Sexual Motivation in the Female and Its Opposition by Stress

Magariños, Ana Maria; Pfaff, Donald

doi:10.1007/7854_2015_392

Ana Maria Magariños⁷ &
Donald Pfaff⁷

Part of the book series: Current Topics in Behavioral Neurosciences ((CTBN,volume 27))

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Abstract

A well worked-out motivational system in laboratory animals produces estrogen-dependent female sex behavior. Here, we review (a) the logical definition of sexual motivation and (b) the basic neuronal and molecular mechanisms that allow the behavior to occur. Importantly, reproductive mechanisms in the female can be inhibited by stress. This is interesting because, in terms of the specificity of neuroendocrine dynamics in space and time, the two families of phenomena, sex and stress, are the opposite of each other. We cover papers that document stress effects on the underlying processes of reproductive endocrinology in the female. Not all of the mechanisms for such inhibition have been clearly laid out. Finally, as a current topic of investigation, this system offers several avenues for new investigation which we briefly characterize.

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References

Arletti R, Bertolini A (1985) Oxytocin stimulates lordosis behavior in female rats. Neuropeptides 6:247–253
Article CAS PubMed Google Scholar
Benelli A, Poggioli R, Luppi P, Ruini L, Bertolini A, Arletti R (1994) Oxytocin enhances, and oxytocin antagonism decreases, sexual receptivity in intact female rats. Neuropeptides 27:245–250
Article CAS PubMed Google Scholar
Berkenbosch F, van Oers J, del Rey A, Tilders F, Besedovsky H (1987) Corticotropin-releasing factor-producing neurons in the rat activated by interleukin-1. Science 238:524–530
Article CAS PubMed Google Scholar
Briski KP, Sylvester PW (1998) Role of endogenous opiates in glucoprivic inhibition of the luteinizing hormone surge and Fos expression by preoptic gonadotropin-releasing hormone neurons in ovariectomized steroid-primed female rats. J Neuroendocrinol 10:769–776
Article CAS PubMed Google Scholar
Castellano JM, Bentsen AH, Mikkelsen JD, Tena-Sempere M (2010) Kisspeptins: bridging energy homeostasis and reproduction. Brain Res 1364:129–138
Article CAS PubMed Google Scholar
Cates PS, Li XF, O’Byrne KT (2004) The influence of 17β-oestradiol on corticotrophin-releasing hormone induced suppression of luteinizing hormone pulses and the role of CRH in hypoglycaemic stress-induced suppression of pulsatile LH secretion in the female rat. Stress 7:113–118
Article CAS PubMed Google Scholar
Chand D, Lovejoy DA (2011) Stress and reproduction: controversies and challenges. Gen Comp Endocrinol 171:253–257
Article CAS PubMed Google Scholar
Chen GA, Feng Q, Zhang LZ, Liu YX (1992) Hypoglycemic stress and gonadotropin-releasing hormone pulse generator activity in the rhesus monkey: role of the ovary. Neuroendocrinology 56:666–673
Article CAS PubMed Google Scholar
Chrousos GP, Gold PW (1992) The concepts of stress and stress system disorders: overview of physical and behavioral homeostasis. JAMA 267:1244–1252
Article CAS PubMed Google Scholar
Chung SR, McCabe JT, Pfaff DW (1991) Estrogen influences on oxytocin mRNA expression in preoptic and anterior hypothalamic regions studied by in situ hybridization. J Comp Neurol 307:281–295
Article CAS PubMed Google Scholar
De Kloet ER, Joëls M, Holsboer F (2005) Stress and the brain: from adaptation to disease. Nat Rev Neurosci 6:463–475
Article PubMed Google Scholar
DeFranco DB, Guerrero J (2000) Nuclear matrix targeting of steroid receptors: specific signal sequences and acceptor proteins. Crit Rev Eukaryotic Gene Expr 10:39–44
CAS Google Scholar
Dellovade T, Zhu Y, Pfaff D (1999) Thyroid hormones and estrogen affect oxytocin gene expression in hypothalamic neurons. J Neuroendocrinol 11:1–10
Article CAS PubMed Google Scholar
Engelbregt MJT, Van Weissenbruch MM, Popp-Snijders C, Lips P, Delemarre-Van de Waal HA (2001) Body mass index, body composition, and leptin at onset of puberty in male and female rats after intrauterine growth retardation and after early postnatal food restriction. Pediatr Res 50:474–478
Article CAS PubMed Google Scholar
Ferin M (2007) Effects of stress on Gonadotropin secretion. In: Fink G (ed) Encyclopedia of stress. Elsevier, Amsterdam, vol 2, pp 283–288
Google Scholar
Frye CA, Walf AA, Kohtz AS, Zhu Y (2013) Horm Behav 64:539–545
Article CAS PubMed PubMed Central Google Scholar
Gagnidze K, Weil ZM, Faustino LC, Schaafsma SM (2013) Pfaff DW early histone modifications in the ventromedial hypothalamus and preoptic area following oestradiol administration. J Neuroendoc 25:939–955
Article CAS Google Scholar
Gorzalka BB, Lesterm GLL (1987) Oxytocin-induced facilitation of lordosis behavior in rats is progesterone-dependent. Neuropeptides 10:55–65
Article CAS PubMed Google Scholar
Grachev P, Li XF, Hu MH, Li SY, Millar RP, Lightman SL, O’Byrne KT (2014) Neurokinin B signaling in the female rat: a novel link between stress and reproduction. Endocrinology 155:2589–2601
Article CAS PubMed Google Scholar
Hujibregts L, Tata B, deRoux N (2015) Gonadotropic axis deficiency: a neurodevelopmental disorder. Res Persp Endoc Interact 13:155–162
Article Google Scholar
Hunter RG, McCarthy KJ, Milne TA, Pfaff DW, McEwen BS (2009) Regulation of hippocampal H3 histone methylation by acute and chronic stress. Proc Natl Acad Sci 109:17657–17662
Article Google Scholar
Hunter RG, Murakami G, Dewell S, Seligsohn M, Baker ME, Datson NA, McEwen BS, Pfaff DW (2012) Acute stress and hippocampal histone H3 lysine 9 trimethylation, a retrotransposon silencing response. Proc Nat Acad Sci 109(43):17657–17662
Article CAS PubMed PubMed Central Google Scholar
Hunter R, Gagnidze K, McEwen B, Pfaff D (2015) Stress and the dynamic genome: steroids, epigenetics and the transposome. Proc Natl Acad Sci 112:6828–6833
Article CAS PubMed PubMed Central Google Scholar
Iwasa T, Matsuzaki T, Murakami M, Fujisawa S, Kinouchi R, Gereltsetseg G, Kuwahara A, Yasui T, Irahara M (2010) J Physiol 588:821–829
Article CAS PubMed PubMed Central Google Scholar
Joëls M, Baram TZ (2009) The neuro-symphony of stress. Nature Rev Neurosci 10:459–466
Google Scholar
Kinsey-Jones JS, Li XF, Bowe JE, Lightman SL, O’Byrne KT (2006) Corticotrophin-releasing factor type 2receptor-mediated suppression of gonadotrophin-releasing hormone mRNA expression in GT1-7 cells. Stress 9:215–222
Article CAS PubMed Google Scholar
Kinsey-Jones JS, Li XF, Knox AMI, Wilkinson ES, Zhu XL, Chaudhary AA, Milligan SR, Lightman SL, O’Byrne KT (2009) Down-regulation of hypothalamic kisspeptin and its receptor, Kiss1r, mRNA expression is associated with stress-induced suppression of luteinizing hormone secretion in the female rat. J Neuroendocrinol 21:20–29
Article CAS PubMed Google Scholar
Knox AMI, Li XF, Kinsey-Jones JS, Wilkinson ES, Wu XQ, Cheng YS, Milligan SR, Lightman SL, O’Byrne KT (2009) Neonatal lipopolysaccharide exposure delays puberty and alters hypothalamic Kiss1 and Kiss 1r mRNA expression in the female rat. J Neuroendoc 21:683–689
Article CAS Google Scholar
Kow L-M, Johnson AE, Ogawa S, Pfaff DW (1991) Electrophysiological actions of oxytocin on hypothalamic neurons, in vitro: neuropharmacological characterization and effects of ovarian steroids. Neuroendocrinology 54:526–535
Article CAS PubMed Google Scholar
Li XF, Bowe JE, Kinsey-Jones JS, Brain SD, Lightman SL, O’Byrne KT (2006) Differential role of corticotropin-releasing factor receptor types 1 and 2 in stress-induced suppression of pulsatile luteinizing hormone secretion in the female rat. J Neuroendoc 18:602–610
Article CAS Google Scholar
Li XF, Bowe JE, Mitchell JC, Brain SD, Lightman SL, O’Byrne KT (2004) Stress-induced suppression of the gonadotropin-releasing hormone pulse generator in the female rat: a novel neural action for calcitonin gene-related peptide. Endocrinology 145:1556–1563
Article CAS PubMed Google Scholar
Magariños AM, Garcia Verdugo JM, McEwen BS (1997) Chronic stress alters synaptic terminal structure in hippocampus. Proc Nat Acad Sci 94:14002–14008
Google Scholar
Matsuwaki T, Watanabe E, Suzuki M, Yamanouchi KN, Nishihara M (2003) Glucocorticoid maintains pulsatile secretion of luteinizing hormone under infectious stress condition. Endocrinology 144:347–3482
Article Google Scholar
Matsukawi T, Suzuki M, Yamanouchi K, Nishihara M (2004) Glucocorticoid counteracts the suppressive effect of tumor necrosis factor-α on the surge of luteinizing hormone secretion in rats. J Endocrinol 181:509–513
Article Google Scholar
Matsuwaki T, Kayasuga Y, Yamanouchi K, Nishihara M (2006) Maintenance of gonadotropin secretion by glucocorticoids under stress conditions through the inhibition of prostaglandin synthesis in the brain. Endocrinology 147:1087–1093
Article CAS PubMed Google Scholar
Matteri RL, Watson JG, Moberg GP (1984) Stress or acute adrenocorticotrophin treatment suppresses LHRH-induced LH release in the ram. J Reprod Fertil 72:385–393
Article CAS PubMed Google Scholar
McCarthy MM, Chung SR, Ogawa S, Kow L-M, Pfaff DW (1991) Behavioral effects of oxytocin: is there a unifying principle? In: Jard S, Jamison R (eds) Vasopressin. Colloque INSERM/John Libbey Eurotext Ltd. vol 208, pp. 195–212
Google Scholar
McCarthy MM, Kleopoulos SP, Mobbs CV, Pfaff DW (1994) Infusion of antisense oligodeoxynucleotides to the oxytocin receptor in the ventromedial hypothalamus reduces estrogen–induced sexual receptivity and oxytocin receptor binding in the female rat. Neuroendocrinology 59:432–440
Article CAS PubMed Google Scholar
McEwen BS, Magariños AM (2001) Stress and hippocampal plasticity: implications for the pathophysiology of affective disorders. Hum Psychopharmacol 16:S7–S19
Article CAS PubMed Google Scholar
McEwen BS (2007) Physiology and neurobiology of stress and adaptation: Central role of the brain. Physiol Rev 87:873–904
Article PubMed Google Scholar
Ono N, Lumpkin MD, Samson WK, McDonald JK, McCann SM (1984) Intrahypothalamic action of corticotrophin-releasing factor (CRF) to inhibit growth hormone and LH release in the rat. Life Sci 35:1117–1123
Article CAS PubMed Google Scholar
Pedersen CA, Boccia ML (2002) Oxytocin maintains as well as initiates female sexual behavior: effects of a highly selective oxytocin antagonist. Horm Behav 41:170–177
Article CAS PubMed Google Scholar
Pfaff DW (1968) Autoradiographic localization of radioactivity in rat brain after injection of tritiated sex hormones. Science 161:1355–1356
Article CAS PubMed Google Scholar
Pfaff DW (ed) (1982) The physiological mechanisms of motivation. Springer, Heidelberg, New York
Google Scholar
Pfaff DW, Schwartz-Giblin S (1988) Cellular mechanisms of female reproductive behaviors. In: Knobil E, Neill J (eds) The physiology of reproduction. Raven Press, New York, pp 1487–1568 (Chapter 35)
Google Scholar
Pfaff DW (2006) Brain Arousal and information theory: neural and genetic mechanisms. Harvard University Press, Cambridge
Google Scholar
Pfaff DW, Martin EM, Ribeiro AC (2007) Relations between mechanisms of CNS arousal and mechanisms of stress. Stress 10:316–325
Article PubMed Google Scholar
Pournajafi-Nazarloo H, Kenkel W, Mohsenpour SR, Sanzenbacher L, Saadat H, Partoo L, Yee J, Azizi F, Carter CS (2013) Exposure to chronic isolation modulates receptors mENAs for oxytocin and vasopressin in the hypothalamus and heart. Peptides 43:20–26
Google Scholar
Quiñones-Jenab V, Jenab S, Ogawa S, Adan RAM, Burbach PH, Pfaff DW (1997) Effects of estrogen on oxytocin receptor messenger ribonucleic acid expression in the uterus, pituitary and forebrain of the female rat. Neuroendocrinology 65:9–17
Article PubMed Google Scholar
Rivier C, Rivest S (1991) Effect of stress on the activity of the hypothalamic-pituitary-gonadal axis: peripheral and central mechanisms. Biol Reprod 45:523–532
Article CAS PubMed Google Scholar
Roland AV, Moenter SM (2011) Regulation of gonadotropin-releasing hormone neurons by glucose. Trends Endocrinol Metab 22:443–449
Article CAS PubMed PubMed Central Google Scholar
Sapolsky RM, Romero LM, Munck AU (2000) How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocr Rev 21:55–89
CAS PubMed Google Scholar
Schulze HG, Gorzalka BB (1991) Oxytocin effects on lordosis frequency and lordosis duration following infusion into the medial preoptic area and ventromedial hypothalamus of female rats. Neuropeptides 18:99–106
Article CAS PubMed Google Scholar
Schumacher M, Coirini H, Pfaff DW, McEwen BS (1990) Behavioral effects of progesterone associated with rapid modulation of oxytocin receptors. Science 250:691–694
Article CAS PubMed Google Scholar
Schumacher M, Coirini H, Flanagan LM, Frankfurt M, Pfaff DW, McEwen BS (1992) Ovarian steroid modulation of oxytocin receptor binding in the ventromedial hypothalamus. In: Pedersen CA et al (eds) Oxytocin in maternal, sexual, and social behaviors. Annals, New York Academy of Sciences, vol 652, pp 374–386
Google Scholar
Selye H (1936) Syndrome produced by diverse nocuous agents. Nature 138:32
Article Google Scholar
Selye H (1939) Effects of adaptation to various damaging agents on the female sex organs in the rat. Endocrinology 25:615–624
Article CAS Google Scholar
Seminara SB, Messager S, Chtzidaki EE, …, Aparicio SAJR, Colledge WH (2003) The GPR54 gene as a regulator of Puberty. New England J Med 349:1614–1627
Google Scholar
Shrestha PK, Briski KP (2015) Hindbrain lactate regulates preoptic gonadotropin-releasing hormone (GnRH) neuron GnRH-I protein but not AMPK responses to hypoglycemia in the steroid-primed ovariectomized female rat. Neuroscience 298:1–8
Article Google Scholar
Swanson LW, Sawchenko PE, Rivier J, Vale WW (1983) Organization of ovine corticotropin-releasing factor immunoreactive cells and fibers in the rat brain: an immunohistochemical study. Neuroendocrinology 36:165–186
Article CAS PubMed Google Scholar
Tellam DJ, Perone M, Dunn IC, Radovick S, Brennand J, Castro MG, Rivier JE, Lovejoy DA (1998) Direct regulation of GnRH transcription by CRF-like peptides in an immortalized neuronal cell line. NeuroReport 9:3135–3140
Article CAS PubMed Google Scholar
Tellam DJ, Mohammad DA, Lovejoy DA (2000) Molecular integration of hypothalamo-pituitary-adrenal axis-related neurohormones on the GnRH neuron. Biochem Cell Biol 78:216–305
Article Google Scholar
Truitt W, Harrison L, Guptarak J, White S, Hiegel C, Uphouse L (2003) Progesterone attenuates the effect of the 5-HT1A receptor agonist, 8-OH-DPAT, and of mild restraint on lordosis behavior. Brain Res 974:202–211
Article CAS PubMed Google Scholar
Uphouse L, Hiegel C (2013) An antiprogestin, CDB4124, blocks progesterone’s attenuation of the negative effects of a mild stress on sexual behavior. Behav Brain Res 240:21–25
Article CAS PubMed PubMed Central Google Scholar
Uphouse L, Selvamani A, Lincoln C, Morales L, Comeaux D (2005) Mild restraint reduces the time hormonally primed rats spend with sexually active males. Behav Brain Res 157:343–350
Article CAS PubMed Google Scholar
Uphouse L, Guptarak J, Hiegel C (2010) Progesterone reduces the inhibitory effect of a serotonin 1B receptor agonist on lordosis behavior. Pharmacol Biochem Behav 97:317–324
Article CAS PubMed PubMed Central Google Scholar
Uphouse L, Heckard D, Hiegel C, Guptarak J, Maswood S (2011) Tropisetron increases the inhibitory effect of mild restraint on lordosis behavior of hormonally primed, ovariectomized rats. Behav Brain Res 219:221–226
Article CAS PubMed PubMed Central Google Scholar
Uphouse L, Hiegel C, Martinez G, Solano C, Gusick W (2015) Repeated estradiol benzoate treatment protects against the lordosis-inhibitory effects of restraint and prevents effects of the antiprogestin, RU486. Pharmacol Biochem Behav 137:1–6
Article CAS PubMed Google Scholar
Waldherr M, Neumann ID (2007) Centrally released oxytocin mediates mating-induced anxiolysis in male rats. PNAS 104:16681–16684
Google Scholar
Whirledge S, Cidlowski JA (2013) A role for glucocorticoids in stress-impaired reproduction: Beyond the hypothalamus and pituitary. Endocrinology 154:4450–4468
Article CAS PubMed PubMed Central Google Scholar
White S, Uphouse L (2004) Estrogen and progesterone dose-dependently reduce disruptive effects of restrain on lordosis behavior. Horm Behav 45:201–208
Article CAS PubMed Google Scholar
Wingfield JC, Sapolsky RM (2003) Reproduction and resistance to stress: when and how. J Neuroendocrinol 15:711–724
Article CAS PubMed Google Scholar
Witt DM, Insel TR (1991) A selective oxytocin antagonist attenuates progesterone facilitation of female sexual behavior. Endocrinology 128:3269–3276
Article CAS PubMed Google Scholar
Zhang C, Bosch MA, Levine JE, Ronnekleiv OK, Kelly MJ (2007) Gonadotropin-releasing hormone neurons express KATP channels that are regulated by estrogen and responsive to glucose and metabolic inhibition. J Neurosci 27:10153–10164
Article CAS PubMed Google Scholar

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Laboratory of Neurobiology and Behavior, The Rockefeller University, New York, NY, USA
Ana Maria Magariños & Donald Pfaff

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Ana Maria Magariños
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Correspondence to Ana Maria Magariños .

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New York State Psychiatric Institute, Columbia University Medical Center, New York, New York, USA
Eleanor H. Simpson
Barnard College, Columbia University Barnard College, New York, New York, USA
Peter D. Balsam

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Magariños, A.M., Pfaff, D. (2015). Sexual Motivation in the Female and Its Opposition by Stress. In: Simpson, E., Balsam, P. (eds) Behavioral Neuroscience of Motivation. Current Topics in Behavioral Neurosciences, vol 27. Springer, Cham. https://doi.org/10.1007/7854_2015_392

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DOI: https://doi.org/10.1007/7854_2015_392
Published: 10 December 2015
Publisher Name: Springer, Cham
Print ISBN: 978-3-319-26933-7
Online ISBN: 978-3-319-26935-1
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