Early predictors of impaired social functioning in male rhesus macaques (Macaca mulatta)

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

Visual attention distribution during the response to conspecific social stimuli test.

<p>Infants later classified as Low-Social (LS) showed a lower rate of gaze aversion to aggression, and looked at the social stimuli less frequently than infants later classified as High-Social (HS), but both monkey groups spent a greater percentage of time looking at aggressive vs. neutral behavioral displays. (a) The rate of gaze aversion differed between infants later classified as LS and HS only during the aggression exemplars. (b) The rate of looking also differed between infants later classified as LS and HS only during the aggression exemplars. Infants later classified as HS, but not LS, differed in their rate of looking between aggression and neutral exemplar types. (c) The percentage of time spent looking at aggression did not differ between monkey groups, and both groups spent more time looking at aggressive displays over neutral ones.</p

Preference for novel faces on the face recognition memory test.

<p>During recognition trials, infants later classified as Low-Social (LS) did not show a preference above chance for the novel face (percentage of time looking on target directed to the novel face) (97.5% CI: 43.6% - 53.3%); whereas infants later classified as High-Social (HS) did (97.5% CI: 51.6% - 61.0%). Data are plotted as LSM +/- SE. Effect size is given in the text as partial eta ().</p

Face recognition memory test.

<p>During a familiarization trial (a) infants were presented with two identical unfamiliar rhesus monkey faces. During the subsequent recognition trial (b) infants were presented with the same rhesus monkey face from the immediately preceding familiarization trial as well as a novel face.</p