Family life and its consequences: insights from the monogamous prairie vole (Microtus ochrogaster) Open Access

Ahern, Todd (2010)

Permanent URL: https://etd.library.emory.edu/concern/etds/8049g5303?locale=en
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Abstract

Family life exerts a profound influence on both adults and children. For humans, family
life is marked by a rich set of dynamic social interactions, including adult pair bonds,
maternal- and paternal-infant bonding and nurturing, and parental coordination.
Differences in the structure, stability, and quality of these family dynamics influence
physiology, behavior, and mental health throughout life, yet little is known about the
neurobiology that mediates this influence. Manipulations of early environment and
mother-infant care in traditional animal models, such as rats and mice, have helped fill
this gap, but their uniparental family structure precludes the study of other family
dynamics, such as partner loss, shifts in family structure, paternal care, and parental
coordination. The goal of this dissertation was to examine how these other types of
family dynamics affect behavioral and neurobiological outcomes using monogamous
prairie voles (Microtus ochrogaster). I began by examining the effects of pair bond
disruption. Male prairie voles exhibited increased passive-coping following partner loss
and this effect was dependent on the activation of both known corticotropin-releasing
factor (CRF) receptors: CRF1 and CRF2. I then characterized the biparental family
dynamics of primiparous prairie voles under laboratory conditions and examined the
effects of altering family structure through the removal of the father. Under biparental
(BP) conditions, prairie vole parents of both sexes engaged in high levels of coordinated
pup care. Removal of the father resulted in single-mother (SM) family units and a
decrease in pup care that had a striking effect on offspring behavior in adulthood,
including changes in social bonding and two types of parenting behavior. I then examined
the effects of family structure on socially-relevant neuropeptide systems and found
significant differences in hypothalamic oxytocin (OT) content and CRF2 densities. Based
on parallels in the action and responses of these two systems to stress and social
environment, I ended with an investigation of the anatomical link between OT and CRF2.
Overall, these findings establish prairie voles as a promising animal model for the study
of family dynamics and offer new insights into how differences in family life can affect
behavior, emotion, and neurobiology.

Table of Contents


TABLE OF CONTENTS

CHAPTER 1 ...................................................................................................................... 1

FAMILY LIFE AND ITS CONTRIBUTIONS TO VARIATION IN BEHAVIOR, EMOTIONALITY,
MENTAL HEALTH, AND VULNERABILITY TO PSYCHOPATHOLOGY: A HUMAN AND ANIMAL
REVIEW ............................................................................................................................ 1
INTRODUCTION ....................................................................................................... 2
What is family? ....................................................................................................... 2
Why families are important .................................................................................... 4
HUMAN FAMILY RELATIONSHIPS ......................................................................... 4
The dynamics and structure of human families ...................................................... 4
Adult-adult selective social bonds and their impact on adult outcomes ................. 6
Family structure and child outcomes ...................................................................... 8
Maternal and paternal investment and child outcomes......................................... 10
Understanding families as networks ..................................................................... 12
BEHAVIORAL AND NEUROBIOLOGICAL INSIGHTS FROM TRADITIONAL
ANIMAL MODELS ................................................................................................... 12

Maternal effects on the development of offspring behavior................................. 13
Maternal effects on the developing brain.............................................................. 16
Limitations ............................................................................................................ 20
A COMPLEMENTARY APPROACH: NON-TRADITIONAL ANIMAL MODELS OF
FAMILY SYSTEMS ................................................................................................... 21

Expanding our view of selective family bonds..................................................... 21
Expanding our view of family relationships......................................................... 25
Cautious Optimism ............................................................................................... 28
AIMS FOR THIS DISSERTATION ........................................................................... 29
CHAPTER 2 .................................................................................................................... 32
THE EFFECTS OF PAIR-BOND DISRUPTION IN MONOGAMOUS PRAIRIE VOLES................... 32
PREFACE ................................................................................................................. 33
ABSTRACT................................................................................................................ 36
INTRODUCTION ..................................................................................................... 37
MATERIALS AND METHODS ................................................................................. 39
Animals ................................................................................................................. 39
Experimental protocol........................................................................................... 39
Detection of ACTH and corticosterone ................................................................ 43
In situ hybridization for CRF Mrna ...................................................................... 44
CRF receptor antagonist selectivity ...................................................................... 45
Long-term intracerebroventricular (icv) administration of CRF receptor
antagonists............................................................................................................. 48
Statistics ................................................................................................................ 49
RESULTS .................................................................................................................. 49
Isolation from a female partner induces passive stress-coping behavior.............. 49
Isolation from a female partner increases basal corticosterone levels .................. 51
Pairing with a female increased CRF mRNA in the mBNST............................... 52


Infusion of d-phe-CRF during the isolation period blocks separation-induced
passive-coping behavior........................................................................................ 55
Both CRF receptor subtypes (CRF1 and CRF2) are involved in mediating passive
stress-coping behavior after separation................................................................. 57
DISCUSSION............................................................................................................ 60
Disclosure / Conflict of interest ............................................................................ 65
Acknowledgments and Funding ........................................................................... 66
CHAPTER 3 .................................................................................................................... 67
PARENTAL DIVISION OF LABOR AND THE EFFECTS OF FAMILY STRUCTURE ON PARENTING
IN MONOGAMOUS PRAIRIE VOLES ................................................................................... 67
PREFACE ................................................................................................................. 68
ABSTRACT................................................................................................................ 70
INTRODUCTION ..................................................................................................... 71
STUDY 1 ................................................................................................................... 73
Do primiparous prairie vole breeders show long-term parental coordination under
laboratory conditions?........................................................................................... 73
MATERIALS AND METHODS (STUDY 1) .............................................................. 73
Animals ................................................................................................................. 73
Family unit observations....................................................................................... 74
Data analysis ......................................................................................................... 75
RESULTS (STUDY 1) ............................................................................................... 76
Nest Occupancy .................................................................................................... 76
Pup exposure......................................................................................................... 78
Nest occupancy swaps .......................................................................................... 79
Licking and grooming........................................................................................... 79
Nursing.................................................................................................................. 81
Pup maturation and parental pup-retrievals .......................................................... 82
STUDY 2 ................................................................................................................... 83
How do primiparous family dynamics change in response to the father's absence?
............................................................................................................................... 83
MATERIALS AND METHODS (STUDY 2) .............................................................. 84
Animals ................................................................................................................. 84
Family unit observations....................................................................................... 85
Data analysis ......................................................................................................... 85
RESULTS (STUDY 2) ............................................................................................... 86
Nest Occupancy .................................................................................................... 86
Pup exposure......................................................................................................... 88
Nest occupancy swaps .......................................................................................... 88
Licking and grooming........................................................................................... 89
Nursing.................................................................................................................. 91
Sustenance............................................................................................................. 92
Exploratory activities ............................................................................................ 92
DISCUSSION............................................................................................................ 93
Parental coordination over time ............................................................................ 94
Single-mother parenting........................................................................................ 97
Conclusions........................................................................................................... 99


Disclosure / Conflict of interest .......................................................................... 100
Acknowledgements and funding......................................................................... 100
CHAPTER 4 .................................................................................................................. 101
THE IMPACT OF EARLY LIFE FAMILY STRUCTURE ON ADULT ATTACHMENT,
ALLOPARENTING, AND PARENTING IN MONOGAMOUS PRAIRIE VOLES .......................... 101
ABSTRACT.............................................................................................................. 102
INTRODUCTION ................................................................................................... 103
MATERIALS AND METHODS ............................................................................... 106
Animals ............................................................................................................... 106
Offspring weights................................................................................................ 107
Open-field ........................................................................................................... 108
Elevated plus maze ............................................................................................. 109
Spontaneous alloparenting test ........................................................................... 110
Partner preference test......................................................................................... 111
Next-generation family unit observations........................................................... 113
RESULTS ................................................................................................................ 114
Pup weights......................................................................................................... 114
Adult offspring spontaneous alloparental care ................................................... 115
Adult offspring partner preference formation..................................................... 117
Adult offspring open-field testing....................................................................... 121
Adult offspring elevated plus maze testing......................................................... 124
Adult offspring gestational measures.................................................................. 125
Adult offspring parenting of the next generation................................................ 125
DISCUSSION.......................................................................................................... 127
Conclusions......................................................................................................... 134
Disclosure / Conflict of interest .......................................................................... 135
Acknowledgements and funding......................................................................... 135
CHAPTER 5 .................................................................................................................. 136
THE IMPACT OF EARLY LIFE FAMILY STRUCTURE ON ADULT NEUROPEPTIDE SYSTEMS IN
MONOGAMOUS PRAIRIE VOLES ..................................................................................... 136
ABSTRACT.............................................................................................................. 137
INTRODUCTION ................................................................................................... 138
MATERIALS AND METHODS ............................................................................... 140
Animals ............................................................................................................... 140
Family unit pup care ........................................................................................... 140
Adult offspring brain and blood analysis............................................................ 141
Plasma corticosterone ......................................................................................... 142
Oxytocin mRNA in situ hybridization................................................................ 142
Oxytocin mRNA in situ quantification and analysis .......................................... 143
Neuropeptide autoradiographic receptor binding ............................................... 144
Autoradiographic receptor binding quantification and analysis ......................... 145
RESULTS ................................................................................................................ 146
Family unit pup care ........................................................................................... 146
Basal plasma corticosterone................................................................................ 147
Oxytocin mRNA expression ............................................................................... 148

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