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. (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)     

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)     

Ordinal judgments of symbolic stimuli by capuchin monkeys (Cebus apella) and rhesus monkeys (Macaca mulatta): The effects of differential and nondifferential reward.

Ordinal learning was investigated in capuchin monkeys (Cebus apella) and rhesus monkeys (Macaca mulatta). In Experiment 1, both species were presented with pairings of the Arabic numerals 0 to 9. Some monkeys were given food rewards equal to the value of the numeral selected and some were rewarded with a single pellet only for choosing the higher numeral within the pair. Both species learned to select the larger numeral, but only rhesus monkeys that were differentially rewarded performed above chance levels when presented with novel probe pairings. In Experiment 2, the monkeys were first presented with arrays of 5 familiar numerals (from the range 0 to 9) and then arrays of 5 novel letters (from the range A to J) with the same reward outcomes in place as in Experiment 1. Both species performed better with the numerals, suggesting that an ordinal sequence of all stimuli had been learned during Experiment 1, rather than a matrix of two-choice discriminations. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Opioids and attachment in rhesus macaque (Macaca mulatta) abusive mothers.

This study investigated the role of the endogenous opioid system in maternal and affiliative behavior of group-living rhesus macaque (Macaca mularta) mothers with a history of abusive parenting. 18 mothers received an injection of the opioid antagonist naltrexone or saline for 5 days per wk for the first 4 wks of the infant's life. After treatment, mother-infant pairs were focally observed. Naltrexone did not significantly affect infant abuse or other measures of maternal behavior. Naltrexone increased the amount of grooming received by mothers from other group members and reduced the mothers' rate of displacement activities such as scratching, yawning, and self-grooming. These results concur with previous primate studies in suggesting that opioids mediate the rewarding effects of receiving grooming and affect anxiety-related behaviors. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Sex differences in physical dependence on orally self-administered phencyclidine (PCP) in rhesus monkeys (Macaca mulatta).

Withdrawal from orally self-administered phencyclidine (PCP) has been shown to alter operant baselines of food-maintained responding. The goal of the present study was to determine whether there are sex differences in these alterations. Seven female and 7 male rhesus monkeys (Macaca mulatta) were given concurrent access to PCP and water under fixed ratio (FR) 8 schedules during 2 daily sessions that alternated with 2 sessions during which pellet deliveries were contingent on lever presses under an FR 64 schedule. After operant responding stabilized, PCP was replaced by water for 10 days, and food access remained under the same schedule. Subsequently, concurrent PCP and water access was reintroduced for 10 days. This procedure was repeated with 3 PCP concentrations (0.125, 0.25, and 0.50 mg/ml) and 3 FR requirements for food-reinforced responding (64, 128, and 256). Disruptions in operant responding for food served as a quantitative measure of withdrawal severity. During PCP withdrawal, males showed a greater suppression of food-maintained behavior than females at the 2 highest PCP concentrations and the lowest FR requirement tested. Males responded more than females for PCP; however, when weight was taken into consideration, PCP intake (milligrams per kilogram) in males and females was equal. The data suggest that males may experience more severe withdrawal effects than females, and the duration of the adverse effects of withdrawal lasts longer in males than in females. This study is the 1st to use nonhuman primates to document sex differences in withdrawal severity as measured by a quantifiable baseline. (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)     

Rearing experience differentially affects somatic and cardiac startle responses in rhesus monkeys (Macaca mulatta).

The present study reports, for the first time, somatic and cardiac responses to acoustic startle in 2 groups of rhesus monkeys (Macaca mulatta) with different rearing experiences. Both groups showed a significant direct relationship between startle amplitude and the intensity of the acoustic startle stimulus (80-120 dB) and rapid heart rate acceleration after a 120-dB stimulus. Monkeys reared with a same-age peer (PR) showed higher startle amplitudes than those reared with their mothers (MR), consistent with rearing effects in rodents. The MR monkeys, however, showed faster heart rate acceleration of greater overall magnitude than that of the PR group. The results are discussed with regard to a monkey model for neuropsychiatric disease. (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)     

Emergence of stereotypies in juvenile monkeys (Macaca mulatta) with neonatal amygdala or hippocampus lesions.

The emergence of stereotypies was examined in juvenile rhesus monkeys (Macaca mulatta) who, at 2 weeks of postnatal age, received selective bilateral ibotenic acid lesions of the amygdala (N = 8) or hippocampus (N = 8). The lesion groups were compared to age-matched control subjects that received a sham surgical procedure (N = 8). All subjects were maternally reared for the first 6 months and provided access to social groups throughout development. Pronounced stereotypies were not observed in any of the experimental groups during the first year of life. However, between 1 to 2 years of age, both amygdala- and hippocampus-lesioned subjects began to exhibit stereotypies. When observed as juveniles, both amygdala- and hippocampus-lesioned subjects consistently produced more stereotypies than the control subjects in a variety of contexts. More interesting, neonatal lesions of either the amygdala or hippocampus resulted in unique repertoires of repetitive behaviors. Amygdala-lesioned subjects exhibited more self-directed stereotypies and the hippocampus-lesioned subjects displayed more head-twisting. We discuss these results in relation to the neurobiological basis of repetitive stereotypies in neurodevelopmental disorders, such as autism. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Rhesus monkeys (Macaca mulatta) lack expertise in face processing.

Faces are salient stimuli for primates that rely predominantly on visual cues for recognizing conspecifics and maintaining social relationships. While previous studies have shown similar face discrimination processes in chimpanzees and humans, data from monkeys are unclear. Therefore, three studies examined face processing in rhesus monkeys using the face inversion effect, a fractured face task, and an individual recognition task. Unlike chimpanzees and humans, the monkeys showed a general face inversion effect reflected by significantly better performance on upright compared to inverted faces (conspecifics, human and chimpanzees faces) regardless of the subjects' expertise with those categories. Fracturing faces alters first- and second-order configural manipulations whereas previous studies in chimpanzees showed selective deficits for second-order configural manipulations. Finally, when required to individuate conspecific's faces, i.e., matching two different photographs of the same conspecific, monkeys showed poor discrimination and repeated training. These results support evolutionary differences between rhesus monkeys and Hominoids in the importance of configural cues and their ability to individuate conspecifics' faces, suggesting a lack of face expertise in rhesus monkeys. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Analogical reasoning and the differential outcome effect: Transitory bridging of the conceptual gap for rhesus monkeys (Macaca mulatta).

Monkeys, unlike chimpanzees and humans, have a marked difficulty acquiring relational matching-to-sample (RMTS) tasks that likely reflect the cognitive foundation upon which analogical reasoning rests. In the present study, rhesus monkeys (Macaca mulatta) completed a categorical (identity and nonidentity) RMTS task with differential reward (pellet ratio) and/or punishment (timeout ratio) outcomes for correct and incorrect choices. Monkeys in either differential reward-only or punishment-only conditions performed at chance levels. However, the RMTS performance of monkeys experiencing both differential reward and punishment conditions was significantly better than chance. Subsequently when all animals experienced nondifferential outcomes tests, their RMTS performance levels were at chance. These results indicate that combining differential reward and punishment contingencies provide an effective, albeit transitory, scaffolding for monkeys to judge analogical relations-between-relations. (PsycINFO Database Record (c) 2011 APA, all rights reserved)     

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. (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)     

What meaning means for same and different: Analogical reasoning in humans (Homo sapiens), chimpanzees (Pan troglodytes), and rhesus monkeys (Macaca mulatta).

Thus far, language- and token-trained apes (e.g., D. Premack, 1976; R. K. R. Thompson, D. L. Oden, & S. T. Boysen, 1997) have provided the best evidence that nonhuman animals can solve, complete, and construct analogies, thus implicating symbolic representation as the mechanism enabling the phenomenon. In this study, the authors examined the role of stimulus meaning in the analogical reasoning abilities of three different primate species. Humans (Homo sapiens), chimpanzees (Pan troglodytes), and rhesus monkeys (Macaca mulatta) completed the same relational matching-to-sample (RMTS) tasks with both meaningful and nonmeaningful stimuli. This discrimination of relations-between-relations serves as the basis for analogical reasoning. Meaningfulness facilitated the acquisition of analogical matching for human participants, whereas individual differences among the chimpanzees suggest that meaning can either enable or hinder their ability to complete analogies. Rhesus monkeys did not succeed in the RMTS task regardless of stimulus meaning, suggesting that their ability to reason analogically, if present at all, may be dependent on a dimension other than the representational value of stimuli. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Rhesus monkeys (Macaca mulatta) hear rising frequency sounds as looming.

Rising sound intensity provides an important cue for the detection of looming objects. Studies with humans indirectly suggest that rising pitch can also signal a looming object. This link between rising intensity and rising frequency is puzzling because no physical rise in frequency occurs when a sound source approaches. Putative explanations include (a) the idea that the loudness of sound depends on its frequency, (b) the frequent co-occurrence of rising intensity with rising frequency in vocalizations generates an association between the 2 features, and (c) auditory neurons process amplitude- and frequency-modulated sounds similarly. If these hypotheses are valid, then rhesus monkeys (Macaca mulatta)—which share some homologies in the vocal production apparatus and auditory system—should also associate rising frequency with rising intensity, and thus should perceive rising frequency as a looming sound source. A head-turning assay and a preferential-looking paradigm revealed that monkeys show an attentional bias toward rising versus falling frequency sounds and link the former to visual looming signals. This suggests that monkeys hear a rising frequency sound as a looming sound source even though, in the real world, no such link exists. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Serial list linking by macaque monkeys (Macaca mulatta): List property limitations.

Four sophisticated macaque monkeys (Macaca mulatta) learned 6 different, 15-item ordinal lists (via conditional, 2-choice discriminations) as part of a study assessing some properties of serial list memory in monkeys. After assuring that the first 3 lists were well retained, the researchers attempted to link these by training only the 2 end-item pairs that ordered all 45 items into an inclusive series. A 20-day test of possible pairings among these 45 items was then conducted. Subsequently, the other 3 lists were trained and tested for retention, but no link training was provided. Then, a test like the one that had followed linking was administered. Unlike previous outcomes with three 5-item lists, linking did not yield immediate merger of three 15-item lists into a 45-item list, although 45-item lists were acquired after sufficient exposure to the testing/training regimen under both linking and nonlinking conditions. List length as a limiting factor in linking suggested processing restrictions analogous to those observed in human list memory. Results supported further investigation of list-linking characteristics. (PsycINFO Database Record (c) 2010 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 sameldifferent 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-itern training but progressively improved with larger set sizes and was complete following 128-itern 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. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Implicit and explicit category learning by macaques (Macaca mulatta) and humans (Homo sapiens).

An influential theoretical perspective differentiates in humans an explicit, rule-based system of category learning from an implicit system that slowly associates different regions of perceptual space with different response outputs. This perspective was extended for the 1st time to the category learning of nonhuman primates. Humans (Homo sapiens) and macaques (Macaca mulatta) learned categories composed of sine-wave gratings that varied across trials in bar width and bar orientation. The categories had either a single-dimensional, rule-based solution or a two-dimensional, information-integration solution. Humans strongly dimensionalized the stimuli and learned the rule-based task far more quickly. Six macaques showed the same performance advantage in the rule-based task. In humans, rule-based category learning is linked to explicit cognition, consciousness, and declarative reports about the contents of cognition. These results demonstrate an empirical continuity between human and nonhuman primate cognition, suggesting that nonhuman primates may have some structural components of humans’ capacity for explicit cognition. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Stages of category learning in monkeys (Macaca mulatta) and humans (Homo sapiens).

Smith and Minda (1998) and Blair and Homa (2001) studied the time course of category learning in humans. They distinguished an early, abstraction-based stage of category learning from a later stage that incorporated a capacity for categorizing exceptional category members. The present authors asked whether similar processing stages characterize the category learning of nonhuman primates. Humans (Homo sapiens) and monkeys (Macaca mulatta) participated in category-learning tasks that extended Blair and Homa’s paradigm comparatively. Early in learning, both species improved on typical items more than on exception items, indicating an initial mastery of the categories’ general structure. Later in learning, both species selectively improved their exception-item performance, indicating exception-item resolution or exemplar memorization. An initial stage of abstraction-based category learning may characterize categorization across a substantial range of the order Primates. This default strategy may have an adaptive resonance with the family resemblance organization of many natural-kind categories. (PsycINFO Database Record (c) 2010 APA, all rights reserved)