Cognitive development from infancy to young adulthood in common marmosets (Callithrix jacchus): Effect of age, sex, and hormones on learning and affective state.

Studies looking at individual variability in cognition have increased in recent years. We followed 43 marmosets (21 males, 22 females) from infancy to young adulthood. At 3-months old, marmosets were trained to touch a rewarded stimulus. At 9-, 15-, and 21-months old, they were given visual discrimination and cognitive bias tests, and urine samples were collected to examine hormone levels. Marmosets were significantly more successful learners at 15 months than 9 months. Individuals who were more successful learners at 9 months were also more successful at 15 months, with more male learners than expected at 15 months. At 9 months, learning success was associated with higher cortisol levels. At 15 months, males with higher estradiol levels were more successful learners, whereas at 21 months, females with higher estradiol and cortisol levels tended to be less successful learners and more pessimistic. Nine months, therefore, appears to be an important developmental timepoint for acquiring cognitive control, which has developed by 15 months. Steroids may have differential effects on each sex, with complex interactions between gonadal and adrenal hormones having an influence on cognitive function over the lifespan. This longitudinal study offers new insight into cognition, including its development and biological underpinnings.

Motivational increase of androgens and behavior by infant distress calls in highly responsive common marmoset fathers, Callithrix jacchus.

Common marmoset fathers are highly involved in care of their infants. However, variability exists in their response to infant behavior even in paternally experienced fathers. Using infant distress cries as a motivation test, we investigated: 1. the differences in paternally experienced fathers' motivation to search for the infant vocalization stimuli; 2. the relationship between a father's motivation to search for the source of the infant cries and testosterone levels; and 3. if there is a rapid steroidogenesis pathway leading to increased testosterone and estradiol in the peripheral circulation. Only 44% of the paternally experienced fathers showed a high frequency of searching for the source of the infant distress cries. Through the use of multisteroid analysis, we found high responsive fathers had significantly higher levels of progesterone and testosterone in response to infant distress cries compared to a control stimulus with progesterone and androstenedione correlating with testosterone, while no differences were seen in low responders. The frequency to search for the infant stimuli was positively correlated with higher testosterone compared to control vocal levels. These results suggest that searching for the source of infant cries represents a motivation behavior for fathers that is activated by testosterone and reflects rapid circulating testosterone.

Early learning in the common marmoset (Callithrix jacchus): Behavior in the family group is related to preadolescent cognitive performance.

Early environment can have a major impact on development, with family life known to play an important role. Longitudinal studies can therefore help increase our understanding of variance in cognitive abilities in young animals, as well as over time. We followed 22 marmosets (11 male and 11 female) from infancy through to early adolescence. At 3 months old, the marmosets were trained to reliably touch a rewarded stimulus. At 5 months, behavior was observed within the natal group. At 9 months, the marmosets were given a visual discrimination task to assess learning ability. Mann-Whitney U tests found no sex or family size differences in number of errors at 3 or 9 months. While no significant relationships were found between behavior in the family and learning at 3 months, significant negative correlations were found between duration spent in locomotion and learning errors (p = .05), as well as between frequency of calm vocalizations and learning errors (p = .001) at 9 months. A U-shape curve was found between amount of social play and learning at 9 months. Positive family interactions, including moderate amounts of play, as well as calm individual behavior, may therefore be important in learning. This study sheds light on cognitive development in much younger marmosets than previously studied, and helps increase understanding of how individual differences in learning may arise.

The long-term impact of infant rearing background on the affective state of adult common marmosets (Callithrix jacchus).

Early life environment, including temporary family separation, can have a major influence on affective state. Using a battery of tests, the current study compared the performance of adult common marmosets (Callithrix jacchus), reared as infants under 3 different conditions: family-reared twins, family-reared animals from triplet litters where only 2 remain (2stays) and supplementary fed triplets. No significant differences were found in latency to approach and obtain food from a human or a novel object between rearing conditions, suggesting no effect on neophobia. There were no differences in cognitive bias task acquisition time, or proportion of responses to each ambiguous probe. Very minor differences were found in response to the probes, with only supplementary fed marmosets making fewer responses to the middle probe, compared to the probe nearest the rewarded stimuli. Similarly, in a test for anhedonia, no difference was found between rearing conditions in consumption of milkshake at different concentrations. There was just one very small difference in reward motivation, with only supplementary fed triplets demonstrating a lack of preference for milkshake over water at the lowest concentration. This consistent pattern of results suggests that the supplementary feeding of large litters of marmosets at this facility did not have a major effect on welfare, and is unlikely to influence performance in reward-related scientific tasks. Therefore, while family separation is not recommended, this particular practice should be used if it is necessary, such as to reduce infant mortality. Regular positive interactions with humans are also encouraged, to reduce fear and improve welfare of marmosets kept in captivity.

Long-term data on reproductive output and longevity in captive female common marmosets (Callithrix jacchus).

The common marmoset (Callithrix jacchus) is widely used in biomedical research, with many housed for breeding purposes world-wide. Significant variation in reproductive output among females has been found compared to other anthropoid primates. The present study explores this reproductive variation, focusing on potential predictors of dam longevity and litter size, as well as changes over time. Back-record analysis was conducted, yielding litter information and reproductive summaries of 360 dams housed at three UK marmoset colonies over four decades (1970s-2000s). Results revealed differences among the colonies, as well as within colonies over decades, suggesting environment may play an important role. Cox proportional hazards regression analyses revealed significant effects of mean litter size and yearly production on dam longevity. Decade, mean inter-birth interval and mean dam weight were found to be significant factors explaining dam longevity when looking at colonies individually. The most commonly recorded cause of death was "poor condition." Linear regression models found that no reproductive variable was useful in explaining mean litter size, except dam weight at conception, data which was only consistently recorded at one colony. While triplets were common at all three colonies, these larger litters were consistently associated with higher infant mortality, despite human intervention to improve survival. This study increases our understanding of marmoset reproduction, and possible improvements to practical aspects of colony management to enhance survival and welfare are discussed.

Linking personality traits and reproductive success in common marmoset (Callithrix jacchus).

Animal personality can affect individual fitness and population growth. Personality traits of either parent or parents' combination may facilitate reproduction and offspring survival across species. However, previous studies focused mainly on the role of only one sex, and the link between personality and fitness has not been confirmed in primates. We examined this link in both sexes of captive common marmosets (Callithrix jacchus), a cooperatively breeding primate with extensive paternal care. We studied the effects of five personality traits of the parents (Agreeableness, Assertiveness, Conscientiousness, Inquisitiveness, and Patience), including their absolute and directional differences within pairs, on key components of reproductive performance. We expected pairs with more similar personality scores to have higher reproductive success as found in other species with long-term pairs and biparental care, but found no evidence for this hypothesis. Instead, we detected strong effects of female traits on inter-birth intervals, which were shorter in more agreeable females, and fecundity rates, which were higher in more inquisitive females. Male traits appeared to have only a limited effect on reproductive success of the pair. Our study demonstrates that various aspects of animal personality underpin reproductive performance in captive common marmosets and provides novel insights into the possible ultimate causes of personality in cooperatively breeding species.

Structural and functional variations in the prefrontal cortex are associated with learning in pre-adolescent common marmosets (Callithrix jacchus).

There is substantial evidence linking the prefrontal cortex (PFC) to a variety of cognitive abilities, with adolescence being a critical period in its development. In the current study, we investigated the neural basis of differences in learning in pre-adolescent common marmosets. At 8 months old, marmosets were given anatomical and resting state MRI scans (n = 24). At 9 months old, association learning and inhibitory control was tested using a 'go/no go' visual discrimination (VD) task. Marmosets were grouped into 'learners' (n = 12) and "non-learners" (n = 12), and associations between cognitive performance and sub-regional PFC volumes, as well as PFC connectivity patterns, were investigated. "Learners" had significantly (p < 0.05) larger volumes of areas 11, 25, 47 and 32 than 'non-learners', although 'non-learners' had significantly larger volumes of areas 24a and 8 v than "learners". There was also a significant correlation between average % correct responses to the 'punished' stimulus and volume of area 47. Further, 'non-learners' had significantly greater global PFC connections, as well as significantly greater numbers of connections between the PFC and basal ganglia, cerebellum and hippocampus, compared to 'learners'. These results suggest that larger sub-regions of the orbitofrontal cortex and ventromedial PFC, as well more refined PFC connectivity patterns to other brain regions associated with learning, may be important in successful response inhibition. This study therefore offers new information on the neurodevelopment of individual differences in cognition during pre-adolescence in non-human primates.

Novel imaging technology and procedures for studying brain function in preadolescent awake marmosets.

BACKGROUND: Novel imaging technology and procedures were developed to study brain function in preadolescent awake marmosets never exposed to anesthesia. METHODS: A radiofrequency transmit and receive, head only volume coil was designed and integrated into a holding system. An acclimation procedure was developed without the use of anesthesia or sedation that allowed for awake imaging. Preadolescent 8-month old male and female marmosets were imaged for resting state BOLD functional connectivity to assess the status of the default mode network. Levels of reactivity during acclimation sessions and behavioral stress following imaging were assessed. RESULTS: Data on functional coupling in the default mode network suggest the organization of connectivity to the prefrontal cortex is not fully developed at 8 months of age. The stress associated with the imaging procedure is comparable to that observed when marmosets are removed from their home cage and temporarily isolated from the family. COMPARISON TO OTHER METHODS: The design of the radiofrequency coil provides B1 homogeneity across the entire brain without signal drop off. The unique design of the head cradle obviates the need for any stabilizing surgery, ear bars or bite bar and could be adapted to any size marmoset. The acclimation requires no anesthesia or sedation at any time in the early life of the developing marmoset, a condition that better reflects the human experience. CONCLUSION: A method is provided for imaging functional activity in the brain of fully awake preadolescent marmosets without any history of anesthesia or sedation.

Measuring physiological stress in the common marmoset (Callithrix jacchus): Validation of a salivary cortisol collection and assay technique.

Cortisol levels are often used as a physiological measure of the stress response in captive primates, with non-invasive measures of this being an important step in welfare assessment. We report a method of collecting saliva samples voluntarily from unrestrained captive common marmosets (Callithrix jacchus), and validate an enzyme-linked immunosorbent assay (ELISA) technique previously unused in this species. Saliva samples were collected from marmosets housed in pairs in a UK laboratory. The assay showed parallelism, precision, accuracy and sensitivity, meeting the criteria typically used to investigate the effectiveness of new analytical techniques. Use of Salimetrics® Oral Swabs considerably increased the amount of cortisol recovered in comparison with previous studies using cotton buds. However, while use of banana on the swabs can encourage chewing, it may influence results. Although increases in cortisol levels have traditionally been interpreted as an indicator of stress in primates, there are many factors that affect the hypothalamic-pituitary-adrenal axis, with some studies showing decreases in cortisol levels post-stressor. Following a likely stressful event (capture for weighing), we also found cortisol levels significantly decreased, possibly due to social buffering or 'blunting' of the HPA axis. Order of weighing also had an effect. The method therefore provided an effective non-invasive means of assessing acute changes in cortisol level that may be more useful than previous methods, improving our ability to study physiological aspects of welfare in primates. We discuss methodological considerations, as well as implications of using cortisol as a measure of stress.

Common marmoset (Callithrix jacchus) personality.

Increasing evidence suggests that personality structure differs between species, but the evolutionary reasons for this variation are not fully understood. We built on earlier research on New World monkeys to further elucidate the evolution of personality structure in primates. We therefore examined personality in 100 family-reared adult common marmosets (Callithrix jacchus) from 3 colonies on a 60-item questionnaire. Principal components analyses revealed 5 domains that were largely similar to those found in a previous study on captive, ex-pet, or formerly laboratory-housed marmosets that were housed in a sanctuary. The interrater reliabilities of domain scores were consistent with the interrater reliabilities of domain scores found in other species, including humans. Four domainsdmdash;conscientiousness, agreeableness, inquisitiveness, and assertiveness-resembled personality domains identified in other nonhuman primates. The remaining domain, patience, was specific to common marmosets. We used linear models to test for sex and age differences in the personality domains. Males were lower than females in patience, and this difference was smaller in older marmosets. Older marmosets were lower in inquisitiveness. Finally, older males and younger females had higher scores in agreeableness than younger males and older females. These findings suggest that cooperative breeding may have promoted the evolution of social cognition and influenced the structure of marmoset prosocial personality characteristics. (PsycINFO Database Record