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Comparing Social Cognitive, Non-Social Cognitive, and Resting Brain Activity in Chimpanzees (Pan troglodytes)

Barks, Sarah Kate (2010)
Dissertation (202 pages)
Committee Chair / Thesis Adviser: Rilling, James K
Committee Members: Gouzoules, Sarah ; Parr, Lisa ; Preuss, Todd M
Research Fields: Anthropology, Physical; Biology, Neuroscience
Keywords: social cognition; default mode network; chimpanzee; FDG PET
Program: Laney Graduate School, Anthropology
Permanent url: http://pid.emory.edu/ark:/25593/7shz7

Abstract

The evolution of the human brain and cognition represents a long-standing question of
biological anthropology. Skillful interaction with others has been proposed as a primary mover
behind increased intelligence in primates (Dunbar 1998). This study explores the origins of the
neural bases of social cognition in humans, asking whether human patterns of social cognitive
brain function are unique to our species, or shared with chimpanzees (Pan troglodytes). Using
[18F]-fluorodeoxyglucose positron emission tomography, chimpanzee brain function was assessed
during a social cognition task, a non-social cognition task, and at rest. Two primary aims are to
assess the degree to which social cognitive brain function is similar to resting brain function in
chimpanzees, and to examine the neural correlates of chimpanzee social cognition. Similar
patterns of function to those of humans would suggest that these social cognitive networks were
present in our last common ancestor. Conversely, if patterns of activation differ, these species
may have diverged in this regard.


Chimpanzees performed a match-to-sample task with videos depicting conspecific
behaviors with varying social complexity. Functional neuroimaging data obtained during these
task conditions were compared with data from a non-social condition and a resting condition.
These conditions were compared both qualitatively and on a voxel-by-voxel basis using paired t-
tests.


Like the resting state, social cognition in chimpanzees activates cortical midline
structures, including the precuneus, posterior cingulate, and medial prefrontal cortex. Social
cognition also activates the insula and amygdala; higher levels of social complexity activate the
ventral striatum. At rest, these areas are active to a greater degree. Whole brain averages of each
condition examined independently show the same cortical midline areas of greatest activation
across all conditions. Rest, however, produces a higher maximum activation and a wider spread
of intensity.


This study bolsters previous findings that the resting state in chimpanzees shows similar patterns of brain activity as that of humans, with cortical midline structures highly
active, and shows that these areas consistently deactivate in a variety of task conditions much like
the human default network. Further, these data demonstrate similarity in brain function during
social cognition and at rest in chimpanzees.

Table of Contents

Table of contents

List of figures and tables

Introduction 1

Chapter 1: Background 4

Human social cognitive neuroscience 4

Theory of mind 4

Anatomy of theory of mind 5

Theory of mind and imitation 8

Development of theory of mind 11

The default mode network 13

The default mode network and social cognition 16

Chimpanzee social cognition 17

Social structure in the wild 18

Social learning 21

Social cognitive capacities 23

Self-awareness 24

Deception and false belief 25

Joint attention 27

Theory of mind in chimpanzees 31

Comparative research methodology 33

Non-human primate models of brain function 33

Functional neuroimaging of non-human primates 34

Chapter 2: Research design and methods 37

Research design 37

Hypotheses 37

Subjects 38

Creation of stimulus set 39

Training of subjects 41

FDG PET methodology 41

Acquisition of PET images 44

Acquisition of MR images 46

Analysis of PET images 47

T-tests 48

Whole brain averages 49

Subtraction contrasts 49

Chapter 3: Results 51

Behavioral results 51

Overview of imaging results 53

T-tests in whole brain 54

T-tests in whole brain, exclusive of cerebellum and brain stem 56

Rest-related activity 56

High social-related activity 58

Low social-related activity 59

Non-social-related activity 60

Combined social-related activity 61

Summary of t-tests 63

T-tests within resting state ROI 69

Whole brain averages 74

Subtraction contrasts 84

Chapter 4: Discussion 86

Contrasts among conditions 86

Activity in precuneus and posterior cingulate cortex 86

Activity in medial prefrontal cortex 89

Activity in insula 90

Activity in amygdala 91

Activity in fusiform gyrus 92

Activity in ventral striatum 93

Whole brain averages 94

Replicability 95

Task-positive and task-negative areas of activation 97

Variables between rest and tasks 100

Conclusion 102

Caveats and limitations 103

Directions for future research 104

Appendix 107

Maximum t-statistic values in each contrast 107

Results for each contrast, whole brain exclusive of cerebellum

and brain stem 109

Results for each contrast, resting state ROI 141

Condition averages in whole brain 173

Bibliography 176

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