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Involvement of pregnane xenobiotic receptor in mating-induced allopregnanolone formation in the midbrain and hippocampus and brain-derived neurotrophic factor in the hippocampus among female rats

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Abstract

Rationale

Given that the pregnane neurosteroid, 5α-pregnan-3α-ol-20-one (3α,5α-THP), is increased following behavioral challenges (e.g., mating), and that there is behavioral-induced biosynthesis of 3α,5α-THP in midbrain and mesocorticolimbic structures, 3α,5α-THP likely has a role in homeostasis and motivated reproduction and reproduction-related behaviors (e.g., affect, affiliation). The role of pregnane xenobiotic receptor (PXR), involved in cholesterol metabolism, for these effects is of continued interest.

Objectives

We hypothesized that there would be differences in brain levels of 3α,5α-THP following varied behavioral experiences, an effect abrogated by knockdown of PXR in the midbrain.

Methods

Proestrous rats were infused with PXR antisense oligonucleotides (AS-ODNs) or vehicle to the ventral tegmental area before different behavioral manipulations and assessments. Endpoints were expression levels of PXR in the midbrain, 3α,5α-THP, and ovarian steroids (estradiol, progesterone, dihydroprogesterone) in the midbrain, striatum, hippocampus, hypothalamus, prefrontal cortex, and plasma.

Results

Across experiments, knocking down PXR reduced PXR expression and 3α,5α-THP levels in the midbrain and hippocampus. There were differences in terms of the behavioral manipulations, such that paced mating had the most robust effects to increase 3α,5α-THP levels and reduce open field exploration and social interaction. An additional question that was addressed is whether brain-derived neurotrophic factor (BDNF) is a downstream factor for regulating effects of behavioral-induced 3α,5α-THP biosynthesis. Rats infused with PXR AS-ODNs had lower levels of BDNF in the hippocampus.

Conclusion

Thus, PXR may be a regulator of mating-induced 3α,5α-THP formation and behavioral changes and neural plasticity, such as BDNF.

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References

  • Agís-Balboa RC, Pinna G, Pibiri F, Kadriu B, Costa E, Guidotti A (2007) Down-regulation of neurosteroid biosynthesis in corticolimbic circuits mediates social isolation-induced behavior in mice. Proc Natl Acad Sci U S A 104:18736–18741

    Article  PubMed Central  PubMed  Google Scholar 

  • Aguirre CC, Baudry M (2009) Progesterone reverses 17beta-estradiol-mediated neuroprotection and BDNF induction in cultured hippocampal slices. Eur J Neurosci 29:447–454

    Article  PubMed Central  PubMed  Google Scholar 

  • Aguirre C, Jayaraman A, Pike C, Baudry M (2010) Progesterone inhibits estrogen-mediated neuroprotection against excitotoxicity by down-regulating estrogen receptor-beta. J Neurochem 115:1277–1287

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Akwa Y, Purdy RH, Koob GF, Britton KT (1999) The amygdala mediates the anxiolytic-like effect of the neurosteroid allopregnanolone in rat. Behav Brain Res 106:119–125

    Article  CAS  PubMed  Google Scholar 

  • Angelucci F, Aloe L, Iannitelli A, Gruber SH, Mathé AA (2005) Effect of chronic olanzapine treatment on nerve growth factor and brain-derived neurotrophic factor in the rat brain. Eur Neuropsychopharmacol 15:311–317

    Article  CAS  PubMed  Google Scholar 

  • Arzate DM, Portillo W, Corona R, Paredes RG (2012) Repeated paced mating promotes the arrival of more newborn neurons in the main and accessory olfactory bulbs of adult female rats. Neuroscience. doi:10.1016/j.neuroscience.2012.12.014

    PubMed  Google Scholar 

  • Barbaccia ML, Roscetti G, Trabucchi M, Mostallino MC, Concas A, Purdy RH, Biggio G (1996) Time-dependent changes in rat brain neuroactive steroid concentrations and GABAA receptor function after acute stress. Neuroendocrinology 63:166–172

  • Barde YA, Edgar D, Thoenen H (1982) Purification of a new neurotrophic factor from mammalian brain. EMBO J 1(5):49–53

    Google Scholar 

  • Bath KG, Chuang J, Spencer-Segal JL, Amso D, Altemus M, McEwen BS, Lee FS (2012) Variant brain-derived neurotrophic factor (Valine66Methionine) polymorphism contributes to developmental and estrous stage-specific expression of anxiety-like behavior in female mice. Biol Psychiatry 72:499–504

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Bauer B, Hartz AM, Fricker G, Miller DS (2004) Pregnane X receptor up-regulation of P-glycoprotein expression and transport function at the blood-brain barrier. Mol Pharmacol 66:413–419

    CAS  PubMed  Google Scholar 

  • Bauer B, Yang X, Hartz AM, Olson ER, Zhao R, Kalvass JC, Pollack GM, Miller DS (2006) In vivo activation of human pregnane X receptor tightens the blood-brain barrier to methadone through P-glycoprotein up-regulation. Mol Pharmacol 70:1212–9

  • Bimonte-Nelson HA, Granholm AC, Nelson ME, Moore AB (2008) Patterns of neurotrophin protein levels in male and female Fischer 344 rats from adulthood to senescence: how young is “young” and how old is “old”? Exp Aging Res 34:13–26

    Article  PubMed Central  PubMed  Google Scholar 

  • Bimonte-Nelson HA, Nelson ME, Granholm AC (2004) Progesterone counteracts estrogen-induced increases in neurotrophins in the aged female rat brain. Neuroreport 15:2659–2663

    Article  CAS  PubMed  Google Scholar 

  • Bortolato M, Devoto P, Roncada P, Frau R, Flore G, Saba P, Pistritto G, Soggiu A, Pisanu S, Zappala A, Ristaldi MS, Tattoli M, Cuomo V, Marrosu F, Barbaccia ML (2011) Isolation rearing-induced reduction of brain 5α-reductase expression: relevance to dopaminergic impairments. Neuropharmacology 60:1301–1308

    Article  CAS  PubMed  Google Scholar 

  • Brambilla F, Mellado C, Alciati A, Pisu MG, Purdy RH, Zanone S, Perini G, Serra M, Biggio G (2005) Plasma concentrations of anxiolytic neuroactive steroids in men with panic disorder. Psychiatry Res 135:185–190

    Article  CAS  PubMed  Google Scholar 

  • Brunton PJ, Russell JA (2011) Neuroendocrine control of maternal stress responses and fetal programming by stress in pregnancy. Prog Neuropsychopharmacol Biol Psychiatry 35:1178–1191

    Article  CAS  PubMed  Google Scholar 

  • Camacho FJ, García-Horsman P, Paredes RG (2009) Hormonal and testing conditions for the induction of conditioned place preference by pacedmating. Horm Behav 56:410–415

    Article  CAS  PubMed  Google Scholar 

  • Causing CG, Gloster A, Aloyz R, Bamji SX, Chang E, Fawcett J, Kuchel G, Miller FD (1997) Synaptic innervation density is regulated by neuron-derived BDNF. Neuron 18:257–267

    Article  CAS  PubMed  Google Scholar 

  • Corona R, Larriva-Sahd J, Paredes RG (2011) Paced-mating increases the number of adult new born cells in the internal cellular (granular) layer of the accessory olfactory bulb. PLoS One 6:e19380

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Dong E, Matsumoto K, Uzunova V, Sugaya I, Takahata H, Nomura H, Watanabe H, Costa E, Guidotti A (2001) Brain 5alpha-dihydroprogesterone and allopregnanolone synthesis in a mouse model of protracted social isolation. Proc Natl Acad Sci U S A 98:2849–2854

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Duman RS, Monteggia LM (2006) A neurotrophic model for stress-related mood disorders. Biol Psychiatry 59:1116–1127

    Article  CAS  PubMed  Google Scholar 

  • Dussault I, Forman BM (2002) The nuclear receptor PXR: a master regulator of “homeland” defense. Crit Rev Eukaryot Gene Expr 12:53–64

    Article  CAS  PubMed  Google Scholar 

  • Engler-Chiurazzi E, Tsang C, Nonnenmacher S, Liang WS, Corneveaux JJ, Prokai L, Huentelman MJ, Bimonte-Nelson HA (2011) Tonic premarin dose-dependently enhances memory, affects neurotrophin protein levels and alters gene expression in middle-aged rats. Neurobiol Aging 32:680–697

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Francis GA, Fayard E, Picard F, Auwerx J (2002) Nuclear receptors and the control of metabolism. Annu Rev Physiol 65:261–311

    Article  PubMed  Google Scholar 

  • Franklin TB, Perrot-Sinal TS (2006) Sex and ovarian steroids modulate brain-derived neurotrophic factor (BDNF) protein levels in rat hippocampus under stressful and non-stressful conditions. Psychoneuroendocrinology 31:38–48

    Article  CAS  PubMed  Google Scholar 

  • Frye CA (2011) Novel substrates for, and sources of, progestogens for reproduction. J Neuroendocrinol 23:961–973

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Frye CA, Erskine MS (1990) Influence of time of mating and paced copulation on induction of pseudopregnancy in cyclic female rats. J Reprod Fertil 90:375–385

    Article  CAS  PubMed  Google Scholar 

  • Frye CA, Bayon LE, Pursnani NK, Purdy RH (1998) The neurosteroids, progesterone and 3alpha,5alpha-THP, enhance sexual motivation, receptivity, and proceptivity in female rats. Brain Res 808:72–83

    CAS  PubMed  Google Scholar 

  • Frye CA, Koonce CJ, Walf AA (2014) Role of pregnane xenobiotic receptor in the midbrain ventral tegmental area for estradiol- and 3α,5α-THP-facilitated lordosis of female rats. Psychopharmacology (in press)

  • Frye CA, Koonce CJ, Walf AA, Rusconi JC (2013a) Motivated behaviors and levels of 3α,5α-THP in the midbrain are attenuated by knocking down expression of pregnane xenobiotic receptor in the midbrain ventral tegmental area of proestrous rats. J Med Sex 10:1692–1706

    Article  CAS  Google Scholar 

  • Frye CA, Koonce CJ, Walf AA (2013b) Progesterone, compared to medroxyprogesterone acetate, to C57BL/6, but not 5α-reductase mutant, mice enhances object recognition and placement memory and is associated with higher BDNF levels in the hippocampus and cortex. Neurosci Lett 551:53–57

    Article  CAS  PubMed  Google Scholar 

  • Frye CA, Rhodes ME (2005) Estrogen-priming can enhance progesterone's anti-seizure effects in part by increasing hippocampal levels of allopregnanolone.  Pharmacol Biochem Behav 81:907–16

  • Frye CA, Walf AA (2004) Estrogen and/or progesterone administered systemically or to the amygdala can have anxiety-, fear-, and pain-reducing effects in ovariectomized rats. Behav Neurosci 118:306–313

    Article  CAS  PubMed  Google Scholar 

  • Frye CA, Walf AA, Paris JJ (2010) Conjugated equine estrogen, with medroxyprogesterone acetate, enhances formation of 5α-reduced progestogens and reduces anxiety-like behavior of middle-aged rats. Behav Pharmacol 21:530–539

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • García-Horsman SP, Agmo A, Paredes RG (2008) Infusions of naloxone into the medial preoptic area, ventromedial nucleus of the hypothalamus, and amygdala block conditioned place preference induced by paced mating behavior. Horm Behav 54:709–716

    Article  PubMed  Google Scholar 

  • Geick A, Eichelbaum M, Burk O (2001) Nuclear receptor response elements mediate induction of intestinal MDR1 by rifampin. J Biol Chem 276:14581–14587

    Article  CAS  PubMed  Google Scholar 

  • Genazzani AR, Stomati M, Bernardi F, Luisi S, Casarosa E, Puccetti S, Genazzani AD, Palumbo M, Luisi M (2004) Conjugated equine estrogens reverse the effects of aging on central and peripheral allopregnanolone and beta-endorphin levels in female rats. Fertil Steril 81:757–766

    Article  CAS  PubMed  Google Scholar 

  • Gibbs RB (1998) Levels of trkA and BDNF mRNA, but not NGF mRNA, fluctuate across the estrous cycle and increase in response to acute hormone replacement. Brain Res 787:259–268

    CAS  PubMed  Google Scholar 

  • González SL, Labombarda F, González Deniselle MC, Guennoun R, Schumacher M, De Nicola AF (2004) Progesterone up-regulates neuronal brain-derived neurotrophic factor expression in the injured spinal cord. Neuroscience 125:605–614

    Article  PubMed  Google Scholar 

  • Gonzalez Deniselle MC, Garay L, Gonzalez S, Saravia F, Labombarda F, Guennoun R, Schumacher M, De Nicola AF (2007) Progesterone modulates brain-derived neurotrophic factor and choline acetyltransferase in degenerating Wobbler motoneurons. Exp Neurol 203:406–414

    Article  CAS  PubMed  Google Scholar 

  • González-Flores O, Camacho FJ, Domínguez-Salazar E, Ramírez-Orduna JM, Beyer C, Paredes RG (2004) Progestins and place preference conditioning after paced mating. Horm Behav 46:151–157

    Article  PubMed  Google Scholar 

  • Holder MK, Mong JA (2010) Methamphetamine enhances paced mating behaviors and neuroplasticity in the medial amygdala of female rats. Horm Behav 58:519–525

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Jodhka PK, Kaur P, Underwood W, Lydon JP, Singh M (2009) The differences in neuroprotective efficacy of progesterone and medroxyprogesterone acetate correlate with their effects on brain-derived neurotrophic factor expression. Endocrinology 150:3162–3168

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Klein AB, Williamson R, Santini MA, Clemmensen C, Ettrup A, Rios M, Knudsen GM, Aznar S (2011) Blood BDNF concentrations reflect brain-tissue BDNF levels across species. Int J Neuropsychopharmacol 14:347–353

    Article  CAS  PubMed  Google Scholar 

  • Kliewer SA, Goodwin B, Willson TM (2002) The nuclear pregnane X receptor: a key regulator of xenobiotic metabolism. Endocr Rev 23:687–702

    Article  CAS  PubMed  Google Scholar 

  • Lamba V, Yasuda K, Lamba JK, Assem M, Davila J, Strom S, Schuetz EG (2004) PXR (NR1I2): splice variants in human tissues, including brain, and dentification of neurosteroids and nicotine as PXR activators. Toxicol Appl Pharmacol 199:251–265.10

  • Lieberwirth C, Liu Y, Jia X, Wang Z (2012) Social isolation impairs adult neurogenesis in the limbic system and alters behaviors in female prairie voles. Horm Behav 62:357–366

    Article  PubMed Central  PubMed  Google Scholar 

  • Lieberwirth C, Wang Z (2012) The social environment and neurogenesis in the adult mammalian brain. Front Hum Neurosci 6:118

    Article  PubMed Central  PubMed  Google Scholar 

  • Llidó A, Mòdol L, Darbra S, Pallarès M (2013) Interaction between neonatal allopregnanolone administration and early maternal separation: effects on adolescent and adult behaviors in male rat. Horm Behav S0018-506X(13):00037-8

    Google Scholar 

  • Lorenz L, Dang J, Misiak M, Tameh Abolfazl A, Beyer C, Kipp M (2009) Combined 17beta-oestradiol and progesterone treatment prevents neuronal cell injury in cortical but not midbrain neurones or neuroblastoma cells. J Neuroendocrinol 21:841–849

    Article  CAS  PubMed  Google Scholar 

  • Ma X, Idle JR, Gonzalez FJ (2008) The pregnane X receptor: from bench to bedside. Expert Opin Drug Metab Toxicol 4:895–908

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Marini S, Nannelli A, Sodini D, Dragoni S, Valoti M, Longo V, Gervasi PG (2007) Expression, microsomal and mitochondrial activities of cytochrome P450 enzymes in brain regions from control and phenobarbital-treated rabbits. Life Sci 80:910–917

    Article  CAS  PubMed  Google Scholar 

  • Matsumoto K, Uzunova V, Pinna G, Taki K, Uzunov DP, Watanabe H, Mienville JM, Guidotti A, Costa E (1999) Permissive role of brain allopregnanolone content in the regulation of pentobarbital-induced righting reflex loss. Neuropharmacology 38:955–963

    Article  CAS  PubMed  Google Scholar 

  • Mellon SH, Gong W, Schonemann MD (2008) Endogenous and synthetic neurosteroids in treatment of Niemann-Pick type C disease. Brain Res Rev 57:410–420

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Meyer M, Gonzalez Deniselle MC, Gargiulo-Monachelli G, Garay LI, Schumacher M, Guennoun R, De Nicola AF (2012) Progesterone effects on neuronal brain-derived neurotrophic factor and glial cells during progression of Wobbler mouse neurodegeneration. Neuroscience 201:267–279

    Article  CAS  PubMed  Google Scholar 

  • Mòdol L, Darbra S, Pallarès M (2011) Neurosteroids infusion into the CA1 hippocampal region on exploration, anxiety-like behaviour and aversive learning. Behav Brain Res 222:223–229

    Article  PubMed  Google Scholar 

  • Naert G, Maurice T, Tapia-Arancibia L, Givalois L (2007) Neuroactive steroids modulate HPA axis activity and cerebral brain-derived neurotrophic factor (BDNF) protein levels in adult male rats. Psychoneuroendocrinology 32:1062–1078

    Article  CAS  PubMed  Google Scholar 

  • National Research Council (US) Committee on Guidelines for the Use of Animals in Neuroscience and Behavioral Research (2003) Guidelines for the Care and Use of Mammals in Neuroscience and Behavioral Research.  Washington (DC): National Academies Press (US)

  • Nelson M, Pinna G (2011) S-Norfluoxetine microinfused into the basolateral amygdala increases allopregnanolone levels and reduces aggression in socially isolated mice. Neuropharmacology 60:1154–1159

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Nilsen J, Brinton RD (2002) Impact of progestins on estrogen-induced neuroprotection: synergy by progesterone and 19-norprogesterone and antagonism by medroxyprogesterone acetate. Endocrinology 143:205–212

    Article  CAS  PubMed  Google Scholar 

  • Nin MS, Martinez LA, Pibiri F, Nelson M, Pinna G (2011) Neurosteroids reduce social isolation-induced behavioral deficits: a proposed link with neurosteroid-mediated upregulation of BDNF expression. Front Endocrinol 2:73

    Article  Google Scholar 

  • Nyuyki KD, Waldherr M, Baeuml S, Neumann ID (2011) Yes, I am ready now: differential effects of paced versus unpaced mating on anxiety and central oxytocin release in female rats. PLoS One 6:e23599

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Ott M, Fricker G, Bauer B (2009) Pregnane X receptor (PXR) regulates P-glycoprotein at the blood–brain barrier: functional similarities between pig and human PXR. J Pharmacol Exp Ther 329:141–149

    Article  CAS  PubMed  Google Scholar 

  • Paris JJ, Brunton PJ, Russell JA, Frye CA (2011) Immune stress in late pregnant rats decreases length of gestation and fecundity, and alters later cognitive and affective behaviour of surviving pre-adolescent offspring. Stress 14:652–664

    CAS  PubMed Central  PubMed  Google Scholar 

  • Paxinos G, Watson C (1986) The rat brain. Academic Press, New York

    Google Scholar 

  • Pibiri F, Nelson M, Guidotti A, Costa E, Pinna G (2008) Decreased corticolimbic allopregnanolone expression during social isolation enhances contextual fear: a model relevant for posttraumatic stress disorder. Proc Natl Acad Sci U S A 105:5567–5572

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Pinna G, Agis-Balboa RC, Pibiri F, Nelson M, Guidotti A, Costa E (2008) Neurosteroid biosynthesis regulates sexually dimorphic fear and aggressive behavior in mice. Neurochem Res 33:1990–2007

    Article  CAS  PubMed  Google Scholar 

  • Pinna G, Rasmusson AM (2012) Up-regulation of neurosteroid biosynthesis as a pharmacological strategy to improve behavioural deficits in a putative mouse model of post-traumatic stress disorder. J Neuroendocrinol 24:102–116

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Pluchino N, Russo M, Santoro AN, Litta P, Cela V, Genazzani AR (2013) Steroids hormones and BDNF. Neuroscience 3(239):271–279

    Article  Google Scholar 

  • Porcu P, Mostallino MC, Sogliano C, Santoru F, Berretti R, Concas A (2012) Long-term administration with levonorgestrel decreases allopregnanolone levels and alters GABA(A) receptor subunit expression and anxiety-like behavior. Pharmacol Biochem Behav 102:366–372

    Article  CAS  PubMed  Google Scholar 

  • Pruginin-Bluger M, Shelton DL, Kalcheim C (1997) A paracrine effect for neuron-derived BDNF in development of dorsal root ganglia: stimulation of Schwann cell myelin protein expression by glial cells. Mech Dev 61:99–111

    Article  CAS  PubMed  Google Scholar 

  • Purdy RH, Morrow AL, Moore PH Jr, Paul SM (1991) Stress-induced elevations of gamma-aminobutyric acid type A receptor-active steroids in the rat brain. Proc Natl Acad Sci U S A 88(10):4553–4557

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Santoru F, Berretti R, Locci A, Porcu P, Concas A (2014) Decreased allopregnanolone induced by hormonal contraceptives is associated with a reduction in social behavior and sexual motivation in female rats. Psyhcopharmacology, under consideration

  • Serra M, Pisu MG, Floris I, Floris S, Cannas E, Mossa A, Trapani G, Latrofa A, Purdy RH, Biggio G (2004) Social isolation increases the response of peripheral benzodiazepine receptors in the rat. Neurochem Int 45:141–148

    Article  CAS  PubMed  Google Scholar 

  • Singh M, Su C (2013) Progesterone, brain-derived neurotrophic factor and neuroprotection. Neuroscience 239:84–91

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Vallée M, Rivera JD, Koob GF, Purdy RH, Fitzgerald RL (2000) Quantification of neurosteroids in rat plasma and brain following swim stress and allopregnanolone administration using negative chemical ionization gas chromatography/mass spectrometry. Anal Biochem 287:153–166

    Article  PubMed  Google Scholar 

  • Xu DX, Wei W, Sun MF, Wei LZ, Wang JP (2005) Melatonin attenuates lipopolysaccharide-induced down-regulation of pregnane X receptor and its target gene CYP3A in mouse liver. J Pineal Res 38:27–34

    Article  CAS  PubMed  Google Scholar 

  • Yao J, Chen S, Cadenas E, Brinton RD (2011) Estrogen protection against mitochondrial toxin-induced cell death in hippocampal neurons: antagonism by progesterone. Brain Res 16(1379):2–10

    Google Scholar 

  • Zimmerberg B, Blaskey LG (1998) Prenatal stress effects are partially ameliorated by prenatal administration of the neurosteroidallopregnanolone. Pharmacol Biochem Behav 59:819–827

    Article  CAS  PubMed  Google Scholar 

  • Zhang B, Xie W, Krasowski MD (2008) PXR: a xenobiotic receptor of diverse function implicated in pharmacogenetics. Pharmacogenomics 9:1695–1709

    Article  CAS  PubMed Central  PubMed  Google Scholar 

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Acknowledgments

Research herein was supported by grants from the National Institute of Mental Health (MH0676980; RMH067698B). Technical assistance, provided by Drs. Paris and Rusconi, and Julianne Power, Anthony Santarelli, Eric Selke, Jennifer Torgersen, and Zhenhong Zhao, is greatly appreciated.

Conflict of interest

All authors report that they have no conflicts of interest (financial or otherwise) that would bias them to the outcome of these experiments.

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Authors and Affiliations

  1. Department of Psychology, The University at Albany-SUNY, Life Sciences 01058, 1400 Washington Avenue, Albany, NY, 12222, USA

    C. A. Frye, C. J. Koonce & A. A. Walf

  2. Department of Biological Sciences, The University at Albany-SUNY, Life Sciences 01058, 1400 Washington Avenue, Albany, NY, 12222, USA

    C. A. Frye

  3. The Center for Neuroscience Research, The University at Albany-SUNY, Life Sciences 01058, 1400 Washington Avenue, Albany, NY, 12222, USA

    C. A. Frye

  4. The Center Life Sciences Research, The University at Albany-SUNY, Life Sciences 01058, 1400 Washington Avenue, Albany, NY, 12222, USA

    C. A. Frye

  5. Department of Chemistry and Biochemistry, The University of Alaska–Fairbanks, Fairbanks, AK, 99775, USA

    C. A. Frye

  6. Institute of Arctic Biology, The University of Alaska–Fairbanks, Fairbanks, AK, 99775, USA

    C. A. Frye, C. J. Koonce & A. A. Walf

  7. IDeA Network of Biomedical Excellence (INBRE), The University of Alaska–Fairbanks, Fairbanks, AK, 99775, USA

    C. A. Frye, C. J. Koonce & A. A. Walf

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Correspondence to C. A. Frye.

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Frye, C.A., Koonce, C.J. & Walf, A.A. Involvement of pregnane xenobiotic receptor in mating-induced allopregnanolone formation in the midbrain and hippocampus and brain-derived neurotrophic factor in the hippocampus among female rats. Psychopharmacology 231, 3375–3390 (2014). https://doi.org/10.1007/s00213-014-3569-3

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