Behavioral and Neuroendocrine Effects of Neonatal AmygdalaLesion on Rhesus Monkeys Living in a Semi-NaturalisticEnvironment. Open Access

Abstract

Abstract Neonatal amygdala (AMY) lesions yield changes in social and emotional behavior. Previous studies have indicated that neonatal AMY lesions produced decreased social and increased fear behavior in presence of peers (Thompson et al, Phys Behav, 1969: 4; Bauman et al., J. Cogn Neurosci, 2004:16). Because in the earlier developmental studies, fear behavior was measured while the animals were placed in small social groups, here we assessed whether similar social and emotional changes will emerge after neonatal AMY lesions in male rhesus monkeys ( Macaca mulatta) reared in a rich and complex semi-naturalistic social environment composed of 98 adult females and 76 offspring organized in 12 matrilines. Results show that neonatal AMY lesions produce behavioral changes, which become more pronounced as subjects mature. Yet, in contrast to previous findings, neonatal AMY damage does not result in increased fear behavior when animals are navigating in a rich and complex social environment, but instead yields increased maternal independence, play, dominance, and aggressive behaviors. Additionally, neonatal AMY lesions produce blunted emotional reactivity to stressful and potentially dangerous situations. These changes are indicative of reduced fear behaviors, presumably resulting from an inability to recognize potential social risks. Thus, behavioral outcomes of neonatal AMY lesions are critically dependent on the complexity of the social context.

Table of Contents

Table of Contents INTRODUCTION ............................................................................................................ 1 Structure and Electrical Properties of the Primate Amygdala ................................... 3 Aspiration Lesion of Adult Primates: ............................................................................. 5 Emotional Behavior .................................................................................................... 5 Social Behavior ........................................................................................................... 7 Neurotoxic Lesion of Adult Primates ........................................................................... 10 Emotional Behavior .................................................................................................. 10 Neuroendocrine Response to Stress.......................................................................... 12 Social Behavior ......................................................................................................... 13 Behavioral Developmental and Amygdala Maturation ................................................ 15 Neonatal Aspiration Lesion of Primates ....................................................................... 17 Emotional Behavior .................................................................................................. 17 Social Behavior ......................................................................................................... 19 Neonatal Neurotoxic Lesion of Primates ...................................................................... 22 Emotional Behavior .................................................................................................. 22 Neuroendocrine Response to Stress.......................................................................... 22 Social Behavior ......................................................................................................... 23 Environmental Considerations...................................................................................... 25 Hypothesis 1: Social Behavior................................................................................. 27 Hypothesis 2: Emotional and Neuroendocrine Responses to Stress........................ 27 METHODS ...................................................................................................................... 29 Subjects ......................................................................................................................... 30 Magnetic Resonance Imaging (MRI) Procedures and Injection Coordinates .............. 30 Surgical Procedure ....................................................................................................... 31 Post-surgical MRI Scan ................................................................................................ 32 Sham Surgery................................................................................................................ 33

Lesion Extent Histology............................................................................................... 33 Perfusion ................................................................................................................... 33 Staining ..................................................................................................................... 38 Lesion Assessment..................................................................................................... 39 Extent of Lesion ........................................................................................................... 39 Social Behavioral Observations.................................................................................... 41 Emotional Reactivity Testing ....................................................................................... 43 Social Isolation Test.................................................................................................. 43 Human Intruder Test................................................................................................. 43 Social Intruder Test................................................................................................... 44 Neuroendocrine measures ............................................................................................ 44 RESULTS ........................................................................................................................ 46 CHAPTER 1: SOCIAL BEHAVIOR .......................................................................... 46 Mother-infant Interactions........................................................................................ 47 Affiliative Behaviors with Non-mother individuals................................................... 57 Play and Dominance Behaviors................................................................................ 58 Sexual Behaviors....................................................................................................... 63 Aggression, Fear, and Anxiety Behaviors................................................................. 63 Discussion ............................................................................................................. 67 CHAPTER 2: BEHAVIORAL AND NEUROENDOCRINE RESPONSES TO STRESS............................................................................................................................ 80 Social Isolation Test...................................................................................................... 81 Behavioral Reactivity................................................................................................ 81 Hormonal Reactivity ................................................................................................. 82 Human Intruder Test .................................................................................................... 85 Behavioral Reactivity................................................................................................ 85 Hormonal Reactivity ................................................................................................. 92

Social Intruder Test ...................................................................................................... 92 Discussion ............................................................................................................. 95 CONCLUSIONS ........................................................................................................... 104 References...................................................................................................................... 111 Appendix I: Social Behavior Ethogram......................................................................... 123 Appendix II: Reactivity Ethogram................................................................................. 125

Table of Figures Figure 1: Extent of amygdala damage for subject AMY-1.............................................. 34 Figure 2: Extent of amygdala damage for subject AMY-2.............................................. 36 Figure 3: Mother-infant interactions ................................................................................ 54 Figure 4: Affiliative behaviors with non-mothers ........................................................... 59 Figure 5: Play and dominance display behavior .............................................................. 61 Figure 6: Aggressive behaviors ....................................................................................... 65 Figure 7: Fear and Anxiety behaviors.............................................................................. 68 Figure 8: Social Isolation Test: Behavioral reactivity .................................................... 83 Figure 9: Social Isolation Test: Neuroendocrine responsivity........................................ 86 Figure 10: Human Intruder Test: Hostile and Affiliative Reactions............................... 88 Figure 11: Human Intruder Test: Freezing and Vocalization Reactions ........................ 90 Figure 12: Human Intruder Test: Neuroendocrine responsivity ..................................... 93 Figure 13: Social Intruder Test: Behavioral reactivity ................................................... 96

Table of Tables Table 1. Percentage of cell loss within the entire amygdala and adjacent structures ...... 40 Table 2. Percentage of cell loss within amygdala nuclei ................................................. 42 Table 3. Mean rates per minute of social behavior .......................................................... 48 Table 4. Comparison between previous studies and current study................................ 106

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School	Laney Graduate School
Department	Psychology
Subfield / Discipline	Neuroscience and Animal Behavior
Degree	MA
Submission	Dissertation
Language	English
Research Field	Psychology, Psychobiology Psychology, Behavioral Psychology, Developmental
Keyword	Social Behavior Amygdala Neuroendocrine Response
Committee Chair / Thesis Advisor	Bachevalier, Jocelyne, Emory University
Committee Members	Wallen, Kim, Emory University Walker, Elaine, Emory University

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