Early Predictors of Impaired Social Functioning in Male Rhesus Macaques (Macaca mulatta)

Abstract

Autism spectrum disorder (ASD) is characterized by social cognition impairments but its basic disease mechanisms remain poorly understood. Progress has been impeded by the absence of animal models that manifest behavioral phenotypes relevant to ASD. Rhesus monkeys are an ideal model organism to address this barrier to progress. Like humans, rhesus monkeys are highly social, possess complex social cognition abilities, and exhibit pronounced individual differences in social functioning. Moreover, we have previously shown that Low-Social (LS) vs. High-Social (HS) adult male monkeys exhibit lower social motivation and poorer social skills. It is not known, however, when these social deficits first emerge. The goals of this study were to test whether juvenile LS and HS monkeys differed as infants in their ability to process social information, and whether infant social abilities predicted later social classification (i.e., LS vs. HS), in order to facilitate earlier identification of monkeys at risk for poor social outcomes. Social classification was determined for N = 25 LS and N = 25 HS male monkeys that were 1–4 years of age. As part of a colony-wide assessment, these monkeys had previously undergone, as infants, tests of face recognition memory and the ability to respond appropriately to conspecific social signals. Monkeys later identified as LS vs. HS showed impairments in recognizing familiar vs. novel faces and in the species-typical adaptive ability to gaze avert to scenes of conspecific aggression. Additionally, multivariate logistic regression using infant social ability measures perfectly predicted later social classification of all N = 50 monkeys. These findings suggest that an early capacity to process important social information may account for differences in rhesus monkeys’ motivation and competence to establish and maintain social relationships later in life. Further development of this model will facilitate identification of novel biological targets for intervention to improve social outcomes in at-risk young monkeys.

Bridging the gap between rodents and humans: The role of non‐human primates in oxytocin research

“…During this period, rhesus infants form bonds not only with their mothers but also with other adult females in the matriline and develop social skills that will support social bonding with peers later in life (Corcoran et al, 2012; Dettmer et al, 2016; Simpson, Sclafani, et al, 2017; Vanderwert et al, 2015). In this stage of development, face recognition, the discrimination of individuals, and most importantly, the discrimination of social signals such as facial expression, gestures, and postures is perfected (Dettmer et al, 2016; Harlow, 1962; Ruppenthal, Harlow, Eisele, Harlow, & Suomi, 1974; Sclafani et al, 2016; Simpson, Miller, Ferrari, Suomi, & Paukner, 2016). In the second year of their life, juveniles start to learn and understand the social hierarchy of the troupe, and their place within this hierarchy.…”

Acute oxytocin improves memory and gaze following in male but not female nursery-reared infant macaques

“…We chose macaques because they share many aspects of human physiology, development, cognition, and social complexity (Phillips et al 2014) and exhibit pronounced individual differences in sociality across development (Dettmer et al 2016; Sclafani et al 2016). We tested macaque infants reared in a neonatal nursery by human caretakers, a population at risk for impaired social behaviors (e.g., Sclafani et al 2015; Winslow, 2003), and who therefore may benefit the most from OT interventions.…”

Introducing Therioepistemology: the study of how knowledge is gained from animal research

“…Ignoring these differences can be disastrous, if, for instance, normal species differences in anatomy are mistaken as pathological [51][52][53] . Similarly, the complexities of human diagnoses are ignored or glossed over at our peril 17,48,49,54,55 . A recurrent theme of this paper, and this special issue, is that the role that good animal wellbeing plays in good science also cannot be ignored 26,[41][42][43][56][57][58] .…”

“…Criticizing or abandoning a model or measure is often characterized as throwing the baby out with the bathwater. For instance, autistic children show impairments in making eye contact, social play, and in theory of mind; but so do mice as a species 55 . It is nonsensical to attempt to model the pathological absence of a cognitive function in an animal that does not possess it in the first place.…”

“…Autism also shows us how to resolve this problem-sometimes we may have to pick different species for different components of the diagnosis. Developmental delay and repetitive behaviors can be meaningfully modeled in mice 83 , but we will have to turn to species that do possess complex social cognition in order to model the social dimension of the disorder 55 .…”