Expression of bond-related behaviors affects titi monkey responsiveness to oxytocin and vasopressin treatments.

Social bonds influence physiology and behavior, which can shape how individuals respond to physical and affective challenges. Coppery titi monkey (Plecturocebus cupreus) offspring form selective bonds with their fathers, making them ideal for investigating how father-daughter bonds influence juveniles' responses to oxytocin (OT) and arginine-vasopressin (AVP) manipulations. We quantified the expression of father-daughter bond-related behaviors in females (n = 10) and gave acute intranasal treatments of saline, low/medium/high OT, low/high AVP, or an OT receptor antagonist (OTA) to subjects prior to a parent preference test. While females spent more time in proximity to their parents than strangers, we found a large degree of individual variation. Females with greater expression of bonding behaviors responded to OT treatments in a dose-dependent manner. Subjects also spent less time in proximity to strangers when treated with High OT (p = 0.003) and Low OT (p = 0.007), but more time when treated with High AVP (p = 0.007), Low AVP (p = 0.009), and OTA (p = 0.001). Findings from the present study suggest that variation in the expression of bond-related behaviors may alter responsiveness to OT and AVP, increasing engagement with unfamiliar social others. This enhanced sociality with strangers may promote the formation of pair bonds with partners.

The amygdala is not necessary for the familiarity aspect of recognition memory.

Dual-process accounts of item recognition posit two memory processes: slow but detailed recollection, and quick but vague familiarity. It has been proposed, based on prior rodent work, that the amygdala is critical for the familiarity aspect of item recognition. Here, we evaluated this proposal in male rhesus monkeys (Macaca mulatta) with selective bilateral excitotoxic amygdala damage. We used four established visual memory tests designed to assess different aspects of familiarity, all administered on touchscreen computers. Specifically, we assessed monkeys' tendencies to make low-latency false alarms, to make false alarms to recently seen lures, to produce curvilinear ROC curves, and to discriminate stimuli based on repetition across days. Three of the four tests showed no familiarity impairment and the fourth was explained by a deficit in reward processing. Consistent with this, amygdala damage did produce an anticipated deficit in reward processing in a three-arm-bandit gambling task, verifying the effectiveness of the lesions. Together, these results contradict prior rodent work and suggest that the amygdala is not critical for the familiarity aspect of item recognition.

Physiological and behavioral effects of hormonal contraceptive treatment in captive, pair-bonded primates (Plecturocebus cupreus).

Hormonal contraception is an effective, reversible tool for managing birth rates in humans and nonhuman animals alike. However, manipulating reproductive hormones has behavioral consequences that can impact social and sexual behavior between conspecifics. First, we studied 18 pairs of nonreproductive titi monkeys (Plecturocebus cupreus) to test the efficacy of a novel method of hormonal contraception (deslorelin acetate implants) on reproductive hormone cycling in females and found significant reductions in urinary estrogens and progestagens among treated females compared to untreated controls. We then studied 35 nonreproductive pairs of coppery titi monkeys (Plecturocebus cupreus) to ascertain whether treating females with one of 2 different forms of hormonal contraception (deslorelin acetate implants (n = 17) or medroxyprogesterone acetate injections (n = 9)) would influence the relationship between pair mates compared to the relationship between untreated females and their vasectomized male mates (n = 9). Over a 5-month period, we found no differences in affiliative behaviors between pairs containing untreated females compared to pairs in which the female was treated with either deslorelin acetate or medroxyprogesterone acetate. Similarly, we found no differences in affiliation between pairs in the 2 treatment groups. This study is the first to examine behavioral consequences of hormonal contraception in a pair-bonding species. The results are encouraging for captive, managed breeding colonies of such social animals, especially those used in behavioral research.

Intranasal oxytocin does not change partner preference in female titi monkeys (Plecturocebus cupreus), but intranasal vasopressin decreases it.

Strong social bonds are critical to human health; however, the mechanisms by which social bonds are formed and maintained are still being elucidated. The neurohormones oxytocin (OT) and vasopressin (AVP) are considered likely candidates. Primate females, both human and nonhuman, remain understudied populations. Here, we conducted a pharmacological study coupled with a behavioral partner preference test (PPT) to better understand the mechanistic basis of attachment in adult female titi monkeys (Plecturocebus cupreus). This pair-bonding species shares a conserved form of oxytocin with humans and is an excellent model organism to study the neural basis of social bonding. We performed intranasal administration of three doses of oxytocin (IN-OT), two doses of vasopressin (IN-AVP), one dose of an oxytocin antagonist (IN-OTA) and one dose of a saline treatment. We found that compared to the saline control, the IN-AVP treatment (lower dose, 40 IU/kg) decreased the time spent in proximity to the partner and increased lip-smacking toward the stranger. We found no effects of IN-OT or IN-OTA manipulation on partner preference. In contrast, low-dose IN-AVP weakened the partner preference in female titi monkeys.

Titi monkey father-daughter bond-related behaviors explain stress response variability.

Social interactions regulate our behavior and physiology, and strong social bonds can buffer us from stress. Coppery titi monkeys (Plecturocebus cupreus) are socially monogamous South American monkeys that display strong social bonds. Infants form selective bonds with their fathers, making them ideal for studying father-daughter bonds. We established a method for quantifying variability in expression of bond-related behaviors in females (n = 12), and the present study is the second to use this method for explaining titi monkey responses to behavioral tests. We also investigated how manipulations of oxytocin (OT) and vasopressin (AVP) influenced juvenile behavior and physiology. Subjects received acute intranasal treatments of saline, low/medium/high OT, low/high AVP, or OT receptor antagonist (OTA) prior to an acute social separation. General linear mixed-effects model results revealed fathers were significant behavioral and physiological stress buffers for their daughters, as evidenced by fewer distress vocalizations (p < 0.001), less locomotion (p < 0.001), and lower plasma cortisol (p < 0.001) in a social separation paradigm. Females vocalized less if they exhibited greater expression of bond-related behaviors with their fathers as infants (p = 0.01), and this stress-buffering effect remained even when the daughter was separated from the father (p = 0.001). While treatments did not alter behaviors, OTA treatment caused the largest rise in plasma cortisol (p < 0.001), suggesting blockade of OT receptors can inhibit fathers' stress-buffering effects. Remarkably, females with greater expression of father-daughter bond-related behaviors exhibited an overall reduced physiological separation distress response (p = 0.04). Findings from the present study advance current knowledge of the neurobiological mechanisms foundational to female bonds and help inform how social disruptions may differently impact individuals based on expression of bond-related behaviors.

Survival rates and mortality risks of Plecturocebus cupreus at the California National Primate Research Center.

This article describes survivorship and explores factors affecting mortality risks in a captive colony of coppery titi monkeys (Plecturocebus cupreus) housed at the California National Primate Research Center (CNPRC), at UC Davis, in Davis, CA. We analyzed data collected on individuals since the colony's creation in the 1960s, with a sample of 600 animals with partially complete information (date of birth, age at death, body mass, parental lineage). We used three methods: (1) Kaplan-Meier regressions followed by a log-rank test to compare survival in male and female titi monkeys, (2) a breakpoint analysis to identify shifts in the survival curves, and (3) Cox regressions to test the effect of body mass change, parental pair tenure, and parental age on mortality risk. We found that males tend to have a longer median lifespan than females (14.9 and 11.4 years; p = 0.094) and that survival decreases earlier in males than in females during adulthood (9.8 and 16.2 years). A body mass loss of 10% from adulthood to the time of death led to a 26% higher risk of dying (p < 0.001) as compared to an individual with stable body mass. We found no evidence of sociobiological factors on mortality risks (parental age, parental pair tenure), but an exploratory analysis suggested that a higher rate of offspring conceptions increases mortality risks. This description of factors influencing survival and mortality in titi monkeys is a first step toward understanding aging in this species to consider titi monkeys as a primate model for socioemotional aging.

Parental experience is linked with lower vasopressin receptor 1a binding and decreased postpartum androgens in titi monkeys.

Parenting induces many neurological and behavioral changes that enable parents to rear offspring. Vasopressin plays an important role in this process via its effects on cognition, affect, and neuroplasticity, and in some cases, via interactions with decreased parental androgens. Thus far, the role of these hormones has been primarily studied in rodents. To address this gap, we explored vasopressin receptors and androgens in titi monkeys, a pair-bonding and biparental primate species. In Studies 1 and 2, we used receptor autoradiography to correlate arginine vasopressin receptor 1a (AVPR1a) binding in the hippocampus (Study 1, n = 10) and the rest of the forebrain (Study 2, n = 23) with parental status, parental experience, parity, infant carrying, and pair affiliation. We found that parents exhibited lower AVPR1a binding than non-parents throughout most brain regions assessed, with especially strong effects in the hippocampus (ß = -.61), superior colliculus (ß = -.88), lateral septum (ß = -.35), and medial preoptic area (ß = -.29). The other measures of parental experience also tended to be negatively associated with AVPR1a binding across different brain regions. In Study 3 (n = 44), we compared pre- and postpartum urinary androgen levels in parents and non-parents and found that mothers exhibited a sustained androgen decrease across 3-4 months postpartum (relative to 3 months prepartum; ß ranged from -.72 to -.62 for different comparisons). For males, we found that multiparous fathers exhibited decreased androgen levels at 1-2 weeks postpartum (ß = -.25) and at 3-4 months postpartum (ß = -.40) compared to the prepartum, indicating both immediate and long-term reductions with subsequent paternal experience. Together, the results of this study suggest that decreases in AVPR1a binding and circulating androgens are associated with parental behavior and physiology in titi monkeys.

Parenting costs time: Changes in pair bond maintenance across pregnancy and infant rearing in a monogamous primate (Plecturocebus cupreus).

Relationships support social animals' health, but maintaining relationships is challenging. When transitioning to parenthood, new parents balance pair-bond maintenance with infant care. We studied pair-bond maintenance via affiliation in 22 adult titi monkey pairs (Plecturocebus cupreus) for 16 months centered around their first offspring's birth. Pair affiliation peaked during pregnancy, decreased across the postpartum period, and rose after reaching minimum affiliation 32.6 weeks postpartum. Pairs in which fathers carry infants more than average had lower affiliation at the infant's birth and return to an increase in affiliation sooner. Parents of infants who were slow to independence had higher rates of affiliation. Titi monkey infants actively prefer their fathers; mothers may avoid their infant-carrying mate, suggesting infants play an active role in parental affiliative decline. Our data supports previous findings that affiliation between partners declines following an infant's birth, but demonstrates new knowledge about the extent and duration of affiliative decline.

What is a pair bond?

Pair bonding is a psychological construct that we attempt to operationalize via behavioral and physiological measurements. Yet, pair bonding has been both defined differently in various taxonomic groups as well as used loosely to describe not just a psychological and affective phenomenon, but also a social structure or mating system (either social monogamy or just pair living). In this review, we ask the questions: What has been the historical definition of a pair bond? Has this definition differed across taxonomic groups? What behavioral evidence do we see of pair bonding in these groups? Does this observed evidence alter the definition of pair bonding? Does the observed neurobiology underlying these behaviors affect this definition as well? And finally, what are the upcoming directions in which the study of pair bonding needs to head?

Autonomic arousal tracks outcome salience not valence in monkeys making social decisions.

The evolutionary and neural underpinnings of human prosociality are still being identified. A growing body of evidence suggests that some species find the sight of another individual receiving a reward reinforcing, called vicarious reinforcement, and that this capacity is supported by a network of brain areas including the anterior cingulate cortex (ACC) and the amygdala. At the same time, analyses of autonomic arousal have been increasingly used to contextualize and guide neural research, especially for studies of reward processing. Here, we characterized the autonomic pupil response of eight monkeys across two laboratories in two different versions of a vicarious reinforcement paradigm. Monkeys were cued as to whether an upcoming reward would be delivered to them, another monkey, or nobody and could accept or decline the offer. As expected, all monkeys in both laboratories showed a marked preference for juice to the self, together with a reliable prosocial preference for juice to a social partner compared to juice to nobody. However, contrary to our expectations, we found that pupils were widest in anticipation of juice to the self, moderately sized in anticipation of juice to nobody, and narrowest in anticipation of juice to a social partner. This effect was seen across both laboratories and regardless of specific task parameters. The seemingly paradoxical pupil effect can be explained by a model in which pupil size tracks outcome salience, prosocial tendencies track outcome valence, and the relation between salience and valence is U-shaped. (PsycInfo Database Record (c) 2021 APA, all rights reserved).

The anterior cingulate cortex is necessary for forming prosocial preferences from vicarious reinforcement in monkeys.

A key feature of most social relationships is that we like seeing good things happen to others. Research has implicated the anterior cingulate cortex (ACC) in attaching value to social outcomes. For example, single neurons in macaque ACC selectively code reward delivery to the self, a partner, both monkeys, or neither monkey. Here, we assessed whether the ACC's contribution to social cognition is causal by testing rhesus monkeys (Macaca mulatta) on a vicarious reinforcement task before and after they sustained ACC lesions. Prior to surgery, actors learned that 3 different visual cues mapped onto 3 distinct reward outcomes: to self ("Self"), to the other monkey ("Other"), or to neither monkey ("Neither"). On each trial, actors saw a cue that predicted one of the 3 juice offers and could accept the offer by making a saccade to a peripheral target or reject the offer by breaking fixation. Preoperatively, all 6 actors displayed prosocial preferences, indicated by their greater tendency to give reward to Other relative to Neither. Half then received selective, bilateral, excitotoxic lesions of the ACC, and the other half served as unoperated controls. After surgery, all monkeys retained the social preferences they had demonstrated with the preoperatively learned cues, but this preference was reduced in the monkeys with ACC lesions. Critically, none of the monkeys in the ACC lesion group acquired social preferences with a new set of cues introduced after surgery. These data indicate that the primate ACC is necessary for acquisition of prosocial preferences from vicarious reinforcement.

MRI Overestimates Excitotoxic Amygdala Lesion Damage in Rhesus Monkeys.

Selective, fiber-sparing excitotoxic lesions are a state-of-the-art tool for determining the causal contributions of different brain areas to behavior. For nonhuman primates especially, it is advantageous to keep subjects with high-quality lesions alive and contributing to science for many years. However, this requires the ability to estimate lesion extent accurately. Previous research has shown that in vivo T2-weighted magnetic resonance imaging (MRI) accurately estimates damage following selective ibotenic acid lesions of the hippocampus. Here, we show that the same does not apply to lesions of the amygdala. Across 19 hemispheres from 13 rhesus monkeys, MRI assessment consistently overestimated amygdala damage as assessed by microscopic examination of Nissl-stained histological material. Two outliers suggested a linear relation for lower damage levels, and values of unintended amygdala damage from a previous study fell directly on that regression line, demonstrating that T2 hypersignal accurately predicts damage levels below 50%. For unintended damage, MRI estimates correlated with histological assessment for entorhinal cortex, perirhinal cortex and hippocampus, though MRI significantly overestimated the extent of that damage in all structures. Nevertheless, ibotenic acid injections routinely produced extensive intentional amygdala damage with minimal unintended damage to surrounding structures, validating the general success of the technique. The field will benefit from more research into in vivo lesion assessment techniques, and additional evaluation of the accuracy of MRI assessment in different brain areas. For now, in vivo MRI assessment of ibotenic acid lesions of the amygdala can be used to confirm successful injections, but MRI estimates of lesion extent should be interpreted with caution.