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Kalin, N. H., & Shelton, S. E. (2003). Nonhuman primate models to study anxiety, emotion regulation, and psychopathology. Ann N Y Acad Sci, 1008, 189–200.
Abstract: This paper demonstrates that the rhesus monkey provides an excellent model to study mechanisms underlying human anxiety and fear and emotion regulation. In previous studies with rhesus monkeys, stable, brain, endocrine, and behavioral characteristics related to individual differences in anxiety were found. It was suggested that, when extreme, these features characterize an anxious endophenotype and that these findings in the monkey are particularly relevant to understanding adaptive and maladaptive anxiety responses in humans. The monkey model is also relevant to understanding the development of human psychopathology. For example, children with extremely inhibited temperament are at increased risk to develop anxiety disorders, and these children have behavioral and biological alterations that are similar to those described in the monkey anxious endophenotype. It is likely that different aspects of the anxious endophenotype are mediated by the interactions of limbic, brain stem, and cortical regions. To understand the brain mechanisms underlying adaptive anxiety responses and their physiological concomitants, a series of studies in monkeys lesioning components of the neural circuitry (amygdala, central nucleus of the amygdala and orbitofrontal cortex) hypothesized to play a role are currently being performed. Initial findings suggest that the central nucleus of the amygdala modulates the expression of behavioral inhibition, a key feature of the endophenotype. In preliminary FDG positron emission tomography (PET) studies, functional linkages were established between the amygdala and prefrontal cortical regions that are associated with the activation of anxiety.
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Lacreuse, A., Martin-Malivel, J., Lange, H. S., & Herndon, J. G. (2007). Effects of the menstrual cycle on looking preferences for faces in female rhesus monkeys. Anim. Cogn., 10(2), 105–115.
Abstract: Fluctuations of ovarian hormones across the menstrual cycle influence a variety of social and cognitive behaviors in primates. For example, female rhesus monkeys exhibit heightened interest for males and increased agonistic interactions with other females during periods of high estrogen levels. In the present study, we hypothesized that females' preference for males during periods of high estrogen levels is also expressed at the level of face perception. We tested four intact females on two face-tasks involving neutral portraits of male and female rhesus monkeys, chimpanzees and humans. In the visual preference task (VP), monkeys had to touch a button to view a face image. The image remained on the screen as long as the button was touched, and the duration of pressing was taken as an index of the monkey's looking time for the face stimulus. In the Face-Delayed Recognition Span Test (Face-DRST), monkeys were rewarded for touching the new face in an increasing number of serially presented faces. Monkeys were tested 5 days a week across one menstrual cycle. Blood was collected every other day for analysis of estradiol and progesterone. Two of the four females were cycling at the time of testing. We did not find an influence of the cycle on Face-DRST, likely due to a floor effect. In the VP however, the two cycling individuals looked longer at conspecific male faces than female faces during the peri-ovulatory period of the cycle. Such effects were absent for human and chimpanzee faces and for the two noncycling subjects. These data suggest that ovarian hormones may influence females' preferences for specific faces, with heightened preference for male faces during the peri-ovulatory period of the cycle. Heightened interest for stimuli of significant reproductive relevance during periods of high conception risk may help guide social and sexual behavior in the rhesus monkey.
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Maninger, N., Capitanio, J. P., Mendoza, S. P., & Mason, W. A. (2003). Personality influences tetanus-specific antibody response in adult male rhesus macaques after removal from natal group and housing relocation. Am. J. Primatol., 61(2), 73–83.
Abstract: Previous research has suggested that personality is related to immune function in macaques. Using a prospective design, we examined whether variation in the personality dimension “Sociability” in adult male rhesus macaques (Macaca mulatta) was related to the in vivo secondary antibody response to a tetanus toxoid booster immunization following removal from natal groups and relocation to individual housing. We also explored whether the timing of the immunization following relocation had an impact on the immune response. Blood was sampled at the time of booster immunization, at 14 and 28 days post-immunization, and approximately 9 months post-immunization. Plasma was assayed for tetanus-specific IgG by enzyme-linked immunoassay (ELISA). There was no difference between High- and Low-Sociable animals in antibody levels at the time of the booster immunization. Multivariate analysis of variance (MANOVA) revealed that High-Sociable animals had a significantly higher antibody response following relocation and immunization compared to Low-Sociable animals. There was no effect of timing of the immunization on the immune response. The results confirm that personality factors can affect animals' immune responses, and that the dimension Sociability may be influential in a male's response to social separation and relocation.
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Matzke, S. M., Oubre, J. L., Caranto, G. R., Gentry, M. K., & Galbicka, G. (1999). Behavioral and immunological effects of exogenous butyrylcholinesterase in rhesus monkeys. Pharmacol Biochem Behav, 62(3), 523–530.
Abstract: Although conventional therapies prevent organophosphate (OP) lethality, laboratory animals exposed to such treatments typically display behavioral incapacitation. Pretreatment with purified exogenous human or equine serum butyrylcholinesterase (Eq-BuChE), conversely, has effectively prevented OP lethality in rats and rhesus monkeys, without producing the adverse side effects associated with conventional treatments. In monkeys, however, using a commercial preparation of Eq-BuChE has been reported to incapacitate responding. In the present study, repeated administration of commercially prepared Eq-BuChE had no systematic effect on behavior in rhesus monkeys as measured by a six-item serial probe recognition task, despite 7- to 18-fold increases in baseline BuChE levels in blood. Antibody production induced by the enzyme was slight after the first injection and more pronounced following the second injection. The lack of behavioral effects, the relatively long in vivo half-life, and the previously demonstrated efficacy of BuChE as a biological scavenger for highly toxic OPs make BuChE potentially more effective than current treatment regimens for OP toxicity.
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Merchant, H., Fortes, A. F., & Georgopoulos, A. P. (2004). Short-term memory effects on the representation of two-dimensional space in the rhesus monkey. Anim. Cogn., 7(3), 133–143.
Abstract: Human subjects represent the location of a point in 2D space using two independent dimensions (x-y in Euclidean or radius-angle in polar space), and encode location in memory along these dimensions using two levels of representation: a fine-grain value and a category. Here we determined whether monkeys possessed the ability to represent location with these two levels of coding. A rhesus monkey was trained to reproduce the location of a dot in a circle by pointing, after a delay period, on the location where a dot was presented. Five different delay periods (0.5-5 s) were used. The results showed that the monkey used a polar coordinate system to represent the fine-grain spatial coding, where the radius and angle of the dots were encoded independently. The variability of the spatial response and reaction time increased with longer delays. Furthermore, the animal was able to form a categorical representation of space that was delay-dependent. The responses avoided the circumference and the center of the circle, defining a categorical radial prototype around one third of the total radial length. This radial category was observed only at delay durations of 3-5 s. Finally, the monkey also formed angular categories with prototypes at the obliques of the quadrants of the circle, avoiding the horizontal and vertical axes. However, these prototypes were only observed at the 5-s delay and on dots lying on the circumference. These results indicate that monkeys may possess spatial cognitive abilities similar to humans.
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Nelson, E. E., Shelton, S. E., & Kalin, N. H. (2003). Individual differences in the responses of naive rhesus monkeys to snakes. Emotion, 3(1), 3–11.
Abstract: The authors demonstrated individual differences in inhibited behavior and withdrawal responses of laboratory-born rhesus monkeys when initially exposed to a snake. Most monkeys displayed a small significant increase in their behavioral inhibition in the presence of a snake. A few monkeys had marked responses, and some actively withdrew. Although the responses of the most extreme laboratory-born monkeys were comparable to feral-born monkeys, the responses of the laboratory-born monkeys rapidly habituated. The individual differences in the responses of naive monkeys likely reflect a continuum from orienting to wariness to fear. A neurobiological model is presented that addresses potential mechanisms underlying these individual differences, their relation to fear, and how they may predispose to phobia development.
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Neumann, C., Duboscq, J., Dubuc, C., Ginting, A., Irwan, A. M., Agil, M., et al. (2011). Assessing dominance hierarchies: validation and advantages of progressive evaluation with Elo-rating. Animal Behaviour, 82(4), 911–921.
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Owren, M. J., Dieter, J. A., Seyfarth, R. M., & Cheney, D. L. (1993). Vocalizations of rhesus (Macaca mulatta) and Japanese (M. fuscata) macaques cross-fostered between species show evidence of only limited modification. Dev Psychobiol, 26(7), 389–406.
Abstract: Two rhesus and two Japanese macaque infants were cross-fostered between species in order to study the effects of auditory experience on vocal development. Both the cross-fostered and normally raised control subjects were observed over the first 2 years of life and their vocalizations were tape-recorded. We classified 8053 calls by ear, placed each call in one of six acoustic categories, and calculated the rates at which different call-types were used in different social contexts. Species differences were found in the use of “coo” and “gruff” vocalizations among control subjects. Japanese macaques invariably produced coos almost exclusively. In contrast, rhesus macaques produced a mixture of coos and gruffs and showed considerable interindividual variation in the relative use of one call type or the other. Cross-fostered Japanese macaques adhered to their species-typical behavior, rarely using gruffs. Cross-fostered rhesus subjects also exhibited species-typical behavior in many contexts, but in some situations produced coos and gruffs at rates that were intermediate between those shown by normally raised animals of the two species. This outcome suggests that environmentally mediated modification of vocal behavior may have occurred, but that the resulting changes were quite limited.
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Parr, L. A., Winslow, J. T., Hopkins, W. D., & de Waal, F. B. (2000). Recognizing facial cues: individual discrimination by chimpanzees (Pan troglodytes) and rhesus monkeys (Macaca mulatta). J Comp Psychol, 114(1), 47–60.
Abstract: 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.
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Santos, L. R., Miller, C. T., & Hauser, M. D. (2003). Representing tools: how two non-human primate species distinguish between the functionally relevant and irrelevant features of a tool. Anim. Cogn., 6(4), 269–281.
Abstract: Few studies have examined whether non-human tool-users understand the properties that are relevant for a tool's function. We tested cotton-top tamarins (Saguinus oedipus) and rhesus macaques (Macaca mulatta) on an expectancy violation procedure designed to assess whether these species make distinctions between the functionally relevant and irrelevant features of a tool. Subjects watched an experimenter use a tool to push a grape down a ramp, and then were presented with different displays in which the features of the original tool (shape, color, orientation) were selectively varied. Results indicated that both species looked longer when a newly shaped stick acted on the grape than when a newly colored stick performed the same action, suggesting that both species perceive shape as a more salient transformation than color. In contrast, tamarins, but not rhesus, attended to changes in the tool's orientation. We propose that some non-human primates begin with a predisposition to attend to a tool's shape and, with sufficient experience, develop a more sophisticated understanding of the features that are functionally relevant to tools.
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