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.
Human children will select a novel object from among a group of known objects when presented with a novel object name. This disambiguation by exclusion may facilitate new name-object mappings and may play a role in the rapid word learning shown by young children. Animals including dogs, apes, monkeys, and birds make similar exclusion choices. However, evidence regarding whether children and nonhuman animals learn new associations through choice by exclusion is mixed. In the present study we dissociate choice by exclusion from learning by exclusion in rhesus monkeys using a paired-associate task. In experiment 1, monkeys demonstrated choice by exclusion by choosing a novel comparison image from among known comparison images when presented with a novel sample image. In experiment 2, monkeys failed to benefit from choice by exclusion in learning new sets of paired associates. Monkeys learned new sets of four paired associates by trial and error alone or by a combination of exclusion and trial and error. Despite choosing correctly by exclusion on almost 100% of opportunities, monkeys did not learn any faster by exclusion than by trial and error alone. These results indicate that monkeys chose, but do not learn, through exclusion, highlighting the importance of separately evaluating choice and learning in studies of exclusion in word learning.
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.
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.
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.
Human working memory is greatly facilitated by linguistic representations—for example, by verbal rehearsal and by verbal recoding of novel stimuli. The absence of language in nonhumans raises questions about the extent to which nonhuman working memory includes similar mechanisms. There is strong evidence for rehearsal-like active maintenance in working memory when monkeys are tested with highly familiar stimuli, but not when tested with novel stimuli, suggesting that working memory depends on the existence of previously encoded representations. This difference in working memory for familiar and novel images may exist because, lacking language, monkeys cannot recode novel stimuli in a way that permits active maintenance in working memory.
Alternatively, working memory for novel images may have been present, but behaviorally silent, in earlier studies. In tests with novel images, the high familiarity of to-be-remembered stimuli compared to never-before-seen distractors may be such a strong determinant of recognition performance that evidence of working memory is obscured. In the current study, we developed a technique for attenuating the utility of relative familiarity as a mnemonic signal in recognition tests with novel stimuli. In tests with novel images, we observed impairments of memory by concurrent cognitive load and delay interval that indicate actively maintained working memory. This flexibility in monkey working memory suggests that monkeys may recode unfamiliar stimuli to facilitate working memory and establishes new parallels between verbal human working memory and nonverbal nonhuman primate working memory.
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.
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.
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.
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.