Behavioral Neuroscience of Motivation pp 35-49 | Cite as
Sexual Motivation in the Female and Its Opposition by Stress
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.
Keywords
Corticosterone CRF Estrogen Lordosis Oxytocin StressReferences
- Arletti R, Bertolini A (1985) Oxytocin stimulates lordosis behavior in female rats. Neuropeptides 6:247–253CrossRefPubMedGoogle 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 27:245–250CrossRefPubMedGoogle 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 238:524–530CrossRefPubMedGoogle 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 10:769–776CrossRefPubMedGoogle Scholar
- Castellano JM, Bentsen AH, Mikkelsen JD, Tena-Sempere M (2010) Kisspeptins: bridging energy homeostasis and reproduction. Brain Res 1364:129–138CrossRefPubMedGoogle 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 7:113–118CrossRefPubMedGoogle Scholar
- Chand D, Lovejoy DA (2011) Stress and reproduction: controversies and challenges. Gen Comp Endocrinol 171:253–257CrossRefPubMedGoogle 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 56:666–673CrossRefPubMedGoogle Scholar
- Chrousos GP, Gold PW (1992) The concepts of stress and stress system disorders: overview of physical and behavioral homeostasis. JAMA 267:1244–1252CrossRefPubMedGoogle 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 307:281–295CrossRefPubMedGoogle Scholar
- De Kloet ER, Joëls M, Holsboer F (2005) Stress and the brain: from adaptation to disease. Nat Rev Neurosci 6:463–475CrossRefPubMedGoogle Scholar
- DeFranco DB, Guerrero J (2000) Nuclear matrix targeting of steroid receptors: specific signal sequences and acceptor proteins. Crit Rev Eukaryotic Gene Expr 10:39–44Google Scholar
- Dellovade T, Zhu Y, Pfaff D (1999) Thyroid hormones and estrogen affect oxytocin gene expression in hypothalamic neurons. J Neuroendocrinol 11:1–10CrossRefPubMedGoogle 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 50:474–478CrossRefPubMedGoogle Scholar
- Ferin M (2007) Effects of stress on Gonadotropin secretion. In: Fink G (ed) Encyclopedia of stress. Elsevier, Amsterdam, vol 2, pp 283–288Google Scholar
- Frye CA, Walf AA, Kohtz AS, Zhu Y (2013) Horm Behav 64:539–545CrossRefPubMedPubMedCentralGoogle 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 25:939–955CrossRefGoogle Scholar
- Gorzalka BB, Lesterm GLL (1987) Oxytocin-induced facilitation of lordosis behavior in rats is progesterone-dependent. Neuropeptides 10:55–65CrossRefPubMedGoogle 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 155:2589–2601CrossRefPubMedGoogle Scholar
- Hujibregts L, Tata B, deRoux N (2015) Gonadotropic axis deficiency: a neurodevelopmental disorder. Res Persp Endoc Interact 13:155–162CrossRefGoogle 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 109:17657–17662CrossRefGoogle 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):17657–17662CrossRefPubMedPubMedCentralGoogle Scholar
- Hunter R, Gagnidze K, McEwen B, Pfaff D (2015) Stress and the dynamic genome: steroids, epigenetics and the transposome. Proc Natl Acad Sci 112:6828–6833CrossRefPubMedPubMedCentralGoogle Scholar
- Iwasa T, Matsuzaki T, Murakami M, Fujisawa S, Kinouchi R, Gereltsetseg G, Kuwahara A, Yasui T, Irahara M (2010) J Physiol 588:821–829CrossRefPubMedPubMedCentralGoogle Scholar
- Joëls M, Baram TZ (2009) The neuro-symphony of stress. Nature Rev Neurosci 10:459–466Google 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 9:215–222CrossRefPubMedGoogle 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 21:20–29CrossRefPubMedGoogle 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 21:683–689CrossRefGoogle 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 54:526–535CrossRefPubMedGoogle 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 18:602–610CrossRefGoogle 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 145:1556–1563CrossRefPubMedGoogle Scholar
- Magariños AM, Garcia Verdugo JM, McEwen BS (1997) Chronic stress alters synaptic terminal structure in hippocampus. Proc Nat Acad Sci 94:14002–14008Google Scholar
- Matsuwaki T, Watanabe E, Suzuki M, Yamanouchi KN, Nishihara M (2003) Glucocorticoid maintains pulsatile secretion of luteinizing hormone under infectious stress condition. Endocrinology 144:347–3482CrossRefGoogle 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 181:509–513CrossRefGoogle 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 147:1087–1093CrossRefPubMedGoogle Scholar
- Matteri RL, Watson JG, Moberg GP (1984) Stress or acute adrenocorticotrophin treatment suppresses LHRH-induced LH release in the ram. J Reprod Fertil 72:385–393CrossRefPubMedGoogle 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. 195–212Google 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 59:432–440CrossRefPubMedGoogle Scholar
- McEwen BS, Magariños AM (2001) Stress and hippocampal plasticity: implications for the pathophysiology of affective disorders. Hum Psychopharmacol 16:S7–S19CrossRefPubMedGoogle Scholar
- McEwen BS (2007) Physiology and neurobiology of stress and adaptation: Central role of the brain. Physiol Rev 87:873–904CrossRefPubMedGoogle 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 35:1117–1123CrossRefPubMedGoogle Scholar
- Pedersen CA, Boccia ML (2002) Oxytocin maintains as well as initiates female sexual behavior: effects of a highly selective oxytocin antagonist. Horm Behav 41:170–177CrossRefPubMedGoogle Scholar
- Pfaff DW (1968) Autoradiographic localization of radioactivity in rat brain after injection of tritiated sex hormones. Science 161:1355–1356CrossRefPubMedGoogle Scholar
- Pfaff DW (ed) (1982) The physiological mechanisms of motivation. Springer, Heidelberg, New YorkGoogle 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, CambridgeGoogle Scholar
- Pfaff DW, Martin EM, Ribeiro AC (2007) Relations between mechanisms of CNS arousal and mechanisms of stress. Stress 10:316–325CrossRefPubMedGoogle 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 43:20–26Google 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 65:9–17CrossRefPubMedGoogle Scholar
- Rivier C, Rivest S (1991) Effect of stress on the activity of the hypothalamic-pituitary-gonadal axis: peripheral and central mechanisms. Biol Reprod 45:523–532CrossRefPubMedGoogle Scholar
- Roland AV, Moenter SM (2011) Regulation of gonadotropin-releasing hormone neurons by glucose. Trends Endocrinol Metab 22:443–449CrossRefPubMedPubMedCentralGoogle Scholar
- Sapolsky RM, Romero LM, Munck AU (2000) How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocr Rev 21:55–89PubMedGoogle 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 18:99–106CrossRefPubMedGoogle Scholar
- Schumacher M, Coirini H, Pfaff DW, McEwen BS (1990) Behavioral effects of progesterone associated with rapid modulation of oxytocin receptors. Science 250:691–694CrossRefPubMedGoogle 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 374–386Google Scholar
- Selye H (1936) Syndrome produced by diverse nocuous agents. Nature 138:32CrossRefGoogle Scholar
- Selye H (1939) Effects of adaptation to various damaging agents on the female sex organs in the rat. Endocrinology 25:615–624CrossRefGoogle Scholar
- Seminara SB, Messager S, Chtzidaki EE, …, Aparicio SAJR, Colledge WH (2003) The GPR54 gene as a regulator of Puberty. New England J Med 349:1614–1627Google 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 298:1–8CrossRefGoogle 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 36:165–186CrossRefPubMedGoogle 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 9:3135–3140CrossRefPubMedGoogle Scholar
- Tellam DJ, Mohammad DA, Lovejoy DA (2000) Molecular integration of hypothalamo-pituitary-adrenal axis-related neurohormones on the GnRH neuron. Biochem Cell Biol 78:216–305CrossRefGoogle 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 974:202–211CrossRefPubMedGoogle 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 240:21–25CrossRefPubMedPubMedCentralGoogle 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 157:343–350CrossRefPubMedGoogle 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 97:317–324CrossRefPubMedPubMedCentralGoogle 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 219:221–226CrossRefPubMedPubMedCentralGoogle 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 137:1–6CrossRefPubMedGoogle Scholar
- Waldherr M, Neumann ID (2007) Centrally released oxytocin mediates mating-induced anxiolysis in male rats. PNAS 104:16681–16684Google Scholar
- Whirledge S, Cidlowski JA (2013) A role for glucocorticoids in stress-impaired reproduction: Beyond the hypothalamus and pituitary. Endocrinology 154:4450–4468CrossRefPubMedPubMedCentralGoogle Scholar
- White S, Uphouse L (2004) Estrogen and progesterone dose-dependently reduce disruptive effects of restrain on lordosis behavior. Horm Behav 45:201–208CrossRefPubMedGoogle Scholar
- Wingfield JC, Sapolsky RM (2003) Reproduction and resistance to stress: when and how. J Neuroendocrinol 15:711–724CrossRefPubMedGoogle Scholar
- Witt DM, Insel TR (1991) A selective oxytocin antagonist attenuates progesterone facilitation of female sexual behavior. Endocrinology 128:3269–3276CrossRefPubMedGoogle 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 27:10153–10164CrossRefPubMedGoogle Scholar