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)     

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)     

Bilateral neurotoxic amygdala lesions in rhesus monkeys (Macaca mulatta): Consistent pattern of behavior across different social contexts.

[Correction Notice: An erratum for this article was reported in Vol 122(4) of Behavioral Neuroscience (see record 2008-09788-025). In the aforementioned article, Table 1 on page 256 was incorrect. The correct table is printed in the erratum.] Although the amygdala has been repeatedly implicated in normal primate social behavior, great variability exists in the specific social and nonsocial behavioral changes observed in nonhuman primates with bilateral amygdala lesions. One plausible explanation pertains to differences in social context. This study measured the social behavior of amygdala-lesioned and unoperated rhesus monkeys (Macaca mulatta) in 2 contexts. Monkeys interacted in 4-member social groups over 32 test days. They were previously assessed in pairs (N. J. Emery et al., 2001) and were therefore familiar with each other at the beginning of this study. Across the 2 contexts, amygdala lesions produced a highly consistent pattern of social behavior. Operated monkeys engaged in more affiliative social interactions with control partners than did controls. In the course of their interactions, amygdala-lesioned monkeys also displayed an earlier decrease in nervous and fearful personality qualities than did controls. The increased exploration and sexual behavior recorded for amygdala-lesioned monkeys in pairs was not found in the 4-member groups. The authors concluded that the amygdala contributes to social inhibition and that this function transcends various social contexts. (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)     

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)     

"Bilateral neurotoxic amygdala lesions in rhesus monkeys (Macaca mulatta): Consistent pattern of behavior across different social contexts": Correction.

Reports an error in "Bilateral neurotoxic amygdala lesions in rhesus monkeys (Macaca mulatta): Consistent pattern of behavior across different social contexts" by Christopher J. Machado, Nathan J. Emery, John P. Capitanio, William A. Mason, Sally P. Mendoza and David G. Amaral (Behavioral Neuroscience, 2008[Apr], Vol 122[2], 251-266). In the aforementioned article, Table 1 on page 256 was incorrect. The correct table is printed in the erratum. (The following abstract of the original article appeared in record 2008-03769-001.) Although the amygdala has been repeatedly implicated in normal primate social behavior, great variability exists in the specific social and nonsocial behavioral changes observed in nonhuman primates with bilateral amygdala lesions. One plausible explanation pertains to differences in social context. This study measured the social behavior of amygdala-lesioned and unoperated rhesus monkeys (Macaca mulatta) in 2 contexts. Monkeys interacted in 4-member social groups over 32 test days. They were previously assessed in pairs (N. J. Emery et al., 2001) and were therefore familiar with each other at the beginning of this study. Across the 2 contexts, amygdala lesions produced a highly consistent pattern of social behavior. Operated monkeys engaged in more affiliative social interactions with control partners than did controls. In the course of their interactions, amygdala-lesioned monkeys also displayed an earlier decrease in nervous and fearful personality qualities than did controls. The increased exploration and sexual behavior recorded for amygdala-lesioned monkeys in pairs was not found in the 4-member groups. The authors concluded that the amygdala contributes to social inhibition and that this function transcends various social contexts. (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)     

The role of ventral and orbital prefrontal cortex in conditional visuomotor learning and strategy use in rhesus monkeys (Macaca mulatta).

[Correction Notice: An erratum for this article was reported in Vol 115(6) of Behavioral Neuroscience (see record 2007-17010-001). In Figure 1 (p. 974), the extent of the intended lesions in the sections 32 and 28 mm from the interaural plane was misprinted. The correctly printed figure is shown in the erratum.] Four rhesus monkeys (Macaca mulatta) were trained to learn novel sets of visuomotor associations in 50 trials or less, within single test sessions. After bilateral ablation of the orbital and ventral prefrontal cortex, the monkeys lost the ability to learn these associations within a session, although they could learn them when given several daily sessions. Thus, relatively slow, across-session visuomotor learning depends on neither the ventral nor orbital prefrontal cortex, but rapid, within-session learning does. The ablations also eliminated at least 2 response strategies, repeat-stay and lose-shift, which might account, in part, for the deficit in rapid learning. The deficit is unlikely to result from a failure of visual discriminative ability or working memory: The monkeys could discriminate similar stimulus material within a session, and reducing the working memory load did not improve within-session learning. (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)     

Dimensions of response to novelty are associated with social engagement and aggression in adult male rhesus macaques (Macaca mulatta).

In this study, the authors tested the hypothesis that behavioral response across social and nonsocial, novel and familiar conditions may be guided by the same trait(s) related to impulsivity in adult male rhesus macaques. The authors assessed 23 individuals' behavioral response to a series of nonsocial novel scenarios, as well as aggression and sociality within familiar and novel social contexts. Factor analysis of responses to nonsocial novelty identified two factors: Caution, which reflected latency to engage different novel situations, and Interest in Novelty, which consisted of duration and quality of exploration. Each dimension was associated with different social manifestations. Caution was negatively correlated with social aggression in novel and familiar social circumstances; Interest in Novelty was positively associated with social engagement in familiar, but not novel, social circumstances. The authors conclude that traits influencing impulsive response to novelty contribute to risky and normal social behavior across social contexts. (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)     

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)     

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)     

Rhesus monkeys (Macaca mulatta) rapidly learn to select dominant individuals in videos of artificial social interactions between unfamiliar conspecifics.

Social animals, such as primates, must behave appropriately in complex social situations such as dominance interactions. Learning dominance information through trial and error would be dangerous; therefore, cognitive mechanisms for rapid learning of dominance information by observation would be adaptive. We used a set of digitally edited artificial social interactions to examine whether rhesus monkeys (Macaca mulatta) can learn dominance relationships between unfamiliar conspecifics through observation. Our method allowed random assignment of stimulus monkeys to ranks in an artificial hierarchy, controlling for nonbehavioral cues that could indicate dominance. Subject monkeys watched videos depicting 1 stimulus monkey behaving dominantly toward another and were rewarded for selecting the dominant individual. Monkeys rapidly learned this discrimination across 5 behavior types in Experiment 1 and transferred performance to novel videos of new individuals in Experiment 2. In addition, subjects selected the dominant individual more often than expected by chance in probe videos containing no behavioral dominance information, indicating some retention of the relative dominance status of stimulus monkeys from training. Together, our results suggest that monkeys can learn dominance hierarchies through observation of third-party social interactions. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

The effects of orbital frontal cortex damage on the modulation of defensive responses by rats in playful and nonplayful social contexts.

In a series of 3 experiments on rats, 2 hypotheses were tested: (a) that damage to the orbital frontal cortex (OFC) would alter the socially relevant context for executing defensive responses but not their performance and (b) that damage done to the OFC in early infancy would produce more deficits in social behavior than similar damage occurring in adulthood. Bilateral or unilateral OFC damage in adult males did not impair their ability to defend themselves during play fighting and when protecting their food but did impair their ability to modify the pattern of defense in response to different partners. Rats that sustained bilateral damage at 3 days of age not only had deficits in partner-related modulation of defense but also exhibited hyperactivity in their play. The findings thus supported the proposed hypotheses. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

"The role of ventral and orbital prefrontal cortex in conditional visuomotor learning and strategy use in rhesus monkeys (Macaca mulatto)": Correction to Bussey et al (2001).

Reports an error in "The role of ventral and orbital prefrontal cortex in conditional visuomotor learning and strategy use in rhesus monkeys (Macaca mulatta)." by Timothy J. Bussey, Steven P. Wise and Elisabeth A. Murray (Behavioral Neuroscience, 2001[Oct], Vol 115[5], 971-982). In Figure 1 (p. 974), the extent of the intended lesions in the sections 32 and 28 mm from the interaural plane was misprinted. The correctly printed figure is shown in the erratum. (The following abstract of the original article appeared in record 2001-18882-001.) Four rhesus monkeys (Macaca mulatta) were trained to learn novel sets of visuomotor associations in 50 trials or less, within single test sessions. After bilateral ablation of the orbital and ventral prefrontal cortex, the monkeys lost the ability to learn these associations within a session, although they could learn them when given several daily sessions. Thus, relatively slow, across-session visuomotor learning depends on neither the ventral nor orbital prefrontal cortex, but rapid, within-session learning does. The ablations also eliminated at least 2 response strategies, repeat-stay and lose-shift, which might account, in part, for the deficit in rapid learning. The deficit is unlikely to result from a failure of visual discriminative ability or working memory: The monkeys could discriminate similar stimulus material within a session, and reducing the working memory load did not improve within-session learning. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Learning of discriminations is impaired, but generalization to altered views is intact, in monkeys (Macaca mulatta) with perirhinal cortex removal.

Rhesus monkeys (Macaca mulatta) were taught a large number of visual discriminations and then either received bilateral removal of the perirhinal cortex or were retained as unoperated controls. Operated monkeys were impaired in retention of the preoperatively learned problems. To test for generalization to novel views, the monkeys were required to discriminate, in probe trials, familiar pairs of images that were rotated, enlarged, shrunken, presented with color deleted, or degraded by masks. Although these manipulations reduced accuracy in both groups, the operated group was not differentially affected. In contrast, the same operated monkeys were impaired in reversal of familiar discriminations and in acquisition of new single-pair discriminations. These results indicate an important role for perirhinal cortex in visual learning, memory, or both, and show that under a variety of conditions, perirhinal cortex is not critical for the identification of stimuli. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

The amygdala and development of social cognition: Theoretical comment on Bauman, Toscano, Mason, Lavenex, and Amaral (2006).

Nonhuman primate studies, using selective amygdala lesions that spare cortical areas and fibers of passage, have helped to clarify the amygdala's specific contribution to social and emotional behavior. M. D. Bauman, J. E. Toscano, W. A. Mason, P. Lavenex, and D. G. Amaral (2006; see record 2006-09890-001) reported that macaque monkeys (Macaca mulatta) with neonatal neurotoxic amygdala lesions displayed lower rank in social dominance status, reduced aggressive gestures, and enhanced fearful reactions to social cues compared with normal controls and those with neonatal hippocampal lesions when tested as juveniles in a group of peers. These results are discussed in light of a recent study (C. J. Machado & J. Bachevalier, 2006; see record 2006-09890-002) showing that the same selective amygdala damage in adolescent monkeys did not alter presurgical social dominance status. This variability in behavioral changes after selective amygdala lesions underscores the significant interplay between timing of the lesion, genetic traits, and environmental factors and suggests that the amygdala is not the generator of specific emotional responses, but acts as a modulator to ensure that emotional responses are appropriate to the external stimuli and social context. (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)     

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)