The influence of bilateral neonatal lesions of the amygdala on pubertal onset and sexual behavior in female Rhesus Macaques living in social groups Público
Stephens, Shannon Brooke Zoe (2013)
Abstract
Reproduction is regulated by various physiological and environmental factors, one of which is social context. Delayed first ovulation is observed in lower-ranking female rhesus macaques, in comparison to higher-ranking females, and lower-ranking females show a tight coupling of estradiol levels and sexual behavior in social groups (Zehr et al., 2005; Wallen, 1990). The brain mechanisms modulating the effects of social context on puberty onset and sexual behavior are unknown. The amygdala is one potential region of the brain modulating the effects of social context on reproduction because of its importance for behavioral responses to social information (Thompson et al., 1969; Spiteri et al., 2010) as well as its connections to the hypothalamus (Amaral et al., 1992). We examined the effects of neonatal bilateral neurotoxic amygdala lesions on pubertal timing and sexual behavior in female rhesus macaques living in social groups. At one month of age, subjects received either bilateral amygdala lesions or a sham-operated procedure. Beginning in August, 14-17 months of age, vaginal swabs and blood samples were collected to assess the age at menarche and first ovulation. Sexual behavior was examined in a pair test and in the social group. Earlier menarche and first ovulation were observed in lesioned females in comparison to control females. Based on the current study, it is not clear what, if any, effect the amygdala has on modulating social information that alters the timing of puberty. Lesioned females showed lower levels of some female-initiated sexual behaviors in the social group observations, but there was no effect of amygdala lesions on female sexual receptivity. Estradiol did not influence the rate of behavior observed in lesioned females, though some effects were observed in control females. The mechanisms by which the amygdala alters puberty onset and sexual behavior are unknown. It is possible that puberty onset occurred earlier in lesioned females as a result of earlier removal of GABA inhibition on GnRH release, resulting in earlier menarche and ultimately, earlier first ovulation. Sexual behavior differences in amygdala-lesioned females may result from decreased estradiol sensitivity, thereby influencing the modulatory relationship that estradiol can have on female sexual behavior.
Table of Contents
Table of Contents
Chapter 1: General Introduction...................................................................................... 1
Neuroanatomy of the Hypothalamus and the Amygdala................................. 12
The Effect of the Amygdala on Female Sexual Behavior................................ 14
Hormonal Regulation in Adult Females............................................................. 29
Specific Aims and Hypotheses............................................................................ 56
Figure Captions.................................................................................................... 58
Figure 1................................................................................................................. 59
Figure 2................................................................................................................. 60
Figure 3................................................................................................................. 61
Figure 4................................................................................................................. 62
Figure 5................................................................................................................. 63
Figure 6................................................................................................................. 64
Chapter 2: Environmental and social influences on neuroendocrine puberty and
behavior in macaques and other nonhuman primates................................................. 65
(Note: Chapter 2 discusses both males and females, but this dissertation is focused on females)
Abstract................................................................................................................ 66
Puberty Onset....................................................................................................... 69
Seasonal Influences on Puberty Onset............................................................... 74
Body Weight and Puberty Onset........................................................................ 79
Social Rank and Puberty Onset.......................................................................... 87
Pre-and Neonatal Testosterone Levels and Puberty Onset.............................. 99
Pubertal Changes in Behavior.......................................................................... 105
Conclusion.......................................................................................................... 113
Acknowledgements............................................................................................ 115
References.......................................................................................................... 116
Figure Captions.................................................................................................. 131
Figure 1............................................................................................................... 132
Figure 2............................................................................................................... 133
Figure 3............................................................................................................... 134
Chapter 3: Neonatal Amygdala Lesions Advance Pubertal Timing in
Female Rhesus Macaques............................................................................................. 135
Abstract.............................................................................................................. 136
Introduction........................................................................................................ 137
Method................................................................................................................ 140
Results................................................................................................................. 149
Discussion........................................................................................................... 154
Acknowledgements............................................................................................ 159
References.......................................................................................................... 160
Table 1................................................................................................................ 166
Figure Captions.................................................................................................. 167
Figure 1.............................................................................................................. 168
Figure 2.............................................................................................................. 169
Figure 3.............................................................................................................. 170
Figure 4.............................................................................................................. 171
Figure 5.............................................................................................................. 172
Figure 6.............................................................................................................. 173
Figure 7.............................................................................................................. 174
Chapter 4: Effects of Neonatal Amygdala Lesions and Social Context on
Sexual Behavior in Female Rhesus Macaques............................................................ 175
Abstract............................................................................................................. 176
Introduction....................................................................................................... 178
Method............................................................................................................... 181
Results................................................................................................................ 189
Discussion.......................................................................................................... 200
Acknowledgements........................................................................................... 207
References......................................................................................................... 208
Table 1............................................................................................................... 212
Table 2............................................................................................................... 213
Table 3............................................................................................................... 215
Table 4............................................................................................................... 218
Figure Captions................................................................................................. 221
Figure 1.............................................................................................................. 222
Figure 2.............................................................................................................. 223
Figure 3.............................................................................................................. 224
Figure 4.............................................................................................................. 225
General Discussion......................................................................................................... 226
Does the amygdala influence the timing of puberty?..................................... 228
Does the amygdala eliminate the effects of social rank
on pubertal timing?.................................................................................... 232
Does the amygdala influence sexual behavior and how do these
effects differ based on the social context?................................................ 233
Conclusions........................................................................................................ 237
General Introduction and Discussion References.......................................... 239
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