Technical note: Urine collection from vervet monkeys by instrumental conditioning

Gang-caged adult male vervet monkeys were trained to urinate on demand into a plastic beaker by positive reinforcement (peanut rewards). The animals were not separated from their social group during training or sampling.     

Squirrel monkeys' response to inequitable outcomes indicates a behavioural convergence within the primates

Although several primates respond negatively to inequity, it is unknown whether this results from homology or convergent processes. Behaviours shared within a taxonomic group are often assumed to be homologous, yet this distinction is important for a better understanding of the function of the behaviour. Previous hypotheses have linked cooperation and inequity responses. Supporting this, all species in which inequity responses have been documented are cooperative. In this study, we tested this hypothesis by investigating the response to inequity in squirrel monkeys, which share a phylogenetic family with capuchin monkeys, but do not cooperate extensively. Subjects exchanged tokens to receive food rewards in conditions in which the level of effort required and reward received varied. Squirrel monkeys did not respond negatively to inequity. However, the monkeys were sensitive to the variation present in the task; male subjects showed a contrast effect and, as in previous studies, subjects were more sensitive to differences in reward in the context of a task than when rewards were given for free. Taken with other results, these results support the hypothesis that a negative response to inequity evolved convergently in primates, probably as a mechanism for evaluating outcomes relative to one's partners in cooperative species.     

<Emphasis Type="Italic">Cebus apella</Emphasis> Tolerate Intermittent Unreliability in Human Experimenters

Monkeys form expectations for outcomes based on interactions with human experimenters. Capuchins, a cooperative New World monkey species, not only anticipate receiving rewards that the experimenter indicates, but also apparently anticipate rewards based on what the experimenter has given to their partners. However, this could be due to subjects responding to either outcomes or experimenters. Here we examine whether capuchins will continue to interact with human experimenters who are occasionally unreliable. We tested 10 monkeys with a series of familiar human experimenters using an exchange task. The experimenters had never before participated in exchange studies with these monkeys, hence the monkeys learned about their behavior during the course of testing. Occasionally experimenters were unreliable, failing to give a reward after the monkey returned the token. The monkeys did recognize these interactions as different, responding much more quickly in trials following those that were nonrewarded than in other situations with the same experimenter. However, subjects did not change their preference for experimenters when given the opportunity to choose between the unreliable exchanger and another exchanger, nor did subjects learn to prefer reliable experimenters from watching other monkeys’ interactions. Instead, subjects returned the tokens to the same location from which they received it. These results indicate that capuchins may not be sensitive to isolated instances in which experimenters are unreliable, possibly because of a strong bias to returning the token to the location from which it was donated.     

Partner's behavior, not reward distribution, determines success in an unequal cooperative task in capuchin monkeys

It was recently demonstrated that capuchin monkeys notice and respond to distributional inequity, a trait that has been proposed to support the evolution of cooperation in the human species. However, it is unknown how capuchins react to inequitable rewards in an unrestricted cooperative paradigm in which they may freely choose both whether to participate and, within the bounds of their partner's behavior, which reward they will receive for their participation. We tested capuchin monkeys with such a design, using a cooperative barpull, which has been used with great success in the past. Contrary to our expectations, the equity of the reward distribution did not affect success or pulling behavior. However, the behavior of the partner in an unequal situation did affect overall success rates: pairs that had a tendency to alternate which individual received the higher-value food in unequal reward situations were more than twice as successful in obtaining rewards than pairs in which one individual dominated the higher-value food. This ability to equitably distribute rewards in inherently biased cooperative situations has profound implications for activities such as group hunts, in which multiple individuals work together for a single, monopolizable reward.     

Macaque Monkeys Can Learn Token Values from Human Models through Vicarious Reward

Monkeys can learn the symbolic meaning of tokens, and exchange them to get a reward. Monkeys can also learn the symbolic value of a token by observing conspecifics but it is not clear if they can learn passively by observing other actors, e.g., humans. To answer this question, we tested two monkeys in a token exchange paradigm in three experiments. Monkeys learned token values through observation of human models exchanging them. We used, after a phase of object familiarization, different sets of tokens. One token of each set was rewarded with a bit of apple. Other tokens had zero value (neutral tokens). Each token was presented only in one set. During the observation phase, monkeys watched the human model exchange tokens and watched them consume rewards (vicarious rewards). In the test phase, the monkeys were asked to exchange one of the tokens for food reward. Sets of three tokens were used in the first experiment and sets of two tokens were used in the second and third experiments. The valuable token was presented with different probabilities in the observation phase during the first and second experiments in which the monkeys exchanged the valuable token more frequently than any of the neutral tokens. The third experiments examined the effect of unequal probabilities. Our results support the view that monkeys can learn from non-conspecific actors through vicarious reward, even a symbolic task like the token-exchange task.     

Use of spatial, visual, and olfactory information during foraging in wild nocturnal and diurnal anthropoids: A field experiment comparing Aotus, Callicebus, and Saguinus

Early in their evolution, the ancestors of anthropoid primates radiated from a nocturnal to a diurnal niche. Foraging during the night differs from foraging during the day in terms of the availability of light and color cues, and in the movement of odor molecules through the canopy. In this study, we compared the ability of nocturnal and diurnal New World monkeys to use perceptual cues (i.e., the sight or smell of food) and spatial information (place predictability) in within-patch foraging decisions. An experimental field study was conducted on wild groups of night monkeys (Aotus nigriceps), tamarins (Saguinus imperator imperator and S. fuscicollis weddelli), and titi monkeys (Callicebus cupreus) at the Zoobotanical Park/UFAC, Rio Branco, Brazil. Our research design included the construction of feeding stations located in the home range of the study groups. Each feeding station consisted of eight visually identical feeding platforms located in a circular arrangement. In all test settings, two platforms at each feeding station contained a food reward (banana), and the remaining six platforms contained a sham reward (yellow plastic or inaccessible banana). In the night-monkey experiments, each feeding platform was illuminated by a 40-W red bulb to aid the researcher in observing their behavior. When the location of reward sites was predictable over time, individuals in all four species successfully relocated food rewards based solely on spatial information. Each species was also successful in using visual information to distinguish real from sham food rewards. However, only night monkeys and one group of emperor tamarins used olfactory information alone to locate food rewards. Overall, the species' performances did not clearly differentiate Aotus from diurnal New World primates in these experiments.     

Competing demands of prosociality and equity in monkeys

Prosocial decisions may lead to unequal payoffs among group members. Although an aversion to inequity has been found in empirical studies of both human and nonhuman primates, the contexts previously studied typically do not involve a trade-off between prosociality and inequity. Here we investigate the apparent coexistence of these two factors, specifically the competing demands of prosociality and equity. We directly compare the responses of brown capuchin monkeys (Cebus apella) among situations where prosocial preferences conflict with equality, using a paradigm comparable to other studies of cooperation and inequity in this species. By choosing to pull a tray towards themselves, subjects rewarded themselves and/or another in conditions in which the partner either received the same or different rewards, or the subject received no reward. In unequal payoff conditions, subjects could obtain equality by choosing not to pull in the tray, so that neither individual was rewarded. The monkeys showed prosocial preferences even in situations of moderate disadvantageous inequity, preferring to pull in the tray more often when a partner was present than absent. However, when the discrepancy between rewards increased, prosocial behavior ceased.     

Get It While It’s Hot: A Peak-First Bias in Self-Generated Choice Order in Rhesus Macaques

Animals typically must make a number of successive choices to achieve a goal: e.g., eating multiple food items before becoming satiated. However, it is unclear whether choosing the best first or saving the best for last represents the best choice strategy to maximize overall reward. Specifically, since outcomes can be evaluated prospectively (with future rewards discounted and more immediate rewards preferred) or retrospectively (with prior rewards discounted and more recent rewards preferred), the conditions under which each are used remains unclear. On the one hand, humans and non-human animals clearly discount future reward, preferring immediate rewards to delayed ones, suggesting prospective evaluation; on the other hand, it has also been shown that a sequence that ends well, i.e., with the best event or item last, is often preferred, suggesting retrospective evaluation. Here we hypothesized that when individuals are allowed to build the sequence themselves they are more likely to evaluate each item individually and therefore build a sequence using prospective evaluation. We examined the relationship between self-generated choice order and preference in rhesus monkeys in two experiments in which the distinctiveness of options were relatively high and low, respectively. We observed a positive linear relationship between choice order and preference among highly distinct options, indicating that the rhesus monkeys chose their preferred food first: i.e., a peak-first order preference. Overall, choice order depended on the degree of relative preference among alternatives and a peak-first bias, providing evidence for prospective evaluation when choice order is self-generated.     

Responses to a simple barter task in chimpanzees, Pan troglodytes

Chimpanzees (Pan troglodytes) frequently participate in social exchange involving multiple goods and services of variable value, yet they have not been tested in a formalized situation to see whether they can barter using multiple tokens and rewards. We set up a simple barter economy with two tokens and two associated rewards and tested chimpanzees on their ability to obtain rewards by returning the matching token in situations in which their access to tokens was unlimited or limited. Chimpanzees easily learned to associate value with the tokens, as expected, and did barter, but followed a simple strategy of favoring the higher-value token, regardless of the reward proffered, instead of a more complex but more effective strategy of returning the token that matched the reward. This response is similar to that shown by capuchin monkeys in our previous study. We speculate that this response, while not ideal, may be sufficient to allow for stability of the social exchange system in these primates, and that the importance of social barter to both species may have led to this convergence of strategies.     

Absence of Spatial Tuning in the Orbitofrontal Cortex

There is limited data in the literature to explicitly support the notion that neurons in OFC are truly action-independent in their coding. We set out to specifically test the hypothesis that OFC value-related neurons in area 13 m of the monkey do not carry information about the action required to obtain that reward – that activity in this area represents reward values in an abstract and action-independent manner. To accomplish that goal we had two monkeys select and execute saccadic eye movements to 81 locations in the visual field for three different kinds of juice rewards. Our detailed analysis of the response fields indicates that these neurons are insensitive to the amplitude or direction of the saccade required to obtain these rewards. Our data thus validate earlier proposals that neurons of 13 m in the OFC encode subjective value independent of the saccadic action required to obtain that reward.     

Do female tamarins use visual cues to detect fruit rewards more successfully than do males?

Primates are unique among eutherian mammals for possessing trichromatic colour vision. It is generally proposed that trichromacy evolved to aid detection of ripe fruits against mature foliage. However, while trichromacy is routine in all Old World monkeys and apes (the catarrhines), a cone opsin polymorphism in New World monkeys (the platyrrhines) results in foraging groups with mixed capacities for chromatic distinction. Although 50-66% of female platyrrhines are trichromatic, all males are dichromatic. Here, we test the hypothesis that trichromatic platyrrhines use visual cues to detect fruit rewards more successfully than do males. Specifically, we ask whether female emperor tamarins, Saguinus imperator imperator, and saddleback tamarins, S. fuscicollis weddelli, are the first members of their foraging group to locate food patches; and, furthermore, whether they are more successful than males in using colour, shape and size cues to discriminate between sham and reward feeding sites. Our results show that females and males do not differ in their ability to locate or discriminate between feeding sites. We conclude that trichromatic vision in female tamarins does not confer an advantage for detecting yellow fruit rewards against mature foliage. Copyright 2003 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.      

Marmoset monkeys evaluate third-party reciprocity

Many non-human primates have been observed to reciprocate and to understand reciprocity in one-to-one social exchanges. A recent study demonstrated that capuchin monkeys are sensitive to both third-party reciprocity and violation of reciprocity; however, whether this sensitivity is a function of general intelligence, evidenced by their larger brain size relative to other primates, remains unclear. We hypothesized that highly pro-social primates, even with a relatively smaller brain, would be sensitive to others'' reciprocity. Here, we show that common marmosets discriminated between human actors who reciprocated in social exchanges with others and those who did not. Monkeys accepted rewards less frequently from non-reciprocators than they did from reciprocators when the non-reciprocators had retained all food items, but they accepted rewards from both actors equally when they had observed reciprocal exchange between the actors. These results suggest that mechanisms to detect unfair reciprocity in third-party social exchanges do not require domain-general higher cognitive ability based on proportionally larger brains, but rather emerge from the cooperative and pro-social tendencies of species, and thereby suggest this ability evolved in multiple primate lineages.     

Saccade reward signals in posterior cingulate cortex

Movement selection depends on the outcome of prior behavior. Posterior cingulate cortex (CGp) is strongly connected with both limbic and oculomotor circuitry, and CGp neurons respond following saccades, suggesting a role in signaling the motivational outcome of gaze shifts. To test this hypothesis, single CGp neurons were studied in monkeys while they shifted gaze to visual targets for liquid rewards that varied in size or were delivered probabilistically. CGp neurons responded following saccades as well as following reward delivery, and these responses were correlated with reward size. CGp neurons also responded following the omission of predicted rewards. The timing of CGp activation and its modulation by reward could provide signals useful for updating representations of expected saccade value.     

Monkeys and apes: Are their cognitive skills really so different?

Differences in cognitive skills across taxa, and between monkeys and apes in particular, have been explained by different hypotheses, although these often are not supported by systematic interspecific comparisons. Here, we directly compared the cognitive performance of the four great apes and three monkey species (spider monkeys, capuchin monkeys, and long‐tailed macaques), differing in their phylogenetic‐relatedness and socioecology. We tested subjects on their ability to remember object locations (memory task), track object displacements (transposition task), and obtain out‐of‐reach rewards (support task). Our results showed no support for an overall clear‐cut distinction in cognitive skills between monkeys and apes as species performance varied substantially across tasks. Although we found differences in performance at tracking object displacements between monkeys and apes, interspecific differences in the other two tasks were better explained in terms of differential socioecology, especially differential levels of fission–fusion dynamics. A cluster analysis using mean scores of each condition of the three tasks for each species suggested that the only dichotomy might be between members of the genus Pan and the rest of the tested species. These findings evidence the importance of using multiple tasks across multiple species in a comparative perspective to test different explanations for the enhancement of specific cognitive skills. Am J Phys Anthropol 143:188–197, 2010. © 2010 Wiley‐Liss, Inc.     

Cooperative problem solving in a cooperatively breeding primate (Saguinus oedipus)

We investigated cooperative problem solving in unrelated pairs of the cooperatively breeding cottontop tamarin, Saguinus oedipus, to assess the cognitive basis of cooperative behaviour in this species and to compare abilities with other apes and monkeys. A transparent apparatus was used that required extension of two handles at opposite ends of the apparatus for access to rewards. Resistance was applied to both handles so that two tamarins had to act simultaneously in order to receive rewards. In contrast to several previous studies of cooperation, both tamarins received rewards as a result of simultaneous pulling. The results from two experiments indicated that the cottontop tamarins (1) had a much higher success rate and efficiency of pulling than many of the other species previously studied, (2) adjusted pulling behaviour to the presence or absence of a partner, and (3) spontaneously developed sustained pulling techniques to solve the task. These findings suggest that cottontop tamarins understand the role of the partner in this cooperative task, a cognitive ability widely ascribed only to great apes. The cooperative social system of tamarins, the intuitive design of the apparatus, and the provision of rewards to both participants may explain the performance of the tamarins.     

Reward-Induced Phasic Dopamine Release in the Monkey Ventral Striatum and Putamen

In-vivo voltammetry has successfully been used to detect dopamine release in rodent brains, but its application to monkeys has been limited. We have previously detected dopamine release in the caudate of behaving Japanese monkeys using diamond microelectrodes (Yoshimi 2011); however it is not known whether the release pattern is the same in various areas of the forebrain. Recent studies have suggested variations in the dopaminergic projections to forebrain areas. In the present study, we attempted simultaneous recording at two locations in the striatum, using fast-scan cyclic voltammetry (FSCV) on carbon fibers, which has been widely used in rodents. Responses to unpredicted food and liquid rewards were detected repeatedly. The response to the liquid reward after conditioned stimuli was enhanced after switching the prediction cue. These characteristics were generally similar between the ventral striatum and the putamen. Overall, the technical application of FSCV recording in multiple locations was successful in behaving primates, and further voltammetric recordings in multiple locations will expand our knowledge of dopamine reward responses.     

A concept of value during experimental exchange in brown capuchin monkeys, Cebus apella

We evaluated the response of brown capuchin monkeys to two differentially valued tokens in an experimental exchange situation akin to a simple barter. Monkeys were given a series of three tests to evaluate their ability to associate tokens with food, then their responses were examined in a barter situation in which tokens were either limited or unlimited. Capuchins did not perform barter in the typical sense, returning the tokens which were associated with the reward. However, females, but not males, showed a different response, preferring the higher-value token. This may indicate that they learned to prefer one token over the other rather than to associate the tokens with their specific rewards. This sex difference parallels previous findings of greater reciprocity in female brown capuchins than in males.     

Cognitive performance in rhesus monkeys varies by sex and prenatal androgen exposure

Men and women differ on performance and strategy on several spatial tasks. Rodents display similar sex differences, and manipulations of early hormone exposure alter the direction of these differences. However, most cognitive testing of nonhuman primates has utilized sample sizes too small to investigate sexually differentiated behaviors. This study presents an investigation of sex differences and the effects of prenatal androgen on spatial memory and strategy use in rhesus monkeys. Monkeys prenatally exposed to vehicle, testosterone, or the androgen receptor blocker flutamide performed a search task in which 5 of 12 goal boxes contained food rewards. Spatial consistency and the presence of local landmarks were varied. Performance when both spatial and marker cues were available did not differ by sex or prenatal treatment. Contrary to predictions, females easily solved the task when local markers were removed, and their performance outscored males. Although eliminating spatial consistency and requiring subjects to use local markers impaired performance by all monkeys, females continued to locate correct goal boxes at higher than chance levels and scored better than males. Blocking prenatal androgen exposure in males improved use of local markers. These findings suggest that the tendency to attend to landmarks and to use them in solving spatial problems is typical of females across many species, including rodents, humans, and rhesus monkeys. In rhesus monkeys and rodents, developmental androgen eliminates this specialization. However, these results are the only known example of better performance of females than males when salient markers are removed.     

Can Monkeys Choose Optimally When Faced with Noisy Stimuli and Unequal Rewards?

We review the leaky competing accumulator model for two-alternative forced-choice decisions with cued responses, and propose extensions to account for the influence of unequal rewards. Assuming that stimulus information is integrated until the cue to respond arrives and that firing rates of stimulus-selective neurons remain well within physiological bounds, the model reduces to an Ornstein-Uhlenbeck (OU) process that yields explicit expressions for the psychometric function that describes accuracy. From these we compute strategies that optimize the rewards expected over blocks of trials administered with mixed difficulty and reward contingencies. The psychometric function is characterized by two parameters: its midpoint slope, which quantifies a subject''s ability to extract signal from noise, and its shift, which measures the bias applied to account for unequal rewards. We fit these to data from two monkeys performing the moving dots task with mixed coherences and reward schedules. We find that their behaviors averaged over multiple sessions are close to optimal, with shifts erring in the direction of smaller penalties. We propose two methods for biasing the OU process to produce such shifts.     

Prefrontal coding of temporally discounted values during intertemporal choice

Reward from a particular action is seldom immediate, and the influence of such delayed outcome on choice decreases with delay. It has been postulated that when faced with immediate and delayed rewards, decision makers choose the option with maximum temporally discounted value. We examined the preference of monkeys for delayed reward in an intertemporal choice task and the neural basis for real-time computation of temporally discounted values in the dorsolateral prefrontal cortex. During this task, the locations of the targets associated with small or large rewards and their corresponding delays were randomly varied. We found that prefrontal neurons often encoded the temporally discounted value of reward expected from a particular option. Furthermore, activity tended to increase with [corrected] discounted values for targets [corrected] presented in the neuron's preferred direction, suggesting that activity related to temporally discounted values in the prefrontal cortex might determine the animal's behavior during intertemporal choice.