Habitual prospective memory in preschool children.

Habitual prospective memory (PM) refers to situations in which individuals have to remember to perform a future task on a regular and frequent basis. Habitual PM tasks are ubiquitous and the ability to successfully complete these tasks (e.g., remembering to bring your lunch to school every day) is necessary for children as they begin to establish their own independence. The current investigation is the first to explore preschool children's ability to complete this kind of task. At the end of a regular testing session during which children engaged in a variety of unrelated cognitive tasks, participants were instructed to ask for a stamp on their card, which was sitting in a box on the table. Over the course of the first experiment, participants did this 13 times, spanning a time period of several months. The results demonstrated that children initially needed prompting from the experimenter to remember, but with experience, participants were able to retrieve this intention without assistance. Experiment 2 demonstrated that removing the box from participants' line of sight after numerous opportunities to perform the task did not negatively impact performance, although it did make a difference at the outset of this requirement to remember to ask for stamps. Together, these results indicate that with somewhat consistent and repeated practice, preschool children can fairly quickly demonstrate the ability to successfully perform future intentions that are likely to be repeated on numerous occasions.

Focality and prospective memory in preschool children.

We examined the influence of prospective memory (PM) cue focality in a sample of preschool children. Prior investigations in older populations indicated that focal targets were associated with enhanced PM performance, perhaps through more automatic retrieval processes. Importantly, this influential variable has not been thoroughly explored in younger samples. Over three test sessions, preschool children completed a memory task where they were shown a series of animals. During retrieval, participants were shown all of the animals except for one, and they had to name the missing animal. While engaged in this task, participants in the focal PM condition were instructed to remove particular animals (e.g., spider) from the game if they saw them. In the nonfocal condition, participants were told to remove any animal that was entirely one color (e.g., black) if they saw them during the game. The results demonstrated no difference in PM remembering between focal and nonfocal conditions. These results suggest that the effects of focality may not be present at the beginning stages of PM development. The implications for PM retrieval processes also are discussed.

The evolution of quantitative sensitivity.

The ability to represent approximate quantities appears to be phylogenetically widespread, but the selective pressures and proximate mechanisms favouring this ability remain unknown. We analysed quantity discrimination data from 672 subjects across 33 bird and mammal species, using a novel Bayesian model that combined phylogenetic regression with a model of number psychophysics and random effect components. This allowed us to combine data from 49 studies and calculate the Weber fraction (a measure of quantity representation precision) for each species. We then examined which cognitive, socioecological and biological factors were related to variance in Weber fraction. We found contributions of phylogeny to quantity discrimination performance across taxa. Of the neural, socioecological and general cognitive factors we tested, cortical neuron density and domain-general cognition were the strongest predictors of Weber fraction, controlling for phylogeny. Our study is a new demonstration of evolutionary constraints on cognition, as well as of a relation between species-specific neuron density and a particular cognitive ability. This article is part of the theme issue 'Systems neuroscience through the lens of evolutionary theory'.

Performance of Asian elephants (Elephas maximus) on a quantity discrimination task is similar to that of African savanna elephants (Loxodonta africana).

Using an object-choice task, we measured the relative quantity discrimination ability of Asian elephants. Two zoo-housed elephants were given auditory cues of food being dropped into two containers (Nonvisible condition), and in one condition they could also see the food on top of the containers (Visible condition). Elephants received sets of varying ratios and magnitudes. We found that the elephants chose the greater quantity of food significantly above chance in both the Visible and Nonvisible conditions. Additionally, we found the elephants' ability to discriminate between quantities decreased as the ratio, and not the absolute difference, between the quantities increased, which is predicted by the accumulator model. We also compare our findings to those from a study using the same methods with African savanna elephants and found that the two species performed at similar levels, but given our small sample size it is difficult to make strong species-level conclusions. In discussing our results, we consider differences between the two species' wild environments as well as the types of sensory cues provided in human care, and we provide recommendations for extensions of this work.

Divide and Conquer.

We assessed the ability of preschool children to assign the most difficult tasks to a symbolic helper. First, children were taught that a toy "helper" could aid them in remembering the location of a hidden item. Children preferentially assigned the helper to the objectively most difficult locations to remember. Each child then completed eight more tests, assessing a range of different skills such as counting, object identification, and word reading. Children again could assign some stimuli in each task to the helper, leaving the remaining stimuli for themselves to respond to in the given tasks. They were not explicitly told to assign the hardest stimulus to the helper. However, children consistently still did so in most tasks, although some tasks showed an effect of age where older children were more proficient in assigning the objectively more difficult stimuli to the helper. These results highlight a potential form of metacognition in young children in which they can monitor difficulty across varied kinds of assessments and use a generalized tool for asking for help that does not require verbal responding.

Working memory in children assessed with serial chaining and Simon tasks.

In the serial chaining task, participants are required to produce a sequence of responses to stimuli in the correct order, and sometimes must determine the sequence at trial outset if stimuli are masked after the first response is made. Similarly, the Simon memory span task presents a participant with a sequence of colors, and the participant must recreate the sequence after the full series is shown. In efforts to directly link the comparative literature on sequential planning behavior and working memory span with the developmental literature, we presented preschool children with the serial chaining task using masked Arabic numerals (N = 44) and the Simon memory span task (N = 65). Older children outperformed younger children in each task, sequencing a longer string of numbers in the serial chaining task and remembering a greater number of items in the Simon task. Controlling for the role of age, there was a significant positive relationship between task scores. These results highlight the emergence of working memory skills that might underlie planning capacities in children using a task developed for nonhuman animals, and the results indicate that improvement in general executive functions could be measured using either or both of these tasks among human children and nonhuman species.

Chimpanzees show some evidence of selectively acquiring information by using tools, making inferences, and evaluating possible outcomes.

Metacognition refers to thinking about one's thinking or knowing what one knows. Research suggests that this ability is not unique to humans and may be shared with nonhuman animals. In particular, great apes have shown behaviors on a variety of tasks that are suggestive of metacognitive ability. Here we combine a metacognitive task, the information-seeking task, with tool use and variable forms of initial information provided to chimpanzees to explore how informational states impact behavioral responses in these apes. Three chimpanzees were presented with an apparatus that contained five locations where food could be hidden. If they pointed to the correct location, they received the reward, but otherwise they did not. We first replicated several existing findings using this method, and then tested novel hypotheses. The chimpanzees were given different types of information across the experiments. Sometimes, they were shown the location of the food reward. Other times, they were shown only one empty location, which was not useful information. The chimpanzees also could use a tool to search any of those locations before making a selection. Chimpanzees typically used the tool to search out the location of the reward when they could not already know where it was, but they did not use the tool when they already had been given that information. One chimpanzee made inferences about the location of hidden food, even when that food was never shown in that location. The final experiment involved hiding foods of differing preference values, and then presenting the chimpanzees with different initial knowledge states (i.e., where the best food was located, where the less-preferred food was located, or where no food was located). All chimpanzees used the tool when they needed to use it to find the best possible item on that trial, but responded by choosing a location immediately when they did not need the tool. This finding highlights that their behavior was not the result of a simple rule following such as pointing to where any food had been seen.

Irrational choice behavior in human and nonhuman primates.

Choice behavior in humans has motivated a large body of research with a focus on whether decisions can be considered to be rational. In general, humans prefer having choice, as do a number of other species that have been tested, even though having increased choice does not necessarily yield a positive outcome. Humans have been found to choose an option more often only because the opportunity to select it was diminishing, an example of a deviation from economic rationality. Here we extend this paradigm to nonhuman primates in an effort to understand the mechanisms underlying this finding. In this study, we presented two groups of laboratory monkeys, capuchins (Cebus apella) and rhesus macaques (Macaca mulatta), as well as human subjects, with a computerized task in which subjects were presented with two differently colored icons. When the subject selected an icon, differing numbers of food pellets were dispensed (or points were assigned), making each icon correspond to a certain level of risk (one icon yielded 1 or 4 pellets/points and the other yielded 2 or 3). Initially, both options remained constantly available and we established choice preference scores for each subject. Then, we assessed preference patterns once the options were not continuously available. Specifically, choosing one icon would cause the other to shrink in size on the screen and eventually disappear if never selected. Selecting it would restore it to its full size. As predicted, humans shifted their risk preferences in the diminishing options phase, choosing to click on both icons more equally in order to keep both options available. At the group level, capuchin monkeys showed this pattern as well, but there was a great deal of individual variability in both capuchins and macaques. The present work suggests that there is some degree of continuity between human and nonhuman primates in the desire to have choice simply for the sake of having choice.

A computerized testing system for primates: Cognition, welfare, and the Rumbaughx.

Innovations in apparatus technology come about for a variety of reasons such as the need to use the same methodology with various species, the opportunity to present dynamic and carefully controlled stimuli, the goal of using automation to make data collection more precise or efficient, and the need to control for and/or eliminate the presence of experimenters in the testing context. At the Language Research Center (LRC) of Georgia State University, a computer-based system has been developed and used extensively with nonhuman primate species. This system involves the animal working in an enclosure that provides visual access to a computer screen, access to a joystick to control a cursor on the screen, and access to a food dish where pellets are delivered for correct responses. Here we will describe the history and development of this system as well as some considerations that might be applied to expanding this apparatus to a new environment, including the mobility of test stations, equipment needs, training protocols, and the cost and considerations for initial set up of such a system. A variety of computer based programs have been developed for use with this system. These programs have allowed insight into many nonhuman primate cognitive abilities and we highlight some that have been the focus of study at the LRC such as metacognition, numerical cognition, inhibitory processes, prospective memory, attention, and cognitive control. In addition, this cognitive testing apparatus has been shown to create a stimulating and enriching environment for the animals. We advocate that the computerized testing apparatus is useful for advancing our understanding of nonhuman animal cognition and may be uniquely suited to optimizing animal welfare. This area of research is already rapidly expanding in zoos, and we hope to offer some insight from one journey of designing, implementing and adapting a computerized testing paradigm.

The Effect of Computerized Testing on Sun Bear Behavior and Enrichment Preferences.

The field of comparative cognition investigates species' differences and similarities in cognitive abilities, and sheds light on the evolutionary origins of such capacities. Cognitive testing has been carried out in a variety of species; however, there are some taxa that are underrepresented in this field. The current work follows on a recent increase in cognitive research in the order Carnivora with a specific focus on sun bears. Sun bears are the smallest existing bear species and live in tropical regions of Southeast Asia. They have an omnivorous diet and use their tongues to forage for insects and sap. Little is known about sun bear cognition, although much like other bear species, anecdotes suggest a high level of intelligence. The current work explored training sun bears to use a touchscreen computer. This effort allows for insight into cognitive abilities as well as providing a complex source of enrichment for the bears. The bears use their tongues to respond to a touchscreen computer, and the effects on stereotypic behaviors on exhibit and preference for this over other forms of enrichment were examined. Overall, bears performed well on the task and showed a preference for the computer.

Self-control assessments of capuchin monkeys with the rotating tray task and the accumulation task.

Recent studies of delay of gratification in capuchin monkeys using a rotating tray (RT) task have shown improved self-control performance in these animals in comparison to the accumulation (AC) task. In this study, we investigated whether this improvement resulted from the difference in methods between the rotating tray task and previous tests, or whether it was the result of greater overall experience with delay of gratification tasks. Experiment 1 produced similar performance levels by capuchins monkeys in the RT and AC tasks when identical reward and temporal parameters were used. Experiment 2 demonstrated a similar result using reward amounts that were more similar to previous AC experiments with these monkeys. In Experiment 3, monkeys performed multiple versions of the AC task with varied reward and temporal parameters. Their self-control behavior was found to be dependent on the overall delay to reward consumption, rather than the overall reward amount ultimately consumed. These findings indicate that these capuchin monkeys' self-control capacities were more likely to have improved across studies because of the greater experience they had with delay of gratification tasks. Experiment 4 and Experiment 5 tested new, task-naïve monkeys on both tasks, finding more limited evidence of self-control, and no evidence that one task was more beneficial than the other in promoting self-control. The results of this study suggest that future testing of this kind should focus on temporal parameters and reward magnitude parameters to establish accurate measures of delay of gratification capacity and development in this species and perhaps others.

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.

Giant Panda Maternal Care: A Test of the Experience Constraint Hypothesis.

The body condition constraint and the experience condition constraint hypotheses have both been proposed to account for differences in reproductive success between multiparous (experienced) and primiparous (first-time) mothers. However, because primiparous mothers are typically characterized by both inferior body condition and lack of experience when compared to multiparous mothers, interpreting experience related differences in maternal care as support for either the body condition constraint hypothesis or the experience constraint hypothesis is extremely difficult. Here, we examined maternal behaviour in captive giant pandas, allowing us to simultaneously control for body condition and provide a rigorous test of the experience constraint hypothesis in this endangered animal. We found that multiparous mothers spent more time engaged in key maternal behaviours (nursing, grooming, and holding cubs) and had significantly less vocal cubs than primiparous mothers. This study provides the first evidence supporting the experience constraint hypothesis in the order Carnivora, and may have utility for captive breeding programs in which it is important to monitor the welfare of this species' highly altricial cubs, whose survival is almost entirely dependent on receiving adequate maternal care during the first few weeks of life.

The elusive illusion: Do children (Homo sapiens) and capuchin monkeys (Cebus apella) see the Solitaire illusion?

One approach to gaining a better understanding of how we perceive the world is to assess the errors that human and nonhuman animals make in perceptual processing. Developmental and comparative perspectives can contribute to identifying the mechanisms that underlie systematic perceptual errors often referred to as perceptual illusions. In the visual domain, some illusions appear to remain constant across the lifespan, whereas others change with age. From a comparative perspective, many of the illusions observed in humans appear to be shared with nonhuman primates. Numerosity illusions are a subset of visual illusions and occur when the spatial arrangement of stimuli within a set influences the perception of quantity. Previous research has found one such illusion that readily occurs in human adults, the Solitaire illusion. This illusion appears to be less robust in two monkey species, rhesus macaques and capuchin monkeys. We attempted to clarify the ontogeny of this illusion from a developmental and comparative perspective by testing human children and task-naïve capuchin monkeys in a computerized quantity judgment task. The overall performance of the monkeys suggested that they perceived the numerosity illusion, although there were large differences among individuals. Younger children performed similarly to the monkeys, whereas older children more consistently perceived the illusion. These findings suggest that human-unique perceptual experiences with the world might play an important role in the emergence of the Solitaire illusion in human adults, although other factors also may contribute.

Capuchin monkeys (Cebus apella) modulate their use of an uncertainty response depending on risk.

Metacognition refers to thinking about thinking, and there has been a great deal of interest in how this ability manifests across primates. Based on much of the work to date, a tentative division has been drawn with New World monkeys on 1 side and Old World monkeys and apes on the other. Specifically, Old World monkeys, apes, and humans often show patterns reflecting metacognition, but New World monkeys typically do not, or show less convincing behavioral patterns. However, recent data suggest that this difference may relate to other aspects of some experimental tasks. For example, 1 possibility is that risk tolerance affects how capuchin monkeys, a New World primate species, tend to perform. Specifically, it has recently been argued that on tasks in which there are 2 or 3 options, the "risk" of guessing is tolerable for capuchins because there is a high probability of being correct even if they "know they do not know" or feel something akin to uncertainty. The current study investigated this possibility by manipulating the degree of risk (2-choices vs. 6-choices) and found that capuchin monkeys used the uncertainty response more on 6-choice trials than on 2-choice trials. We also found that rate of reward does not appear to underlie these patterns of performance, and propose that the degree of risk is modulating capuchin monkeys' use of the uncertainty response. Thus, the apparent differences between New and Old World monkeys in metacognition may reflect differences in risk tolerance rather than access to metacognitive states.

Rates of reinforcement and measures of compliance in free and protected contact elephant management systems.

Protected contact is an alternative to traditional captive elephant training techniques that emerged as a result of concerns for animal welfare and personnel safety. The present study documented the behavior of elephants and their animal care professionals to determine rates of reinforcement and measures of compliance under two handling systems. Behavioral data were collected from animal care professionals and elephants during the elephants' baths in both free contact (FC) and protected contact (PC). Positive reinforcement, in the form of food, was delivered, on average, nearly eight times more frequently in the PC condition. Further, the mean rate at which the animal care professionals used the ankus in the FC condition as negative reinforcement was similar to the mean rate at which they provided positive reinforcement to the elephants in the FC condition. Latencies between verbal commands and the elephants' behaviors demonstrated an inconsistent pattern, but were generally longer in the PC condition. The mean percent of "refusals" by the elephants was higher for most behaviors across elephants in the PC condition. The findings suggest that animal care professionals did not heavily rely on positive reinforcement in the FC condition to elicit desired behaviors from the elephants, but this was the case in the PC condition. We propose that longer latencies and higher mean percent of refusals by the elephants may indicate that they were exercising choice or control over their environment, which has been associated with improved well-being. Additional studies of this kind are needed to enable other institutions to make informed decisions about elephant management and welfare.

Go when you know: Chimpanzees' confidence movements reflect their responses in a computerized memory task.

Three chimpanzees performed a computerized memory task in which auditory feedback about the accuracy of each response was delayed. The delivery of food rewards for correct responses also was delayed and occurred in a separate location from the response. Crucially, if the chimpanzees did not move to the reward-delivery site before food was dispensed, the reward was lost and could not be recovered. Chimpanzees were significantly more likely to move to the dispenser on trials they had completed correctly than on those they had completed incorrectly, and these movements occurred before any external feedback about the outcome of their responses. Thus, chimpanzees moved (or not) on the basis of their confidence in their responses, and these confidence movements aligned closely with objective task performance. These untrained, spontaneous confidence judgments demonstrated that chimpanzees monitored their own states of knowing and not knowing and adjusted their behavior accordingly.

Waiting for what comes later: capuchin monkeys show self-control even for nonvisible delayed rewards.

Self-control tasks used with nonhuman animals typically involve the choice between an immediate option and a delayed, but more preferred option. However, in many self-control scenarios, not only does the more impulsive option come sooner in time, it is often more concrete than the delayed option. For example, studies have presented children with the option of eating a visible marshmallow immediately, or foregoing it for a better reward that can only be seen later. Thus, the immediately available option is visible and concrete, whereas the delayed option is not visible and more abstract. We tested eight capuchin monkeys to better understand this potential effect by manipulating the visibility of the response options and the visibility of the baiting itself. Monkeys observed two food items (20 or 5 g pieces of banana) each being placed either on top of or inside of one of the two opaque containers attached to a revolving tray apparatus, either in full view of monkeys or occluded by a barrier. Trials ended when monkeys removed a reward from the rotating tray. To demonstrate self-control, monkeys should have allowed the smaller piece of food to pass if the larger piece was forthcoming. Overall, monkeys were successful on the task, allowing a smaller, visible piece of banana to pass from reach in order to access the larger, nonvisible banana piece. This was true even when the entire baiting process took place out of sight of the monkeys. This finding suggests that capuchin monkeys succeed on self-control tasks even when the delayed option is also more abstract than the immediate one-a situation likely faced by primates in everyday life.

Looking ahead? Computerized maze task performance by chimpanzees (Pan troglodytes), rhesus monkeys (Macaca mulatta), capuchin monkeys (Cebus apella), and human children (Homo sapiens).

Human and nonhuman primates are not mentally constrained to the present. They can remember the past and-at least to an extent-anticipate the future. Anticipation of the future ranges from long-term prospection such as planning for retirement to more short-term future-oriented cognition such as planning a route through a maze. Here we tested a great ape species (chimpanzees), an Old World monkey species (rhesus macaques), a New World monkey species (capuchin monkeys), and human children on a computerized maze task. All subjects had to move a cursor through a maze to reach a goal at the bottom of the screen. For best performance on the task, subjects had to "plan ahead" to the end of the maze to move the cursor in the correct direction, avoid traps, and reverse directions if necessary. Mazes varied in difficulty. Chimpanzees were better than both monkey species, and monkeys showed a particular deficit when moving away from the goal or changing directions was required. Children showed a similar pattern to monkeys regarding the effects of reversals and moves away from the goal, but their overall performance in terms of correct maze completion was similar to the chimpanzees. The results highlight similarities as well as differences in planning across species and the role that inhibitory control may play in future-oriented cognition in primates.