Effects of pair bonding on dopamine D1 receptors in monogamous male titi monkeys (Callicebus cupreus).

Pair bonding leads to increases in dopamine D1 receptor (D1R) binding in the nucleus accumbens of monogamous prairie voles. In the current study, we hypothesized that there is similar up-regulation of D1R in a monogamous primate, the titi monkey (Callicebus cupreus). Receptor binding of the D1R antagonist [11 C]-SCH23390 was measured in male titi monkeys using PET scans before and after pairing with a female. We found that within-subject analyses of pairing show significant increases in D1R binding in the lateral septum, but not the nucleus accumbens, caudate, putamen, or ventral pallidum. The lateral septum is involved in a number of processes that may contribute to social behavior, including motivation, affect, reward, and reinforcement. This region also plays a role in pair bonding and paternal behavior in voles. Our observations of changes in D1R in the lateral septum, but not the nucleus accumbens, suggest that there may be broadly similar dopaminergic mechanisms underlying pair bonding across mammalian species, but that the specific changes to neural circuitry differ. This study is the first research to demonstrate neuroplasticity of the dopamine system following pair bonding in a non-human primate; however, substantial variability in the response to pairing suggests the utility of further research on the topic.

Differences in titi monkey (Callicebus cupreus) social bonds affect arousal, affiliation, and response to reward.

Titi monkeys (Callicebus cupreus) are a monogamous, New World primate. Adult pair-mates form a bidirectional social bond and offspring form a selective unidirectional bond to their father. Some of the neurobiology involved in social bonds and maternal behavior is similar to the neural circuitry involved in nonsocial reward. Due to these overlapping mechanisms, social states may affect responses to external rewarding stimuli. We sought to determine whether having a social attachment, and/or being in the presence of that attachment figure, can affect an individual's response to a rewarding stimulus. In addition, we compared affiliative bonds between pair-mates to those between offspring and fathers. Eighteen adult male titi monkeys were either living alone (Lone), with a female pair-mate (Paired), or with the natal group (Natal; N = 6/condition). Each individual went through eight 30-min preference tests for a sweet substance, Tang. For Paired and Natal males, half of the test sessions were with their attachment figure and half were alone. Lone males were always tested alone. Preference scores for Tang, time spent drinking, affiliative, and arousal behaviors were measured. Paired and Natal males emitted significantly more isolation peeps and locomoted more when tested alone compared to when tested with their attachment figure, and paired males engaged in more affiliative behavior than Natal males. Lone males engaged in significantly more behaviors indicative of behavioral arousal such as locomotion and piloerection compared to Paired and Natal males. Finally, Paired males drank significantly more Tang and had a significantly greater preference for Tang compared to Lone and Natal males. These results indicate that offspring undergo a behavioral separation response upon separation from their father that persists into adulthood, Lone males are more behaviorally reactive, and that living with an attachment figure and the type of attachment relationship result in different responses to a rewarding sweet stimulus.

Behavioral inhibition is associated with airway hyperresponsiveness but not atopy in a monkey model of asthma.

OBJECTIVE: To determine whether indicators of behavioral inhibition and cortisol responses to stressful situations, obtained in infancy, were associated with asthma-related measures (atopy and airway hyperresponsiveness [AHR]) approximately 2 years later. METHODS: Measures reflecting inhibited temperament and cortisol response after a 25-hour separation from mother and relocation to a novel room were obtained for 21 rhesus monkeys (mean age, 109 days; range, 91-122 days). Inhibited temperament was measured by reduced emotionality and increased vigilance. Atopy and AHR were assessed after 2 years (age range, 19-35 months) using skin tests to common aeroallergens and inhaled methacholine challenge, respectively. RESULTS: No associations were found between atopy and either behavioral inhibition or cortisol levels (p > .56). Low emotionality was associated with AHR (r = 0.47, p = .03), and a trend was found for blunted cortisol responsiveness and AHR (r = 0.42, p = .06). CONCLUSIONS: Inhibited temperament and blunted cortisol responsiveness may be related to the development of AHR that is common to both nonatopic and atopic asthma phenotypes and may indicate risk for nonatopic asthma specifically.

Serotonin pathway gene-gene and gene-environment interactions influence behavioral stress response in infant rhesus macaques.

A subset of serotonin (5-HT) pathway polymorphisms has been shown to confer risk for psychological dysfunction, particularly in individuals who experience early adversity. Understanding the developmental processes underlying these Gene x Environment interactions will strengthen the search for risk factors for behavioral dysfunction. We investigated the combined influence of two serotonin pathway polymorphisms and species-atypical, and possibly adverse, rearing (nursery rearing [NR]) on two dimensions of behavioral stress response in infant rhesus macaques. We hypothesized that the experience of NR and possession of both "high-risk" genotypes (genotypes that are thought to confer low 5-HT function) would predict the greatest behavioral stress response to maternal/social separation. Using a matched-pair design, the impact of early experience and the serotonin transporter (rh5-HTTLPR) and monoamine oxidase A (rhMAO-A-LPR) promoter polymorphisms on behavioral reactivity of 136 infant rhesus macaques (90-120 days of age) during a 25-hr social separation/relocation procedure was assessed. Each pair included one infant reared with mother in a large, outdoor field enclosure (field rearing) and one infant reared in a nursery (NR). Pairs were matched for putative gene activity of each polymorphism, sex, age, and weight at testing. Behavioral responses in a "human intruder" test were recorded, and activity and emotional reactivity composites were created to detect different aspects of psychological adaptation to stress. Our hypothesis that high-risk groups would be the most reactive to stress was not entirely borne out. Rh5-HTTLPR x rhMAOA-LPR interactions predicted emotional reactivity and tended to predict behavioral activity scores. Carriers of the two "low-risk" alleles exhibited the lowest behavioral activity, as might be predicted, but carriers of both "high-risk" alleles were two of four genotype groups exhibiting the highest observed Emotional Reactivity. Gene x Gene interactions were exacerbated by the experience of nursery rearing, as predicted, however. Finally, we suggest that genetic or environmental factors may mitigate the risk for behavioral dysregulation illustrated in the patterns of behavioral activity and emotional reactivity displayed by infants.

Neonatal amygdala or hippocampus lesions influence responsiveness to objects.

Medial temporal lobe brain structures, such as the amygdala, play an important role in the normal perception and generation of emotional behavior. Little research, however, has assessed the role of such structures across the neurodevelopmental trajectory. We assessed emotional behavioral responses of rhesus macaques that received bilateral ibotenic acid lesions of the amygdala or hippocampus at 2 weeks of age and sham-operated controls. At 9 and 18 months of age, animals interacted with novel objects that varied in visual complexity as a means of varying emotional salience. All animals behaved differently in the presence of visually simple, as compared to complex, objects, suggesting that they were sensitive to variation in emotional salience. Across both experiments, amygdala-lesioned animals appeared to be less behaviorally inhibited insofar as they explored all objects most readily. Interestingly, hippocampus-lesioned animals' propensity for exploration mirrored that of control animals in some contexts but that of amygdala-lesioned animals in other contexts. At 18 months of age, both amygdala-lesioned and hippocampus-lesioned animals were judged to be less fearful than controls during the testing procedure. Implications for understanding the neurobiology of emotional behavior are discussed.

Social stress enhances sympathetic innervation of primate lymph nodes: mechanisms and implications for viral pathogenesis.

Behavioral processes regulate immune system function in part via direct sympathetic innervation of lymphoid organs, but little is known about the factors that regulate the architecture of neural fibers in lymphoid tissues. In the present study, we find that experimentally imposed social stress can enhance the density of catecholaminergic neural fibers within axillary lymph nodes from adult rhesus macaques. This effect is linked to increased transcription of the key sympathetic neurotrophin nerve growth factor and occurs predominately in extrafollicular regions of the paracortex that contain T-lymphocytes and macrophages. Functional consequences of stress-induced increases in innervation density include reduced type I interferon response to viral infection and increased replication of the simian immunodeficiency virus. These data reveal a surprising degree of behaviorally induced plasticity in the structure of lymphoid innervation and define a novel pathway by which social factors can modulate immune response and viral pathogenesis.

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

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.

Personality and serotonin transporter genotype interact with social context to affect immunity and viral set-point in simian immunodeficiency virus disease.

From the beginning of the AIDS epidemic, stress has been a suspected contributor to the wide variation seen in disease progression, and some evidence supports this idea. Not all individuals respond to a stressor in the same way, however, and little is known about the biological mechanisms by which variations in individuals' responses to their environment affect disease-relevant immunologic processes. Using the simian immunodeficiency virus/rhesus macaque model of AIDS, we explored how personality (Sociability) and genotype (serotonin transporter promoter) independently interact with social context (Stable or Unstable social conditions) to influence behavioral expression, plasma cortisol concentrations, SIV-specific IgG, and expression of genes associated with Type I interferon early in infection. SIV viral RNA set-point was strongly and negatively correlated with survival as expected. Set-point was also associated with expression of interferon-stimulated genes, with CXCR3 expression, and with SIV-specific IgG titers. Poorer immune responses, in turn, were associated with display of sustained aggression and submission. Personality and genotype acted independently as well as in interaction with social condition to affect behavioral responses. Together, the data support an "interactionist" perspective [Eysenck, H.J., 1991. Personality, stress and disease: an interactionist perspective. Psychol. Inquiry 2, 221-232] on disease. Given that an important goal of HIV treatment is to maintain viral set-point as low as possible, our data suggest that supplementing anti-retroviral therapy with behavioral or pharmacologic modulation of other aspects of an organism's functioning might prolong survival, particularly among individuals living under conditions of threat or uncertainty.

Neural correlates of pair-bonding in a monogamous primate.

The neurobiology of social bonding, despite its relevance to human mental health, has been studied primarily in rodents. In this study we used position emission tomography (PET), registered with structural magnetic resonance imaging (MRI) to investigate central glucose uptake in 17 males of a monogamous primate species, the titi monkey (Callicebus cupreus). Twelve pair-bonded males (including six with a lesion of the prefrontal cortex) and five lone males were scanned. The five lone males were re-scanned 48 h after pairing with a female. Significant differences in glucose uptake were found between males in long-term pair-bonds and lone males in areas including the nucleus accumbens, ventral pallidum, medial preoptic area, medial amygdala, and the supraoptic nucleus of the hypothalamus. In paired before and after comparisons, males showed significant changes following pairing in the right nucleus accumbens and ventral pallidum but not in other areas. Lesioned males showed significantly higher uptake in the posterior cingulate cortex than all other males. These results indicate some basic similarities between rodents and primates in the formation and maintenance of selective social bonds, but emphasize the importance of studying long-term maintenance in addition to short-term formation of social bonds.

Imaging, Behavior and Endocrine Analysis of "Jealousy" in a Monogamous Primate.

Understanding the neurobiology of social bonding in non-human primates is a critical step in understanding the evolution of monogamy, as well as understanding the neural substrates for emotion and behavior. Coppery titi monkeys (Callicebus cupreus) form strong pair bonds, characterized by selective preference for their pair mate, mate-guarding, physiological and behavioral agitation upon separation, and social buffering. Mate-guarding, or the "maintenance" phase of pair bonding, is relatively under-studied in primates. In the current study, we used functional imaging to examine how male titi monkeys viewing their pair mate in close proximity to a stranger male would change regional cerebral glucose metabolism. We predicted that this situation would challenge the pair bond and induce "jealousy" in the males. Animals were injected with [18F]-fluorodeoxyglucose (FDG), returned to their cage for 30 min of conscious uptake, placed under anesthesia, and then scanned for 1 hour on a microPET P4 scanner. During the FDG uptake, males (n=8) had a view of either their female pair mate next to a stranger male ("jealousy" condition) or a stranger female next to a stranger male (control condition). Blood and cerebrospinal fluid samples were collected and assayed for testosterone, cortisol, oxytocin, and vasopressin. Positron emission tomography (PET) was co-registered with structural magnetic resonance imaging (MRI), and region of interest analysis was carried out. Bayesian multivariate multilevel analyses found that the right lateral septum (Pr(b>0)=93%), left posterior cingulate cortex (Pr(b>0)=99%), and left anterior cingulate (Pr(b>0)=96%) showed higher FDG uptake in the jealousy condition compared to the control condition, while the right medial amygdala (Pr(b>0)=85%) showed lower FDG uptake. Plasma testosterone and cortisol concentrations were higher during the jealousy condition. During the jealousy condition, duration of time spent looking across at the pair mate next to a stranger male was associated with higher plasma cortisol concentrations. The lateral septum has been shown to be involved in mate-guarding and mating-induced aggression in monogamous rodents, while the cingulate cortex has been linked to territoriality. These neural and physiological changes may underpin the emotion of jealousy, which can act in a monogamous species to preserve the long-term integrity of the pair.

Pair bond formation leads to a sustained increase in global cerebral glucose metabolism in monogamous male titi monkeys (Callicebus cupreus).

Social bonds, especially attachment relationships, are crucial to our health and happiness. However, what we know about the neural substrates of these bonds is almost exclusively limited to rodent models and correlational experiments in humans. Here, we used socially monogamous non-human primates, titi monkeys (Callicebus cupreus) to experimentally examine changes in regional and global cerebral glucose metabolism (GCGM) during the formation and maintenance of pair bonds. Baseline positron emission tomography (PET) scans were taken of thirteen unpaired male titi monkeys. Seven males were then experimentally paired with females, scanned and compared, after one week, to six age-matched control males. Five of the six control males were then also paired and scanned after one week. Scans were repeated on all males after four months of pairing. PET scans were coregistered with structural magnetic resonance imaging (MRI), and region of interest (ROI) analysis was carried out. A primary finding was that paired males showed a significant increase in [18F]-fluorodeoxyglucose (FDG) uptake in whole brain following one week of pairing, which is maintained out to four months. Dopaminergic, "motivational" areas and those involved in social behavior showed the greatest change in glucose uptake. In contrast, control areas changed only marginally more than GCGM. These findings confirm the large effects of social bonds on GCGM. They also suggest that more studies should examine how social manipulations affect whole-brain FDG uptake, as opposed to assuming that it does not change across condition.

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.

Challenges to the Pair Bond: Neural and Hormonal Effects of Separation and Reunion in a Monogamous Primate.

Social monogamy at its most basic is a group structure in which two adults form a unit and share a territory. However, many socially monogamous pairs display attachment relationships known as pair bonds, in which there is a mutual preference for the partner and distress upon separation. The neural and hormonal basis of this response to separation from the adult pair mate is under-studied. In this project, we examined this response in male titi monkeys (Callicebus cupreus), a socially monogamous New World primate. Males underwent a baseline scan, a short separation (48 h), a long separation (approximately 2 weeks), a reunion with the female pair mate and an encounter with a female stranger (with nine males completing all five conditions). Regional cerebral glucose metabolism was measured via positron emission tomography (PET) imaging using [18F]-fluorodeoxyglucose (FDG) co-registered with structural magnetic resonance imaging (MRI), and region of interest (ROI) analysis was carried out. In addition, plasma was collected and assayed for cortisol, oxytocin (OT), vasopressin (AVP), glucose and insulin concentrations. Cerebrospinal fluid (CSF) was collected and assayed for OT and AVP. We used generalized estimating equations (GEE) to examine significant changes from baseline. Short separations were characterized by decreases in FDG uptake, in comparison to baseline, in the lateral septum (LS), ventral pallidum (VP), paraventricular nucleus of the hypothalamus (PVN), periaqueductal gray (PAG), and cerebellum, as well as increases in CSF OT, and plasma cortisol and insulin. Long separations differed from baseline in reduced FDG uptake in the central amygdala (CeA), reduced whole brain FDG uptake, increased CSF OT and increased plasma insulin. The response on encounter with a stranger female depended on whether or not the male had previously reproduced with his pair mate, suggesting that transitions to fatherhood contribute to the neurobiology underlying response to a novel female. Reunion with the partner appeared to stimulate coordinated release of central and peripheral OT. The observed changes suggest the involvement of OT and AVP systems, as well as limbic and striatal areas, during separation and reunion from the pair mate.

The amygdala: is it an essential component of the neural network for social cognition?

Observations from human subjects with focal brain lesions and animal subjects with experimental lesions have implicated a variety of brain regions in the mediation of social behavior. Previous studies carried out in the macaque monkey found that lesions of the amygdala not only decrease emotional reactivity but also disrupt normal social interactions. We have re-investigated the relationship between amygdala lesions and social behavior in cohorts of mature and neonatal rhesus monkeys who were prepared with selective and complete bilateral ibotenic acid lesions of the amygdaloid complex. These animals display clear alterations in emotional and social behavior. We interpret these changes as due to a loss of the ability to evaluate environmental stimuli as potential threats. However, adult animals with bilateral lesions of the amygdala demonstrate normal, and even increased, social interactions with conspecifics. Moreover, neonatal animals, prepared with amygdala lesions at 2 weeks of age, also demonstrate species typical social behaviors such as the generation of facial expressions, grooming and play behavior. These results argue against the idea that the amygdala is essential for the interpretation of social communication or for the expression of social behavior. Because it does appear to participate in the evaluation of the "safety" of social interactions, we believe that it does have a role in modulating the amount of social behavior in which an organism will participate. However, our current answer to the question posed in the title of this paper is no!

The amygdala: is it an essential component of the neural network for social cognition?

Observations from human subjects with focal brain lesions and animal subjects with experimental lesions have implicated a variety of brain regions in the mediation of social behavior. Previous studies carried out in the macaque monkey found that lesions of the amygdala not only decrease emotional reactivity but also disrupt normal social interactions. We have re-investigated the relationship between amygdala lesions and social behavior in cohorts of mature and neonatal rhesus monkeys who were prepared with selective and complete bilateral ibotenic acid lesions of the amygdaloid complex. These animals display clear alterations in emotional and social behavior. We interpret these changes as due to a loss of the ability to evaluate environmental stimuli as potential threats. However, adult animals with bilateral lesions of the amygdala demonstrate near normal, and even increased, social interactions with conspecifics. Moreover, neonatal animals, prepared with amygdala lesions at 2 weeks of age, also demonstrate species typical social behaviors such as the generation of facial expressions, grooming and play behavior. These results argue against the idea that the amygdala is essential for the interpretation of social communication or for the expression of social behavior. Because it does appear to participate in the evaluation of the "safety" of social interactions, we believe that it does have a role in modulating the amount of social behavior in which an organism will participate. However, our current answer to the question posed in the title of this paper is no!

Premises, promises, and problems of primatology.

The premises and promises of primatology stem from its focus on a unique biological group whose members are related by evolutionary descent, and from its commitment to discover all there is to know about these animals. The essential multidisciplinary character of primatology is implicit in this commitment. Evolutionary theory provides the field of primatology with its reason for being and its intellecutal coherence, and is the basis for transforming a diversity of potentially disparate and autonomous disciplines into a mutually reinforcing array of interdependent components within a common enterprise. A powerful adjunct to evolutionary theory is the comparative perspective. The distinguishing characteristic of this perspective is its concern with similarities and differences among primate species at all levels of structure and function. It aims to establish shared traits, to distinguish between homologous processes and convergent effects, to identify trends and specializations, and to understand the historical antecedents of living species. Some of the problems that primatology faces can be traced to its multidisciplinary character. The vitality of primatology depends on the continuing infusion of new methods, new findings, and new ideas. This requires an active process of interdisciplinary communication and mutual education. It is also essential to promote basic research on all aspects of primate biology and to affirm the singular importance of the nonhuman primates as a resource for understanding the natural world and the principles that govern its workings. Conservation is the most formidable and intractable problem confronted by modern primatology. Primate conservation is part of the larger problem of preserving biological diversity in the face of accelerating destruction of natural ecosystems. Primatology has made important contributions to conservation and will continue to do so. The scope and complexity of the problem, however, require the cooperative efforts of many different interest groups.

Differentiall behavioral and adrenocortical responses to stress among three macaque species.

Behavioral and adrenocortical responses of rhesus (Macaca mulatta), bonnet (M. radiata), and crabeating (M. fascicularis) macaques were compared in their home cages, during exposure to novelty and during physical restraint. Both behavioral and adrenocortical responses differentiated species in each condition. In all conditions, post-test corticosteroid levels were highest for crabeaters and lowest for rhesus. Rhesus were the most active behaviorally, and bonnets were the most passive, while crabeaters exhibited the greatest signs of behavioral disturbance. Relationships between adrenocortical and behavioral responses varied between groups. Both adrenocortical and behavioral profiles were in accord with the behavior of these three species under more natural conditions. The role of psychophysiological responses in general behavioral dispositions toward the environment is discussed. It is concluded that behavioral dispositions, inclusive of psychophysiological responses, may vary qualitatively even among closely related primate species.

Psychosocial and hormonal aspects of hierarchy formation in groups of male squirrel monkeys.

Accounts of primate social dominance hierarchies often imply that the achievement of superior status is a "goal", akin to a valued resource or commodity, and that hierarchies emerge in multimale groups from prolonged competitive conflicts over social status. This possibility is not consistent with our observations of five newly formed triads of adult male squirrel monkeys (Saimiri sciureus). Stable linear hierarchies based on clear asymmetries in the direction of intermale agonism and genital displays were established quickly, with virtually no reciprocal fighting, and in the absence of rank-related differences in plasma cortisol or testosterone. Although affiliative social overtures were initiated more often by high-ranking and middle-ranking males, affiliative overtures were directed equally often toward all members of each group. From the outset of the study all males, regardless of rank, spent an average of 33% of their time huddling in affiliative contact with male cagemates. These results suggest that in newly formed groups of adult male squirrel monkeys, social hierarchies reflect an expedient convention that reduces conflict and facilitates the formation of small cohesive groups. © 1994 Wiley-Liss, Inc.

Heart rate patterns under stress in three species of macaques.

Cardiac responses during one hour exposures to three stressful experimental conditions were compared among juvenile females of three species of the genus Macaca (M. mulatta, M. radiata, and M. fascicularis). M. fascicularis showed the highest overall heart rate, and M. mulatta the lowest, in all three conditions. The principal difference between species was in the pattern of change in heart rate over the test sessions. Heart rate declined during the hour for all three species in the first two conditions (home cage novel environment), and the change was most rapid in M. mulatta and slowest in M. fascicularis. In the third and most stressful condition (physical restraint), each species showed a distinct temporal pattern. Heart rate increased over the hour in M. fascicularis, declined in M. radiata, and increased rapidly then declined gradually in M. mulatta. Individual differences in heart rate tended to be consistent within and across conditions. Correlations between behavioral measures of somatic activity and heart rate were generally modest. The results are in accord with other behavioral and physiological differences obtained for the same subjects, and suggest that responses to environmental stimuli reflect fundamental aspects of temperament that may vary substantially even among closely related species. © 1994 Wiley-Liss, Inc.

Arthur J. Riopelle (1920-2012).

Presents an obituary for Arthur (Art) J. Riopelle. After graduating from the University of Wisconsin in 1942, Art joined the U.S. Army. He returned to the university after the war as a graduate student in psychology and earned a doctorate in experimental psychology under the supervision of Dave Grant and Fred Mote. In 1950, Art completed his degree and moved to the Psychology Department of Emory University in Georgia. This was the beginning of an unusual and eventful career. At Emory, Art worked with Harlow W. Ades, but when Ades eventually left, Art established a small colony of monkeys to pursue his own projects. Art moved from Emory to Fort Knox, Kentucky, in 1957 to become director of the Psychology Division of the U.S. Army Medical Laboratories. He continued to be involved with primates, including on a well-publicized project that entailed launching monkeys into space. In 1959, Art left Fort Knox to become the new director of what was then known as the Yerkes Laboratories of Primate Biology. Art played an important part in the history of regional primate research centers, which have benefited the nation in numerous ways. He had many admirable qualities. He was a tolerant, supportive, fair-minded, and principled administrator, a careful and dedicated scientist, and a steadfast friend who loved a good joke.