Rapid effects of estradiol on male aggression depend on photoperiod in reproductively non-responsive mice

Trainor, Brian C.; Finy, M. Sima; Nelson, Randy J.

doi:10.1016/j.yhbeh.2007.09.016

Cited by 110 publications

(119 citation statements)

References 55 publications

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“…S8). Our findings are consistent with our learning effects, and with other data demonstrating estrogens begin to affect sexual behavior and aggression ∼15 min after administration (26,27).…”

Section: Discussionsupporting

confidence: 93%

Rapid increases in immature synapses parallel estrogen-induced hippocampal learning enhancements

Phan

Suschkov

Molinaro

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

129

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Dramatic increases in hippocampal spine synapse density are known to occur within minutes of estrogen exposure. Until now, it has been assumed that enhanced spinogenesis increased excitatory input received by the CA1 pyramidal neurons, but how this facilitated learning and memory was unclear. Delivery of 17β-estradiol or an estrogen receptor (ER)-α (but not ER-β) agonist into the dorsal hippocampus rapidly improved general discrimination learning in female mice. The same treatments increased CA1 dendritic spines in hippocampal sections over a time course consistent with the learning acquisition phase. Surprisingly, estrogen-activated spinogenesis was associated with a decrease in CA1 hippocampal excitatory input, rapidly and transiently reducing CA1 AMPA activity via a mechanism likely reflecting AMPA receptor internalization and creation of silent or immature synapses. We propose that estrogens promote hippocampally mediated learning via a mechanism resembling some of the broad features of normal development, an initial overproduction of functionally immature connections being subsequently "pruned" by experience.immature synapse | short-term memory | structural plasticity | synaptic plasticity | signal-to-noise ratio E stradiol rapidly and dramatically increases hippocampal dendritic spine and synapse density within minutes of application (1-4). There is a strong correlative association between estrogeninduced spinogenesis and improvements in cognition (5); however, the relationship of these structural changes to estrogen-induced alterations in hippocampal function is unclear. Our laboratory recently reported that the density of hippocampal CA1 pyramidal dendritic spines increases very rapidly after systemic treatment with 17β-estradiol or estrogen receptor (ER) -selective agonists in ovariectomized female mice, changes that are paralleled by learning enhancements (2, 3). Estrogen-induced rapid structural changes are substantial, increasing spine density by 30-50% within 15-40 min of hormone application (1-3, 6). As a result, adult rodents can experience the addition of thousands of CA1 synapses within a span of minutes after exposure to estradiol. These effects of estrogens reproduce the changes occurring during the 4-d estrous cycle of female rodents, which include the induction of CA1 spines (7).How these processes contribute to the behavioral changes observed after estradiol treatment is not understood. Estradiol enhances excitatory neurotransmission throughout the hippocampus (8-10), and activates BDNF signaling in the mossy fiber system (11). Dendritic spines turn over more rapidly in the hippocampus than in the neocortex (12), particularly in the case of estradiol-induced spines (13). Such rapid, transient, and apparently indiscriminate increases in excitatory synapse formation would seem, at first sight, to be more likely to interfere with preexisting brain circuits and impair normal information processing than to enhance cognitive function.How then, does enhancement of spine formation lead to improved ...

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Section: Discussionsupporting

confidence: 93%

Rapid increases in immature synapses parallel estrogen-induced hippocampal learning enhancements

Phan

Suschkov

Molinaro

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

129

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“…in long (16 h light:8 h dark) and winter-like short days (8 h light:16 h dark). Estradiol injection into male P. polionotus experiencing short days increases aggressive behavior within 15 min [37] , but there is no signifi cant effect on behavior during long days. These results suggest that estradiol increases aggression during short days in mice by activation of a non-genomic mechanism, as it is generally thought that 15 min is insufficient for gene expression changes mediated by estrogen receptors [38] .…”

Section: Discussionmentioning

confidence: 93%

“…There is evidence that estradiol induces anxiolytic behavior [16,36] . The non-genomic effects of estradiol have been studied by Trainor et al [37] . Estradiol has rapid effects on the behavior of male deer mice (Peromyscus sp.)…”

Section: Discussionmentioning

confidence: 99%

Effects of testosterone and estradiol on anxiety and depressive-like behavior via a non-genomic pathway

et al. 2015

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Besides their known slow genomic effects, testosterone and estradiol have rapid effects in the brain. However, their impact on mood-related behavior is not clear. The aim of this study was to investigate the non-genomic pathway of testosterone and estradiol in the amygdala in relation to anxiety and depressive-like behavior. Sham-operated and gonadectomized male rats (GDX) supplemented with testosterone propionate, estradiol, or olive oil were used. Five minutes after administration, anxiety and depression-like behavior were tested. Estradiol increased anxiolytic behavior in the open-field test compared to the GDX group, but administration of testosterone had no significant effect. Besides, c-Fos expression in the medial nucleus of the amygdala significantly increased after testosterone treatment compared to the GDX group, while no significant difference was observed in the central and the basolateral nuclei of the amygdala in the testosterone-treated group compared to the GDX group. In conclusion, estradiol had an anxiolytic effect via a rapid pathway, but no rapid effect of testosterone on anxiety was found. Further studies elucidating whether the rapid effect is mediated by a non-genomic pathway are needed.

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“…Female-female aggression in Syrian (Fleming et al 1988) and Siberian (Scotti et al 2007) hamsters is also increased under short days. In hamsters and Peromyscus, studies using c-fos as an indirect marker of neuronal activity found no differences in c-fos expression in several brain regions between long day and short day aggression tested males (Kramer et al 2008;Trainor et al 2008), even though short day males were more aggressive. We recently used measurements of phosphorylated extracellular signalregulated kinase (pERK, also known as mitogen activated protein kinase or pMAPK) as an alternative marker of brain activity (Trainor et al 2010).…”

Section: Introductionmentioning

confidence: 91%

Effects of photoperiod and experience on aggressive behavior in female California mice

Trainor¹

2010

PsycEXTRA Dataset

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Aggressive behavior among females is observed in many species, but the mechanisms of this behavior have historically been understudied. In many species of rodents, winter-like short day photoperiods induce increased aggression levels compared to summer-like long day photoperiods. Recent reports in hamsters show that short days also increase aggression in females. We examined the effects of photoperiod on aggression in female California mice, and for the first time compare brain activity of aggression-tested female rodents under different photoperiods. We observed that female California mice were more aggressive when housed in short days versus long days. Intriguingly, we also observed that under long days female attack latency decreases with repeated testing in resident intruder tests. These data suggest that winner effects that have been described in males may also occur in females. We also used the expression of phosphorylated extracellular signal-regulated kinases (pERK) in the brain to estimate brain activity during aggression tests. pERK can alter neuronal activity in the short term and in the long term can act as a transcription factor. Using immunoblot analyses we observed that aggression-induced pERK expression in the female bed nucleus of the stria terminalis (BNST) and medial amygdala occurs under both long and short days. Thus, the mechanisms controlling increased aggression under short days are still unclear and additional study is needed.

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Rapid effects of estradiol on male aggression depend on photoperiod in reproductively non-responsive mice

Cited by 110 publications

References 55 publications

Rapid increases in immature synapses parallel estrogen-induced hippocampal learning enhancements

Rapid increases in immature synapses parallel estrogen-induced hippocampal learning enhancements

Effects of testosterone and estradiol on anxiety and depressive-like behavior via a non-genomic pathway

Effects of photoperiod and experience on aggressive behavior in female California mice

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