learn to select dominant individuals in videos of artificial social interactions between unfamiliar conspecifics.

Social animals, such as primates, must behave appropriately in complex social situations such as dominance interactions. Learning dominance information through trial and error would be dangerous; therefore, cognitive mechanisms for rapid learning of dominance information by observation would be adaptive. We used a set of digitally edited artificial social interactions to examine whether rhesus monkeys (Macaca mulatta) can learn dominance relationships between unfamiliar conspecifics through observation. Our method allowed random assignment of stimulus monkeys to ranks in an artificial hierarchy, controlling for nonbehavioral cues that could indicate dominance. Subject monkeys watched videos depicting 1 stimulus monkey behaving dominantly toward another and were rewarded for selecting the dominant individual. Monkeys rapidly learned this discrimination across 5 behavior types in Experiment 1 and transferred performance to novel videos of new individuals in Experiment 2. In addition, subjects selected the dominant individual more often than expected by chance in probe videos containing no behavioral dominance information, indicating some retention of the relative dominance status of stimulus monkeys from training. Together, our results suggest that monkeys can learn dominance hierarchies through observation of third-party social interactions.

Dissociation of active working memory and passive recognition in rhesus monkeys

Active cognitive control of working memory is central in most human memory models, but behavioral evidence for such control in nonhuman primates is absent and neurophysiological evidence, while suggestive, is indirect. We present behavioral evidence that monkey memory for familiar images is under active cognitive control. Concurrent cognitive demands during the memory delay impaired matching-to-sample performance for familiar images in a demand-dependent manner, indicating that maintaining these images in memory taxed limited cognitive resources. Performance with unfamiliar images was unaffected, dissociating active from passive memory processes. Active cognitive control of memory in monkeys demonstrates that language is unnecessary for active memory maintenance.

Rhesus monkeys (Macaca mulatta) show robust primacy and recency in memory for lists from small, but not large, image sets

The combination of primacy and recency produces a U-shaped serial position curve typical of memory for lists. In humans, primacy is often thought to result from rehearsal, but there is little evidence for rehearsal in nonhumans. To further evaluate the possibility that rehearsal contributes to primacy in monkeys, we compared memory for lists of familiar stimuli (which may be easier to rehearse) to memory for unfamiliar stimuli (which are likely difficult to rehearse). Six rhesus monkeys saw lists of five images drawn from either large, medium, or small image sets. After presentation of each list, memory for one item was assessed using a serial probe recognition test. Across four experiments, we found robust primacy and recency with lists drawn from small and medium, but not large, image sets. This finding is consistent with the idea that familiar items are easier to rehearse and that rehearsal contributes to primacy, warranting further study of the possibility of rehearsal in monkeys. However, alternative interpretations are also viable and are discussed.

Monkeys show recognition without priming in a classification task.

Humans show visual perceptual priming by identifying degraded images faster and more accurately if they have seen the original images, while simultaneously failing to recognize the same images. Such priming is commonly thought, with little evidence, to be widely distributed phylogenetically. Following Brodbeck (1997), we trained rhesus monkeys (Macaca mulatta) to categorize photographs according to content (e.g., birds, fish, flowers, people). In probe trials, we tested whether monkeys were faster or more accurate at categorizing degraded versions of previously seen images (primed) than degraded versions of novel images (unprimed). Monkeys categorized reliably, but showed no benefit from having previously seen the images. This finding was robust across manipulations of image quality (color, grayscale, line drawings), type of image degradation (occlusion, blurring), levels of processing, and number of repetitions of the prime. By contrast, in probe matching-to-sample trials, monkeys recognized the primes, demonstrating that they remembered the primes and could discriminate them from other images in the same category under the conditions used to test for priming. Two experiments that replicated Brodbecks (1997) procedures also produced no evidence of priming. This inability to find priming in monkeys under perceptual conditions sufficient for recognition presents a puzzle.

Dissociation of item and source memory in rhesus monkeys

Source memory, or memory for the context in which a memory was formed, is a defining characteristic of human episodic memory and source memory errors are a debilitating symptom of memory dysfunction. Evidence for source memory in nonhuman primates is sparse despite considerable evidence for other types of sophisticated memory and the practical need for good models of episodic memory in nonhuman primates. A previous study showed that rhesus monkeys confused the identity of a monkey they saw with a monkey they heard, but only after an extended memory delay. This suggests that they initially remembered the source - visual or auditory - of the information but forgot the source as time passed. Here, we present a monkey model of source memory that is based on this previous study. In each trial, monkeys studied two images, one that they simply viewed and touched and the other that they classified as a bird, fish, flower, or person. In a subsequent memory test, they were required to select the image from one source but avoid the other. With training, monkeys learned to suppress responding to images from the to-be-avoided source. After longer memory intervals, monkeys continued to show reliable item memory, discriminating studied images from distractors, but made many source memory errors. Monkeys discriminated source based on study method, not study order, providing preliminary evidence that our manipulation of retention interval caused errors due to source forgetting instead of source confusion. Finally, some monkeys learned to select remembered images from either source on cue, showing that they did indeed remember both items and both sources. This paradigm potentially provides a new model to study a critical aspect of episodic memory in nonhuman primates.

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.

Two-item same/different discrimination in rhesus monkeys (Macaca mulatta)

Abstract Almost all nonhuman animals can recognize when one item is the same as another item. It is less clear whether nonhuman animals possess abstract concepts of “same” and “different” that can be divorced from perceptual similarity. Pigeons and monkeys show inconsistent performance, and often surprising difficulty, in laboratory tests of same/different learning that involve only two items. Previous results from tests using multi-item arrays suggest that nonhumans compute sameness along a continuous scale of perceptual variability, which would explain the difficulty of making two-item same/different judgments. Here, we provide evidence that rhesus monkeys can learn a two-item same/different discrimination similar to those on which monkeys and pigeons have previously failed. Monkeys’ performance transferred to novel stimuli and was not affected by perceptual variations in stimulus size, rotation, view, or luminance. Success without the use of multi-item arrays, and the lack of effect of perceptual variability, suggests a computation of sameness that is more categorical, and perhaps more abstract, than previously thought.

Dissociation of visual localization and visual detection in rhesus monkeys (Macaca mulatta)

Abstract Conscious and unconscious cognitive processes contribute independently to human behavior and can be dissociated. For example, humans report failing to see objects clearly in the periphery while simultaneously being able to grasp those objects accurately (Milner in Proc R Soc B Biol Sci 279:2289–2298, 2012). Knowing whether similar dissociations are present in nonverbal species is critical to our understanding of comparative psychology and the evolution of brains. However, such dissociations are difficult to detect in nonhumans because verbal reports of experience are the main way we discriminate putative conscious from unconscious processing. We trained monkeys in a localization task in which they responded to the location where a target appeared, and a matched detection task in which they reported the presence or absence of the same target. We used masking to manipulate the visibility of targets. Accuracy was high in both tasks when stimuli were unmasked and was attenuated by visual masking. At the strongest level of masking, performance in the detection task was at chance, while localization remained significantly above chance. Critically, errors in the detection task were predominantly misses, indicating that the monkeys’ behavior remained under stimulus control, but that the monkeys did not detect the target despite above-chance localization. While these results cannot establish the existence of phenomenal vision in monkeys, the dissociation of visually guided action from detection parallels the dissociation of conscious and unconscious vision seen in humans.