Perceived control in rhesus monkeys (Macaca mulatta): enhanced video-task performance

This investigation was designed to determine whether perceived control effects found in humans extend to rhesus monkeys (Macaca mulatta) tested in a video-task format, using a computer-generated menu program, SELECT. Choosing one of the options in SELECT resulted in presentation of 5 trials of a corresponding task and subsequent return to the menu. In Experiments 1-3, the animals exhibited stable, meaningful response patterns in this task (i.e., they made choices). In Experiment 4, performance on tasks that were selected by the animals significantly exceeded performance on identical tasks when assigned by the experimenter under comparable conditions (e.g., time of day, order, variety). The reliable and significant advantage for performance on selected tasks, typically found in humans, suggests that rhesus monkeys were able to perceive the availability of choices.     

Information seeking by rhesus monkeys (Macaca mulatta) and capuchin monkeys (Cebus apella)

Animal metacognition is an active, growing research area, and one part of metacognition is flexible information-seeking behavior. In Roberts et al. (2009), pigeons failed an intuitive information-seeking task. They basically refused, despite multiple fostering experiments, to view a sample image before attempting to find its match. Roberts et al. concluded that pigeons’ lack of an information-seeking capacity reflected their broader lack of metacognition. We report a striking species contrast to pigeons. Eight rhesus macaques and seven capuchin monkeys passed the Roberts et al. test of information seeking—often in their first testing session. Members of both primate species appreciated immediately the lack of information signaled by an occluded sample, and the need for an information-seeking response to manage the situation. In subsequent testing, macaques demonstrated flexible/varied forms of information management. Capuchins did not. The research findings bear on the phylogenetic distribution of metacognition across the vertebrates, and on the underlying psychological requirements for metacognitive and information-seeking performances.     

Perceptual completion in rhesus monkeys (Macaca mulatta) and pigeons (Columbia livia)

In a two-dimensional drawing, when the narrow edge of a bar appears to touch the edge of a large rectangle, humans overestimate the length of the bar (Kanizsa, 1979). Kanizsa has suggested that this illusion occurs because humans perceive the bar as continuing behind the rectangle and complete the "occluded" portion of the bar. Rhesus monkeys and pigeons were trained to classify black target bars with a variety of lengths as "long" or "short." In training, the bar was always located at the same distance from a gray box. After learning this discrimination, the subjects were tested on novel stimuli, in which the bar was located at three new locations. Monkeys showed a consistent response bias for "long" when the bar touched the box, but pigeons did not. Monkeys appear to have completed the "occluded" part like humans, whereas pigeons failed to do so. Because this procedure does not require animals to complete the "occluded" part with any particular form, their failure suggests that pigeons do not even perceive the target bar as continuing behind the "occluding" figure. The failure of pigeons may be due to difficulty in perceiving depth from two-dimensional drawings.     

Discrimination of artificial polymorphous categories by rhesus monkeys (Macaca mulatta)

Monkeys (Macaca mulatta) were trained to discriminate between sets of artificial stimuli such as those used by Jitsumori (1993) for pigeons and humans. The stimuli were arrays of symbols differing along three two-valued (positive or negative) dimensions. The discrimination required was between polymorphous categories in which a positive stimulus was defined by possession of any 2 out of 3 positive features. Of the 5 monkeys, 3 learned the discrimination much faster than did pigeons, but transfer to novel stimuli was less impressive than had been shown in pigeons. The 3 monkeys showed high levels of transfer to the stimuli that contained either all 3 positive or all 3 negative features, but 2 of the 3 monkeys failed to show transfer to stimuli that had 1 of the 3 features replaced with a novel one. Analysis of the monkeys' performance raised doubts on the additive integration of features but supported learning of feature combinations as a basis for the discrimination of polymorphous categories by this species.     

Perceptual completion in rhesus monkeys (Macaca mulatta) and pigeons (Columba livia)

In a two-dimensional drawing, when the narrow edge of a bar appears to touch the edge of a large rectangle, humans overestimate the length of the bar (Kanizsa, 1979). Kanizsa has suggested that this illusion occurs because humans perceive the bar as continuing behind the rectangle and complete the “occluded” portion of the bar. Rhesus monkeys and pigeons were trained to classify black target bars with a variety of lengths as “long” or “short.” In training, the bar was always located at the same distance from a gray box. After learning this discrimination, the subjects were tested on novel stimuli, in which the bar was located at three new locations. Monkeys showed a consistent response bias for “long” when the bar touched the box, but pigeons did not. Monkeys appear to have completed the “occluded” part like humans, whereas pigeons failed to do so. Because this procedure does not require animals to complete the “occluded” part with any particular form, their failure suggests that pigeons do not even perceive the target bar as continuing behind the “occluding” figure. The failure of pigeons may be due to difficulty in perceiving depth from two-dimensional drawings.     

Amygdalectomy and responsiveness to novelty in rhesus monkeys (Macaca mulatta): generality and individual consistency of effects

Rhesus monkeys (Macaca mulatta) with bilateral ibotenic acid-produced lesions of the amygdala were compared with controls in several novel situations, including exposures to metal objects, toy animals, and a person. Early in testing, the monkeys with lesions showed reduced inhibitions on responsiveness compared with controls. With continuing exposures, differences between groups diminished sharply as inhibitions waned in the controls. This outcome is consistent with the hypothesis that the amygdala mediates caution in initial reactions to ambiguous or threatening novel situations, which, in the absence of adverse consequences, diminishes with repetition. Consistency of individual responsiveness across different situations, including pairing with other monkeys, was substantial in lesioned and normal monkeys, suggesting that stable qualities of temperament influenced the results in both groups.     

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

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.     

Social responding to mirrors in rhesus monkeys (Macaca mulatta): effects of temporary mirror removal.

As a result of a long-term, longitudinal project initiated in 1978, a pair of rhesus macaques (Macaca mulatta) housed together in front of a mirror all their lives now exhibit relatively little interest in their reflection. Previous work has shown, however, that simply moving the mirror to a new location produces a short-term reinstatement of social responding to their images. As an extension of these findings, in this study the mirror was left in the same position but turned away from the cage. On turning the mirror back to face the cage 5 days later, both animals reacted as if confronted with another pair of monkeys and directed a burst of social responses at the mirror.     

Detection of directed gaze in rhesus monkeys (Macaca mulatta).

To examine the ability of monkeys to detect the direction of attention of other individuals, the authors quantitatively investigated the visual scanning pattern of rhesus monkeys (Macaca mulatta) in response to visually presented images of a human frontal face. The present results demonstrated not only that monkeys predominantly gaze at the eyes as compared with other facial areas in terms of duration and number of fixations, but also that they gaze at the eyes for a longer time period and more frequently when a human face, presented as a stimulus, gazed at them than when the gaze was shifted. These results indicate that rhesus monkeys are sensitive to the directed gaze of humans, suggesting that monkeys pay more attention to the human whose attention is directed to them.     

Social competence is reduced in socially deprived rhesus monkeys (Macaca mulatta)

Rhesus monkeys deprived for some period from their mother have often served as a model for the effect of adverse rearing conditions on social competence in humans. Social competence is the capacity to react in a species-specific way to social interactions. The current study assesses whether early deprivation from peers also affects the rates of behavior and social competence in rhesus monkeys. This was studied in groups of rhesus monkeys with different rearing conditions: subadult females that were mother-only reared during their first year of life and subsequently housed with peers were compared with subadult females from five naturalistic social groups. Socially deprived monkeys showed higher rates of submission and stereotypic behaviors than socially reared individuals. In addition, they show socially incompetent behavior, since they react with agonistic behavior to nonthreatening social situations. The results suggest that this socially incompetent behavior is rooted in a general feeling of anxiety toward group companions. The authors hypothesize that anxiety negatively affects social information processing, which results in socially incompetent behavior.     

Developmental consequences of behavioral inhibition: a model in rhesus monkeys (Macaca mulatta)

In children, behavioral inhibition is characterized by a disposition to withdraw in the presence of strangers and novel situations. Later in life, behavioral inhibition can result in an increased risk for anxiety and depression and a decrease in social behavior. We selected rhesus monkeys that, during infancy, showed evidence of behavioral inhibition in response to separation, and contrasted them with non‐inhibited peers. To understand the development of behavioral inhibition at juvenile age, we collected behavioral data in response to relocation; in response to a human intruder challenge; and in naturalistic outdoor field corrals. At 4 years of age (young adulthood), we again collected behavioral data in the outdoor field corrals to understand the adult social consequences of behavioral inhibition. We also included sex, dominance rank, and number of available kin in our analyses. Finally, to understand the consistency in behavior in behaviorally inhibited animals, we conducted exploratory analyses contrasting behaviorally inhibited animals that showed high vs. low durations of non‐social behaviors as adults. At juvenile age, behaviorally inhibited animals continued to show behavioral differences in the novel testing room and during the human intruder challenge, generally showing evidence of greater anxiety and emotionality compared to non‐inhibited controls. In their outdoor corrals, behaviorally inhibited juveniles spent more time alone and less time in proximity and grooming with mother and other adult females. In young adulthood, we found that behavioral inhibition was not related to time spent alone. We did find that duration of time alone in adulthood was related to time alone exhibited as juveniles; sex, dominance rank, or the number of kin were not influential in adult non‐social duration, either as main effects or as moderators. Finally, exploratory analyses revealed that behaviorally inhibited females that were more sociable (less time spent alone) as adults had spent more time grooming as juveniles, suggesting that high‐quality social interaction at a young age might mitigate the social consequences of behavioral inhibition. Overall, we believe that the many similarities with the human data that we found suggest that this monkey model of naturally occurring behavioral inhibition can be valuable for understanding social development.     

Change detection by rhesus monkeys (Macaca mulatta) and pigeons (Columba livia)

Two monkeys (Macaca mulatta) learned a color change-detection task where two colored circles (selected from a 4-color set) were presented on a 4 × 4 invisible matrix. Following a delay, the correct response was to touch the changed colored circle. The monkeys' learning, color transfer, and delay transfer were compared to a similar experiment with pigeons. Monkeys, like pigeons (Columba livia), showed full transfer to four novel colors, and to delays as long as 6.4 s, suggesting they remembered the colors as opposed to perceptual based attentional capture process that may work at very short delays. The monkeys and pigeons were further tested to compare transfer with other dimensions. Monkeys transferred to shape and location changes, unlike the pigeons, but neither species transferred to size changes. Thus, monkeys were less restricted in their domain to detect change than pigeons, but both species learned the basic task and appear suitable for comparative studies of visual short-term memory. (PsycINFO Database Record (c) 2012 APA, all rights reserved).     

Mechanisms of same/different abstract-concept learning by rhesus monkeys (Macaca mulatta)

Experiments with 9 rhesus monkeys (Macaca mulatta) showed, for the first time, that abstract-concept learning varied with the training stimulus set size. In a same/different task, monkeys required to touch a top picture before choosing a bottom picture (same) or white rectangle (different) learned rapidly. Monkeys not required to touch the top picture or presented with the top picture for a fixed time learned slowly or not at all. No abstract-concept learning occurred after 8-item training but progressively improved with larger set sizes and was complete following 128-item training. A control monkey with a constant 8-item set ruled out repeated training and testing. Contrary to the unique-species account, it is argued that different species have quantitative, not qualitative, differences in abstract-concept learning.     

Disconnect in concept learning by rhesus monkeys (Macaca mulatta): judgment of relations and relations-between-relations

The authors investigated the role that entropy measures, discriminative cues, and symbolic knowledge play for rhesus monkeys (Macaca mulatta) in the acquisition of the concepts of same and different for use in a computerized relational matching-to-sample task. After repeatedly failing to perceive relations between pairs of stimuli in a 2-choice discrimination paradigm, monkeys rapidly learned to discriminate between 8-element arrays. Subsequent tests with smaller arrays, however, suggested that, although important for the initial acquisition of the concept, entropy is not a variable on which monkeys are dependent. Not only do monkeys choose a corresponding relational pair in the presence of a cue, but they also choose the cue itself in the presence of the relational pair--in essence, labeling those relations. Subsequent failure in the judgment of relations-between-relations, however, suggests that perhaps a qualitatively different cognitive component exists that prevents monkeys from behaving analogically.     

Mechanisms of inferential order judgments in humans (Homo sapiens) and rhesus monkeys (Macaca mulatta)

If A > B, and B > C, it follows logically that A > C. The process of reaching that conclusion is called transitive inference (TI). Several mechanisms have been offered to explain transitive performance. Scanning models claim that the list is scanned from the ends of the list inward until a match is found. Positional discrimination models claim that positional uncertainty accounts for accuracy and reaction time patterns. In Experiment 1, we trained rhesus monkeys (Macaca mulatta) and humans (Homo sapiens) on adjacent pairs (e.g., AB, BC, CD, DE, EF) and tested them with previously untrained nonadjacent pairs (e.g., BD). In Experiment 2, we trained a second list and tested with nonadjacent pairs selected between lists (e.g., B from List 1, D from List 2). We then introduced associative competition between adjacent items in Experiment 3 by training 2 items per position (e.g., B?C?, B?C?) before testing with untrained nonadjacent items. In all 3 experiments, humans and monkeys showed distance effects in which accuracy increased, and reaction time decreased, as the distance between items in each pair increased (e.g., BD vs. BE). In Experiment 4, we trained adjacent pairs with separate 9- and 5-item lists. We then tested with nonadjacent pairs selected between lists to determine whether list items were chosen according to their absolute position (e.g., D, 5-item list > E, 9-item list), or their relative position (e.g., D, 5-item list < E, 9-item list). Both monkeys' and humans' choices were most consistent with a relative positional organization.