The role of progesterone in pregnancy-induced aggression in mice

doi:10.1016/0018-506X(84)90039-4

Hormones and Behavior

Volume 18, Issue 2, June 1984, Pages 140-160

https://doi.org/10.1016/0018-506X(84)90039-4 Get rights and content

Abstract

A series of six experiments was performed in order to explore the potential involvement of progesterone (P) in pregnancy-induced aggression (PIA) displayed by Rockland-Swiss mice toward adult male intruders. In Experiment 1, circulating levels of P and aggression were low on gestation Days 6 and 10 while both the behavior and the steroid reached peak levels by gestation Day 14. By gestation Day 18 (the day prior to parturition), serum P was at its lowest level yet aggressive behavior was still intense. Also, individual differences in the display of fighting behavior by pregnant females were not related to circulating P. Experiments 2 and 3 showed that supplemental P treatment to early pregnant female mice did not advance the onset of aggression. Experiment 4 showed that P treatment promoted the onset and elevated the incidence of aggression in virgin mice, but only in those females with intact ovaries. Experiment 5 showed that the aggressive behavior of P-stimulated virgin females was qualitatively and quantitatively different from that exhibited by pregnant mice in that the former exhibited fewer attacks and lunges than the latter. Finally, Experiment 6 showed that the removal of P from aggressive, P-stimulated virgins dramatically attenuated levels of the behavior. This contrasts sharply with the continued fighting behavior observed in late pregnant P-deficient mice. Thus, although P augments aggression in female mice it apparently is not a sufficient stimulus for producing pregnancy-like aggressive behavior.

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From sexual attraction to maternal aggression: When pheromones change their behavioural significance
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Citation Excerpt :
This leads us again to the interesting issue of whether the same maleness chemosignals are responsible for attraction of females and for promoting attacks on male intruders during the postpartum period. A second interesting question is what causes females to change their behavioural response to male chemosignals, from attraction and mating facilitation to aggression after parturition (in fact a few days before, Mann et al., 1984; Bosch, 2013). In this respect, since olfactory cues (likely derived from pups) are critical for other aspects of maternal behaviour, we wondered whether intimate contact with pups providing full access to these olfactory cues might be a causal factor facilitating this change in behaviour.
This article is part of a Special Issue “Chemosignals and Reproduction”.
This paper reviews the role of chemosignals in the socio-sexual interactions of female mice, and reports two experiments testing the role of pup-derived chemosignals and the male sexual pheromone darcin in inducing and promoting maternal aggression. Female mice are attracted to urine-borne male pheromones. Volatile and non-volatile urine fractions have been proposed to contain olfactory and vomeronasal pheromones. In particular, the male-specific major urinary protein (MUP) MUP20, darcin, has been shown to be rewarding and attractive to females. Non-urinary male chemosignals, such as the lacrimal protein ESP1, promote lordosis in female mice, but its attractive properties are still to be tested. There is evidence indicating that ESP1 and MUPs are detected by vomeronasal type 2 receptors (V2R).
When a female mouse becomes pregnant, she undergoes dramatic changes in her physiology and behaviour. She builds a nest for her pups and takes care of them. Dams also defend the nest against conspecific intruders, attacking especially gonadally intact males. Maternal behaviour is dependent on a functional olfactory system, thus suggesting a role of chemosignals in the development of maternal behaviour. Our first experiment demonstrates, however, that pup chemosignals are not sufficient to induce maternal aggression in virgin females. In addition, it is known that vomeronasal stimuli are needed for maternal aggression. Since MUPs (and other molecules) are able to promote intermale aggression, in our second experiment we test if the attractive MUP darcin also promotes attacks on castrated male intruders by lactating dams. Our findings demonstrate that the same chemosignal, darcin, promotes attraction or aggression according to female reproductive state.
Extracts from salivary glands stimulate aggression and inositol-1, 4, 5-triphosphate (IP<inf>3</inf>) production in the vomeronasal organ of mice
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Mammals use chemical cues to coordinate social and reproductive behaviors. Chemical cues are detected by the VNO organ (VNO), which is a cartilage-encased elongated organ associated with the vomer bone in the rostral nasal cavity. The resident intruder paradigm was utilized to examine the ability of saliva and its feeder exocrine glands, the submaxillary, parotid, and sublingual glands to mediate aggression in mice. Saliva and extracts from submaxillary and parotid glands, but not extracts from sublingual glands of male CD-1 mice, induced a greater number of attacks and lower latencies to sniff and attack (p < 0.05) and significantly increased IP₃ production (p < 0.05) versus vehicle (PBS) in CD-1 male mice VNO. We further show that CD-1 male mouse saliva and submaxillary gland extract induced significantly more attacks and a lower latency to attack in lactating female CD-1 mice and produced significantly more inositol triphosphate (IP₃), indicative of phospholipase C_β signaling which mediates pheromonal activity, in CD-1 female VNO compared to PBS. Castrated CD-1 male mouse saliva, and exocrine gland extracts induced significantly less IP₃ production in male VNO and less aggression by CD-1 males and lactating females compared to responses to normal CD-1 male mouse saliva and gland extracts. Thus, chemical cues present in saliva, submaxillary and parotid glands of CD-1 male mice are capable of stimulating aggression in male and female congenic mice which are correlated with significant production of IP₃ in the VNO. Additionally, these stimulations of aggression and IP₃ production are shown to be androgen-dependent.
Role of Corticotropin Releasing Factor-Related Peptides in the Neural Regulation of Maternal defense
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The primary interest of this discussion is the central actions of corticotropin releasing factor (CRF)-related peptides. CRF is a potent activator of the hypothalamic–pituitary–adrenal (HPA) axis, a peripheral effect, and recent work suggests Ucn 1 and 3 can also trigger HPA responses. Importantly, the end product of HPA activation, elevated glucocorticoids (corticosterone), though, do not affect maternal aggression output. In fact, during maternal aggression, glucocorticoids are elevated, which is not surprising given that the primary function of corticosterone is glucose mobilization and fighting involves high metabolic output. Although stress reactivity in terms of HPA responses to some stressors are muted during lactation, study is concerned with altered central stress reactivity that underlies the behavioral responses to stressors. Because CRF neurotransmission is decreased during lactation, researchers are interested in testing the hypothesis that CRF levels are inversely linked to levels of maternal aggression. First approach was to use icv injections CRF to test whether this peptide could decrease defense as predicted. It was found CRF dose dependently impair maternal aggression. An effect of a CRF receptor antagonist on aggression was found and this finding was interpreted as reflecting a “floor effect.” In other words, CRF neurotransmission may already be low in key areas during lactation and keeping it low does not affect intensity. This interpretation suggests some other modulators are involved in positively regulating levels of aggression.
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Gene array profiling of large hypothalamic CNS regions in lactating and randomly cycling virgin mice
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A dramatic example of neuronal and physiological plasticity in adult mammals occurs during the transition from a non-maternal to a maternal, lactating state. In this study, we compared gene expression within a large continuous region of the CNS involved in maternal behaviors (hypothalamus, preoptic regions, and nucleus accumbens) between lactating (L) (postpartum Day 7) and randomly cycling virgin (V) outbred mice. Using high-density oligonucleotide arrays representing 11,904 genes, two statistical algorithms were used to identify significant differences in gene expression: robust multiarray (P < 0.001) (n = 92 genes) and significance analysis of microarrays using a 10% false discover rate (n = 114 genes). 27 common genes were identified as significant using both techniques. A subset of genes (n = 5) were selected and examined by real-time PCR. Our findings were consistent with previous published work. For example, neuropeptide Y (NPY) and proenkephalin were elevated in L mice, whereas POMC was decreased. Increased levels of NPY Y2 receptor and polo-like kinase and decreased levels of endothelin receptor type b in L mice are examples of novel gene expression changes not previously identified. Expression differences occurred in broad classes. Together, our findings provide possible new material on gene expression changes that may support maternal behaviors. The advantages and drawbacks of sampling large CNS regions using arrays are discussed.
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^☆: This work was supported in part by a Research Grant from the Harry Frank Guggenheim Foundation, by Grant BNS80-08546 from NSF, and by Grant AG01319 from NIA.

²: Martha Mann now is at Department of Psychology, University of Texas at Arlington, Arlington, Tex. 76019.

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The role of progesterone in pregnancy-induced aggression in mice☆

Abstract

Horm. Behav.

Horm. Behav.

Anim. Behav.

Anim. Behav.

Behav. Neural Biol.

Physiol. Behav.

Horm. Behav.

Physiol. Behav.

Behav. Biol.

Physiol. Behav.

Horm. Behav.

Biobehav. Rev.

Horm. Behav.

Contraception

The gestational pattern of estradiol, testosterone and progesterone secretion in selected strains of mice

Biol. Reprod.

Plasma testosterone during pregnancy in the mouse

Endocrinology

The effect of various dosages of lynestrenol on the plasma levels of oestrogens and progesterone during the menstrual cycle in the Rhesus monkey

Contraception