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Available online at Hormones and Behavior 53 (2008) 192 – 199 Rapid effects of estradiol on male aggression depend on photoperiod in reproductively non-responsive mice Brian C. Trainor a,b,⁎, M. Sima Finy b, Randy J. Nelson b a Department of Psychology, University of California, Davis, CA 95616, USA b Departments of Psychology and Neuroscience, Institute for Behavioral Medicine Research, Ohio State University, Columbus, OH 43210, USA Received 27 July 2007; revised 12 September 2007; accepted 21 September 2007 Available online 29 September 2007 In three genuses and four species of rodents, housing in winter-like short days (8L:16D) increases male aggressive behavior. In all of these species, males undergo short-day induced regression of the reproductive system. Some studies, however, suggest that the effect of photoperiod onaggression may be independent of reproductive responses. We examined the effects of photoperiod on aggressive behavior in California mice(Peromyscus californicus), which do not display reproductive responsiveness to short days. As expected, short days had no effect on plasmatestosterone. Estrogen receptor alpha and estrogen receptor beta immunostaining did not differ in the lateral septum, medial preoptic area, bednucleus of the stria terminalis, or medial amygdala. However, males housed in short days were significantly more aggressive than males housed inlong days. Similar to previous work in beach mice (Peromyscus polionotus), estradiol rapidly increased aggression when male California micewere housed in short days but not when housed in long days. These data suggest that the effects of photoperiod on aggression and estrogensignaling are independent of reproductive responses. The rapid action of estradiol on aggression in short-day mice also suggests that nongenomicmechanisms mediate the effects of estrogens in short days.
2007 Elsevier Inc. All rights reserved.
Keywords: Aggressive behavior; Peromyscus californicus; California mouse; c-fos; Nongenomic effects; Estrogen receptor alpha; Estrogen receptor beta conditions (Haemisch et al., 1994; Marashi et al., 2003). Thesestudies document that the environmental context has important The physiological bases of aggressive behavior are typically effects on the function of physiological pathways that regulate examined under constant environmental conditions. However, the environment can have important effects on aggression and Several laboratories have reported a consistent effect of can even alter the effects of specific physiological systems. For photoperiod (day length) on male aggression in rodents. In example, adverse behavioral effects associated with the short Syrian hamsters (Mesocricetus auratus) (Garrett and Campbell, form of the monoamine oxidase A (MAOA) gene are typically 1980; Jasnow et al., 2002; Caldwell and Albers, 2004), Siberian observed only in individuals who have been exposed to adverse hamsters (Phodopus sungorus) (Jasnow et al., 2000; Demas et environmental conditions (Caspi et al., 2003; Kim-Cohen et al., al., 2004; Wen et al., 2004), beach mice (Peromyscus polionotus) 2006; Frazzetto et al., 2007). In rodents, males are typically (Trainor et al., 2007a), and deer mice (Peromyscus maniculatus) more aggressive when confronted in a familiar environment (Trainor et al., 2007b), males are more aggressive in a resident– (e.g., a resident–intruder test) as compared to a neutral setting intruder test when tested in short days (8L:16D) as opposed to (Bester-Meredith et al., 1999), and males from some mouse long days (16L:8D). This effect has been considered paradox- strains are more aggressive when housed in environmentally ical, because in each of these species housing in short days enriched housing compared to the standard laboratory housing causes regression of testes and a corresponding decrease intestosterone (Jasnow et al., 2000, 2002; Trainor et al., 2006c). InSiberian hamsters there is evidence that the effect of photoperiod ⁎ Corresponding author. Department of Psychology, 1 Shields Ave., on aggression is independent of gonadal responses (Demas et al., University of California, Davis, CA 95616, USA.
E-mail address: (B.C. Trainor).
2004). Photoperiod has no significant effect on reproductive 0018-506X/$ - see front matter 2007 Elsevier Inc. All rights reserved.
doi:10.1016/j.yhbeh.2007.09.016 Author's personal copy
B.C. Trainor et al. / Hormones and Behavior 53 (2008) 192–199 physiology or aggression in CD-1 mice (Trainor et al., 2006a), estrogens regulate aggressive behavior. Estrogen receptor alpha but this stock of mice has been bred in captivity since at least the and beta are expressed in the LS, medial preoptic area (MPOA), 1920s. Recent studies in P. polionotus suggest that changes in BNST, ventromedial hypothalamus (VMH), and MEA. These estrogen signaling are involved in mediating the effect of photo- brain areas are part of a circuit that regulates social behavior period on aggression in rodents.
(Newman, 1999; Goodson, 2005), including aggression Estrogens can affect aggression in male vertebrates because (Nelson and Trainor, 2007). It was previously reported that, as aromatase present in the brain can convert androgens to estro- in P. polionotus, fadrozole increased aggression in P. californicus gens. The effects of estrogens on male aggression are variable, housed in long days (Trainor et al., 2004). In the current study, we increasing aggression in some species and decreasing aggression tested whether estradiol acts rapidly to increase aggression in in others (Trainor et al., 2006b). This could reflect differences in short-day P. californicus.
the expression of estrogen receptor (ER) subtypes. Selectivedeletion of ERα is associated with reduced male aggression in domestic mice (Ogawa et al., 1997; Scordalakes and Rissman,2003). The deletion of ERβ is generally associated with increased aggression (Ogawa et al., 1999; Nomura et al.,2006), although this effect appears to be context-dependent P. californicus were obtained from Dr. Catherine Marler (University of Wisconsin, Madison, WI, USA). California mice form monogamous mating (Nomura et al., 2002). Deletion of both receptors is associated pairs in the field (Ribble and Salvioni, 1990) and males do not respond to short with increased male aggression (Ogawa et al., 2000). In male days by reducing testes mass (Nelson et al., 1995). Males were individually P. polionotus, and P. maniculatus, ERα expression in the lateral housed and provided with filtered tap water and Teklad 8640 food (Harlan, septum (LS) and bed nucleus of the stria terminalis (BNST) is Madison, WI) ad libitum. Field studies show that male P. californicus defend increased in short days whereas ERβ expression in the BNST exclusive territories (Ribble and Salvioni, 1990), which indicates that to acertain extent, single housing approximates the social organization of young and medial amygdala (MEA) is increased in long days (Trainor unpaired males in this species. All experimental procedures were approved et al., 2007b). This led to the attractive hypothesis that changes by the Ohio State University Institutional Animal Care and Use Committee in ER expression mediate the effect of photoperiod on and animals were maintained in accordance with the recommendations of the National Institutes of Health Guide for the Care and Use of Laboratory Animals.
The estrogen receptor hypothesis was tested with hormone manipulation experiments (Trainor et al., 2007a). In male Effect of photoperiod on behavior and physiology P. polionotus, treatment with the aromatase inhibitor fadrozoleincreased aggression in long days but decreased aggression in Males (residents) were randomly assigned to be housed in long (n = 9, LD 16:8) or short (n = 7, LD 8:16) days for 8 weeks. One week before resident– short days. The estrogen receptor hypothesis was not supported intruder aggression tests, retroorbital blood samples were collected under light because the effects of fadrozole were reversed by co-treatment isoflurane anesthesia. Plasma samples were frozen at −80 °C. Resident–intruder with either ERα or ERβ selective agonists, regardless of tests were conducted 1 h after lights out (1500 EDT) under dim red light. A photoperiod. These data suggested that differential expression of group-housed, sexually inexperienced male intruder (weight matched to within estrogen receptors could not explain the effect of photoperiod on 4 g) was introduced into each resident's cage for 7 min. Observations werevideotaped and scored offline by an observer blind to treatment assignments.
aggression. Instead, it appears that photoperiod changes the One hour after aggression tests residents were anesthetized with isoflurane and molecular activity of estrogen receptors. Results from a micro- rapidly decapitated. This time course was chosen because previous studies have array experiment showed that estrogen-dependent gene expres- reported that maximal c-fos expression occurs between 1 and 2 h after sion in the BNST was decreased in short days compared to long stimulation (Kovacs and Sawchenko, 1996; Hoffman and Lyo, 2002). Brains days (Trainor et al., 2007a). Furthermore, estradiol injections were quickly removed and fixed in 5% acrolein overnight at 4 °C. Brains werethen transferred to 30% sucrose for 24 h and frozen for immunocytochemistry.
increased aggression within 15 min in male P. polionotus housed Plasma was collected from trunk blood samples to measure post-encounter in short days, but had no effect on males housed in long days.
testosterone and testes were dissected and weighed. Total testosterone was These data suggested that estrogens increase aggression in short- measured with a 125I testosterone RIA kit (DSL-4100; Diagnostic Systems day mice by activating nongenomic mechanisms, as it is Laboratories, Webster, TX). The intra-assay coefficient of variation was 2.8%.
generally thought that 15 min is insufficient time for changes Hormone concentrations were not normally distributed and were log trans-formed for statistical analyses.
in estrogen-dependent changes in gene expression to occur Immunocytochemistry for ERα and ERβ was conducted using the methods (Vasudevan and Pfaff, 2006). Together, these results suggest that of Trainor et al. (2007b). Briefly, six brains from each group were sectioned at the effect of photoperiod on aggression is independent of 40 μm on a cryostat and free-floating sections were then incubated in 1% sodium changes in estrogen receptor expression and is mediated instead borohydride in 0.1 M phosphate-buffered saline (PBS) for 10 min. Sections were by changes in receptor activity (genomic or nongenomic).
then rinsed in 20% normal goat serum and 0.3% hydrogen peroxide in PBS for20 min. Alternate sections were incubated in either primary ERα antibody In the present study we examined the effect of photoperiod (C1355, Upstate Biotechnology, concentration 1:20 K), primary ERβ (D7N, on aggression in California mice (P. californicus), a species in Invitrogen, Carlsbad, CA, concentration 1:400), or primary c-fos (rabbit anti c- which males do not regress testes when housed in short days fos, Chemicon 1:10 K) in 1% normal goat serum in 0.5% PBS + triton X (PBS (Nelson et al., 1995). We hypothesized that if the effect of TX) for 40 h at 4 °C. Sections were rinsed in PBS and incubated for 2 h with photoperiod is indeed independent of gonadal responses to short biotinylated goat–anti-rabbit antibody (1:500, Vector Laboratories, Burlingame,CA) in PBS + TX. The sections were rinsed in PBS and then incubated for 30 min days, then male California mice would increase aggressive in avidin–biotin complex (ABC Elite kit, Vector Laboratories). After rinses in behavior in short days. We also examined whether photoperiod PBS, the sections were developed in hydrogen peroxide and diaminobenzidine influences the effects of estrogen receptor expression and how for 2 min. Sections were mounted on gel-coated slides, dehydrated and Author's personal copy
B.C. Trainor et al. / Hormones and Behavior 53 (2008) 192–199 coverslipped. A Nikon E800 microscope was used to capture representative generally occur on a time scale of hours or days, whereas nongenomic effects of photomicrographs of each of the following brain areas using a mouse brain atlas estrogens can occur within minutes or seconds (Nabekura et al., 1986). Previous (Paxinos and Franklin, 2002): ventral lateral septum (bregma 0.26), BNST studies have used the delivery of water soluble cE2 to study the nongenomic (bregma 0.02), MPOA (bregma 0.02), VMH (bregma −1.70), paraventricular effects of estrogens on reproductive behavior (Cross and Roselli, 1999; Cornil nucleus (PVN, bregma −1.22), and posterodorsal MEA (bregma −1.82). In these et al., 2006). Fifteen minutes after injections males were tested in resident– areas the number of ER and c-fos immunoreactive (-ir) cells was counted using intruder aggression tests as described above.
Image J (NIMH, Bethesda, MD) by an observer unaware of treatmentassignments. We counted the number of cells in a box in the MPOA (l × w, 400 × 250 μm), LS (330 × 480 μm), BNST (500 × 350 μm), PVN (330 × 480 μm),and MEA (450 × 450 μm) similar to our previous study quantifying estrogenreceptor expression in P. polionotus and P. maniculatus (Trainor et al., 2007b). In Effects of photoperiod on physiology, receptor expression, and the VMH, the number of ERα and c-fos positive cells in a circle with a radius of 180 μm was counted. In the anterior hypothalamus (bregma −1.22) we countedc-fos positive cells (box size, 520 × 520 μm) but not ER positive cells because Photoperiod did not affect testes mass (Fig. 1A; t14 = 1.15, there are no ERα or ERβ cells in this region of the brain in this species. The p = 0.27), baseline testosterone concentrations (Fig. 1B, t aggressive behavior data and cell counts from the males assigned to the long-day group in this study were also analyzed (as virgin males) in the accompanying p = 0.42), or the number of ERα-ir cells in the LS (Figs. 2A and B, paper examining the effect of parental experience on aggression and estrogen t10 = 0.28, p = 0.80), BNST (t10 = 1.26, p = 0.26), MPOA (Figs. 2C receptor expression (Trainor et al., 2008-this issue).
and D, t10 = 0.17, p = 0.90), MEA (t10 = 1.1, p = 0.28), PVN(t10 = 0.28, p = 0.80), or VMH (t10 = 1.40, p = 0.2). There was Effects of acute estradiol injections in long days and short days also no effect of photoperiod on the number of ERβimmunostained cells in the BNST (Figs. 2E and F, t10 = 0.96, Male California mice were randomly assigned to be housed in long or short p = 0.36), MPOA (t days for 8 weeks. All males were then bilaterally castrated under isoflurane 10 = 0.74, p = 0.48), PVN (t10 = 1.11, p = 0.26), anesthesia. Each male was implanted with a Silastic implant (1.47 mm i.d.; or MEA (Figs. 2G and H, t10 = 0.54, p = 0.60).
1.96 mm o.d.) packed with 1 mm of testosterone. All males were also implanted Despite the absence of differences in estrogen receptor with an osmotic minipump (model 2002, Alzet, Palo Alto, CA) containing expression or testosterone concentrations, males housed in fadrozole (0.25 mg/kg/day), a potent aromatase inhibitor. After surgery all short days were significantly more aggressive than males animals were treated with an s.c. injection of buprenorphine (0.38 mg/kg). After housed in long days. Males housed in short days showed 10 days, all males were tested in a resident–intruder aggression test. Fifteenminutes before testing, each male was injected with either saline or 100 μg/kg shorter attack latencies (Fig. 1C, t14 = 2.90, p = 0.01) and more cyclodextrin conjugated estradiol (cE offensive attacks (Fig. 1D, t 2). The genomic effects of estrogens 14 = 2.23, p = 0.04) in aggression Fig. 1. Effect of photoperiod on physiology and behavior. There was no effect of photoperiod on testes mass (A) or baseline plasma testosterone (B). In resident–intruder aggression tests, males housed in short days showed significantly shorter mean attack latency (C) and increased bites (D) compared to males housed in longdays. ⁎p b 0.05. For all panels; long days n = 9, short days n = 7.

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B.C. Trainor et al. / Hormones and Behavior 53 (2008) 192–199 Fig. 2. Representative photomicrographs of estrogen receptor alpha immunoreactivity in long days (A, C) and short days (B, D) in the lateral septum (A, B) and medialpreoptic area (C, D). Representative photomicrographs of estrogen receptor beta immunoreactivity in long days (E, G) and short days (F, H) in the bed nucleus of thestria terminalis (E, F) and medial amygdala (G, H). Abbreviations: anterior commissure (ac), third ventricle (3v). Scale bars = 100 μm.
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B.C. Trainor et al. / Hormones and Behavior 53 (2008) 192–199 tests than males housed in long days. In general the frequency were no significant photoperiod by injection interactions (all of boxing in long-day (mean ± SE, 6.8 ± 2.4) and short-day p's N 0.16), planned comparisons showed that the effects of (5.4 ± 2.2) mice was low, and unaffected by photoperiod (t14 = estradiol injections were stronger when mice were housed in 0.69, p = 0.41).
short days. Estradiol injections caused a significant increase in One hour after aggression tests, males housed in short days bites in short (Fig. 3A, p b 0.01), but not long days (p N 0.05).
(0.38 ± 0.1 ng/ml) had significantly higher testosterone concen- Similarly, estradiol injections caused a significant decrease in trations compared to long-day males (0.12 ± 0.2 ng/ml, t14 = attack latency in short days (Fig. 3B, p b 0.05) but not long days 2.26, p = 0.04). In the MPOA there were more c-fos positive (p N 0.05). There were no significant differences for boxing cells in short-day males compared to long-day males (Supple- behavior (Fig. 3C).
mentary Table 1, t10 = 2.80, p = 0.02). There were no significantdifferences in c-fos positive cells in any other brain region.
Rapid effects of estradiol on aggression The biology of P. californicus allowed us to test hypotheses on the relationship between photoperiod and aggression from a We detected significant main effects of estradiol injections unique perspective. The effects of photoperiod on aggression in on biting (F1,32 = 4.94, p b 0.05) and attack latency (F1,32 = 4.37, P. californicus occur in the absence of gonadal regression, a result p b 0.05), but not boxing (F1,32 = 0.1, p N 0.05). Although there that supports the hypothesis that the effect of photoperiod onaggression is independent of changes in gonadal hormones(Demas et al., 2004; Wen et al., 2004). We also observed thatphotoperiod affected aggression in the absence of changes in ERαand ERβ expression. This result supports the hypothesisdeveloped in P. polionotus that the effects of photoperiod onaggression are independent of changes in ER expression (Trainoret al., 2007a). Finally, we observed that in P. californicus estradiolinjections act rapidly to increase aggression in mice housed inshort days but not long days. These data suggest that estrogensincrease aggression by activating nongenomic pathways in short,but not long days. These data indicate that the environment hasimportant effects on how estrogens regulate aggression.
Previously, the effect of photoperiod on aggression had only been observed in species that undergo gonadal regression andreduced testosterone when housed in short days (Matochiket al., 1986; Jasnow et al., 2000, 2002; Caldwell and Albers,2004; Trainor et al., 2007b). Our results demonstrate that theeffect of photoperiod on aggression can be dissociated fromreproductive responses, because P. californicus were more ag-gressive in short days in the absence of reproductive changes.
A previous study reported that exogenous testosterone admin-istered to short-day Siberian hamsters decreased aggressivebehavior in a resident–intruder test (Jasnow et al., 2000), but asubsequent report showed that short-day non-responders (whichdo not decrease testes size or testosterone production in shortdays) are just as aggressive as short-day males with regressedtestes (Wen et al., 2004). Our results suggest that the effect ofphotoperiod on aggression occurs independently of changes ingonadal testosterone. Studies in hamsters suggest that the pri-mary source of aromatizable androgen in Peromyscus may beproduced in the brain, most likely from adrenal steroids such asdehydroepiandrosterone (DHEA) (Demas et al., 2004). DHEAcan be converted to the aromatizable androgen androsteindioneby 3 β-hydroxysteroid dehydrogenase.
In closely related P. polionotus and P. maniculatus, increased aggression in short days is associated with increased expression Fig. 3. Rapid effects of estradiol on aggression in a resident–intruder test.
of ERα and decreased expression of ERβ (Trainor et al., Estradiol injections (100 μg/kg) administered 15 min before aggression tests 2007b). In contrast, we observed in the present study that caused a significant increase in bites (A) and a decrease in attack latency (B) in increased aggression in short days occurs in the absence of short-day males but not long-day males. There was no effect of photoperiod orestradiol injections on boxing behavior (C). ⁎⁎p b 0.01, ⁎p b 0.05.
differences in ERα and ERβ expression in the hypothalamus Author's personal copy
B.C. Trainor et al. / Hormones and Behavior 53 (2008) 192–199 and limbic system. It has been hypothesized that the effect of These findings suggest that corticosterone might inhibit aggres- photoperiod on aggression is independent of changes in ERα or sion in rats via genomic processes and increase aggression via ERβ in the brain (Trainor et al., 2007a), and the current ex- nongenomic processes, similar to how estrogens appear to perimental results are consistent with this hypothesis. Although regulate aggression in Peromyscus. An intriguing possibility is we have not tested this directly, we suspect that the effect of that nongenomic estrogen receptor and glucocorticoid receptor photoperiod on ERα and ERβ expression in P. polionotus is activity may tap into similar second messenger systems to related to changes in testosterone and resulting negative feed- facilitate aggressive behavior. Presently, it is unclear which back (Clancy and Michael, 1994). We observed no effect of pathways mediate the rapid actions of estrogens or glucocorti- estradiol injections on aggression in P. californicus housed in coids on aggressive behavior.
long days whereas studies of wild-type Mus musculus (housed We have demonstrated in two species of Peromyscus that in a 12-h light cycle) report that a similar dose of estradiol estrogens act rapidly to increase aggression in short days and increases aggression in males (Nomura et al., 2006). These that this effect is weaker or absent in long days. A previous contrasting results could be attributed to several factors. First, in study reported that estrogens inhibited aggression in P.
the Nomura study estradiol was administered over a 3-week californicus housed in long days (14 L) (Trainor et al., 2004), period via implants whereas we conducted our tests 15 min after indicating that a photoperiod-mediated reversal of the effects of a subcutaneous injection. A 3-week time period is sufficient to estrogens on aggression in Peromyscus is not limited to a single induce genomic changes mediated by estrogen receptors, and species. It remains unspecified how differences in day length most researchers agree that 15 min is not enough time for can exert such a profound effect on hormone action. One genomic effects to occur. In P. californicus, treatment with intriguing possibility is suggested by in vitro studies. In cell fadrozole for 10 days is associated with increased aggression.
culture, melatonin interacts with the DNA binding domain of This suggests that estrogens may indeed affect aggression in ERα and inhibits its transcriptional activity (Rato et al., 1999; P. californicus by affecting gene expression, but in the opposite Kiefer et al., 2002, 2005). Mice housed in short days have direction observed in M. musculus. This raises a second pos- increased melatonin concentrations in the brain for prolonged sibility. Species differences in estrogen receptor expression periods of time compared to mice housed in long days, and may contribute to differences in how estrogens affect aggres- recent data suggest that classical estrogen receptors can have sion. For example, ERα positive cells are present in the PVN of nongenomic effects (Abraham et al., 2004). One possible P. californicus but not M. musculus, whereas ERα positive cells explanation for our results is that melatonin may inhibit the are present in the AHA of M. musculus but not P. californicus transcriptional activity of classical estrogen receptors without (Merchenthaler et al., 2004). The AHA is known to have im- interfering with nongenomic activity. This would explain why portant effects on aggressive behavior in rodents (Ferris et al., nongenomic action of estradiol is more prevalent in short days.
1997), so the absence of ERα in this area may influence how Another possibility is that melatonin could affect the secretion of estrogens affect aggression in Peromyscus. The availability adrenal hormones that could provide the substrate for aromatiz- of selective ER agonists should facilitate examination of able androgen in the brain. Studies in M. musculus (Paterson and the effects of the two ER subtypes on behavior in different Vickers, 1981) and P. sungorous (Demas et al., 2004) have species that exhibit different distributions of estrogen receptor demonstrated that the facilitating effect of melatonin on male aggression can be blocked via adrenalectomy. It is also possible Estradiol acts within 15 min to increase aggression in (and perhaps likely) that melatonin affects aggressive behavior P. californicus housed in short days, suggesting that estrogens by working at multiple levels of hormone function act nongenomically to increase aggression. This result is con- sistent with a previous study in P. polionotus which reported The effects of photoperiod on aggressive behavior were first that estradiol injections increased bites in short- but not long- described in species that exhibit reproductive suppression in day mice (Trainor et al., 2007a). It is thought that such rapid short days (Garrett and Campbell, 1980; Jasnow et al., 2000).
behavioral effects of estradiol must be mediated by nongenomic Our observations in P. californicus, a species that does not processes (Nilsson et al., 2001; Vasudevan and Pfaff, 2006).
exhibit reproductive inhibition in short days, suggest that these Previous studies showed that estradiol acts rapidly to increase findings may be applicable to a wider array of species, male mating behavior in rats (Cross and Roselli, 1999) and quail including humans. There is some evidence that components (Cornil et al., 2006), but these effects did not differ from those of aggression in humans exhibit seasonal rhythms. Patients observed in response to systemic estradiol treatment. Non- diagnosed with seasonal affective disorder tend to be more genomic effects of glucocorticoids on behavior have been likely to exhibit anger attacks compared to patients diagnosed reported in several species. In rough skinned newts (Taricha with non-seasonal depression (Winkler et al., 2006). Anger and granulosa), corticosterone rapidly inhibits male mating behav- hostility scores, as measured using Emotion Rating scales ior (Moore and Miller, 1984), presumably by binding to (Beck et al., 1961), have also reported seasonal variation, with glucocorticoid receptors positioned at the membrane (Orchinik higher scores being recorded in winter (Harmatz et al., 2000).
et al., 1991). Corticosterone also acts rapidly to increase ag- Accumulating evidence indicates that the effect of photoperiod gression in rats (Mikics et al., 2004) and mice (Poole and Brain, on aggression is decoupled from reproductive responses, sug- 1974). In contrast, over longer time frames corticosterone gesting that hamsters and Peromyscus may be effective models appears to inhibit rat aggression (Haller et al., 2001, 2004).
for studying seasonal changes in aspects of human behavior.
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B.C. Trainor et al. / Hormones and Behavior 53 (2008) 192–199 Jasnow, A.M., Huhman, K.L., Bartness, T.J., Demas, G.E., 2000. Short-day increases in aggression are inversely related to circulating testosteroneconcentrations in male Siberian hamsters (Phodopus sungorus). Horm.
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supported by NIH MH076313 to B.C.T., SBS Undergraduate Jasnow, A.M., Huhman, K.L., Bartness, T.J., Demas, G.E., 2002. Short days and Research Award to M.S.F., and NIH MH57535 to R.J.N.
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