Chimpanzees (Pan troglodytes) navigate to find hidden fruit in a virtual environment.

Almost all animals navigate their environment to find food, shelter, and mates. Spatial cognition of nonhuman primates in large-scale environments is notoriously difficult to study. Field research is ecologically valid, but controlling confounding variables can be difficult. Captive research enables experimental control, but space restrictions can limit generalizability. Virtual reality technology combines the best of both worlds by creating large-scale, controllable environments. We presented six chimpanzees with a seminaturalistic virtual environment, using a custom touch screen application. The chimpanzees exhibited signature behaviors reminiscent of real-life navigation: They learned to approach a landmark associated with the presence of fruit, improving efficiency over time; they located this landmark from novel starting locations and approached a different landmark when necessary. We conclude that virtual environments can allow for standardized testing with higher ecological validity than traditional tests in captivity and harbor great potential to contribute to longstanding questions in primate navigation, e.g., the use of landmarks, Euclidean maps, or spatial frames of reference.

Post-event misinformation effects in a language-trained chimpanzee (Pan troglodytes).

Errors of source monitoring are widespread human memory challenges, and our memories are subject to distortion upon the presentation of subsequent misinformation. Less is known about if and when misinformation effects occur in nonhuman species' memory. Here we tested a symbol-trained chimpanzee's recall memory of a hidden food item's identity after a 10-min delay. During this delay, the subject was sometimes (depending on the condition) shown consistent or inconsistent video information about the identity of the food, before being asked to name the item to a second experimenter blind to the reward and condition. Across all conditions, our subject, Sherman, correctly named the food item at above chance levels. In the Inconsistent condition, in which Sherman was shown a video with misleading information, his performance was the worst of all conditions (although accuracy was still high). Interestingly, however, during three of the four trials in this condition in which Sherman made a mistake, he incorrectly named the food item shown during the misleading video information. These results provide evidence that chimpanzees, like humans, may be vulnerable to misinformation effects, even when that misleading information is presented in a different modality (video) than the original live event memory, demonstrating further commonality between human and ape memory systems.

Risk sensitivity, phylogenetic reconstruction, and four chimpanzees.

Sensitivity to variance, or risk, has been considered elementary to economic decision making, featured prominently in discussions of primate species-typical behaviors and phylogeny, and heralded as a challenge to deterministic foraging theory. Most risk sensitivity studies involve dichotomous choices and small spatial scales, providing only limited bases for predicting how variance information might be used across contexts. We examined foraging risk-sensitivity in four chimpanzees (Pan troglodytes) which were presented containers associated with particular mean food rewards/variances. Preferences were measured via indoor dichotomous choice tests. Subsequent tasks, designed to assess how well these preferences held up across situations, involved a differing food type, rank-ordering arrays of containers, and/or recovering them in a large outdoor testing area. In addition, some variations involved memory for containers previously observed being hidden. Risk preferences varied by subject, experimental context, reward type, and mean reward quantity. In rank-ordering experiments, under the reward contingencies utilized, mean food quantity was a better predictor of selection order than variance. These results bring into question arguments that species-typical primate risk traits-in the sense of enduring, generalized dispositional features of organisms-have been firmly identified, and suggest that many popular experimental strategies are alone inadequate for reconstructing risk-related traits in primate/human evolution. Models from classical foraging theory, which do not address variance, have likely been successful because they include crucial variables with robust predictive value. Determining the importance of variance to naturalistic decision-making, on the other hand, will require further testing in a wide range of experimental and observational contexts.

Primate cognition: attention, episodic memory, prospective memory, self-control, and metacognition as examples of cognitive control in nonhuman primates.

Primate Cognition is the study of cognitive processes, which represent internal mental processes involved in discriminations, decisions, and behaviors of humans and other primate species. Cognitive control involves executive and regulatory processes that allocate attention, manipulate and evaluate available information (and, when necessary, seek additional information), remember past experiences to plan future behaviors, and deal with distraction and impulsivity when they are threats to goal achievement. Areas of research that relate to cognitive control as it is assessed across species include executive attention, episodic memory, prospective memory, metacognition, and self-control. Executive attention refers to the ability to control what sensory stimuli one attends to and how one regulates responses to those stimuli, especially in cases of conflict. Episodic memory refers to memory for personally experienced, autobiographical events. Prospective memory refers to the formation and implementation of future-intended actions, such as remembering what needs to be done later. Metacognition consists of control and monitoring processes that allow individuals to assess what information they have and what information they still need, and then if necessary to seek information. Self-control is a regulatory process whereby individuals forego more immediate or easier to obtain rewards for more delayed or harder to obtain rewards that are objectively more valuable. The behavioral complexity shown by nonhuman primates when given tests to assess these capacities indicates psychological continuities with human cognitive control capacities. However, more research is needed to clarify the proper interpretation of these behaviors with regard to possible cognitive constructs that may underlie such behaviors. WIREs Cogn Sci 2016, 7:294-316. doi: 10.1002/wcs.1397 For further resources related to this article, please visit the WIREs website.

Chimpanzees modify intentional gestures to coordinate a search for hidden food.

Humans routinely communicate to coordinate their activities, persisting and elaborating signals to pursue goals that cannot be accomplished individually. Communicative persistence is associated with complex cognitive skills such as intentionality, because interactants modify their communication in response to another's understanding of their meaning. Here we show that two language-trained chimpanzees effectively use intentional gestures to coordinate with an experimentally naive human to retrieve hidden food, providing some of the most compelling evidence to date for the role of communicative flexibility in successful coordination in nonhumans. Both chimpanzees (named Panzee and Sherman) increase the rate of non-indicative gestures when the experimenter approaches the location of the hidden food. Panzee also elaborates her gestures in relation to the experimenter's pointing, which enables her to find food more effectively than Sherman. Communicative persistence facilitates effective communication during behavioural coordination and is likely to have been important in shaping language evolution.

Using virtual reality to investigate comparative spatial cognitive abilities in chimpanzees and humans.

The purpose of the present study was to determine the efficacy of investigating spatial cognitive abilities across two primate species using virtual reality. In this study, we presented four captive adult chimpanzees and 16 humans (12 children and 4 adults) with simulated environments of increasing complexity and size to compare species' attention to visuo-spatial features during navigation. The specific task required participants to attend to landmarks in navigating along routes in order to localize the goal site. Both species were found to discriminate effectively between positive and negative landmarks. Assessing path efficiency revealed that both species and all age groups used relatively efficient, distance reducing routes during navigation. Compared to the chimpanzees and adult humans however, younger children's performance decreased as maze complexity and size increased. Surprisingly, in the most complex maze category the humans' performance was less accurate compared to one female chimpanzee. These results suggest that the method of using virtual reality to test captive primates, and in particular, chimpanzees, affords significant cross-species investigations of spatial cognitive and developmental comparisons.

Memory and foraging theory: Chimpanzee utilization of optimality heuristics in the rank-order recovery of hidden foods.

Many models from foraging theory and movement ecology assume that resources are encountered randomly. If food locations, types and values are retained in memory, however, search time could be significantly reduced, with concurrent effects on biological fitness. Despite this, little is known about what specific characteristics of foods, particularly those relevant to profitability, nonhuman animals can remember. Building upon previous observations, we hypothesized that chimpanzees (Pan troglodytes), after observing foods being hidden in a large wooded test area they could not enter, and after long delays, would direct (through gesture and vocalization) experimentally naïve humans to the reward locations in an order that could be predicted beforehand by the spatial and physical characteristics of those items. In the main experiment, various quantities of almonds, both in and out of shells and sealed in transparent bags, were hidden in the test area. The chimpanzees later directed searchers to those items in a nonrandom order related to quantity, shell presence/absence, and the distance they were hidden from the subject. The recovery sequences were closely related to the actual e/h profitability of the foods. Predicted recovery orders, based on the energetic value of almonds and independently-measured, individual-specific expected pursuit and processing times, were closely related to observed recovery orders. We argue that the information nonhuman animals possess regarding their environment can be extensive, and that further comparative study is vital for incorporating realistic cognitive variables into models of foraging and movement.

Prospective Memory in a Language-Trained Chimpanzee (Pan troglodytes).

Prospective memory involves the encoding, retention, and implementation of an intended future action. Although humans show many forms of prospective memory, less is known about the future oriented processes of nonhuman animals, or their ability to use prospective memory. In this experiment, a chimpanzee named Panzee, who had learned to associate geometric forms called lexigrams with real-world referents, was given a prospective memory test. Panzee selected between two foods the one she wanted to receive more immediately. That food was scattered in an outdoor yard where she could forage for it. Also outdoors were lexigram tokens, one of which represented the food item that remained indoors throughout a 30 minute period, and that could be obtained if Panzee brought in the token that matched that food item. After foraging for the selected food item, Panzee consistently remembered to retrieve and return the correct token when food was available indoors, whereas on control trials involving no indoor food she rarely returned a token. This indicated that Panzee encoded information relevant to the future action of token retrieval after extended delays for one type of food, even when a more immediately preferred food was available.

Development of maze navigation by tufted capuchins (Cebus apella).

Theories of spatial navigation hypothesize that animals use vector or topological information to choose routes, often including detours, to move objects or themselves to goals. We assessed adult capuchin monkeys' (Cebus apella) navigation through 192 virtual two-dimensional mazes that incorporated detour problems. Six monkeys initially were significantly less likely to choose the correct paths when detours were required than when not. Three of the six monkeys repeatedly practiced the 192 mazes to asymptotic mastery; the other three did not practice the mazes again. In a subsequent transfer test, each monkey made correct choices equivalently often on familiar and novel mazes, which suggests that they used general planning skills for maze navigation. Of the three monkeys that practiced the 192 maze-set repeatedly, one efficiently detoured and the other two significantly improved detouring compared to their initial performance. Two monkeys, contrary to their performance when completing the 192 maze-set for the first time, made correct choices at the same rate as chimpanzees. Some evidence suggested that two monkeys used topological information, but utilization of vector information was obvious for all monkeys. Our findings suggest that the boundaries of any individual's navigational abilities are not predicted by species, but depend on experience.

How young children and chimpanzees (Pan troglodytes) perceive objects in a 2D display: putting an assumption to the test.

Object recognition research is typically conducted using 2D stimuli in lieu of 3D objects. This study investigated the amount and complexity of knowledge gained from 2D stimuli in adult chimpanzees (Pan troglodytes) and young children (aged 3 and 4 years) using a titrated series of cross-dimensional search tasks. Results indicate that 3-year-old children utilize a response rule guided by local features to solve cross-dimensional tasks. Four-year-old toddlers and adult chimpanzees use information about object form and compositional structure from a 2D image to guide their search in three dimensions. Findings have specific implications to research conducted in object recognition/perception and broad relevance to all areas of research and daily living that incorporate 2D displays.

An efficient computerized testing method for the capuchin monkey (Cebus apella): adaptation of the LRC-CTS to a socially housed nonhuman primate species.

Even with advances in automated testing techniques, the capuchin monkey (Cebus apella) can be a difficult species to test in the laboratory, given its social/behavioral tendencies and typical activity pattern. Laboratories that maintain social colonies of capuchin monkeys are able to separate and test individuals, but the process can be very effortful and time consuming, and the resulting data can be modest in quantity. The present article describes procedures and apparatuses that were used to train a colony of computer-naive capuchin monkeys to quickly and reliably isolate themselves from group members and interact with a computerized test system in order to produce a large volume of data. Several elements that were important in motivating the monkeys to participate are discussed.

Chimpanzees (Pan troglodytes) use markers to monitor the movement of a hidden item.

Four chimpanzees (Pan troglodytes) monitored the movement of hidden items in arrays of opaque cups. A chocolate candy was hidden in an array of four cups and temporarily presented paper markers indicated the location of the candy (which otherwise was not visible). These markers were either non-symbolic or symbolic (lexigram) stimuli that in other contexts acted as a label for the hidden candy, and the array was either rotated 180 degrees after the marker was removed or the array remained in the same location. For three of four chimpanzees, performance was better than chance in all conditions and there was no effect of the type of marker. These experiments indicate that chimpanzees can track the movement of a hidden item in an array of identical cups even when they never see the item itself, but only see a temporarily presented marker for the location of that item. However, there was no benefit to the use of symbolic as opposed to non-symbolic stimuli in this performance.

Spatial memory and monitoring of hidden items through spatial displacements by chimpanzees (Pan troglodytes).

This study examined chimpanzee (Pan troglodytes) short-term memory for food location in near space. In Experiments 1 and 2, either 1 or 2 items (chocolate pieces) were hidden in an array of 3 or 5 containers that either remained stationary or were rotated 180 degrees or 360 degrees. When the array remained stationary, the chimpanzees remembered both item locations. When arrays were rotated, however, chimpanzees found only 1 item. In Experiment 3, 2 items were hidden in an array of 7 cups. Both items were found at levels significantly better than chance. Ninety percent of errors were made after the 1st item was found, and errors reflected memory failure rather than a failure of inhibitory control.