Object permanence in rhesus monkeys (Macaca mulatta).

We evaluated the performance of 6 adult rhesus monkeys (Macaca mulatta) on object permanence tasks. In Experiment 1, monkeys received search tasks that correspond to Stages 4, 5, and 6 of object permanence. Subjects were successful on tasks of visible displacements (Stages 4 and 5) but failed to find the object in invisible displacements (Stage 6). The monkeys adopted a search strategy of investigating a specific hiding location. In Experiment 2, monkeys were given a second opportunity to find the object if they investigated a location that was part of the displacement on their first search. Subjects relied on the same search strategy identified in Experiment 1. In Experiment 3, the experimenter hid the object in her hand rather than a container. The monkeys failed to recover the object, and individual differences were found in the strategies used. These results suggest that the upper limit of object permanence in rhesus monkeys is Stage 5. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Long-term effects of neonatal medial temporal ablations on socioemotional behavior in monkeys (Macaca mulatta).

Socioemotional abnormalities, including decreased social interactions and increased self-directed activity, were reported when rhesus monkeys with neonatal ablations of either the medial temporal lobe (AH) or the inferior temporal cortex (TE) were paired with unoperated peers at two and six months of age, though these abnormalities were more severe in Group AH (Bachevalier et al., 2001). As adults (Experiment 1), the monkeys were re-evaluated in the same dyads and their reactivity to novel toys, social status, and reactions to separation were also assessed. Group TE now showed only few if any of the abnormal behaviors observed in infancy. In contrast, Group AH continued to display decreased social interactions and increased self-directed activity and showed also increased submission and reduced responses to separation, but normal reactivity to novel toys. To determine whether this degree of socioemotional impairment was less severe than that produced by the same damage in adulthood, we assessed dyadic social interactions of monkeys raised until adulthood in laboratory conditions similar to those in Experiment 1 and then given the AH ablations (Experiment 2). Two months postoperatively these monkeys showed a small reduction in social interactions that became more pronounced six months postoperatively, yet remained less severe than that seen in the infant-lesioned monkeys. No other socioemotional effects, except for an increase in food/water consumption, were observed. The finding that neonatal AH lesions produce more severe socioemotional disturbances than the same lesion in adulthood is the reverse of the effect commonly reported for other cognitive functions after cerebral damage. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

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. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Prospective memory in the formation of learning sets by rhesus monkeys (Macaca mulatta).

In conventional discrimination learning-set formation, it is possible that rhesus monkeys (Macaca mulatta) learn to lay down prospective memories by anticipating the next trial and deciding in advance what choice will be made. To test this hypothesis, the authors administered discrimination problems with 24-hr intertrial intervals, predicting that these long intervals would disrupt or prevent the putative anticipation of the next trial. Confirming their expectation, the authors found no indication of learning-set formation under these conditions. (PsycINFO Database Record (c) 2011 APA, all rights reserved)     

Memory of auditory lists by rhesus monkeys (Macaca mulatta).

Monkey auditory memory was tested with increasing list lengths of 4, 6, 8, and 10 sounds. Five-hundred and twenty environmental sounds of 3-s duration were used. In Experiment 1, the monkeys initiated each list by touching the center speaker. They touched 1 of 2 side speakers to indicate whether a single test sound (presented from both side speakers simultaneously) was or was not in the list. The serial-position functions showed prominent primacy effects (good first-item memory) and recency effects (good last-item memory). Experiment 2 repeated the procedure without the list-initiation response and with a variable intertrial interval. The results of both experiments were similar and are discussed in relation to theories and hypotheses of serial-position effects. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Gaze following and joint attention in rhesus monkeys (Macaca mulatta).

Gaze and attention direction provide important sources of social information for primates. Behavioral studies show that chimpanzees spontaneously follow human gaze direction. By contrast, non-ape species such as macaques fail to follow gaze cues. The authors investigated the reactions of rhesus macaques (Macaca mulatta) to attention cues of conspecifics. Two subjects were presented with videotaped images of a stimulus monkey with its attention directed to 1 of 2 identical objects. Analysis of eye movements revealed that both subjects inspected the target (object or position attended by the stimulus monkey) more often than the distractor (nonattended object or position). These results provide evidence that rhesus monkeys follow gaze and use the attention cues of other monkeys to orient their own attention to objects. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Status, age, and sex effects on performance of discrimination tasks in group-tested rhesus monkeys (Macaca mulatta).

To assess the relation between performance and social or demographic variables, this study group tested a captive monkey colony on visual and manual discrimination problems. Animals could choose between differently colored, sand-filled boxes, where hue signaled the initial probability of finding buried food items. Dominant animals and subadults were most successful in locating and retrieving incentives, but sex did not affect performance. Rank effects occurred without overt aggression, suggesting deference by subordinates as a mediating mechanism. Age effects may reflect changing attention patterns only evident in complex arenas where cue salience becomes diluted. Because these findings differ from studies of singly tested animals, they show that, in a social context, an individual's rank and age may define opportunities to gain or efficiently use information. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Rhinal cortex ablations fail to disrupt reinforcer devaluation effects in rhesus monkeys (Macaca mulatta).

Studies have shown that excitotoxic lesions of the amygdala attenuate reinforcer devaluation effects in monkeys and rats. Because the rhinal (i.e., entorhinal and perirhinal) cortex has prominent reciprocal connections with the amygdala and has been suggested to store knowledge about objects, it is possible that it too composes part of the critical circuitry subserving learning about objects and their associated reinforcement value. To test this possibility, rhesus monkeys with rhinal cortex removals as well as unoperated controls were tested using a reinforcer devaluation procedure. Monkeys with rhinal cortex removals and controls, unlike those with amygdala lesions, tended to avoid displacing objects overlying a devalued food. These results indicate that the rhinal cortex is not a critical part of the neural circuitry mediating the effects of reinforcer devaluation. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

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. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Peers as primary attachment sources in yearling rhesus monkeys (Macaca mulatta).

Peer bonds were examined in 2 experiments using juvenile rhesus monkeys to determine (1) whether specific attachment bonds are formed between age-mates, (2) whether preferred age-mates can provide a secure base, and (3) whether a previous attachment bond affects the quality of subsequent attachment bonds. In Exp 1, 8 peer-only reared (POR) monkeys demonstrated a specific preference for a predicted favorite peer when given a choice between a familiar and 2 unfamiliar peers. In Exp 2, POR Ss were placed in a novel setting with either their most preferred peer, a familiar but not preferred peer, or an unfamiliar peer, and their responses were compared with those of a 2nd group of monkeys, reared for their 1st 6 mo of life by their mother. Both mother-reared (MP) and POR monkeys displayed significantly more intimate contact and significantly less distress when with their most preferred peer; nevertheless, even when they were with their most preferred peer, POR Ss exhibited more distress than MP Ss. Findings are discussed with reference to current attachment theory. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Age and sex differences in the effects of selective temporal lobe lesion on the formation of visual discrimination habits in rhesus monkeys (Macaca mulatta).

Three-month-old infant monkeys with neonatal ablations of either cortical area TE or the amygdala and hippocampus and age-matched normal infants were trained in a concurrent object discrimination task with 24-hr intertrial intervals. Neonatal area TE lesions yielded a transient deficit in visual habit formation, present in the female monkeys only, whereas the same lesions in adult monkeys yielded a severe and long-lasting deficit in both males and females. Although pointing to a greater neural compensation for the early loss as compared with the later loss of cortical area TE, the results also corroborate a recent suggestion (J. Bachevalier et al; see record 1990-03600-001) that, at 3 mo of age, area TE is more fully functional in females than in males. Neither early nor late amygdalohippocampal lesions impaired the ability to form visual discrimination habits, strengthening the proposal that the habit system uses a corticononlimbic circuit. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Prototype abstraction by monkeys (Macaca mulatta).

The authors analyze the shape categorization of rhesus monkeys (Macaca mulatta) and the role of prototype- and exemplar-based comparison processes in monkeys' category learning. Prototype and exemplar theories make contrasting predictions regarding performance on the Posner-Homa dot-distortion categorization task. Prototype theory--which presumes that participants refer to-be-categorized items to a representation near the category's center (the prototype)--predicts steep typicality gradients and large prototype-enhancement effects. Exemplar theory--which presumes that participants refer to-be-categorized items to memorized training exemplars-predicts flat typicality gradients and small prototype-enhancement effects. Across many categorization tasks that, for the first time, assayed monkeys' dot-distortion categorization, monkeys showed steep typicality gradients and large prototype-enhancement effects. These results suggest that monkeys--like humans--refer to-be-categorized items to a prototype-like representation near the category's center rather than to a set of memorized training exemplars. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Effects of selective neonatal temporal lobe lesions on socioemotional behavior in infant rhesus monkeys (Macaca mulatta).

Normal infant monkeys and infant monkeys with neonatal damage to either the medial temporal lobe or the inferior temporal visual area were assessed in dyadic social interactions at 2 and 6 months of age. Unlike the normal infant monkeys, which developed strong affiliative bonds and little or no behavioral disturbances, the lesioned monkeys (each of which was observed with an unoperated control) exhibited socioemotional abnormalities and aberrant behaviors. The socioemotional changes predominated at 6 months of age and were particularly severe in monkeys with medial temporal lesions. In both the pattern and time course, the socioemotional deficits produced by the neonatal medial temporal lesions bear a striking resemblance to the behavioral syndrome in children with autism. Further analysis of these lesion-induced abnormalities in nonhuman primates may therefore provide insight into this debilitating human developmental disorder. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Trajectory-selective neuronal activity in the motor cortex of rhesus monkeys (Macaca mulatta).

Neuronal activity recorded in the primate motor cortex reflected movement parameters in addition to the distance and direction of a target. These neurons may reflect the selection, from memory, of a detailed movement trajectory to be executed in response to visuospatial instructions. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Recognizing facial cues: Individual discrimination by chimpanzees (Pan troglodytes) and rhesus monkeys (Macaca mulatta).

Faces are one of the most salient classes of stimuli involved in social communication. Three experiments compared face-recognition abilities in chimpanzees (Pan troglodytes) and rhesus monkeys (Macaca mulatta). In the face-matching task, the chimpanzees matched identical photographs of conspecifics' faces on Trial 1, and the rhesus monkeys did the same after 4 generalization trials. In the individual-recognition task, the chimpanzees matched 2 different photographs of the same individual after 2 trials, and the rhesus monkeys generalized in fewer than 6 trials. The feature-masking task showed that the eyes were the most important cue for individual recognition. Thus, chimpanzees and rhesus monkeys are able to use facial cues to discriminate unfamiliar conspecifics. Although the rhesus monkeys required many trials to learn the tasks, this is not evidence that faces are not as important social stimuli for them as for the chimpanzees. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

The effects of bilateral lesions of the amygdala on dyadic social interactions in rhesus monkeys (Macaca mulatta).

The role of the amygdala in dyadic social interactions of adult rhesus monkeys (Macaca mulatta) was assessed after bilateral ibotenic acid lesions. Social, nonsocial, and spatial behaviors of amygdalectomized and control monkeys were assessed in 3 dyadic experiments: constrained, unconstrained, and round robin. Lesions produced extensive bilateral damage to the amygdala. Across all experiments, the amygdalectomized monkeys demonstrated increased social affiliation, decreased anxiety, and increased confidence compared with control monkeys, particularly during early encounters. Normal subjects also demonstrated increased social affiliation toward the amygdalectomized subjects. These results indicate that amygdala lesions in adult monkeys lead to a decrease in the species-normal reluctance to immediately engage a novel conspecific in social behavior. The altered behavior of the amygdalectomized monkeys may have induced the increased social interactions from their normal companions. This is contrary to the idea that amygdalectomy produces a decrease in social interaction and increased aggression from conspecifics. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Affiliative vocalizations in infant rhesus macaques (Macaca mulatta).

In Exp 1, infant rhesus monkeys were separated and then reunited with mothers, united with a male, or placed into an empty cage. Infants girned more when with mothers or the male than when alone. Girns declined over time when infants were united with the male. Coo rates were high when the infant was alone or with the male. Shrieks, barks, and fear-related behavior were higher with the male. In Exp 2, the vocalizations of infants were examined during separation when alone or when mothers or a male were in the same room. Infants cooed more when mothers or a male were present. Cooing increased over time, with a greater increase in the mothers' presence. Girns were given to both mothers and males, but more were given to mothers. Coos and girns are both affiliative vocalizations but are differentially modulated as infants cease cooing when they receive contact comfort. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Respondent conditioning of self-injurious behavior in early socially deprived rhesus monkeys (Macaca mulatta).

Examined whether certain environmental events could elicit self-injurious behavior (SIB) and whether the resulting SIB could be conditioned to an antecedently presented external stimulus. Exp I showed that SIB could be elicited in 4 socially isolated rhesus monkeys by the application of brief, mild, electric footshock. In Exp II, 3 socially isolated Ss were exposed to a procedure that paired a 10-sec tone with a 1-sec electric footshock. Three control Ss received presentations of the tone alone. Results show that Ss in the experimental group began to show SIB during the tone periods, thereby providing evidence of respondent conditioning. Data expand the scope of the learning model of SIB from primarily operant interpretations to respondent conditioning as well. (15 ref) (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

The expression of social dominance following neonatal lesions of the amygdala or hippocampus in rhesus monkeys (Macaca mulatta).

As part of ongoing studies on the neurobiology of socioemotional behavior in the nonhuman primate, the authors examined the social dominance hierarchy of juvenile macaque monkeys (Macaca mulatta) that received bilateral ibotenic acid lesions of the amygdala or the hippocampus or a sham surgical procedure at 2 weeks of age. The subjects were reared by their mothers with daily access to large social groups. Behavioral observations were conducted while monkeys were given access to a limited preferred food. This testing situation reliably elicited numerous species-typical dominance behaviors. All subjects were motivated to retrieve the food when tested individually. However, when a group of 6 monkeys was given access to only 1 container of the preferred food, the amygdala-lesioned monkeys had less frequent initial access to the food, had longer latencies to obtain the food, and demonstrated fewer species-typical aggressive behaviors. They were thus lower ranking on all indices of social dominance. The authors discuss these findings in relation to the role of the amygdala in the establishment of social rank and the regulation of aggression and fear. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Effects on executive function following damage to the prefrontal cortex in the rhesus monkey (Macaca mulatta).

[Correction Notice: An erratum for this article was reported in Vol 123(3) of Behavioral Neuroscience (see record 2009-07961-027). There was an error in the first sentence of the third full paragraph in the text on p. 235. The sentence should read “Based on the lesion reconstructions it was determined, as intended, that all monkeys had complete damage to areas 46, 8a, 8b, 9 and slight damage to area 10.”] Executive function is a term used to describe the cognitive processes subserved by the prefrontal cortex (PFC). An extensive body of work has characterized the effects of damage to the PFC in nonhuman primates, but it has focused primarily on the capacity of recognition and working memory. One limitation in studies of the functional parcellation of the PFC has been the absence of tests that assess executive function or its functional components. The current study used an adaptation of the Wisconsin Card Sorting Test, a classic test of frontal lobe and executive function in humans, to assess the effects of bilateral lesions in the dorsolateral PFC on executive function in the rhesus monkey (Macaca mulatta). The authors used the category set-shifting task, which requires the monkey to establish a pattern of responding to a specific category (color or shape) based on reward contingency, maintain that pattern of responding, and then shift to responding to a different category when the reward contingency changes. Rhesus monkeys with lesions of the dorsolateral PFC were impaired in abstraction, establishing a response pattern to a specific category and maintaining and shifting that response pattern on the category set-shifting task. (PsycINFO Database Record (c) 2010 APA, all rights reserved)