Neural adaptations for social learning: Structural and functional investigations of action observation networks in macaques, chimpanzees, and humans Open Access

Abstract

Social learning is an important ability in primate life, and human specializations for social learning are part of what set us apart from the rest of the animal kingdom. In particular, humans' ability to copy not only the outcomes of observed actions but also their movement details has been linked to the emergence of cumulative culture. Social learning involves an action observation network that is distributed across frontal, parietal, and occipitotemporal cortex. This dissertation reports species differences in the structure and function of these networks that may underlie species differences in social learning. First, diffusion tensor imaging studies revealed progressively greater parietal and inferotemporal connectivity from macaques to chimpanzees to humans. These structural differences parallel, and may underlie, functional differences. FDG-PET neuroimaging studies in chimpanzees revealed that like humans and unlike macaques, chimpanzees have overlapping brain responses for performed action, observed transitive action, and observed intransitive action. Since chimpanzees and humans but not macaques are capable of copying movement details (imitating), this suggests that the ability to "mirror" not only action outcomes but also movement details is a correlate to the ability to copy those movement details. Furthermore, the chimpanzee neural response to observed action was situated mainly in prefrontal cortex, which may reflect top-down processing related to a conceptual, abstract representation of the observed action, while humans had greater parietal and occipitotemporal activation, which may reflect greater bottom-up processing on the details of movements, body parts, and objects. This may explain why humans tend to copy movement details while chimpanzees tend to copy action outcomes. Finally, chimpanzees with greater activation in ventral premotor cortex and lateral occipital cortex performed better in a separate behavioral test on copying action outcomes/movements and tool use, suggesting that selection pressure for social learning behavior could act on brain responses to observed action. These results are relevant to the evolution of action observation, social learning, and possibly culture.

Table of Contents

Table of Contents

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Chapter 1: Introduction

1.1. Why study the evolution of social learning? - p. 2

1.2. What can other animals tell us about human social learning? - p. 3

1.2.1. The big picture: Self-other matching phenomena across the animal kingdom - p. 6

1.2.3. Self-other matching in the motor domain: somatomotor movements - p. 7

1.2.4. Self-other matching in the perceptual domain: eye movements and cognition about perception - p. 17

1.2.5. Self-other matching in the emotional domain - p. 21

1.2.6. General patterns and principles of self-other matching - p. 27

1.3. Theoretical framework and hypotheses for studying the evolution of human social learning - p. 30

1.3.1. Neural networks involved in action observation - p. 31

1.3.2. Specific hypotheses to be investigated - p. 33

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Chapter 2: Connectivity

2.1. Comparative diffusion tensor imaging of neural systems for action execution-observation matching in macaques, chimpanzees, and humans

2.1.1. Summary - p. 40

2.1.2. Materials and methods - p. 41

2.1.3. Results - p. 46

2.1.4. Discussion - p. 53

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Chapter 3: Activation

3.1. Characterization of chimpanzee regional cerebral glucose metabolism during the perception and execution of object-directed and non-object-directed grasping actions

3.1.1. Summary - p. 97

3.1.2. Materials and methods - p. 98

3.1.3. Results - p. 102

3.1.4. Discussion - p. 105

3.2. Comparison between chimpanzee and human regional cerebral glucose metabolism during the perception of object-directed grasping

3.2.1. Summary - p. 134

3.2.2. Materials and methods - p. 135

3.2.3. Results - p. 137

3.2.4. Discussion - p. 138

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Chapter 4: Behavior

4.1. Correlations between behavior and brain activation in chimpanzees

4.1.1. Summary - p. 154

4.1.2. Materials and methods - p. 155

4.1.3. Results - p. 157

4.1.4. Discussion - p. 160

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Chapter 5: Conclusions

5.1. Summary of results - p. 179

5.2. Conclusions and future directions - p. 184

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Appendix

A.1 Comparisons between action execution/observation chimpanzee FDG-PET scans from the present dissertation and previously published chimpanzee resting state FDG-PET scans - p. 188

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References - p. 246

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Figure Index

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Chapter 1: Introduction

Table 1.2-1. Self-other matching terms and definitions - p. 35

Table 1.2-2. Unanswered questions in self-other matching research - p. 37

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Chapter 2: Connectivity

Table 2.1-1. Acquisition details for diffusion tensor imaging scans and corresponding structural scans - p. 62

Table 2.1-2. Quantification and statistical tests - p. 64

Figure 2.1-3. Control tractography - p. 67

Figure 2.1-4. Overview of mirror system tractography - p. 69

Figure 2.1-5. Additional views of connections between frontal mirror region, parietal mirror region, and superior temporal sulcus

---- A.In vivo humans - p. 71

---- B.In vivo chimpanzees - p. 72

---- C.In vivo macaques - p. 73

Figure 2.1-6. Overview of connections between frontal and parietal mirror regions - p. 74

Figure 2.1-7. Additional views of connections between frontal and parietal mirror regions

---- A.In vivo humans - p. 75

---- B.In vivo chimpanzees - p. 76

---- C.In vivo macaques - p. 77

Figure 2.1-8. Overview of connections between superior temporal sulcus and frontal mirror region - p. 78

Figure 2.1-9. Additional views of connections between superior temporal sulcus and frontal mirror region

---- A.In vivo humans - p. 79

---- B.In vivo chimpanzees - p. 80

---- C.In vivo macaques - p. 81

Figure 2.1-10. Overview of connections between inferior temporal cortex and frontal mirror region - p. 82

Figure 2.1-11. Additional views of connections between inferior temporal cortex and frontal mirror region.

---- A. In vivo humans - p. 83

---- B. In vivo chimpanzees - p. 84

---- C. In vivo macaques - p. 85

Figure 2.1-12. Overview of connections between superior temporal sulcus and parietal mirror region - p. 86

Figure 2.1-13. Additional views of connections between superior temporal sulcus and parietal mirror region

---- A. In vivo humans - p. 87

---- B. In vivo chimpanzees - p. 88

---- C. In vivo macaques - p. 89

Figure 2.1-14. Overview of connections between inferior temporal cortex and parietal mirror region. - p. 90

Figure 2.1-15. Additional views of connections between inferior temporal cortex and parietal mirror region

---- A. In vivo humans - p. 91

---- B. In vivo chimpanzees - p. 92

---- C. In vivo macaques - p. 93

Figure 2.1-16. Product versus product in social learning: A model linking species differences in mirror system circuitry, mirror system functional responses, and social learning behavior. - p. 94

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Chapter 3: Activation

Figure 3.1-1. Behavioral tasks for functional neuroimaging - p. 111

Table 3.1-2. Chimpanzee behavior during FDG uptake periods prior to scans - p. 113

Figure 3.1-3. Chimpanzee cortical anatomy and regions of interest - p. 114

Figure 3.1-4. Group statistical comparisons between experimental conditions and rest before masking cerebellum and brainstem - p. 116

Figure 3.1-5. 3D surface renderings of group statistical comparisons between experimental conditions and rest - p. 118

Figure 3.1-6. Coronal slices of group statistical comparisons between experimental conditions and rest - p. 119

Figure 3.1-7. 3D surface renderings of group statistical comparisons for observation > execution - p. 120

Figure 3.1-8. Coronal slices of group statistical comparisons for observation > execution - p. 121

Figure 3.1-9. 3D surface renderings of group statistical comparisons for execution > observation - p. 122

Figure 3.1-10. Coronal slices of group statistical comparisons for execution > observation - p. 123

Figure 3.1-11. 3D surface renderings of group statistical comparisons between transitive and intransitive observation - p. 124

Figure 3.1-12. Coronal slices of group statistical comparisons between transitive and intransitive observation - p. 125

Figure 3.1-13. Top 1% of activity in chimpanzee brains during each individual scan. - p. 126

Figure 3.1-14. 3D surface renderings of composite group map of top 1% of activity in chimpanzee brains during each individual scan - p. 127

Figure 3.1-15. Coronal slices of composite group map of top 1% of activity in chimpanzee brains during each individual scan - p. 128

Figure 3.1-16. Overlapping activity in individual subjects between action execution and both transitive and intransitive action observation - p. 129

Figure 3.1-17. 3D surface rendering of composite group maps of overlapping activity for action execution and transitive and intransitive action observation - p. 130

Figure 3.1-18. Coronal slices of composite group maps of overlapping activity for action execution and transitive and intransitive action observation - p. 131

Figure 3.1-19. Quantification of activity in individual conditions - p. 132

Figure 3.2-1. Visual stimuli for human functional neuroimaging - p. 142

Table 3.2-2. Human behavior during FDG uptake periods prior to scans, with comparison chimpanzee behavior - p. 143

Figure 3.2-3. Regions of interest - p. 144

Table 3.2-4. Anatomical definitions of regions of interest - p. 145

Figure 3.2-5. Individual scans - p. 148

Figure 3.2-6. Composite group analysis of thresholded images - p. 149

Figure 3.2-7. Composite group analysis of unthresholded images - p. 150

Figure 3.2-8. Quantification of above-threshold activation in humans and comparison to chimpanzees - p. 151

Table 3.2-9. Methodological differences between chimpanzees and humans - p. 152

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Chapter 4: Behavior

Table 4.1-1. Objects and actions for test of means/ends copying - p. 165

Table 4.1-2. Chimpanzee behavior during test of means/ends copying - p. 166

Figure 4.1-3. Scores on test of means/ends copying - p. 175

Figure 4.1-4. Training X activation effects - p. 176

Figure 4.1-5. Correlations between behavior and activation - p. 177

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Appendix

Figure A.1-1. Overlap between top 1% of voxels in execution-rest subtraction, and top 1% of voxels in transitive observation-rest subtraction. - p. 195

Figure A.1-2. Overlap between top 1% of voxels in execution-rest subtraction, and top 1% of voxels in intransitive observation-rest subtraction - p. 196

Figure A.1-3. Quantification of activations within ROIs in top 1% of voxels in execution-rest/transitive observation-rest overlap images, and execution-rest/intransitive observation-rest overlap images - p. 197

Figure A.1-4. Top 1% of voxels in execution-rest subtraction - p. 198

Figure A.1-5. Top 1% of voxels in transitive observation-rest subtraction - p. 199

Figure A.1-6. Top 1% of voxels in intransitive observation-rest subtraction - p. 200

Figure A.1-7. Quantification of activations within ROIs in top 1% of voxels in execution-rest, transitive observation-rest, and intransitive observation-rest - p. 201

Figure A.1-8. Top 1% of voxels in rest condition - p. 202

Figure A.1-9. Quantification of top 1% of voxels in execution and rest conditions in a broader set of frontal, parietal, and occipitotemporal ROIs - p. 203

Figure A.1-10. Chimpanzee resting state study: analysis of video from each scanning session - p. 204 - p.

Figure A.1-11. Ethogram and existing notes on videos from chimpanzee resting state scans - p. 205

Figure A.1-12. Overlap between top 25% of voxels in execution-rest subtraction, and top 25% of voxels in transitive observation-rest subtraction - p. 239

Figure A.1-13. Overlap between top 25% of voxels in execution-rest subtraction, and top 25% of voxels in intransitive observation-rest subtraction - p. 240

Figure A.1-14. Quantification activations within ROIs in top 25% of voxels in overlap analyses incorporating rest - p. 241

Figure A.1-15. Top 25% of voxels in execution-rest subtraction - p. 242

Figure A.1-16. Top 25% of voxels in transitive observation-rest subtraction - p. 243

Figure A.1-17. Top 25% of voxels in intransitive observation-rest subtraction - p. 244

Figure A.1-18. Quantification activations within ROIs in top 25% of voxels in individual conditions-rest - p. 245

About this Dissertation

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School	Laney Graduate School
Department	Biological and Biomedical Sciences
Subfield / Discipline	Neuroscience
Degree	PhD
Submission	Dissertation
Language	English
Research Field	Psychology, Psychobiology Biology, Neuroscience Anthropology, Physical
Keyword	brain evolution evolution simulation chimpanzees social learning action observation imitation mirror neurons macaques motor resonance
Committee Chair / Thesis Advisor	Parr, Lisa, Emory University
Committee Members	Barsalou, Lawrence, Emory University Rilling, James K, Emory University Preuss, Todd M, Emory University Sathian, Krish, Emory University

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