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Mood, Food, and Fertility: Adaptations of the Maternal Brain

Barbara Woodside

10.1002/cphy.c150036

Source: Volume 6, Issue 3, July 2016

Published online: June 2016

Full Article on Wiley Online Library



ABSTRACT

Successfully rearing young places multiple demands on the mammalian female. These are met by a wide array of alterations in maternal physiology and behavior that are coordinated with the needs of the developing young, and include adaptations in neuroendocrine systems not directly involved in maternal behavior or lactation. In this article, attenuations in the behavioral and neuroendocrine responses to stressors, the alterations in metabolic pathways facilitating both increased food intake and conservation of energy, and the changes in fertility that occur postpartum are described. The mechanisms underlying these processes as well as the factors that contribute to them and the relative contributions of these stimuli at different times postpartum are also reviewed. The induction and maintenance of the adaptations observed in the postpartum maternal brain are dependent on mother‐young interaction and, in most cases, on suckling stimulation and its consequences for the hormonal profile of the mother. The peptide hormone prolactin acting on receptors within the brain makes a major contribution to changes in metabolic pathways, suppression of fertility and the attenuation of the neuroendocrine response to stress during lactation. Oxytocin is also released, both into the circulation and in some hypothalamic nuclei, in response to suckling stimulation and this hormone has been implicated in the decrease in anxiety behavior seen in the early postpartum period. The relative importance of these hormones changes across lactation and it is becoming increasingly clear that many of the adaptations to motherhood reviewed here reflect the outcome of multiple influences. © 2016 American Physiological Society. Compr Physiol 6:1493‐1518, 2016.

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Figure 1. Figure 1. Adaptations in the response of the extended stress circuitry and hypothalamic pituitary adrenal system to an acute stressor during lactation. Suckling induced PRL acts at the PVN to suppress the hormonal response to stress. The presence of PRL‐Rs in some areas of the extended stress circuitry suggests a potential role for this peptide hormone in stress appraisal. Arrows represent direction of change.
Figure 2. Figure 2. Lactation associated changes in peripheral signals of energy balance and the hypothalamic circuitry controlling food intake and metabolism. Circulating levels of anorectic factors such as leptin, insulin, and estrogen are decreased during lactation and those of orexigenic factors, such as glucocorticoids and PRL are increased. Although evidence supports a role for PRL in the hyperphagia of lactation, the precise mechanism(s) and sites of action are not yet defined. Arrows represent direction of change. Red indicates anorectic signals and green orexigenic signals.
Figure 3. Figure 3. Changes in the pathways controlling GnRH release as a function of reproductive state. Early in lactation suckling‐induced neural pathways have a greater suppressive effect on GnRH release than do suckling induced changes in hormonal state. By contrast in late lactation suckling‐induced PRL release and perhaps changes in GHSR1a in the arcuate nucleus make a major contribution to diminished GnRH release. Arrows represent direction of change. fx1 indicate receptors. Green indicates stimulatory effects and red inhibitory effects.


Figure 1. Adaptations in the response of the extended stress circuitry and hypothalamic pituitary adrenal system to an acute stressor during lactation. Suckling induced PRL acts at the PVN to suppress the hormonal response to stress. The presence of PRL‐Rs in some areas of the extended stress circuitry suggests a potential role for this peptide hormone in stress appraisal. Arrows represent direction of change.


Figure 2. Lactation associated changes in peripheral signals of energy balance and the hypothalamic circuitry controlling food intake and metabolism. Circulating levels of anorectic factors such as leptin, insulin, and estrogen are decreased during lactation and those of orexigenic factors, such as glucocorticoids and PRL are increased. Although evidence supports a role for PRL in the hyperphagia of lactation, the precise mechanism(s) and sites of action are not yet defined. Arrows represent direction of change. Red indicates anorectic signals and green orexigenic signals.


Figure 3. Changes in the pathways controlling GnRH release as a function of reproductive state. Early in lactation suckling‐induced neural pathways have a greater suppressive effect on GnRH release than do suckling induced changes in hormonal state. By contrast in late lactation suckling‐induced PRL release and perhaps changes in GHSR1a in the arcuate nucleus make a major contribution to diminished GnRH release. Arrows represent direction of change. fx1 indicate receptors. Green indicates stimulatory effects and red inhibitory effects.
References
 1.The World Health Organization Multinational Study of Breast‐feeding and Lactational Amenorrhea. II. Factors associated with the length of amenorrhea. World Health Organization Task Force on Methods for the Natural Regulation of Fertility. Fertil Steril 70: 461‐471, 1998.
 2.The World Health Organization multinational study of breast‐feeding and lactational amenorrhea. III. Pregnancy during breast‐feeding. World Health Organization Task Force on Methods for the Natural Regulation of Fertility. Fertil Steril 72: 431‐440, 1999.
 3.Abelenda M, Puerta ML. Inhibition of diet‐induced thermogenesis during pregnancy in the rat. Pflugers Arch 409: 314‐317, 1987.
 4.Abizaid A. Ghrelin and dopamine: New insights on the peripheral regulation of appetite. J Neuroendocrinol 21: 787‐793, 2009.
 5.Abizaid A, Gao Q, Horvath TL. Thoughts for food: Brain mechanisms and peripheral energy balance. Neuron 51: 691‐702, 2006.
 6.Abizaid A, Horvath TL. Brain circuits regulating energy homeostasis. Regul Pept 149: 3‐10, 2008.
 7.Abizaid A, Jafferali S, Pelletier G, Woodside B. Effect of metabolic fuel availability on fertility varies with reproductive state. Physiol Behav 74: 77‐83.
 8.Abizaid A, Kyriazis D, Woodside B. Effects of leptin administration on lactational infertility in food‐restricted rats depend on milk delivery. Am J Physiol Regul Integr Comp Physiol 286: R217‐225, 2004.
 9.Abizaid A, Liu ZW, Andrews ZB, Shanabrough M, Borok E, Elsworth JD, Roth RH, Sleeman MW, Picciotto MR, Tschop MH, Gao XB, Horvath TL. Ghrelin modulates the activity and synaptic input organization of midbrain dopamine neurons while promoting appetite. J Clin Invest 116: 3229‐3239, 2006.
 10.Abizaid A, Schiavo L, Diano S. Hypothalamic and pituitary expression of ghrelin receptor message is increased during lactation. Neurosci Lett 440: 206‐210, 2008.
 11.Abizaid A, Service G, Woodside B. Food restriction during lactation results in prolonged hyposensitivity to the positive‐feedback effects of oestradiol. J Neuroendocrinol 15: 1037‐1045, 2003.
 12.Abizaid A, Service G, Woodside BC. Effects of estradiol on immediate early gene expression associated with ovulation in lactating rats: Role of nutritional status. Brain Res 1001: 72‐77, 2004.
 13.Abizaid A, Walker CD, Woodside B. Changes in neuropeptide Y immunoreactivity in the arcuate nucleus during and after food restriction in lactating rats. Brain Res 761: 306‐312, 1997.
 14.Abizaid A, Woodside B. Food intake and neuronal activation after acute 2DG treatment are attenuated during lactation. Physiol Behav 75: 483‐491, 2002.
 15.Adamantidis A, de Lecea L. Physiological arousal: A role for hypothalamic systems. Cell Mol Life Sci 65: 1475‐1488, 2008.
 16.Afonso VM, King S, Chatterjee D, Fleming AS. Hormones that increase maternal responsiveness affect accumbal dopaminergic responses to pup‐ and food‐stimuli in the female rat. Horm Behav 56: 11‐23, 2009.
 17.Agrati D, Browne D, Jonas W, Meaney M, Atkinson L, Steiner M, Fleming AS. Maternal anxiety from pregnancy to 2 years postpartum: Transactional patterns of maternal early adversity and child temperament. Arch Womens Ment Health, 2015.
 18.Altemus M, Deuster PA, Galliven E, Carter CS, Gold PW. Suppression of hypothalmic‐pituitary‐adrenal axis responses to stress in lactating women. J Clin Endocrinol Metab 80: 2954‐2959, 1995.
 19.Altemus M, Redwine LS, Leong YM, Frye CA, Porges SW, Carter CS. Responses to laboratory psychosocial stress in postpartum women. Psychosom Med 63: 814‐821, 2001.
 20.Araujo‐Lopes R, Crampton JR, Aquino NS, Miranda RM, Kokay IC, Reis AM, Franci CR, Grattan DR, Szawka RE. Prolactin regulates kisspeptin neurons in the arcuate nucleus to suppress LH secretion in female rats. Endocrinology 155: 1010‐1020, 2014.
 21.Asarian L, Geary N. Modulation of appetite by gonadal steroid hormones. Philos Trans R Soc Lond B Biol Sci 361: 1251‐1263, 2006.
 22.Augustine RA, Grattan DR. Induction of central leptin resistance in hyperphagic pseudopregnant rats by chronic prolactin infusion. Endocrinology 149: 1049‐1055, 2008.
 23.Augustine RA, Ladyman SR, Grattan DR. From feeding one to feeding many: Hormone‐induced changes in bodyweight homeostasis during pregnancy. J Physiol 586: 387‐397, 2008.
 24.Baird DT, McNeilly AS, Sawers RS, Sharpe RM. Failure of estrogen‐induced discharge of luteinizing hormone in lactating women. J Clin Endocrinol Metab 49: 500‐506, 1979.
 25.Bakowska JC, Morrell JI. Atlas of the neurons that express mRNA for the long form of the prolactin receptor in the forebrain of the female rat. J Comp Neurol 386: 161‐177, 1997.
 26.Barash I, Madar Z, Gertler A. Short‐term in vivo regulation of prolactin receptors in the liver, testes, kidneys, and mammary gland of rats. Receptor 2: 39‐44, 1992.
 27.Barbosa‐Vargas E, Pfaus JG, Woodside B. Sexual behavior in lactating rats: Role of estrogen‐induced progesterone receptors. Horm Behav 56: 246‐253, 2009.
 28.Bechtold DA, Luckman SM. Prolactin‐releasing peptide mediates cholecystokinin‐induced satiety in mice. Endocrinology 147: 4723‐4729, 2006.
 29.Bellefontaine N, Elias CF. Minireview: Metabolic control of the reproductive physiology: Insights from genetic mouse models. Horm Behav 66: 7‐14, 2014.
 30.Bernard V, Young J, Chanson P, Binart N. New insights in prolactin: Pathological implications. Nature Rev 11: 265‐275, 2015.
 31.Blume A, Torner L, Liu Y, Subburaju S, Aguilera G, Neumann ID. Prolactin activates mitogen‐activated protein kinase signaling and corticotropin releasing hormone transcription in rat hypothalamic neurons. Endocrinology 150: 1841‐1849, 2009.
 32.Bongaarts J. Does malnutrition affect fecundity? A summary of evidence. Science 208: 564‐569, 1980.
 33.Bosch OJ. Maternal nurturing is dependent on her innate anxiety: The behavioral roles of brain oxytocin and vasopressin. Horm Behav 59: 202‐212, 2011.
 34.Bosch OJ, Musch W, Bredewold R, Slattery DA, Neumann ID. Prenatal stress increases HPA axis activity and impairs maternal care in lactating female offspring: Implications for postpartum mood disorder. Psychoneuroendocrinology 32: 267‐278, 2007.
 35.Bowen WD, Oftedal OT, Boness DJ. Birth to weaning in 4 days: Remarkable growth in the hooded seal, Cystophora cristata. Can J Zool 63: 2841‐2846, 1985.
 36.Boyne R, Fell BF, Robb I. The surface area of the intestinal mucosa in the lactating rat. J Physiol 183: 570‐575, 1966.
 37.Brandao ML, Troncoso AC, de Souza Silva MA, Huston JP. The relevance of neuronal substrates of defense in the midbrain tectum to anxiety and stress: Empirical and conceptual considerations. Eur J Pharmacol 463: 225‐233, 2003.
 38.Bridges R, Zarrow MX, Gandelman R, Denenberg VH. Differences in maternal responsiveness between lactating and sensitized rats. Dev Psychobiol 5: 123‐127, 1972.
 39.Bridges RS. Neuroendocrine regulation of maternal behavior. Front Neuroendocrinol 36: 178‐196, 2015.
 40.Bridges RS, Numan M, Ronsheim PM, Mann PE, Lupini CE. Central prolactin infusions stimulate maternal behavior in steroid‐treated, nulliparous female rats. Proc Natl Acad Sci U S A 87: 8003‐8007, 1990.
 41.Broad KD, Kendrick KM, Sirinathsinghji DJ, Keverne EB. Changes in oxytocin immunoreactivity and mRNA expression in the sheep brain during pregnancy, parturition and lactation and in response to oestrogen and progesterone. J Neuroendocrinol 5: 435‐444, 1993.
 42.Brogan RS, Grove KL, Smith MS. Differential regulation of leptin receptor but not orexin in the hypothalamus of the lactating rat. J Neuroendocrinol 12: 1077‐1086, 2000.
 43.Brogan RS, Mitchell SE, Trayhurn P, Smith MS. Suppression of leptin during lactation: Contribution of the suckling stimulus versus milk production. Endocrinology 140: 2621‐2627, 1999.
 44.Brommage R. Measurement of calcium and phosphorus fluxes during lactation in the rat. J Nutr 119: 428‐438, 1989.
 45.Bronson F. Mammalian reproduction: An ecological perspective. Funct Orthod v 2: 11‐55, 1985.
 46.Bronson FH. Food‐restricted, prepubertal, female rats: Rapid recovery of luteinizing hormone pulsing with excess food, and full recovery of pubertal development with gonadotropin‐releasing hormone. Endocrinology 118: 2483‐2487, 1986.
 47.Bronson FH, Heideman PD. Short‐term hormonal responses to food intake in peripubertal female rats. Am J Physiol 259: R25‐31, 1990.
 48.Brown RS, Herbison AE, Grattan DR. Prolactin regulation of kisspeptin neurones in the mouse brain and its role in the lactation‐induced suppression of kisspeptin expression. J Neuroendocrinol 26: 898‐908, 2014.
 49.Brown RS, Kokay IC, Herbison AE, Grattan DR. Distribution of prolactin‐responsive neurons in the mouse forebrain. J Comp Neurol 518: 92‐102, 2010.
 50.Bruning JC, Gautam D, Burks DJ, Gillette J, Schubert M, Orban PC, Klein R, Krone W, Muller‐Wieland D, Kahn CR. Role of brain insulin receptor in control of body weight and reproduction. Science 289: 2122‐2125, 2000.
 51.Brunton PJ, Russell JA. The expectant brain: Adapting for motherhood. Nat Rev Neurosci 9: 11‐25, 2008.
 52.Brunton PJ, Russell JA, Douglas AJ. Adaptive responses of the maternal hypothalamic‐pituitary‐adrenal axis during pregnancy and lactation. J Neuroendocrinol 20: 764‐776, 2008.
 53.Budin RE, Wellman M, Abizaid A, Woodside B. Functional role of ghrelin during lactation. Society for Behavioral Neuroendocrinology, June, Toronto, Canada, 2010.
 54.Budin RE, Woodside B. Behavioral effects of central leptin administration during lactation. Society for Behavioral Neuroendocrinology, June, Toronto, Canada, 2010.
 55.Buonfiglio DC, Ramos‐Lobo AM, Silveira MA, Furigo IC, Hennighausen L, Frazao R, Donato J, Jr. Neuronal STAT5 signaling is required for maintaining lactation but not for postpartum maternal behaviors in mice. Horm Behav 71: 60‐68, 2015.
 56.Butte NF, Ellis KJ, Wong WW, Hopkinson JM, Smith EO. Composition of gestational weight gain impacts maternal fat retention and infant birth weight. Am J Obstet Gynecol 189: 1423‐1432, 2003.
 57.Butte NF, King JC. Energy requirements during pregnancy and lactation. Public Health Nutr 8: 1010‐1027, 2005.
 58.Caldwell JD, Greer ER, Johnson MF, Prange AJ, Jr, Pedersen CA. Oxytocin and vasopressin immunoreactivity in hypothalamic and extrahypothalamic sites in late pregnant and postpartum rats. Neuroendocrinology 46: 39‐47, 1987.
 59.Campbell RE, ffrench‐Mullen JM, Cowley MA, Smith MS, Grove KL. Hypothalamic circuitry of neuropeptide Y regulation of neuroendocrine function and food intake via the Y5 receptor subtype. Neuroendocrinology 74: 106‐119, 2001.
 60.Carter CS, Altemus M, Chrousos GP. Neuroendocrine and emotional changes in the post‐partum period. Prog Brain Res 133: 241‐249, 2001.
 61.Chalivoix S, Bagnolini A, Caraty A, Cognie J, Malpaux B, Dufourny L. Effects of photoperiod on kisspeptin neuronal populations of the ewe diencephalon in connection with reproductive function. J Neuroendocrinol 22: 110‐118, 2010.
 62.Chen P, Li C, Haskell‐Luevano C, Cone RD, Smith MS. Altered expression of agouti‐related protein and its colocalization with neuropeptide Y in the arcuate nucleus of the hypothalamus during lactation. Endocrinology 140: 2645‐2650, 1999.
 63.Chen P, Smith MS. Regulation of hypothalamic neuropeptide Y messenger ribonucleic acid expression during lactation: Role of prolactin. Endocrinology 145: 823‐829, 2004.
 64.Cheung CC, Thornton JE, Nurani SD, Clifton DK, Steiner RA. A reassessment of leptin's role in triggering the onset of puberty in the rat and mouse. Neuroendocrinology 74: 12‐21, 2001.
 65.Ciofi P, Crowley WR, Pillez A, Schmued LL, Tramu G, Mazzuca M. Plasticity in expression of immunoreactivity for neuropeptide Y, enkephalins and neurotensin in the hypothalamic tubero‐infundibular dopaminergic system during lactation in mice. J Neuroendocrinol 5: 599‐602, 1993.
 66.Clarke IJ. Interface between metabolic balance and reproduction in ruminants: Focus on the hypothalamus and pituitary. Horm Behav 66: 15‐40, 2014.
 67.Clarke PE, Rousham EK, Gross H, Halligan AW, Bosio P. Activity patterns and time allocation during pregnancy: A longitudinal study of British women. Ann Hum Biol 32: 247‐258, 2005.
 68.Clarkson J, Boon WC, Simpson ER, Herbison AE. Postnatal development of an estradiol‐kisspeptin positive feedback mechanism implicated in puberty onset. Endocrinology 150: 3214‐3220, 2009.
 69.Clegg DJ, Brown LM, Woods SC, Benoit SC. Gonadal hormones determine sensitivity to central leptin and insulin. Diabetes 55: 978‐987, 2006.
 70.Clegg DJ, Brown LM, Zigman JM, Kemp CJ, Strader AD, Benoit SC, Woods SC, Mangiaracina M, Geary N. Estradiol‐dependent decrease in the orexigenic potency of ghrelin in female rats. Diabetes 56: 1051‐1058, 2007.
 71.Cohen LR, Woodside BC. Self‐selection of protein during pregnancy and lactation in rats. Appetite 12: 119‐136, 1989.
 72.Cripps AW, Williams VJ. The effect of pregnancy and lactation on food intake, gastrointestinal anatomy and the absorptive capacity of the small intestine in the albino rat. Br J Nutr 33: 17‐323, 1975.
 73.Crowley WR. Neuroendocrine regulation of lactation and milk production. Compr Physiol 5: 255‐291, 2015.
 74.Crowley WR, Armstrong WE. Neurochemical regulation of oxytocin secretion in lactation. Endocr Rev 13: 33‐65, 1992.
 75.Crowley WR, Ramoz G, Hurst B. Evidence for involvement of neuropeptide Y and melanocortin systems in the hyperphagia of lactation in rats. Pharmacol Biochem Behav 74: 417‐424, 2003.
 76.Crowley WR, Ramoz G, Torto R, Kalra SP. Role of leptin in orexigenic neuropeptide expression during lactation in rats. J Neuroendocrinol 16: 637‐644, 2004.
 77.Crowley WR, Ramoz G, Torto R, Keefe KA, Wang JJ, Kalra SP. Neuroendocrine actions and regulation of hypothalamic neuropeptide Y during lactation. Peptides 28: 447‐452, 2007.
 78.Cservenak M, Bodnar I, Usdin TB, Palkovits M, Nagy GM, Dobolyi A. Tuberoinfundibular peptide of 39 residues is activated during lactation and participates in the suckling‐induced prolactin release in rat. Endocrinology 151: 5830‐5840, 2010.
 79.Cui JG, Tang GB, Wang DH, Speakman JR. Effects of leptin infusion during peak lactation on food intake, body composition, litter growth, and maternal neuroendocrine status in female Brandt's voles (Lasiopodomys brandtii). Am J Physiol Regul Integr Comp Physiol 300: R447‐459, 2011.
 80.Cummings S, Seybold V. Relationship of alpha‐1‐ and alpha‐2‐adrenergic‐binding sites to regions of the paraventricular nucleus of the hypothalamus containing corticotropin‐releasing factor and vasopressin neurons. Neuroendocrinology 47: 523‐532, 1988.
 81.Curley JP, Jensen CL, Franks B, Champagne FA. Variation in maternal and anxiety‐like behavior associated with discrete patterns of oxytocin and vasopressin 1a receptor density in the lateral septum. Horm Behav 61: 454‐461, 2012.
 82.Da Costa AP, Kampa RJ, Windle RJ, Ingram CD, Lightman SL. Region‐specific immediate‐early gene expression following the administration of corticotropin‐releasing hormone in virgin and lactating rats. Brain Res 770: 151‐162, 1997.
 83.Da Costa AP, Ma X, Ingram CD, Lightman SL, Aguilera G. Hypothalamic and amygdaloid corticotropin‐releasing hormone (CRH) and CRH receptor‐1 mRNA expression in the stress‐hyporesponsive late pregnant and early lactating rat. Brain Res Mol Brain Res 91: 119‐130, 2001.
 84.Da Costa AP, Wood S, Ingram CD, Lightman SL. Region‐specific reduction in stress‐induced c‐fos mRNA expression during pregnancy and lactation. Brain Res 742: 177‐184, 1996.
 85.Delgado H, Brineman E, Lechtig A, Bongaarts J, Martorell R, Klein RE. Effect of maternal nutritional status and infant supplementation during lactation on postpartum amenorrhea. Am J Obstet Gynecol 135: 303‐307, 1979.
 86.Delgado HL, Martorell R, Klein RE. Nutrition, lactation, and birth interval components in rural Guatemala. Am J Clin Nutr 35: 1468‐1476, 1982.
 87.Denis RG, Williams G, Vernon RG. Regulation of serum leptin and its role in the hyperphagia of lactation in the rat. J Endocrinol 176: 193‐203, 2003.
 88.Deschamps S, Woodside B, Walker CD. Pups presence eliminates the stress hyporesponsiveness of early lactating females to a psychological stress representing a threat to the pups. J Neuroendocrinol 15: 486‐497, 2003.
 89.Divall SA, Williams TR, Carver SE, Koch L, Bruning JC, Kahn CR, Wondisford F, Radovick S, Wolfe A. Divergent roles of growth factors in the GnRH regulation of puberty in mice. J Clin Invest 120: 2900‐2909, 2010.
 90.Dobolyi A. Novel potential regulators of maternal adaptations during lactation: Tuberoinfundibular peptide 39 and amylin. J Neuroendocrinol 23: 1002‐1008, 2011.
 91.Donato J, Jr, Cravo RM, Frazao R, Gautron L, Scott MM, Lachey J, Castro IA, Margatho LO, Lee S, Lee C, Richardson JA, Friedman J, Chua S, Jr, Coppari R, Zigman JM, Elmquist JK, Elias CF. Leptin's effect on puberty in mice is relayed by the ventral premammillary nucleus and does not require signaling in Kiss1 neurons. J Clin Invest 121: 355‐368, 2011.
 92.Donato J, Jr, Elias CF. The ventral premammillary nucleus links metabolic cues and reproduction. Front Endocrinol 2: 57, 2011.
 93.Donner N, Bredewold R, Maloumby R, Neumann ID. Chronic intracerebral prolactin attenuates neuronal stress circuitries in virgin rats. Eur J Neurosci 25: 1804‐1814, 2007.
 94.Douglas AJ. Central noradrenergic mechanisms underlying acute stress responses of the Hypothalamo‐pituitary‐adrenal axis: Adaptations through pregnancy and lactation. Stress 8: 5‐18, 2005.
 95.Douglas AJ, Bicknell RJ, Leng G, Russell JA, Meddle SL. Beta‐endorphin cells in the arcuate nucleus: Projections to the supraoptic nucleus and changes in expression during pregnancy and parturition. J Neuroendocrinol 14: 768‐777, 2002.
 96.Douglas AJ, Johnstone LE, Leng G. Neuroendocrine mechanisms of change in food intake during pregnancy: A potential role for brain oxytocin. Physiol Behav 91: 352‐365, 2007.
 97.Douglas AJ, Meddle SL, Kroemer S, Muesch W, Bosch OJ, Neumann ID. Social stress induces hypothalamo‐pituitary‐adrenal axis responses in lactating rats bred for high trait anxiety. Eur J Neurosci 25: 1599‐1603, 2007.
 98.Ellison PT, Valeggia CR. C‐peptide levels and the duration of lactational amenorrhea. Fertil Steril 80: 1279‐1280, 2003.
 99.Erickson JC, Clegg KE, Palmiter RD. Sensitivity to leptin and susceptibility to seizures of mice lacking neuropeptide Y. Nature 381: 415‐421, 1996.
 100.Eriksson M, Bjorkstrand E, Smedh U, Alster P, Matthiesen AS, Uvnas‐Moberg K. Role of vagal nerve activity during suckling. Effects on plasma levels of oxytocin, prolactin, VIP, somatostatin, insulin, glucagon, glucose and of milk secretion in lactating rats. Acta Physiol Scand 151: 453‐459, 1994.
 101.Eriksson M, Ceccatelli S, Uvnas‐Moberg K, Iadarola M, Hokfelt T. Expression of Fos‐related antigens, oxytocin, dynorphin and galanin in the paraventricular and supraoptic nuclei of lactating rats. Neuroendocrinology 63: 356‐367, 1996.
 102.Ermisch A, Barth T, Ruhle HJ, Skopkova J, Hrbas P, Landgraf R. On the blood‐brain barrier to peptides: Accumulation of labelled vasopressin, DesGlyNH2‐vasopressin and oxytocin by brain regions. Endocrinol Exp 19: 29‐37, 1985.
 103.Evans JJ, Anderson GM. Balancing ovulation and anovulation: Integration of the reproductive and energy balance axes by neuropeptides. Hum Reprod Update 18: 313‐332, 2012.
 104.Evans MC, Rizwan M, Mayer C, Boehm U, Anderson GM. Evidence that insulin signalling in gonadotrophin‐releasing hormone and kisspeptin neurones does not play an essential role in metabolic regulation of fertility in mice. J Neuroendocrinol 26: 468‐479, 2014.
 105.Fabic MS Choi Y. Assessing the quality of data regarding use of the lactational amenorrhea method. Stud Fam Plann 44: 205‐221, 2013.
 106.Fenelon VS, Theodosis DT, Poulain DA. Fos synthesis in identified magnocellular neurons varies with phenotype, stimulus, location in the hypothalamus and reproductive state. Brain Res 662: 165‐177, 1994.
 107.Fernandez‐Fernandez R, Tena‐Sempere M, Aguilar E, Pinilla L. Ghrelin effects on gonadotropin secretion in male and female rats. Neurosci Lett 362: 103‐107, 2004.
 108.Fernandez‐Fernandez R, Tena‐Sempere M, Navarro VM, Barreiro ML, Castellano JM, Aguilar E, Pinilla L. Effects of ghrelin upon gonadotropin‐releasing hormone and gonadotropin secretion in adult female rats: In vivo and in vitro studies. Neuroendocrinology 82: 245‐255, 2005.
 109.Figueira RJ, Peabody MF, Lonstein JS. Oxytocin receptor activity in the ventrocaudal periaqueductal gray modulates anxiety‐related behavior in postpartum rats. Behav Neurosci 122: 618‐628, 2008.
 110.Fleming AS, Luebke C. Timidity prevents the virgin female rat from being a good mother: Emotionality differences between nulliparous and parturient females. Physiol Behav 27: 863‐868, 1981.
 111.Flint DJ. Role of insulin and the insulin receptor in nutrient partitioning between the mammary gland and adipose tissue. Biochem Soc Trans 13: 828‐829, 1985.
 112.Flint DJ, Sinnett‐Smith PA, Clegg RA, Vernon RG. Role of insulin receptors in the changing metabolism of adipose tissue during pregnancy and lactation in the rat. Biochem J 182: 421‐427, 1979.
 113.Flugge G, Van Kampen M, Mijnster MJ. Perturbations in brain monoamine systems during stress. Cell Tissue Res 315: 1‐14, 2004.
 114.Fox SR, Smith MS. The suppression of pulsatile luteinizing hormone secretion during lactation in the rat. Endocrinology 115: 2045‐2051, 1984.
 115.Frazao R, Dungan Lemko HM, da Silva RP, Ratra DV, Lee CE, Williams KW, Zigman JM, Elias CF. Estradiol modulates Kiss1 neuronal response to ghrelin. Am J Physiol Endocrinol Metab 306: E606‐614, 2014.
 116.Freemark M, Avril I, Fleenor D, Driscoll P, Petro A, Opara E, Kendall W, Oden J, Bridges S, Binart N, Breant B, Kelly PA. Targeted deletion of the PRL receptor: Effects on islet development, insulin production, and glucose tolerance. Endocrinology 143: 1378‐1385, 2002.
 117.Freemark M, Fleenor D, Driscoll P, Binart N, Kelly P. Body weight and fat deposition in prolactin receptor‐deficient mice. Endocrinology 142: 532‐537, 2001.
 118.Freund‐Mercier MJ, Stoeckel ME, Klein MJ. Oxytocin receptors on oxytocin neurones: Histoautoradiographic detection in the lactating rat. J Physiol 480(Pt 1): 155‐161, 1994.
 119.Friedman JM. The function of leptin in nutrition, weight, and physiology. Nutr Rev 60: S1‐14; discussion S68‐S84, 85‐17, 2002.
 120.Frontera M, Pujol E, Rodriguez‐Cuenca S, Catala‐Niell A, Roca P, Garcia‐Palmer FJ, Gianotti M. Rat brown adipose tissue thermogenic features are altered during mid‐pregnancy. Cell Physiol Biochem 15: 203‐210, 2005.
 121.Fulton S, Pissios P, Manchon RP, Stiles L, Frank L, Pothos EN, Maratos‐Flier E, Flier JS. Leptin regulation of the mesoaccumbens dopamine pathway. Neuron 51: 811‐822, 2006.
 122.Fulton S, Richard D, Woodside B, Shizgal P. Interaction of CRH and energy balance in the modulation of brain stimulation reward. Behav Neurosci 116: 651‐659, 2002.
 123.Furuta M, Funabashi T, Kimura F. Intracerebroventricular administration of ghrelin rapidly suppresses pulsatile luteinizing hormone secretion in ovariectomized rats. Biochem Biophys Res Commun 288: 780‐785, 2001.
 124.Gale S, Harlow BL. Postpartum mood disorders: A review of clinical and epidemiological factors. J Psychosom Obstet Gynaecol 24: 257‐266, 2003.
 125.Gao Q, Horvath TL. Cross‐talk between estrogen and leptin signaling in the hypothalamus. Am J Physiol Endocrinol Metab 294: E817‐826, 2008.
 126.Gao Q, Mezei G, Nie Y, Rao Y, Choi CS, Bechmann I, Leranth C, Toran‐Allerand D, Priest CA, Roberts JL, Gao XB, Mobbs C, Shulman GI, Diano S, Horvath TL. Anorectic estrogen mimics leptin's effect on the rewiring of melanocortin cells and Stat3 signaling in obese animals. Nat Med 13: 89‐94, 2007.
 127.Glasier A, McNeilly AS, Baird DT. Induction of ovarian activity by pulsatile infusion of LHRH in women with lactational amenorrhoea. Clin Endocrinol (Oxf) 24: 243‐252, 1986.
 128.Glasier A, McNeilly AS, Howie PW. Pulsatile secretion of LH in relation to the resumption of ovarian activity post partum. Clin Endocrinol (Oxf) 20: 415‐426, 1984.
 129.Grattan DR. The actions of prolactin in the brain during pregnancy and lactation. Prog Brain Res 133: 153‐171, 2001.
 130.Grattan DR. Behavioural significance of prolactin signalling in the central nervous system during pregnancy and lactation. Reproduction 123: 497‐506, 2002.
 131.Grattan DR, Jasoni CL, Liu X, Anderson GM, Herbison AE. Prolactin regulation of gonadotropin‐releasing hormone neurons to suppress luteinizing hormone secretion in mice. Endocrinology 148: 4344‐4351, 2007.
 132.Grattan DR, Kokay IC. Prolactin: A pleiotropic neuroendocrine hormone. J Neuroendocrinol 20: 752‐763, 2008.
 133.Grattan DR, Pi XJ, Andrews ZB, Augustine RA, Kokay IC, Summerfield MR, Todd B, Bunn SJ. Prolactin receptors in the brain during pregnancy and lactation: Implications for behavior. Horm Behav 40: 115‐124, 2001.
 134.Grattan DR, Steyn FJ, Kokay IC, Anderson GM, Bunn SJ. Pregnancy‐induced adaptation in the neuroendocrine control of prolactin secretion. J Neuroendocrinol 20: 497‐507, 2008.
 135.Grill HJ, Hayes MR. The nucleus tractus solitarius: A portal for visceral afferent signal processing, energy status assessment and integration of their combined effects on food intake. Int J Obes (Lond) 33 (Suppl 1): S11‐15, 2009.
 136.Grill HJ, Kaplan JM. Interoceptive and integrative contributions of forebrain and brainstem to energy balance control. Int J Obes Relat Metab Disord 25(Suppl 5): S73‐S77, 2001.
 137.Grill HJ, Kaplan JM. The neuroanatomical axis for control of energy balance. Front Neuroendocrinol 23: 2‐40, 2002.
 138.Grosvenor CE, Mena F. Effect of suckling upon the secretion and release of prolactin from the pituitary of the lactating rat. J Anim Sci 32: 115‐136, 1971.
 139.Grota LJ, Ader R. Behavior of lactating rats in a dual‐chambered maternity cage. Horm Behav 5: 275‐282, 1974.
 140.Grota LJ, Eik‐Nes KB. Plasma progesterone concentrations during pregnancy and lactation in the rat. J Reprod Fertil 13: 83‐91, 1967.
 141.Guyon A, Conductier G, Rovere C, Enfissi A, Nahon JL. Melanin‐concentrating hormone producing neurons: Activities and modulations. Peptides 30: 2031‐2039, 2009.
 142.Gyengesi E, Liu ZW, D'Agostino G, Gan G, Horvath TL, Gao XB, Diano S. Corticosterone regulates synaptic input organization of POMC and NPY/AgRP neurons in adult mice. Endocrinology 151: 5395‐5402, 2010.
 143.Hansen S, Ferreira A. Effects of bicuculline infusions in the ventromedial hypothalamus and amygdaloid complex on food intake and affective behavior in mother rats. Behav Neurosci 100: 410‐415, 1986.
 144.Hansen S, Ferreira A, Selart ME. Behavioural similarities between mother rats and benzodiazepine‐treated non‐maternal animals. Psychopharmacology (Berl) 86: 344‐347, 1985.
 145.Hansen S, Sodersten P, Eneroth P. Mechanisms regulating hormone release and the duration of dioestrus in the lactating rat. J Endocrinol 99: 173‐180, 1983.
 146.Hard E, Hansen S. Reduced fearfulness in the lactating rat. Physiol Behav 35: 641‐643, 1985.
 147.Hayssen V. Empirical and theoretical constraints on the evolution of lactation. J Dairy Sci 76: 3213‐3233, 1993.
 148.Heinrichs M, Meinlschmidt G, Neumann I, Wagner S, Kirschbaum C, Ehlert U, Hellhammer DH. Effects of suckling on hypothalamic‐pituitary‐adrenal axis responses to psychosocial stress in postpartum lactating women. J Clin Endocrinol Metab 86: 4798‐4804, 2001.
 149.Heinrichs M, Neumann I, Ehlert U. Lactation and stress: Protective effects of breast‐feeding in humans. Stress 5: 195‐203, 2002.
 150.Herbison AE. Estrogen positive feedback to gonadotropin‐releasing hormone (GnRH) neurons in the rodent: The case for the rostral periventricular area of the third ventricle (RP3V). Brain Res Rev 57: 277‐287, 2008.
 151.Herman JP, Figueiredo H, Mueller NK, Ulrich‐Lai Y, Ostrander MM, Choi DC, Cullinan WE. Central mechanisms of stress integration: Hierarchical circuitry controlling hypothalamo‐pituitary‐adrenocortical responsiveness. Front Neuroendocrinol 24: 151‐180, 2003.
 152.Herman JP, Ostrander MM, Mueller NK, Figueiredo H. Limbic system mechanisms of stress regulation: Hypothalamo‐pituitary‐adrenocortical axis. Prog Neuropsychopharmacol Biol Psychiatry 29: 1201‐1213, 2005.
 153.Higuchi T, Honda K, Takano S, Negoro H. Reduced oxytocin response to osmotic stimulus and immobilization stress in lactating rats. J Endocrinol 116: 225‐230, 1988.
 154.Higuchi T, Negoro H, Arita J. Reduced responses of prolactin and catecholamine to stress in the lactating rat. J Endocrinol 122: 495‐498, 1989.
 155.Hillerer KM, Neumann ID, Slattery DA. From stress to postpartum mood and anxiety disorders: How chronic peripartum stress can impair maternal adaptations. Neuroendocrinology 95: 22‐38, 2012.
 156.Hillerer KM, Reber SO, Neumann ID, Slattery DA. Exposure to chronic pregnancy stress reverses peripartum‐associated adaptations: Implications for postpartum anxiety and mood disorders. Endocrinology 152: 3930‐3940, 2011.
 157.Hommel JD, Trinko R, Sears RM, Georgescu D, Liu ZW, Gao XB, Thurmon JJ, Marinelli M, DiLeone RJ. Leptin receptor signaling in midbrain dopamine neurons regulates feeding. Neuron 51: 801‐810, 2006.
 158.Howie PW, McNeilly AS, Houston MJ, Cook A, Boyle H. Effect of supplementary food on suckling patterns and ovarian activity during lactation. Br Med J (Clin Res Ed) 283: 757‐759, 1981.
 159.Illingworth PJ, Seaton JE, McKinlay C, Reid‐Thomas V, McNeilly AS. Low dose transdermal oestradiol suppresses gonadotrophin secretion in breast‐feeding women. Hum Reprod 10: 1671‐1677, 1995.
 160.Imai‐Matsumara K, Matsumura K, Morimoto A, Nakayama T. Suppression of cold‐induced thermogenesis in full‐term pregnant rats. J Physiol 425: 271‐281, 1990.
 161.Insel TR. Postpartum increases in brain oxytocin binding. Neuroendocrinology 44: 515‐518, 1986.
 162.Insel TR. Regional changes in brain oxytocin receptors post‐partum: Time‐course and relationship to maternal behaviour. J Neuroendocrinol 2: 539‐545, 1990.
 163.Isler D, Trayhurn P, Lunn PG. Brown adipose tissue metabolism in lactating rats: The effect of litter size. Ann Nutr Metab 28: 101‐109, 1984.
 164.Jahn GA, Deis RP. Stress‐induced prolactin release in female, male and androgenized rats: Influence of progesterone treatment. J Endocrinol 110: 423‐428, 1986.
 165.Jahn GA, Edery M, Belair L, Kelly PA, Djiane J. Prolactin receptor gene expression in rat mammary gland and liver during pregnancy and lactation. Endocrinology 128: 2976‐2984, 1991.
 166.Jenness R. Lactational performance of various mammalian species. J Dairy Sci 69: 869‐885, 1986.
 167.Johnston JM, Amico JA. A prospective longitudinal study of the release of oxytocin and prolactin in response to infant suckling in long term lactation. J Clin Endocrinol Metab 62: 653‐657, 1986.
 168.Johnstone LE, Higuchi T. Food intake and leptin during pregnancy and lactation. Prog Brain Res 133: 215‐227, 2001.
 169.Jonas K, Johansson LM, Nissen E, Ejdeback M, Ransjo‐Arvidson AB, Uvnas‐Moberg K. Effects of intrapartum oxytocin administration and epidural analgesia on the concentration of plasma oxytocin and prolactin, in response to suckling during the second day postpartum. Breastfeed Med 4: 71‐82, 2009.
 170.Jonas W, Nissen E, Ransjo‐Arvidson AB, Matthiesen AS, Uvnas‐Moberg K. Influence of oxytocin or epidural analgesia on personality profile in breastfeeding women: A comparative study. Arch Womens Ment Health 11: 335‐345, 2008.
 171.Jonas W, Nissen E, Ransjo‐Arvidson AB, Wiklund I, Henriksson P, Uvnas‐Moberg K. Short‐ and long‐term decrease of blood pressure in women during breastfeeding. Breastfeed Med 3: 103‐109, 2008.
 172.Jurek B, Slattery DA, Maloumby R, Hillerer K, Koszinowski S, Neumann ID, van den Burg EH. Differential contribution of hypothalamic MAPK activity to anxiety‐like behaviour in virgin and lactating rats. PloS One 7: e37060, 2012.
 173.Kalra PS, Dube MG, Kalra SP. Effects of centrally administered antisense oligodeoxynucleotides on feeding behavior and hormone secretion. Methods Enzymol 314: 184‐200, 2000.
 174.Kaye J, Soothill P, Hunt M, Lightman S. Responses to the 35% CO challenge in postpartum women. Clin Endocrinol (Oxf) 61: 582‐588, 2004.
 175.Kennedy KI, Labbok MH, Van Look PF. Lactational amenorrhea method for family planning. Int J Gynaecol Obstet 54: 55‐57, 1996.
 176.Kent S, Hurd M, Satinoff E. Interactions between body temperature and wheel running over the estrous cycle in rats. Physiol Behav 49: 1079‐1084, 1991.
 177.Kim JD, Leyva S, Diano S. Hormonal regulation of the hypothalamic melanocortin system. Front Physiol 5: 480, 2014.
 178.Knollema S, Brown ER, Vale W, Sawchenko PE. Novel hypothalamic and preoptic sites of prepro‐melanin‐concentrating hormone messenger ribonucleic Acid and Peptide expression in lactating rats. J Neuroendocrinol 4: 709‐717, 1992.
 179.Kokay IC, Bull PM, Davis RL, Ludwig M, Grattan DR. Expression of the long form of the prolactin receptor in magnocellular oxytocin neurons is associated with specific prolactin regulation of oxytocin neurons. Am J Physiol Regul Integr Comp Physiol 290: R1216‐1225, 2006.
 180.Kokay IC, Grattan DR. Expression of mRNA for prolactin receptor (long form) in dopamine and pro‐opiomelanocortin neurones in the arcuate nucleus of non‐pregnant and lactating rats. J Neuroendocrinol 17: 827‐835, 2005.
 181.Ladyman SR, Grattan DR. Region‐specific reduction in leptin‐induced phosphorylation of signal transducer and activator of transcription‐3 (STAT3) in the rat hypothalamus is associated with leptin resistance during pregnancy. Endocrinology 145: 3704‐3711, 2004.
 182.Ladyman SR, Grattan DR. Suppression of leptin receptor messenger ribonucleic acid and leptin responsiveness in the ventromedial nucleus of the hypothalamus during pregnancy in the rat. Endocrinology 146: 3868‐3874, 2005.
 183.Ladyman SR, Woodside B. Food restriction during lactation suppresses Kiss1 mRNA expression and kisspeptin‐stimulated LH release in rats. Reproduction 147: 743‐751, 2014.
 184.Ladyman SR, Woodside B. Regulation of maternal food intake and mother‐pup interactions by the Y5 receptor. Physiol Behav 97: 91‐97, 2009.
 185.Lamming G. Control of Ovulation. London: Butterworth, 1978.
 186.Larsen CM, Grattan DR. Prolactin‐induced mitogenesis in the subventricular zone of the maternal brain during early pregnancy is essential for normal postpartum behavioral responses in the mother. Endocrinology 151: 3805‐3814, 2010.
 187.Lehman MN, Coolen LM, Goodman RL. Minireview: Kisspeptin/neurokinin B/dynorphin (KNDy) cells of the arcuate nucleus: A central node in the control of gonadotropin‐releasing hormone secretion. Endocrinology 151: 3479‐3489, 2010.
 188.Lehman MN, Hileman SM, Goodman RL. Neuroanatomy of the kisspeptin signaling system in mammals: Comparative and developmental aspects. Adv Exp Med Biol 784: 27‐62, 2013.
 189.Lehman MN, Merkley CM, Coolen LM, Goodman RL. Anatomy of the kisspeptin neural network in mammals. Brain Res 1364: 90‐102, 2010.
 190.Leng G, Ludwig M. Intranasal oxytocin: Myths and delusions. Biol Psychiatry 79: 243‐250, 2015.
 191.Leng G, Meddle SL, Douglas AJ. Oxytocin and the maternal brain. Curr Opin Pharmacol 8: 731‐734, 2008.
 192.Li C, Chen P, Smith MS. The acute suckling stimulus induces expression of neuropeptide Y (NPY) in cells in the dorsomedial hypothalamus and increases NPY expression in the arcuate nucleus. Endocrinology 139: 1645‐1652, 1998.
 193.Li C, Chen P, Smith MS. Morphological evidence for direct interaction between arcuate nucleus neuropeptide Y (NPY) neurons and gonadotropin‐releasing hormone neurons and the possible involvement of NPY Y1 receptors. Endocrinology 140: 5382‐5390, 1999.
 194.Li C, Chen P, Smith MS. Neural populations in the rat forebrain and brainstem activated by the suckling stimulus as demonstrated by cFos expression. Neuroscience 94: 117‐129, 1999.
 195.Li C, Chen P, Smith MS. Neuropeptide Y (NPY) neurons in the arcuate nucleus (ARH) and dorsomedial nucleus (DMH), areas activated during lactation, project to the paraventricular nucleus of the hypothalamus (PVH). Regul Pept 75‐76: 93‐100, 1998.
 196.Li G, Zhang Y, Rodrigues E, Zheng D, Matheny M, Cheng KY, Scarpace PJ. Melanocortin activation of nucleus of the solitary tract avoids anorectic tachyphylaxis and induces prolonged weight loss. Am J Physiol Endocrinol Metab 293: E252‐258, 2007.
 197.Lightman SL, Windle RJ, Wood SA, Kershaw YM, Shanks N, Ingram CD. Peripartum plasticity within the hypothalamo‐pituitary‐adrenal axis. Prog Brain Res 133: 111‐129, 2001.
 198.Lightman SL, Young WS, III. Lactation inhibits stress‐mediated secretion of corticosterone and oxytocin and hypothalamic accumulation of corticotropin‐releasing factor and enkephalin messenger ribonucleic acids. Endocrinology 124: 2358‐2364., 1989.
 199.Lincoln DW, Paisley AC. Neuroendocrine control of milk ejection. J Reprod Fertil 65: 571‐586, 1982.
 200.Linden A. Role of cholecystokinin in feeding and lactation. Acta Physiol Scand Suppl 585: i‐vii, 1‐49, 1989.
 201.Linden A, Eriksson M, Hansen S, Uvnas‐Moberg K. Suckling‐induced release of cholecystokinin into plasma in the lactating rat: Effects of abdominal vagotomy and lesions of central pathways concerned with milk ejection. J Endocrinol 127: 257‐263, 1990.
 202.Liu X, Brown RS, Herbison AE, Grattan DR. Lactational anovulation in mice results from a selective loss of kisspeptin input to GnRH neurons. Endocrinology 155: 193‐203, 2014.
 203.Liu X, Herbison A. Kisspeptin regulation of arcuate neuron excitability in kisspeptin receptor knockout mice. Endocrinology 156: 1815‐1827, 2015.
 204.Lof M, Forsum E. Activity pattern and energy expenditure due to physical activity before and during pregnancy in healthy Swedish women. Br J Nutr 95: 296‐302, 2006.
 205.Lonstein JS. Reduced anxiety in postpartum rats requires recent physical interactions with pups, but is independent of suckling and peripheral sources of hormones. Horm Behav 47: 241‐255, 2005.
 206.Lonstein JS. Regulation of anxiety during the postpartum period. Front Neuroendocrinol 28: 115‐141, 2007.
 207.Lonstein JS, Maguire J, Meinlschmidt G, Neumann ID. Emotion and mood adaptations in the peripartum female:complementary contributions of GABA and oxytocin. J Neuroendocrinol 26: 649‐664, 2014.
 208.Lonstein JS, Stern JM. Role of the midbrain periaqueductal gray in maternal nurturance and aggression: c‐fos and electrolytic lesion studies in lactating rats. J Neurosci 17: 3364‐3378, 1997.
 209.Loudon AS, McNeilly AS, Milne JA. Nutrition and lactational control of fertility in red deer. Nature 302: 145‐147, 1983.
 210.Louis GW, Greenwald‐Yarnell M, Phillips R, Coolen LM, Lehman MN, Myers MG, Jr. Molecular mapping of the neural pathways linking leptin to the neuroendocrine reproductive axis. Endocrinology 152: 2302‐2310, 2011.
 211.Luo N, Marcelin G, Liu SM, Schwartz G, Chua S, Jr. Neuropeptide Y and agouti‐related peptide mediate complementary functions of hyperphagia and reduced energy expenditure in leptin receptor deficiency. Endocrinology 152: 883‐889, 2011.
 212.Maeda K, Tsukamura H, Yokoyama A. Suppression of luteinizing hormone secretion is removed at late lactation in ovariectomized lactating rats. Endocrinol Jpn 34: 709‐716, 1987.
 213.Maeda K, Uchida E, Tsukamura H, Ohkura N, Ohkura S, Yokoyama A. Prolactin does not mediate the suppressive effect of the suckling stimulus on luteinizing hormone secretion in ovariectomized lactating rats. Endocrinol Jpn 37: 405‐411., 1990.
 214.Maestripieri D. Emotions, stress, and maternal motivation in primates. Am J Primatol 73: 516‐529, 2011.
 215.Mann PE, Rubin RS, Bridges RS. Differential proopiomelanocortin gene expression in the medial basal hypothalamus of rats during pregnancy and lactation. Brain Res Mol Brain Res 46: 9‐16, 1997.
 216.Marshall JC, Dalkin AC, Haisenleder DJ, Paul SJ, Ortolano GA, Kelch RP. Gonadotropin‐releasing hormone pulses: Regulators of gonadotropin synthesis and ovulatory cycles. Recent Prog Horm Res 47: 155‐187; discussion 188‐159, 1991.
 217.Martin C, Navarro VM, Simavli S, Vong L, Carroll RS, Lowell BB, Kaiser UB. Leptin‐responsive GABAergic neurons regulate fertility through pathways that result in reduced kisspeptinergic tone. J Neurosci 34: 6047‐6056, 2014.
 218.Martin RH, Glass MR, Chapman C, Wilson GD, Woods KL. Suppression by bromocriptine of the serum lactalbumin peak associated with human lactogenesis. Clin Endocrinol (Oxf) 14: 363‐366, 1981.
 219.Mattheij JA, Gruisen EF, Swarts JJ. The suckling‐induced rise of plasma prolactin in lactating rats: Its dependence on stage of lactation and litter size. Horm Res 11: 325‐336, 1979.
 220.Mattheij JA, Swarts HJ, Verstijnen CP. The response of plasma prolactin to suckling during normal and prolonged lactation in the rat. Horm Res 20: 261‐268, 1984.
 221.Mattson BJ, Williams S, Rosenblatt JS, Morrell JI. Comparison of two positive reinforcing stimuli: Pups and cocaine throughout the postpartum period. Behav Neurosci 115: 683‐694, 2001.
 222.McNeilly AS. Lactational control of reproduction. Reprod Fertil Dev 13: 583‐590, 2001.
 223.McNeilly AS. Neuroendocrine changes and fertility in breast‐feeding women. In: Russell JA, Douglas AJ, Windle RJ, Ingram CD, editors. The Maternal Brain: Neurobiological and Neuroendocvrine Adaptation and Disorders in Pregnancy and Post Partum. Bristol, U.K.: Elsevier, 2001, pp. 207‐214.
 224.McNeilly AS. Neuroendocrine changes and fertility in breast‐feeding women. Prog Brain Res 133: 207‐214, 2001.
 225.McNeilly AS, Glasier AF, Howie PW, Houston MJ, Cook A, Boyle H. Fertility after childbirth: Pregnancy associated with breast feeding. Clin Endocrinol (Oxf) 19: 167‐173, 1983.
 226.McNeilly AS, Howie PW, Houston MJ, Cook A, Boyle H. Fertility after childbirth: Adequacy of post‐partum luteal phases. Clin Endocrinol (Oxf) 17: 609‐615, 1982.
 227.Mens WB, Witter A, van Wimersma Greidanus TB. Penetration of neurohypophyseal hormones from plasma into cerebrospinal fluid (CSF): Half‐times of disappearance of these neuropeptides from CSF. Brain Res 262: 143‐149, 1983.
 228.Mezzacappa ES, Kelsey RM, Katkin ES. Breast feeding, bottle feeding, and maternal autonomic responses to stress. J Psychosom Res 58: 351‐365, 2005.
 229.Millelire L, Woodside B. Factors influencing the self‐selection of calcium in lactating rats. Physiol Behav 46: 429‐434, 1989.
 230.Miller SC, Shupe JG, Redd EH, Miller MA, Omura TH. Changes in bone mineral and bone formation rates during pregnancy and lactation in rats. Bone 7: 283‐287, 1986.
 231.Miller SM, Piasecki CC, Peabody MF, Lonstein JS. GABA(A) receptor antagonism in the ventrocaudal periaqueductal gray increases anxiety in the anxiety‐resistant postpartum rat. Pharmacol Biochem Behav 95: 457‐465, 2010.
 232.Misaki N, Higuchi H, Yamagata K, Miki N. Identification of glucocorticoid responsive elements (GREs) at far upstream of rat NPY gene. Neurochem Int 21: 185‐189, 1992.
 233.Mitchell JB, Gratton A. Involvement of mesolimbic dopamine neurons in sexual behaviors: Implications for the neurobiology of motivation. Rev Neurosci 5: 317‐329, 1994.
 234.Morales T, Sawchenko PE. Brainstem prolactin‐releasing peptide neurons are sensitive to stress and lactation. Neuroscience 121: 771‐778, 2003.
 235.Naef L, Woodside B. Prolactin/leptin interactions in the control of food intake in rats. Endocrinology 148: 5977‐5983, 2007.
 236.Nagatani S, Guthikonda P, Thompson RC, Tsukamura H, Maeda KI, Foster DL. Evidence for GnRH regulation by leptin: Leptin administration prevents reduced pulsatile LH secretion during fasting. Neuroendocrinology 67: 370‐376, 1998.
 237.Nagy G, Kacsoh B, Halasz B. Episodic prolactin and growth hormone secretion not related to the actual suckling activity in lactating rats. J Endocrinol 111: 137‐142, 1986.
 238.Naismith DJ, Morgan BL. The biphasic nature of protein metabolism during pregnancy in the rat. Br J Nutr 36: 563‐566, 1976.
 239.Naismith DJ, Richardson DP, Pritchard AE. The utilization of protein and energy during lactation in the rat, with particular regard to the use of fat accumulated in pregnancy. Br J Nutr 48: 433‐441, 1982.
 240.Nephew BC, Bridges RS, Lovelock DF, Byrnes EM. Enhanced maternal aggression and associated changes in neuropeptide gene expression in multiparous rats. Behav Neurosci 123: 949‐957, 2009.
 241.Neumann I, Koehler E, Landgraf R, Summy‐Long J. An oxytocin receptor antagonist infused into the supraoptic nucleus attenuates intranuclear and peripheral release of oxytocin during suckling in conscious rats. Endocrinology 134: 141‐148, 1994.
 242.Neumann I, Pittman QJ, Landgraf R. Release of oxytocin within the supraoptic nucleus. Mechanisms, physiological significance and antisense targeting. Adv Exp Med Biol 395: 173‐183, 1995.
 243.Neumann ID, Kromer SA, Toschi N, Ebner K. Brain oxytocin inhibits the (re)activity of the hypothalamo‐pituitary‐adrenal axis in male rats: Involvement of hypothalamic and limbic brain regions. Regul Pept 96: 31‐38, 2000.
 244.Neumann ID, Torner L, Wigger A. Brain oxytocin: Differential inhibition of neuroendocrine stress responses and anxiety‐related behaviour in virgin, pregnant and lactating rats. Neuroscience 95: 567‐575, 2000.
 245.Neumann ID, Wigger A, Torner L, Holsboer F, Landgraf R. Brain oxytocin inhibits basal and stress‐induced activity of the hypothalamo‐pituitary‐adrenal axis in male and female rats: Partial action within the paraventricular nucleus. J Neuroendocrinol 12: 235‐243, 2000.
 246.Nissen E, Gustavsson P, Widstrom AM, Uvnas‐Moberg K. Oxytocin, prolactin, milk production and their relationship with personality traits in women after vaginal delivery or Cesarean section. J Psychosom Obstet Gynaecol 19: 49‐58, 1998.
 247.Noel MB, Woodside B. Effects of systemic and central prolactin injections on food intake, weight gain, and estrous cyclicity in female rats. Physiol Behav 54: 151‐154, 1993.
 248.Numan M, Fleming AS, Levy F. Maternal behavior. In: Neill JD, editor. Knobil and Neill's Physiology of Reproduction. New York: Elsevier, 2006, pp. 1921‐1993.
 249.Numan M, Insel TR. The Neurobiology of Parental Behavior. New York: Springer Verlag, 2003.
 250.Numan M, Woodside B. Maternity: Neural mechanisms, motivational processes, and physiological adaptations. Behav Neurosci 124: 715‐741, 2010.
 251.Oftedal OT. Use of maternal reserves as a lactation strategy in large mammals. Proc Nutr Soc 59: 99‐106, 2000.
 252.Ohkura S, Uenoyama Y, Yamada S, Homma T, Takase K, Inoue N, Maeda K, Tsukamura H. Physiological role of metastin/kisspeptin in regulating gonadotropin‐releasing hormone (GnRH) secretion in female rats. Peptides 30: 49‐56, 2009.
 253.Okamura H, Tsukamura H, Ohkura S, Uenoyama Y, Wakabayashi Y, Maeda K. Kisspeptin and GnRH pulse generation. Adv Exp Med Biol 784: 297‐323, 2013.
 254.Oltmans GA, Lorden JF, Margules DL. Food intake and body weight: Effects of specific and non‐specific lesions in the midbrain path of the ascending noradrenergic neurons of the rat. Brain Res 128: 293‐308, 1977.
 255.Palkovits M, Usdin TB, Makara GB, Dobolyi A. Tuberoinfundibular peptide of 39 residues‐ immunoreactive fibers in the zona incerta and the supraoptic decussations terminate in the neuroendocrine hypothalamus. Neurochem Res 35: 2078‐2085, 2010.
 256.Paul AA, Muller EM, Whitehead RG. Seasonal variations in energy intake, body‐weight and skinfold thickness in pregnant and lactating women in rural Gambia. Proc Nutr Soc 38: 28A, 1979.
 257.Pawluski JL, Charlier TD, Lieblich SE, Hammond GL, Galea LA. Reproductive experience alters corticosterone and CBG levels in the rat dam. Physiol Behav 96: 108‐114, 2009.
 258.Pedersen CA, Caldwell JD, Walker C, Ayers G, Mason GA. Oxytocin activates the postpartum onset of rat maternal behavior in the ventral tegmental and medial preoptic areas. Behav Neurosci 108: 1163‐1171, 1994.
 259.Pelleymounter MA, Cullen MJ, Baker MB, Hecht R, Winters D, Boone T, Collins F. Effects of the obese gene product on body weight regulation in ob/ob mice. Science 269: 540‐543, 1995.
 260.Perheentupa A, Critchley HO, Illingworth PJ, McNeilly AS. Enhanced sensitivity to steroid‐negative feedback during breast‐feeding: Low‐dose estradiol (transdermal estradiol supplementation) suppresses gonadotropins and ovarian activity assessed by inhibin B. J Clin Endocrinol Metab 85: 4280‐4286, 2000.
 261.Peterson AE, Perez‐Escamilla R, Labbok MH, Hight V, von Hertzen H, Van Look P. Multicenter study of the lactational amenorrhea method (LAM) III: Effectiveness, duration, and satisfaction with reduced client‐provider contact. Contraception 62: 221‐230, 2000.
 262.Pinilla L, Aguilar E, Dieguez C, Millar RP, Tena‐Sempere M. Kisspeptins and reproduction: Physiological roles and regulatory mechanisms. Physiol Rev 92: 1235‐1316, 2012.
 263.Plotsky PM. Facilitation of immunoreactive corticotropin‐releasing factor secretion into the hypophysial‐portal circulation after activation of catecholaminergic pathways or central norepinephrine injection. Endocrinology 121: 924‐930, 1987.
 264.Plotsky PM. Regulation of hypophysiotropic factors mediating ACTH secretion. Ann N Y Acad Sci 512: 205‐217, 1987.
 265.Plotsky PM, Otto S, Sutton S. Neurotransmitter modulation of corticotropin releasing factor secretion into the hypophysial‐portal circulation. Life Sci 41: 1311‐1317, 1987.
 266.Popeski N, Woodside B. Effect of nitric oxide synthase inhibition on fos expression in the hypothalamus of female rats following central oxytocin and systemic urethane administration. J Neuroendocrinol 13: 596‐607, 2001.
 267.Quennell JH, Mulligan AC, Tups A, Liu X, Phipps SJ, Kemp CJ, Herbison AE, Grattan DR, Anderson GM. Leptin indirectly regulates gonadotropin‐releasing hormone neuronal function. Endocrinology 150: 2805‐2812, 2009.
 268.Radley JJ, Arias CM, Sawchenko PE. Regional differentiation of the medial prefrontal cortex in regulating adaptive responses to acute emotional stress. J Neurosci 26: 12967‐12976, 2006.
 269.Radley JJ, Gosselink KL, Sawchenko PE. A discrete GABAergic relay mediates medial prefrontal cortical inhibition of the neuroendocrine stress response. J Neurosci 29: 7330‐7340, 2009.
 270.Radley JJ, Sawchenko PE. A common substrate for prefrontal and hippocampal inhibition of the neuroendocrine stress response. J Neurosci 31: 9683‐9695, 2011.
 271.Ragan CM, Lonstein JS. Differential postpartum sensitivity to the anxiety‐modulating effects of offspring contact is associated with innate anxiety and brainstem levels of dopamine beta‐hydroxylase in female laboratory rats. Neuroscience 256: 433‐444, 2014.
 272.Ramos MP, Crespo‐Solans MD, del Campo S, Cacho J, Herrera E. Fat accumulation in the rat during early pregnancy is modulated by enhanced insulin responsiveness. Am J Physiol Endocrinol Metab 285: E318‐328, 2003.
 273.Richter CP, Barelare B. Nutritional requirements of pregnant and lactating rats studied by the self‐selection method. Endocrinology 23: 15‐24, 1938.
 274.Riediger T. The receptive function of hypothalamic and brainstem centres to hormonal and nutrient signals affecting energy balance. Proc Nutr Soc 71: 463‐477, 2012.
 275.Ritter RC, Slusser PG, Stone S. Glucoreceptors controlling feeding and blood glucose: Location in the hindbrain. Science 213: 451‐452, 1981.
 276.Ritter S, Bugarith K, Dinh TT. Immunotoxic destruction of distinct catecholamine subgroups produces selective impairment of glucoregulatory responses and neuronal activation. J Comp Neurol 432: 197‐216, 2001.
 277.Ritter S, Dinh TT, Zhang Y. Localization of hindbrain glucoreceptive sites controlling food intake and blood glucose. Brain Res 856: 37‐47, 2000.
 278.Roa J, Herbison AE. Direct regulation of GnRH neuron excitability by arcuate nucleus POMC and NPY neuron neuropeptides in female mice. Endocrinology 153: 5587‐5599, 2012.
 279.Roa J, Vigo E, Castellano JM, Navarro VM, Fernandez‐Fernandez R, Casanueva FF, Dieguez C, Aguilar E, Pinilla L, Tena‐Sempere M. Hypothalamic expression of KiSS‐1 system and gonadotropin‐releasing effects of kisspeptin in different reproductive states of the female Rat. Endocrinology 147: 2864‐2878, 2006.
 280.Robinson CJ, Spanos E, James MF, Pike JW, Haussler MR, Makeen AM, Hillyard CJ, MacIntyre I. Role of prolactin in vitamin D metabolism and calcium absorption during lactation in the rat. J Endocrinol 94: 443‐453, 1982.
 281.Romano N, Yip SH, Hodson DJ, Guillou A, Parnaudeau S, Kirk S, Tronche F, Bonnefont X, Le Tissier P, Bunn SJ, Grattan DR, Mollard P, Martin AO. Plasticity of hypothalamic dopamine neurons during lactation results in dissociation of electrical activity and release. J Neurosci 33: 4424‐4433, 2013.
 282.Rondini TA, Donato J, Jr, Rodrigues Bde C, Bittencourt JC, Elias CF. Chemical identity and connections of medial preoptic area neurons expressing melanin‐concentrating hormone during lactation. J Chem Neuroanat 39: 51‐62, 2010.
 283.Rothchild I. The corpus luteum‐pituitary relationship: The association between the cause of luteotrophin secretion and the cause of follicular quiescence during lactation; the basis for a tentative theory of the corpus luteum‐pituitary relationship in the rat. Endocrinology 67: 9‐41, 1960.
 284.Roy AF, Benomar Y, Bailleux V, Vacher CM, Aubourg A, Gertler A, Djiane J, Taouis M. Lack of cross‐desensitization between leptin and prolactin signaling pathways despite the induction of suppressor of cytokine signaling 3 and PTP‐1B. J Endocrinol 195: 341‐350, 2007.
 285.Salamone JD, Mahan K, Rogers S. Ventrolateral striatal dopamine depletions impair feeding and food handling in rats. Pharmacol Biochem Behav 44: 605‐610, 1993.
 286.Salamone JD, Zigmond MJ, Stricker EM. Characterization of the impaired feeding behavior in rats given haloperidol or dopamine‐depleting brain lesions. Neuroscience 39: 17‐24, 1990.
 287.Santos NR, Huston JP, Brandao ML. Blockade of histamine H2 receptors of the periaqueductal gray and inferior colliculus induces fear‐like behaviors. Pharmacol Biochem Behav 75: 25‐33, 2003.
 288.Sar M, Meites J. Effects of suckling on pituitary release of prolactin, GH, and TSH in postpartum lactating rats. Neuroendocrinology 4: 25‐31, 1969.
 289.Sauve D, Woodside B. The effect of central administration of prolactin on food intake in virgin female rats is dose‐dependent, occurs in the absence of ovarian hormones and the latency to onset varies with feeding regimen. Brain Res 729: 75‐81, 1996.
 290.Schlein PA, Zarrow MX, Denenberg VH. The role of prolactin in the depressed or ‘buffered’ adrenocorticosteroid response of the rat. J Endocrinol 62: 93‐99, 1974.
 291.Schneider JE. Energy balance and reproduction. Physiol Behav 81: 289‐317, 2004.
 292.Segal‐Lieberman G, Trombly DJ, Juthani V, Wang X, Maratos‐Flier E. NPY ablation in C57BL/6 mice leads to mild obesity and to an impaired refeeding response to fasting. Am J Physiol Endocrinol Metab 284: E1131‐1139, 2003.
 293.Shanks N, Windle RJ, Perks P, Wood S, Ingram CD, Lightman SL. The hypothalamic‐pituitary‐adrenal axis response to endotoxin is attenuated during lactation. J Neuroendocrinol 11: 857‐865, 1999.
 294.Slattery DA, Neumann ID. No stress please! Mechanisms of stress hyporesponsiveness of the maternal brain. J Physiol 586: 377‐385, 2008.
 295.Slonaker JR. The effect of copulation, pregnancy, pseudopregnancy and lactation on the voluntary activity and food consumption of the albino rat. Am J Physiol 71: 362‐394, 1924.
 296.Smith JT, Acohido BV, Clifton DK, Steiner RA. KiSS‐1 neurones are direct targets for leptin in the ob/ob mouse. J Neuroendocrinol 18: 298‐303, 2006.
 297.Smith JT, Reichenbach A, Lemus M, Mani BK, Zigman JM, Andrews ZB. An eGFP‐expressing subpopulation of growth hormone secretagogue receptor cells are distinct from kisspeptin, tyrosine hydroxylase, and RFamide‐related peptide neurons in mice. Peptides 47: 45‐53, 2013.
 298.Smith MS. A comparison of pituitary responsiveness to luteinizing hormone‐ releasing hormone during lactation and the estrous cycle of the rat. Endocrinology 102: 114‐120, 1978.
 299.Smith MS. Hypothalamic‐pituitary responsiveness during lactation in the rat: Estrogen‐induced luteinizing hormone surges. Endocrinology 102: 121‐127, 1978.
 300.Smith MS. Lactation alters neuropeptide‐Y and proopiomelanocortin gene expression in the arcuate nucleus of the rat. Endocrinology 133: 1258‐1265, 1993.
 301.Smith MS. The relative contribution of suckling and prolactin to the inhibition of gonadotropin secretion during lactation in the rat. Biol Reprod 19: 77‐83, 1978.
 302.Smith MS. Release of luteinizing hormone and follicle‐stimulating hormone from pituitaries of lactating rats by gonadotropin‐releasing hormone and high potassium concentration. Endocrinology 116: 1826‐1834, 1985.
 303.Smith MS, Fox SR. Regulation of gonadotropin secretion during lactation. Arch Biol Med Exp (Santiago) 17: 231‐238, 1984.
 304.Smith MS, Grove KL. Integration of the regulation of reproductive function and energy balance: Lactation as a model. Front Neuroendocrinol 23: 225‐256, 2002.
 305.Smith MS, Neill JD. Inhibition of gonadotropin secretion during lactation in the rat: Relative contribution of suckling and ovarian steroids. Biol Reprod 17: 255‐261, 1977.
 306.Smotherman WP, Brown CP, Levine S. Maternal responsiveness following differential pup treatment and mother‐pup interactions. Horm Behav 8: 242‐253, 1977.
 307.Sodersten P, Eneroth P. Suckling and serum prolactin and LH concentrations in lactating rats. J Endocrinol 102: 251‐256., 1984.
 308.Stern JM, Goldman L, Levine S. Pituitary‐adrenal responsiveness during lactation in rats. Neuroendocrinology 12: 179‐191, 1973.
 309.Stern JM, Levine S. Pituitary‐adrenal activity in the postpartum rat in the absence of suckling stimulation. Horm Behav 3: 237‐246, 1972.
 310.Stern JM, Levine S. Psychobiological aspects of lactation in rats. Prog Brain Res 41: 433‐444, 1974.
 311.Steyn FJ, Anderson GM, Grattan DR. Expression of ovarian steroid hormone receptors in tuberoinfundibular dopaminergic neurones during pregnancy and lactation. J Neuroendocrinol 19: 788‐793, 2007.
 312.Stolzenberg DS, Numan M. Hypothalamic interaction with the mesolimbic DA system in the control of the maternal and sexual behaviors in rats. Neurosci Biobehav Rev 35: 826‐847, 2011.
 313.Strubbe JH, Gorissen J. Meal patterning in the lactating rat. Physiol Behav 25: 775‐777, 1980.
 314.Stuebe AM, Grewen K, Meltzer‐Brody S. Association between maternal mood and oxytocin response to breastfeeding. J Womens Health 22: 352‐361, 2013.
 315.Sullivan SD, Moenter SM. Gamma‐aminobutyric acid neurons integrate and rapidly transmit permissive and inhibitory metabolic cues to gonadotropin‐releasing hormone neurons. Endocrinology 145: 1194‐1202, 2004.
 316.Suzuki Y, Kurose Y, Takahashi H, Asakuma S, Azuma Y, Kobayashi S. The differences in feeding‐inhibitory responses to peripheral and central leptin between non‐lactating and lactating rats. J Endocrinol 207: 105‐111, 2010.
 317.Szabo FK, Snyder N, Usdin TB, Hoffman GE. A direct neuronal connection between the subparafascicular and ventrolateral arcuate nuclei in non‐lactating female rats. Could this pathway play a role in the suckling‐induced prolactin release? Endocrine 37: 62‐70, 2010.
 318.Tay CC, Glasier AF, McNeilly AS. The 24 h pattern of pulsatile luteinizing hormone, follicle stimulating hormone and prolactin release during the first 8 weeks of lactational amenorrhoea in breastfeeding women. Hum Reprod 7: 951‐958, 1992.
 319.Tay CC, Glasier AF, McNeilly AS. Effect of antagonists of dopamine and opiates on the basal and GnRH‐ induced secretion of luteinizing hormone, follicle stimulating hormone and prolactin during lactational amenorrhoea in breastfeeding women. Hum Reprod 8: 532‐539, 1993.
 320.Tay CC, Glasier AF, McNeilly AS. Twenty‐four hour patterns of prolactin secretion during lactation and the relationship to suckling and the resumption of fertility in breast‐ feeding women. Hum Reprod 11: 950‐955, 1996.
 321.Taya K, Greenwald GS. Peripheral blood and ovarian levels of sex steroids in the lactating rat. Endocrinol Jpn 29: 453‐459, 1982.
 322.Thoman EB, Conner RL, Levine S. Lactation suppresses adrenal corticosteroid activity and aggressiveness in rats. J Comp Physiol Psychol 70: 364‐369, 1970.
 323.Tomogane H, Ota K, Yokoyama A. Decrease in litter weight gain and in progesterone secretion in lactating rats treated with antiserum to rat prolactin. J Reprod Fertil 47: 347‐349, 1976.
 324.Tomogane H, Ota K, Yokoyama A. Suppression of progesterone secretion in lactating rats by administration of ergocornine and the effect of prolactin replacement. J Endocrinol 65: 155‐161, 1975.
 325.Torner L, Maloumby R, Nava G, Aranda J, Clapp C, Neumann ID. In vivo release and gene upregulation of brain prolactin in response to physiological stimuli. Eur J Neurosci 19: 1601‐1608, 2004.
 326.Torner L, Neumann ID. The brain prolactin system: Involvement in stress response adaptations in lactation. Stress 5: 249‐257, 2002.
 327.Torner L, Toschi N, Nava G, Clapp C, Neumann ID. Increased hypothalamic expression of prolactin in lactation: Involvement in behavioural and neuroendocrine stress responses. Eur J Neurosci 15: 1381‐1389, 2002.
 328.Torner L, Toschi N, Pohlinger A, Landgraf R, Neumann ID. Anxiolytic and anti‐stress effects of brain prolactin: Improved efficacy of antisense targeting of the prolactin receptor by molecular modeling. J Neurosci 21: 3207‐3214, 2001.
 329.Toufexis DJ, Kyriazis D, Woodside B. Chronic neuropeptide Y Y5 receptor stimulation suppresses reproduction in virgin female and lactating rats. J Neuroendocrinol 14: 492‐497, 2002.
 330.Toufexis DJ, Rochford J, Walker CD. Lactation‐induced reduction in rats' acoustic startle is associated with changes in noradrenergic neurotransmission. Behav Neurosci 113: 176‐184, 1999.
 331.Toufexis DJ, Tesolin S, Huang N, Walker C. Altered pituitary sensitivity to corticotropin‐releasing factor and arginine vasopressin participates in the stress hyporesponsiveness of lactation in the rat. J Neuroendocrinol 11: 757‐764, 1999.
 332.Toufexis DJ, Thrivikraman KV, Plotsky PM, Morilak DA, Huang N, Walker CD. Reduced noradrenergic tone to the hypothalamic paraventricular nucleus contributes to the stress hyporesponsiveness of lactation. J Neuroendocrinol 10: 417‐427, 1998.
 333.Toufexis DJ, Walker CD. Noradrenergic facilitation of the adrenocorticotropin response to stress is absent during lactation in the rat. Brain Res 737: 71‐77, 1996.
 334.Trayhurn P. Brown adipose tissue thermogenesis and the energetics of lactation in rodents. Int J Obes 9(Suppl 2): 81‐88, 1985.
 335.Trayhurn P. Thermogenesis and the energetics of pregnancy and lactation. Can J Physiol Pharmacol 67: 370‐375, 1989.
 336.Treece BR, Ritter RC, Burns GA. Lesions of the dorsal vagal complex abolish increases in meal size induced by NMDA receptor blockade. Brain Res 872: 37‐43, 2000.
 337.True C, Kirigiti M, Ciofi P, Grove KL, Smith MS. Characterisation of arcuate nucleus kisspeptin/neurokinin B neuronal projections and regulation during lactation in the rat. J Neuroendocrinol 23: 52‐64, 2011.
 338.True C, Kirigiti MA, Kievit P, Grove KL, Smith MS. Leptin is not the critical signal for kisspeptin or luteinising hormone restoration during exit from negative energy balance. J Neuroendocrinol 23: 1099‐1112, 2011.
 339.Tsukamura H, Maeda K. Non‐metabolic and metabolic factors causing lactational anestrus: Rat models uncovering the neuroendocrine mechanism underlying the suckling‐ induced changes in the mother. Prog Brain Res 133: 187‐205, 2001.
 340.Tsukamura H, Maeda KI, Yokoyama A. Effect of the suckling stimulus on daily LH surges induced by chronic oestrogen treatment in ovariectomized lactating rats. J Endocrinol 118: 311‐316., 1988.
 341.Tu MT, Lupien SJ, Walker CD. Multiparity reveals the blunting effect of breastfeeding on physiological reactivity to psychological stress. J Neuroendocrinol 18: 494‐503, 2006.
 342.Tucker HA, Schwalm JW. Glucocorticoids in Mammary Tissue and Milk. J Anim Sci 45: 627‐634, 1977.
 343.Uenoyama Y, Tsukamura H, Maeda KI. Kisspeptin/metastin: A key molecule controlling two modes of gonadotrophin‐releasing hormone/luteinising hormone release in female rats. J Neuroendocrinol 21: 299‐304, 2009.
 344.Ulrich‐Lai YM, Herman JP. Neural regulation of endocrine and autonomic stress responses. Nat Rev Neurosci 10: 397‐409, 2009.
 345.Uvnas‐Moberg K. Role of efferent and afferent vagal nerve activity during reproduction: Integrating function of oxytocin on metabolism and behaviour. Psychoneuroendocrinology 19: 687‐695, 1994.
 346.Valeggia C, Ellison PT. Interactions between metabolic and reproductive functions in the resumption of postpartum fecundity. Am J Hum Biol 21: 559‐566, 2009.
 347.Valeggia C, Ellison PT. Lactational amenorrhoea in well‐nourished Toba women of Formosa, Argentina. J Biosoc Sci 36: 573‐595, 2004.
 348.Vernon RG, Pond CM. Adaptations of maternal adipose tissue to lactation. J Mammary Gland Biol Neoplasia 2: 231‐241, 1997.
 349.Voogt JL, Lee Y, Yang S, Arbogast L. Regulation of prolactin secretion during pregnancy and lactation. Prog Brain Res 133: 173‐185, 2001.
 350.Wade GN. Obesity without overeating in golden hamsters. Physiol Behav 29: 701‐707, 1982.
 351.Wade GN, Schneider JE, Li HY. Control of fertility by metabolic cues. Am J Physiol 270: E1‐19, 1996.
 352.Wahab F, Ullah F, Chan YM, Seminara SB, Shahab M. Decrease in hypothalamic Kiss1 and Kiss1r expression: A potential mechanism for fasting‐induced suppression of the HPG axis in the adult male rhesus monkey (Macaca mulatta). Horm Metab Res 43: 81‐85, 2011.
 353.Wakerley JB, Jiang QB, Housham SJ, Terenzi MG, Ingram CD. Influence of reproductive state and ovarian steroids on facilitation of the milk‐ejection reflex by central oxytocin. Adv Exp Med Biol 395: 117‐132, 1995.
 354.Wakerley JB, Lincoln DW. Intermittent release of oxytocin during suckling in the rat. Nat New Biol 233: 180‐181, 1971.
 355.Walker CD, Deschamps S, Proulx K, Tu M, Salzman C, Woodside B, Lupien S, Gallo‐Payet N, Richard D. Mother to infant or infant to mother? Reciprocal regulation of responsiveness to stress in rodents and the implications for humans. J Psychiatry Neurosci 29: 364‐382, 2004.
 356.Walker CD, Lightman SL, Steele MK, Dallman MF. Suckling is a persistent stimulus to the adrenocortical system of the rat. Endocrinology 130: 115‐125, 1992.
 357.Walker CD, Mitchell JB, Woodside BC. Suppression of LH secretion in food‐restricted lactating females: Effects of ovariectomy and bromocriptine treatment. J Endocrinol 146: 95‐104, 1995.
 358.Walker CD, Tilders FJ, Burlet A. Increased colocalization of corticotropin‐releasing factor and arginine vasopressin in paraventricular neurones of the hypothalamus in lactating rats: Evidence from immunotargeted lesions and immunohistochemistry. J Neuroendocrinol 13: 74‐85, 2001.
 359.Walker CD, Toufexis DJ, Burlet A. Hypothalamic and limbic expression of CRF and vasopressin during lactation: Implications for the control of ACTH secretion and stress hyporesponsiveness. Prog Brain Res 133: 99‐110, 2001.
 360.Walker CD, Trottier G, Rochford J, Lavallee D. Dissociation between behavioral and hormonal responses to the forced swim stress in lactating rats. J Neuroendocrinol 7: 615‐622, 1995.
 361.Walsh RJ, Slaby FJ, Posner BI. A receptor‐mediated mechanism for the transport of prolactin from blood to cerebrospinal fluid. Endocrinology 120: 1846‐1850, 1987.
 362.Wang HJ, Hoffman GE, Smith MS. Suppressed tyrosine hydroxylase gene expression in the tuberoinfundibular dopaminergic system during lactation. Endocrinology 133: 1657‐1663, 1993.
 363.Wang YF, Hatton GI. Milk ejection burst‐like electrical activity evoked in supraoptic oxytocin neurons in slices from lactating rats. J Neurophysiol 91: 2312‐2321, 2004.
 364.Wellman M, Abizaid A. Knockdown of central ghrelin O‐acyltransferase by vivo‐morpholino reduces body mass of rats fed a high‐fat diet. Peptides 70: 17‐22, 2015.
 365.Widstrom AM, Christensson K, Ransjo‐Arvidson AB, Matthiesen AS, Winberg J, Uvnas‐Moberg K. Gastric aspirates of newborn infants: pH, volume and levels of gastrin‐ and somatostatin‐like immunoreactivity. Acta Paediatr Scand 77: 502‐508, 1988.
 366.Widstrom AM, Marchini G, Matthiesen AS, Werner S, Winberg J, Uvnas‐Moberg K. Nonnutritive sucking in tube‐fed preterm infants: Effects on gastric motility and gastric contents of somatostatin. J Pediatr Gastroenterol Nutr 7: 517‐523, 1988.
 367.Windle RJ, Brady MM, Kunanandam T, Da Costa AP, Wilson BC, Harbuz M, Lightman SL, Ingram CD. Reduced response of the hypothalamo‐pituitary‐adrenal axis to alpha1‐agonist stimulation during lactation. Endocrinology 138: 3741‐3748, 1997.
 368.Windle RJ, Kershaw YM, Shanks N, Wood SA, Lightman SL, Ingram CD. Oxytocin attenuates stress‐induced c‐fos mRNA expression in specific forebrain regions associated with modulation of hypothalamo‐pituitary‐adrenal activity. J Neurosci 24: 2974‐2982, 2004.
 369.Windle RJ, Wood S, Shanks N, Perks P, Conde GL, da Costa AP, Ingram CD, Lightman SL. Endocrine and behavioural responses to noise stress: Comparison of virgin and lactating female rats during non‐disrupted maternal activity. J Neuroendocrinol 9: 407‐414, 1997.
 370.Windle RJ, Wood SA, Kershaw YM, Lightman SL, Ingram CD. Adaptive changes in basal and stress‐induced HPA activity in lactating and post‐lactating female rats. Endocrinology 154: 749‐761, 2013.
 371.Wood CE, Walker CD. Fetal and neonatal HPA axis. Compr Physiol 6: 33‐62, 2015.
 372.Woodside B. Effects of food restriction on the length of lactational diestrus in rats. Horm Behav 25: 70‐83, 1991.
 373.Woodside B. Prolactin and the hyperphagia of lactation. Physiol Behav 91: 375‐382, 2007.
 374.Woodside B, Abizaid A, Jafferali S. Effect of acute food deprivation on lactational infertility in rats is reduced by leptin administration. Am J Physiol 274: R1653‐1658, 1998.
 375.Woodside B, Abizaid A, Walker C. Changes in leptin levels during lactation: Implications for lactational hyperphagia and anovulation. Horm Behav 37: 353‐365, 2000.
 376.Woodside B, Augustine R, Naef L, Ladyman S, Grattan D. Role of prolactin in the metabolic adaptations to pregnancy and lactation. In: Bridges RS, editor. The Parental Brain. Amsterdam, the Netherlands: Elsevier, 2008.
 377.Woodside B, Popeski N. The contribution of changes in milk delivery to the prolongation of lactational infertility induced by food restriction or increased litter size. Physiol Behav 65: 711‐715, 1999.
 378.Woodside C, Jans JE. Role of the nutritional status of the litter and length and frequency of mother‐litter contact bouts in prolonging lactational diestrus in rats. Horm Behav 29: 154‐176, 1995.
 379.Wu Q, Boyle MP, Palmiter RD. Loss of GABAergic signaling by AgRP neurons to the parabrachial nucleus leads to starvation. Cell 137: 1225‐1234, 2009.
 380.Wu Q, Clark MS, Palmiter RD. Deciphering a neuronal circuit that mediates appetite. Nature 483: 594‐597, 2012.
 381.Wu Q, Howell MP, Cowley MA, Palmiter RD. Starvation after AgRP neuron ablation is independent of melanocortin signaling. Proc Natl Acad Sci U S A 105: 2687‐2692, 2008.
 382.Wu Q, Palmiter RD. GABAergic signaling by AgRP neurons prevents anorexia via a melanocortin‐independent mechanism. Eur J Pharmacol 660: 21‐27, 2011.
 383.Xiao XQ, Grove KL, Grayson BE, Smith MS. Inhibition of uncoupling protein expression during lactation: Role of leptin. Endocrinology 145: 830‐838, 2004.
 384.Xiao XQ, Grove KL, Smith MS. Metabolic adaptations in skeletal muscle during lactation: Complementary deoxyribonucleic acid microarray and real‐time polymerase chain reaction analysis of gene expression. Endocrinology 145: 5344‐5354, 2004.
 385.Xu J, Kirigiti MA, Cowley MA, Grove KL, Smith MS. Suppression of basal spontaneous gonadotropin‐releasing hormone neuronal activity during lactation: Role of inhibitory effects of neuropeptide Y. Endocrinology 150: 333‐340, 2009.
 386.Xu J, Kirigiti MA, Grove KL, Smith MS. Regulation of food intake and gonadotropin‐releasing hormone/luteinizing hormone during lactation: Role of insulin and leptin. Endocrinology 150: 4231‐4240, 2009.
 387.Yamada S, Uenoyama Y, Deura C, Minabe S, Naniwa Y, Iwata K, Kawata M, Maeda KI, Tsukamura H. Oestrogen‐dependent suppression of pulsatile luteinising hormone secretion and kiss1 mRNA expression in the arcuate nucleus during late lactation in rats. J Neuroendocrinol 24: 1234‐1242, 2012.
 388.Yamada S, Uenoyama Y, Kinoshita M, Iwata K, Takase K, Matsui H, Adachi S, Inoue K, Maeda KI, Tsukamura H. Inhibition of metastin (kisspeptin‐54)‐GPR54 signaling in the arcuate nucleus‐median eminence region during lactation in rats. Endocrinology 148: 2226‐2232, 2007.
 389.Zigmond MJ, Stricker EM. Deficits in feeding behavior after intraventricular injection of 6‐hydroxydopamine in rats. Science 177: 1211‐1214, 1972.
 390.Zinaman MJ, Cartledge T, Tomai T, Tippett P, Merriam GR. Pulsatile GnRH stimulates normal cyclic ovarian function in amenorrheic lactating postpartum women. J Clin Endocrinol Metab 80: 2088‐2093, 1995.
 391.Zuure WA, Roberts AL, Quennell JH, Anderson GM. Leptin signaling in GABA neurons, but not glutamate neurons, is required for reproductive function. J Neurosci 33: 17874‐17883, 2013.

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Article Title: Mood, Food, and Fertility: Adaptations of the Maternal Brain
 

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Barbara Woodside. Mood, Food, and Fertility: Adaptations of the Maternal Brain. Compr Physiol 2016, 6: 1493-1518. doi: 10.1002/cphy.c150036