The Neurobiology of Consolation in the Prairie Vole Público

Abstract

Consolation behavior toward distressed others is common in humans and great apes, yet our ability to explore the biological mechanisms underlying this behavior is limited by its apparent absence in laboratory animals. Here we provide empirical evidence that a rodent species, the highly social and monogamous prairie vole (Microtus ochrogaster), greatly increases partner-directed grooming toward familiar conspecifics (but not strangers) that have experienced an unobserved stressor, providing social buffering. The combination of directed pro-social behavior with social buffering constitutes consolation behavior. We then extensively explore the hypothesis that consolation in prairie voles is based on an empathy mechanism. To address this question, we detail multiple pieces of supporting evidence demonstrating related characteristics and capacities, including state matching, emotional contagion, self-other differentiation, and familiarity bias. We then explore the neural mechanisms underlying consolation behavior in the prairie vole. Exposure to the stressed cagemate increases activity in anterior cingulate cortex, and oxytocin receptor antagonist infused into this region abolishes the partner-directed response, showing conserved neural mechanisms between prairie vole and human. We conclude that prairie voles show an empathy-based consolation behavior that likely evolved through deep homology from shared mechanisms supporting mammalian maternal care.

Table of Contents

CHAPTER 1: INTRODUCTION

1. Introduction. 1

1.1. Evolutionary considerations. 4

1.2. Prairie vole model. 7

2. Multi-level model of empathy. 7

2.1. Emotional empathy. 9

2.1.1. State matching/emotional contagion. 10

2.1.2. Self-other differentiation. 11

2.1.3. Familiarity bias. 12

2.2. Cognitive empathy. 13

2.2.1. Theory of mind. 13

2.2.2. Empathetic perspective-taking. 14

2.3. Synergy between emotional and cognitive empathy. 15

3. Laboratory tests of empathy in animals. 15

3.1. Instrumental responses. 16

3.2. Social modulation of pain. 18

3.3. Observational fear learning. 18

3.4. Consolation in animals. 20

4. Biological mechanisms of empathy. 22

4.1. Autonomic mechanisms. 22

4.2. Oxytocin. 23

4.3. Neural circuitry. 24

5. Research strategy. 25

CHAPTER 2: BEHAVIORAL OBSERVATIONS

1. Introduction. 27

2. Terminology. 29

3. Experiment 1. 29

4. Experiment 2. 35

5. Experiment 3. 37

6. Experiment 4. 42

7. Experiment 5. 45

8. Summary Discussion. 47

CHAPTER 3: CONSSOLATION AND EMPATHY

1. Introduction. 51

2. Terminology. 53

3. Experiment 1. 54

4. Experiment 2. 61

5. Experiment 3. 64

6. Experiment 4. 70

7. Summary Discussion. 72

CHAPTER 4: NEUROBIOLOGY OF CONSOLATION

1. Introduction. 75

2. Terminology. 77

3. Experiment 1. 78

4. Experiment 2. 81

5. Experiment 3. 87

6. Meta-analysis. 90

7. Summary Discussion. 95

CHAPTER 5: DISCUSSION

1. General discussion. 97

2. Future directions. 102

REFERENCES. 106

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	Biology, Neuroscience
Palavra-chave	Prairie Vole Oxytocin Empathy Consoling Consolation Neuroscience
Committee Chair / Thesis Advisor	Young, Larry J, Emory University
Committee Members	De Waal, Frans B M, Emory University Sanchez, Mar, Emory University Walker, David L, Emory University Ressler, Kerry, Emory University

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