Individual variation in typically developing rhesus macaque infants (Macaca mulatta): The role of matrilineal social rank Restricted; Files Only

Abstract

Newborn primates acquire vital information about the social world first and foremost through caregivers, relying on dynamic, species-typical exchanges of vocalizations, facial expressions, and shared gaze. Infant-caregiver interactions are facilitated by neonates’ attentional preference for socially informative cues like conspecifics’ eyes. In studies of this early-emerging visual preference, rhesus macaques (Macaca mulatta) are an indispensable model system due to the species’ altricial birth, extended development, and complex social life. Rhesus macaques live in matriarchal groups structured around highly stable, linear dominance hierarchies. Ranking is transferred intergenerationally from dams to their offspring. For infants, the social environment is shaped from birth by their dams’ social status, yet it is not clear to what extent rank explains interindividual variation in social development, or at what age(s) such differences emerge. The goals of this dissertation were to: (1) investigate the role of matrilineal rank in the social development of male rhesus macaques during the first year of life and (2) identify behavioral measures in early infancy that predict social competency in the juvenile stage. Development was tracked longitudinally from birth to 1 year of age in male infants born and reared at the Emory National Primate Research Center Field Station (Lawrenceville, GA). In Study I, maternal behavior and focal infants’ interactions with groupmates were analyzed from 2 weeks of age through 1 year. The data showed effects of matrilineal rank on some maternal behaviors, but not on infants’ interactions with groupmates. In Study II, eye-tracking data were collected over 14 sessions spanning the first 6 months of life, during which infants voluntarily viewed videoclips depicting a single conspecific or dam-infant interactions. The results suggested that by 4 to 5 months of age, low-ranking infants developed covert viewing strategies in order to monitor social cues while avoiding direct eye contact with conspecifics. In addition, rates of initiating social play at 1 year were positively predicted by saccades to dam-infant videos, but negatively predicted by both maternal cradling and rates of withdrawing at younger ages. Overall, this dissertation demonstrated the value of the rhesus macaque model for investigating the neurobiological processes supporting evolutionarily conserved social abilities among primates, as well as the disruption of these processes in atypically developing infants and children.

Table of Contents

GENERAL INTRODUCTION.................................................................................................................1

ATYPICAL SOCIAL DEVELOPMENT: ECOLOGICAL & CLINICAL PERSPECTIVES....................................3

Ontogenetic Niche Construction..........................................................................................................3

Developmental Endophenotypes..........................................................................................................3

Continuity, Discontinuity, & Early Prediction.......................................................................................5

A NON-HUMAN PRIMATE MODEL OF SOCIAL DEVELOPMENT.............................................................6

MATERNAL RANK “INHERITANCE” & NICHE CONSTRUCTION.............................................................8

SUMMARY OF STUDIES......................................................................................................................10

REFERENCES.....................................................................................................................................12

STUDY I: Social status shapes maternal style towards rhesus macaque infants in the first year of life........18

ABSTRACT.........................................................................................................................................19

INTRODUCTION................................................................................................................................20

METHODS.........................................................................................................................................25

Subjects and Housing.........................................................................................................................25

Behavioral Data Collection.................................................................................................................26

Data Handling & Statistical Analyses..................................................................................................30

RESULTS...........................................................................................................................................36

Mother-Infant Proximity & Hinde Index..............................................................................................36

Focal Infant Behavioral Measures.......................................................................................................37

Maternal Style...................................................................................................................................39

Predictive Models...............................................................................................................................40

DISCUSSION......................................................................................................................................41

Mother-Infant Proximity.....................................................................................................................43

Maternal Care Behaviors.....................................................................................................................43

Interactions with Groupmates.............................................................................................................44

Maternal Style & the IMMC................................................................................................................44

Early Behavioral Markers of Social Functioning in the Juvenile Stage.....................................................45

Infant Sex Differences........................................................................................................................46

Social Instability................................................................................................................................47

Interspecies Differences.....................................................................................................................48

Limitations.......................................................................................................................................49

Conclusion........................................................................................................................................50

FIGURES & TABLES...........................................................................................................................51

APPENDIX: Equations for Generalized Multilevel Mixed Models...........................................................64

REFERENCES....................................................................................................................................65

STUDY II: Developmental trajectories of social-visual attention in rhesus macaque infants....................72

ABSTRACT........................................................................................................................................73

INTRODUCTION...............................................................................................................................74

METHODS........................................................................................................................................78

Subjects & Housing...........................................................................................................................78

Eye-tracking Procedures....................................................................................................................80

Experimental Stimuli.........................................................................................................................81

ROI Analysis.....................................................................................................................................82

Statistical Analysis............................................................................................................................83

RESULTS..........................................................................................................................................88

Analysis of Conspecific Videos...........................................................................................................88

Analysis of Mother-Infant Videos.......................................................................................................93

Predictive Models.............................................................................................................................96

DISCUSSION....................................................................................................................................97

Developmental Trajectory of Percent Fixation to Eyes.........................................................................98

Developmental Trajectories of Percent Fixation to Social-Visual Cues................................................100

Global Measures of Social-Visual Attention: Total Fixations, Saccades, & Lost Data.............................102

Eye-tracking Measures as Predictors of Social Functioning in the Juvenile Stage.................................103

Convergence Across Age to Salient Areas of Social Scenes..................................................................105

Future Directions...........................................................................................................................107

FIGURES & TABLES........................................................................................................................108

APPENDIX I: Detailed Methods.......................................................................................................125

Eye-tracking Procedures.................................................................................................................125

Functional Principal Component Analysis via PACE..........................................................................126

Salience Mapping...........................................................................................................................127

APPENDIX II: Moment-by-Moment Convergence.............................................................................130

REFERENCES.................................................................................................................................131

GENERAL DISCUSSION..................................................................................................................137

SUMMARY OF FINDINGS...............................................................................................................138

CONTINUITY, DISCONTINUITY, & PREDICTORS.............................................................................139

MATRILINEAL RANK & ONTOGENETIC NICHES.............................................................................141

IMPLICATIONS FOR FUTURE RESEARCH........................................................................................143

CONCLUSION................................................................................................................................145

REFERENCES................................................................................................................................146

About this Dissertation

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School	Laney Graduate School
Department	Psychology
Subfield / Discipline	Neuroscience and Animal Behavior
Degree	Ph.D.
Submission	Dissertation
Language	English
Research Field	Psychology, Developmental Psychology, Behavioral Psychology, Psychobiology
Keyword	infant development maternal care social visual engagement rhesus macaque niche construction nonhuman primate social development social ranking eye-tracking
Committee Chair / Thesis Advisor	Jocelyne Bachevalier, Emory University
Committee Members	Patricia Bauer, Emory University Donna Maney, Emory University Mar Sanchez, Emory University Warren Jones, Emory University

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