Abstract:
Successful reproduction requires transmission of traits from one generation to the next by ensuring that offspring carrying the genetic basis of these traits survive to reproductive age. Maternal caregiving is the most crucial behavioral pattern ensuring the survival of young in most mammals. Expression of maternal behavior requires complex interactions between internal and external sensory cues, numerous endocrine systems, and the brain. We herein summarize the components of maternal care, and the hormonal, sensory, and neural underpinnings of its expression, with the laboratory rat model as an exemplar. The impetus to act maternally is similar to other goal-directed behaviors, in that it requires an appropriate motivational state. We emphasize how endocrine systems during pregnancy, parturition, and lactation may interact with traditional neural motivation systems, including the mesolimbic and nigrosriatal dopamine systems, to facilitate the transition from indifference to infants to a state of irresistible nurturance toward them.
This is a preview of subscription content, log in via an institution to check access.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
Abbreviations
- 6-OHDA:
-
6 hydroxydopamine
- AMYbl:
-
basolateral nucleus of the amygdala
- AVP:
-
arginine vasopression
- BNST:
-
bed nucleus of the stria terminalis
- CCK:
-
cholecystokinin
- CNS:
-
central nervous system
- cPAGl :
-
caudal lateral subregion of the periaqueductal gray
- cPAGvl :
-
caudal ventrolateral subregion of the periaquaductal gray
- D1:
-
dopamine receptor subtype 1
- D2:
-
dopamine receptor subtype 2
- D3:
-
Dopamine receptor subtype 3
- DA:
-
dopamine
- DAergic:
-
dopaminergic
- DOPAC:
-
dihydroxyphenylacetic acid
- DHT:
-
dihydrotestosterone
- EB:
-
estradiol benzoate
- ER:
-
estrogen receptor
- ERα:
-
estrogen receptor alpha
- ERβ:
-
estrogen receptor beta
- Fos:
-
protein product of the immediate early gene c-fos
- FSH:
-
follicle stimulating hormone
- GABA:
-
γ-aminobutyric acid
- GABAA :
-
γ-aminobutyric acid receptor subtype A
- h:
-
hours
- Hbc:
-
habenular complex
- H-O:
-
hysterectomy-ovariectomy
- ICV:
-
intracerebroventricular
- IR:
-
immunoreactive
- Lhb:
-
lateral subdivision of the habenular complex
- LH:
-
luteinizing hormone
- lPOA:
-
lateral preoptic area
- LS:
-
lateral septum
- MeA:
-
medial nucleus of the amygdala
- mPOA:
-
medial preoptic area
- MRI:
-
magnetic resonance imaging
- mRNA:
-
messenger ribonucleic acid
- N:
-
number of animals
- NA:
-
nucleus accumbens
- OT:
-
oxytocin
- OTR:
-
oxytocin receptor
- PAG:
-
periaqueductal gray
- PFC:
-
prefrontal cortex
- POA:
-
preoptic area
- PR:
-
progestin receptor
- PRL:
-
prolactin
- PRL-R:
-
prolactin receptor
- PVN:
-
paraventricular nucleus of the hypothalamus
- s.c.:
-
subcutaneous
- SEM:
-
standard error of the mean
- SN:
-
substantia nigra
- SNpc:
-
substantia nigra pars compacta
- T:
-
testosterone
- TH-ir:
-
tyrosine hydroxylase immunoreactivity
- V1a:
-
vasopressin receptor 1a
- vBNST:
-
ventral area of bed nucleus of the stria terminalis
- VMN:
-
ventromedial nucleus of the hypothalamus
- VMH:
-
ventromedial hypothalamus
- VTA:
-
ventral tegmental area
References
Ahdieh HB, Mayer AD, Rosenblatt JS. 1987. Effects of brain antiestrogen implants on maternal behavior and on postpartum estrus in pregnant rats. Neuroendocrinology 46(6): 522–531.
Amateau SK, Alt JJ, Stamps CL, McCarthy MM. 2004. Brain estradiol content in newborn rats: sex differences, regional heterogeneity, and possible de novo synthesis by the female telencephalon. Endocrinology 145: 2906–2917.
Augustine RA, Kokay IC, Andrews ZB, Ladyman SR, Grattan DR, 2003. Quantitation of prolactin receptor mRNA in the maternal rat brain during pregnancy and lactation. J Mol Endocrinol 31(1): 221–232.
Bakowska JC. 1998. Prolactinergic and dopaminergic components of the neural chemistry that underlies maternal behavior in the rat. PhD Thesis Rutgers, Newark NJ: The State University of New Jersey. pp. 1–199.
Bakowska JC, Morrell JI. 1995. Quantitative autoradiographic analysis of D1 and D2 dopamine receptors in rat brain in early and late pregnancy. Brain Res 703 (1–2): 191–200.
Bakowska JC, Morrell JI. 1997. 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(2): 161–177.
Bale TL, Dorsa DM. 1995. Sex differences in and effects of estrogen on oxytocin receptor messenger ribonucleic acid expression in the ventromedial hypothalamus. Endocrinology 136: 27–32.
Bakowska JC, Morrell JI. 2003. Neurons that express the mRNA for the short form of the prolactin receptor. Molecular Brain Research 116: 50–58.
Bale TL, Pedersen CA, Dorsa DM. 1995. CNS oxytocin receptor mRNA expression and regulation by gonadal steroids. Adv Exp Med Biol 395: 269–280.
Balthazart J, Ball GF. 1998. New insights into the regulation and function of brain estrogen synthase (aromatase). Trends Neurosci 21: 243–249.
Balthazart J, Absil P, Gerard M, Appeltants D, Ball GF. 1998. Appetitive and consummatory male sexual behavior in Japanese quail are differentially regulated by subregions of the preoptic medial nucleus. J Neurosci 18: 6512–6527.
Bauer JH. 1983. Effects of maternal state on the responsiveness to nest odors of hooded rats. Physiol Behav 30(2): 229–232.
Becker JB. 1990. Estrogen rapidly potentiates amphetamine-induced striatal dopamine release and rotational behavior during microdialysis. Neurosci Lett 118(2): 169–171.
Becker JB, Beer ME. 1986. The influence of estrogen on nigrostriatal dopamine activity: behavioral and neurochemical evidence for both pre- and postsynaptic components. Behav Brain Res 19(1): 27–33.
Becker JB, Beer ME, Robinson TE. 1984. Striatal dopamine release stimulated by amphetamine or potassium: influence of ovarian hormones and the light–dark cycle. Brain Res 311: 157–160.
Becker JB, Ramirez VD. 1981. Sex differences in the amphetamine stimulated release of catecholamines from rat striatal tissue in vitro. Brain Res 204: 361–372.
Benuck I, Rowe FA. 1975. Centrally and peripherally induced anosmia: influences on maternal behavior in lactating female rats. Physiol Behav 14: 439–447.
Birrell JM, Brown VJ. 2000. Medial frontal cortex mediates perceptual attentional set shifting in the rat. J Neurosci 20: 4320–4324.
Bole-Feysot C, Goffin V, Edery M, Binart N, Kelly PA. 1998. Prolactin (PRL) and its receptor: actions, signal transduction pathways, and phenotypes observed in PRL receptor knockout mice. Endocr Rev 19: 225–268.
Bosse R, Rivest R, Di Paolo T. 1997. Ovariectomy and estradiol treatment affect the dopamine transporter and its gene expression in the rat brain. Brain Res Mol Brain Res 46(1–2): 343–346.
Brewster J, Leon M. 1980. Relocation of the site of mother–young contact: maternal transport behavior in Norway rats. J Comp Physiol Psychol 94: 69–79.
Bridges RS. 1990. Endocrine regulation of parental behavior in rodents. Mammalian parenting biochemical, neurobiological, and behavioral determinants. Krasnegor NA, Bridges RS, editors. New York: Oxford Press; pp. 93–117.
Bridges RS. 1996. Biochemical basis of parental behavior in the rat. Parental care – evolution, mechanisms, and adaptive significance. Advances in the study of behavior, vol. 25. Rosenblatt JS, Snowdon CT, editors. Academic Press; New York: pp. 215–242.
Bridges RS, Clifton DK, Sawyer CH. 1982. Postpartum luteinizing hormone release and maternal behavior in the rat after late-gestational depletion of hypothalamic norepinephrine. Neuroendocrinology 34(4): 286–291.
Bridges RS, Di Biase R, Loundes DD, Doherty PC. 1985. Prolactin stimulation of maternal behavior in female rats. Science 782–784.
Bridges RS, Mann PE, Coppeta JS. 1999. Hypothalamic involvement in the regulation of maternal behaviour in the rat: inhibitory roles for the ventromedial hypothalamus and the dorsal/anterior hypothalamic areas. J Neuroendocrinol 11(4): 259–266.
Bridges RS, Numan M, Ronsheim PM, Mann PE, Lupini CE. 1990. Central prolactin infusions stimulate maternal behavior in steroid-treated, nulliparous female rats. Proc Natl Acad Sci USA 87(20): 8003–8007.
Bridges RS, Rosenblatt JS, Feder HH. 1978. Serum progesterone concentrations and maternal behavior in rats after pregnancy termination: behavioral stimulation after progesterone withdrawal and inhibition of progesterone maintenance. Endocrinology 102: 258–267.
Bridges RS, Robertson MC, Shiu RPC, Friesen HG, Stuer AM, et al 1996. Endocrine communication between conceptus and mother: placental lactogen stimulation of maternal behavior. Neuroendocrinology 64: 57–64.
Bridges RS, Robertson MC, Shiu RP, Sturgis JD, Henriquez BM, et al 1997. Central lactogenic regulation of maternal behavior in rats: steroid dependence, hormone specificity, and behavioral potencies of rat prolactin and rat placental lactogen I. Endocrinology 138(2): 756–763.
Bridges R, Zarrow MX, Gandelman R, Denenberg VH. 1972. Differences in maternal responsiveness between lactating and sensitized rats. Dev Psychobiol 5: 123–127.
Brown VJ, Bowman EM. 2002. Rodent models of prefrontal cortical function. Trends Neurosci 25: 340–343.
Brown EE, Fibiger HC. 1993. Differential effects of excitotoxic lesions of the amygdala on cocaine-induced conditioned locomotion and conditioned place preference. Psychopharmacology 113: 123–130.
Brown EE, Robertson GS, Fibiger HC. 1992. Evidence for conditional neuronal activation following exposure to a cocaine-paired environment: role of forebrain limbic structures. J Neurosci 12: 4112–4121.
Brown JR, Ye H., Bronson RT, Dikkes P, Greenberg ME. 1996 A defect in nurturing in mice lacking the immediate early gene fosB. Cell 86: 297–309.
Buijs RM, DeVries GJ, van Leeuwne FW. 1985. The distribution and synaptic release of oxytocin in the central nervous system. Oxytocin: clinical and laboratory studies. Amico JA, Robinson AG, editors. Amsterdam, New York, Oxford: Elsevier Science Publishers BV.
Buzsaki G. 2004. Large-scale recording of neuronal ensembles. Nat Neurosci 7: 446–451.
Byrnes EM, Rigero BA, Bridges RS. 2002. Dopamine antagonists during parturition disrupt maternal care and the retention of maternal behavior in rats. Pharmacol Biochem Behav 73: 869–875.
Cabrera R, Diaz A, Pinter A, Belmar J. 1993. In vitro progesterone effects on 3H-dopamine release from rat corpus striatum slices obtained under difference endocrine conditions. Life Sci 53: 1767–1777.
Caldwell JD, Walker CH, Pedersen CA, Barakat AS, Mason GA. 1994. Estrogen increases affinity of oxytocin receptors in the medial preoptic area-anterior hypothalamus. Peptides 15: 1079–1084.
Carelli RM, Ijames SG, Crumling AJ. 2000. Evidence that separate neural circuits in the nucleus accumbens encode cocaine versus “natural” (water and food) reward. J Neurosci 20: 4255–4266.
Carelli RM, Wondolowski J. 2003. Selective encoding of cocaine versus natural rewards by nucleus accumbens neurons is not related to chronic drug exposure. J Neurosci 23: 11214–11223.
Casado M, Diaz-Guerra MJ, Rodrigo J, Fernandez AP, Bosca L, et al 1997. Expression of the calcium-independent cytokine-inducible (iNOS) isoform of nitric oxide synthase in rat placenta. Biochem J 324: 201–207.
Castner SA, Xiao L, Becker JB, 1993. Sex differences in striatal dopamine: in vivo microdialysis and behavioral studies. Brain Res 610(1): 127–134.
Cebeira M, Hernandez ML, Rodriguez de Fonseca F, de Miguel R, Fernandez-Ruiz JJ, et al 1991. Lack of effect of prolactin on the dopaminergic receptor sensitivity in striatal and limbic areas after exprimentally-induced alterations in its peripheral levels. Life Sci 48: 531–541.
Champagne F, Diorio J, Sharma S, Meaney MJ. 2001. Naturally occurring variations in maternal behavior in the rat are associated with differences in estrogen-inducible central oxytocin receptors. Proc Natl Acad Sci USA 98: 12736–12741.
Champagne FA, Chretien P, Stevenson CW, Zhang TY, Gratton A, Meaney MJ. 2004. Variations in nucleus accumbens dopamine associated with individual differences in maternal behavior in the rat. J Neurosci 24: 4113–4123.
Champtiaux N, Changeux JP. 2004 Knockout and knockin mice to investigate the role of nicotinic receptors in the central nervous system. Prog Brain Res 145: 235–251.
Chen YF, Ramirez VD. 1982. Prolactin stimulates dopamine release from males but not female rats striatal tissue superfuse in vitro. Endocrinology 111: 1740–1742.
Chen JC, Ramirez VD. 1988. In vivo dopaminergic activity from nucleus accumbens, substantia nigra and ventral tegmental area in the freely moving rat: basal neurochemical output and prolactin effect. Neuroendocrinology 48: 329–335.
Chiodo LA, Caggiula AR, 1980. Alterations in basal firing rate and autoreceptor sensitivity of dopamine neurons in the substantia nigra following acute and extended exposure to estrogen. Eur J Pharmacol 67(1): 165–166.
Clapp CL, Torner L, Butierrez-Ospina G, Alcantara E, Lopez-Gomez FJ, et al 1994. The prolactin gene is expressed in the hypothalamic neurohypophyseal system and the protein is processed into a 14-kDa fragment with activity like 16-kDa prolactin. Proc Natl Acad Sci USA 91: 10384–10388.
Clarke DL, Linzer DI. 1993. Changes in prolactin receptor expression during pregnancy in the mouse ovary. Endocrinology 133: 224–232.
Coirini H, Schumacher M, Flanagan LM, McEwen BS. 1991. Transport of estrogen-induced oxytocin receptors in the ventromedial hypothalamus. J Neurosci 11: 3317–3324.
Connor JR, Davis HN. 1980a. Postpartum estrous in Norway rats: I Behavior. Biol Reprod 23: 994–999.
Connor JR, Davis HN. 1980b. Postpartum estrous in Norway rats II Physiology. Biol Reprod 23: 1000–1006.
Cornish JL, Duffy P, Kalivas PW. 1999. A role for nucleus accumbens glutamate transmission in the relapse to cocaine-seeking behavior. Neuroscience 93: 1359–1367.
Consiglio AR, Lucion AB, 1996. Lesion of hypothalamic paraventricular nucleus and maternal aggressive behavior in female rats. Physiol Behav 59(4–5): 591–596.
Corodimas KP, Morrell JI. 1990. Estradiol-sensitive neurons in the preoptic area are afferent to the medial basal hypothalamus. Exp Brain Res 80: 381–386.
Corodimas KP, Rosenblatt JS, Canfield ME, Morrell JI. 1993. Neurons in the lateral subdivision of the habenular complex mediate the hormonal onset of maternal behavior in rats. Behav Neurosci 107: 827–843.
Corodimas KP, Rosenblatt JS, Morrell JI. 1992. The habenular complex mediates hormonal stimulation of maternal behavior in rats. Behav Neurosci 106: 853–865.
Creutz LM, Kritzer MF, 2002. Estrogen receptor-beta immunoreactivity in the midbrain of adult rats: regional, subregional, and cellular localization in the A10, A9, and A8 dopamine cell groups. J Comp Neurol 446(3): 288–300.
Crowley WR, O'Donohue TL, Jacobowitz DM. 1978a. Changes in catecholamine content in discrete brain nuclei during the estrous cycle of the rat. Brain Res 147(2): 315–326.
Crowley WR, O'Donohue TL, Wachslicht H, Jacobowitz DM. 1978b. Effects of estrogen and progesterone on plasma gonadotropins and on catecholamine levels and turnover in discrete brain regions of ovariectomized rats. Brain Res 154: 345–357.
Cummings AM, Laws SC. 1981. Endocrine control of implantation and delayed implantation in rats and mice. J Reprod Fertil Supp 29: 97–109.
Curran-Rauhut MA, Petersen SL, 2002. The distribution of progestin receptor mRNA in rat brainstem. Brain Res Gene Expr Patterns 1(3–4): 151–157.
De Kloet ER, Voorhuis DA, Boschma Y, Elands J. 1986. Estradiol modulates denstiry of putative “oxytocin receptors” in discrete rat brain regions. Neuroendcrinology 44: 415–421.
Del Cerro MC, Izquierdo MA, Collado P, Segovia S, Guillamon A. 1991. Bilateral lesions of the bed nucleus of the accessory olfactory tract facilitate maternal behavior in virgin female rats. Physiol Behav 50: 67–71.
Devito WJ, Avakian C, Stone S, Ace CI. 1992. Estardiol increases prolactin synthesis and prolactin messenger ribonucleic acid in selected brain regions in the hypohyposectomized female rat. Endocrinology 131: 2154–2160.
Di Paolo T, Bedard PJ, Dupont A, Poyet P, Labrie F. 1982a. Effects of estradiol on intact and denervated striatal dopamine receptors and on dopamine levels: a biochemical and behavioral study. Can J Physiol Pharmacol 60(3): 350–357.
Di Paolo T, Dupont A, Daigle M, 1982b. Effect of chronic estradiol treatment on dopamine concentrations in discrete brain nuclei of hypophysectomized female rats. Neurosci Lett 32(3): 295–300.
Di Paolo T, Falardeau P, Morissette M. 1988. Striatal D-2 dopamine agonist binding sites fluctuate during the rat estrous cycle. Life Sci 43: 665–672.
Disshon KA, Boja JW, Dluzen DE. 1998. Inhibition of striatal dopamine transporter activity by 17 beta estradiol. Eur J Pharmacol 345: 207–211.
Dluzen DE, Ramirez VD. 1984. Bimodal effect of progesterone on in vitro dopamine function of the rat corpus stritum. Neuroendocrinology 39: 149–155.
Dluzen DE, Ramirez VD. 1987. Intermittent infusion of progesterone potentiates where continuous infusion reduces amphetamine-stimulated dopamine release from ovariectomized estrogen-primed rat striatal fragments superfused in vitro. Brain Res 406: 1–9.
Dluzen DE, Ramirez VD. 1989a. Progesterone effects upon dopamine release from the corpus striatum of female rats. I. Evidence for interneuronal control. Brain Res 476: 332–337.
Dluzen DE, Ramirez VD. 1989b. Progesterone effects upon dopamine release from the corpus striatum of female rats. II. Evidence for a membrane site of action and the role of albumen. Brain Res 476: 338–344.
Dluzen DE, Ramirez VD. 1990. In vivo changes in responsiveness of the caudate nucleus to l-dopa infusion as a function of the estrous cycle. Brain Res 536: 163–168.
Doerr HK, Siegel HI, Rosenblatt JS. 1981. Effects of progesterone withdrawal and estrogen on maternal behavior in nulliparious rats. Behav Neural Biol 32: 35–44
DonCarlos LL, Greene GL, Morrell JI. 1989. Estrogen plus progesterone increases progestin receptor immunoreactivity in the brain of ovariectomized guinea pigs. Neuroendocrinology 50: 613–623.
Drago F, Bohus B, Canonico PL, Scapagnini U. 1981. Prolactin induces grooming in the rat: possible involvement of nigrostriatal dopaminergic system. Pharmacol Biochem Behav 15(1): 61–63.
Drago F, Caldwell JD, Pedersen CA, Continella G, Scapagnini U, et al 1986. Dopamine neurotransmission in the nucleus accumbens may be involved in oxytocin-enhanced grooming behavior of the rat. Pharmacol Biochem Behav 24: 1185–1188.
Dupont A, Di Paolo T, Gagne B, Barden N. 1981. Effects of chronic estrogen treatment on dopamine concentrations and turnover in discrete brain nuclei of ovariectomized rats. Neurosci Lett 22(1): 69–74.
Eichenbaum H, Cohen NJ. 2001. From conditioning to conscious recollection: memory systems of the brain. Working memory and the prefrontal cortex. New York: Oxford University Press; pp. 471–506.
Emanuele NV, Jurgens JK, Halloran MM, Tentler JJ, Lawrence AM, et al 1992. The rat prolactin gene is expressed in brain tissue: detection of normal and alternatively spliced prolactin messenger RNA. Mol Endocrinol 6: 35–42.
Euvard C, Oberlander C, Bossier JR. 1980. Antidopaminergic effect of estrogens at the striatal level. J Pharmacol Exp Ther 214: 179–185.
Everitt BJ, Wolf ME. 2002. Psychomotor stimulant addiction: a neural systems perspective. J Neurosci 22: 3312–3320.
Fahrbach SE, Morrell JI, Pfaff DW. 1985. Role of oxytocin in the onset of estrogen-facilitated maternal behavior. Oxytocin:clinical and laboratory studies. Amico JA, Robinson AG, editors. Amsterdam: Elsevier; pp. 372–388.
Fahrbach SE, Morrell JI, Pfaff DW. 1986. Identification of medial preoptic neurons that concentrate estradiol and project to the midbrain in the rat. J Comp Neurol 247: 364–382.
Fahrbach SE, Pfaff DW. 1982. Hormonal and neural mechanisms underlying maternal behavior in the rat. The physiological mechanisms of motivation. Pfaff DW, editor. New York: Springer-Verlag; pp. 253–285.
Fahrbach SE, Pfaff DW. 1986. Effect of preoptic region implants of dilute estradiol on the maternal behavior of ovariectomized, nulliparous rats. Horm Behav 20: 354–363.
Febo M, Gonzalez-Rodriguez LA, Capo-Ramos DE, Gonzalez-Segarra NY, Segarra AC. 2003. Estrogen-dependent alterations in D2/D3-induced G protein activation in cocaine-sensitized female rats. J Neurochem 86(2): 405–412.
Felton TM, Linton L, Rosenblatt JS, Morrell JI. 1999. First and Second order afferents of the lateral hebenula relevant for maternal behavior. Neuro report 10: 883-887.
Felton TM, Linton L, Rosenblatt JS, Morrell JI. 1998. Intact neurons of the lateral habenular nucleus are necessary for the nonhormonal, pup-mediated display of maternal behavior in sensitized virgin female rats. Behav Neurosci 112(6): 1458–1465.
Fernandez-Ruiz JJ, Hernandez ML, de Miguel R, Ramos JA. 1991. Nigrostriatal and mesolimbic dopaminergic activities were modified throughout the ovarian cycle of female rats. J Neural Transm Gen Sect 85(3): 223–229.
Ferris CF, Kulkarni P, Sullivan JM, Harder JA, Messenger TL, et al 2005. Pup suckling is more rewarding than cocaine: evidence from functional magnetic resonance imaging and three-dimensional computational analysis. J Neurosci 25: 149–156.
Fields JZ, Gordon JH. 1982. Estrogen inhibits the dopaminergic supersensitivity induced by neuroleptics. Life Sci 30: 229–234.
Fisher AE. 1956. Maternal and sexual behavior induced by intracranial chemical stimulation. Science 124: 228–229.
Flannelly KJ, Kemble ED, Blanchard DC, Blanchard RJ. 1986. Effects of septal-forebrain lesions on maternal aggression and maternal care. Behav Neural Biol 45(1): 17–30.
Fleischer S, Slotnick BM. 1978. Disruption of maternal behavior in rats with lesions of the septal area. Physiol Behav 21(2): 189–200.
Fleming AS. 1976. Control of food intake in the lactating rat: role of suckling and hormones. Physiol Behav 17: 841–848.
Fleming AS, Cheung U, Myhal N, Kessler Z. 1989. Effects of maternal hormones on ‘timidity’ and attraction to pup-related odors in female rats. Physiol Behav 46(3): 449–453.
Fleming AS, Korsmit M, Deller M. 1994. Rat pups are potent reinforcers to the maternal animal: effects of experience, partiy, hormones, and dopamine function. Psychobiology 22: 44–53.
Fleming AS, Luebke C. 1981. Timidity prevents the virgin female rat from being a good mother: emotionality differences between nulliparous and parturient females. Physiol Behav 27(5): 863–868.
Fleming AS, Rosenblatt JS. 1974a. Olfactory regulation of maternal behavior in rats. I. effects of olfactory bulb removal in experienced and inexperienced lactating and cycling females. J Comp Physiol Psychol 86(2): 221–232.
Fleming AS, Rosenblatt JS. 1974b. Olfactory regulation of maternal behavior in rats. II. Effects of peripherally induced anosmia and lesions of the lateral olfactory tract in pup-induced virgins. J Comp Physiol Psychol 86(2): 233–246.
Fleming AS, Walsh C. 1994. Neuropsychology of maternal behavior in the rat: c-fos expression during mother litter interactions. Psychoneuroendocrinology 19: 429–443.
Fleming AS, Vaccarino F, Luebke C. 1980. Amygdaloid inhibition of maternal behavior in the nulliparous female rat. Physiol Behav 25(5): 731–743.
Fliestra RJ, Voogt JL. 1997. Lactogenic hormones of the placenta and pituitary inhibit suckling-induced prolactin (PRL) release but not the ante-partum PRL surge. Proc Soc Exp Biol Med 214: 258–264.
Francis DD, Champagne FC, Meaney MJ. 2000. Variations in maternal behaviour are associated with differences in oxytocin receptor levels in the rat. J Neuroendocrinol 12: 1145–1148.
Friedman MI, Bruno JP, Alberts JR. 1981. Physiological and behavior consequences in rats of water recycling during lactation. J Comp Physiol Psychol 95: 26–35.
Franklin TR, Druhan JP. 2000a. Expression of fos-related antigens in the nucleus accumbens and associated regions following exposure to a cocaine-paired environment. Eur J Neurosci 12: 2097–2106.
Franklin TR, Druhan JP. 2000b. Involvement of the nucleus accumbens and medial prefrontal cortex in the expression of conditioned hyperactivity to a cocaine associated environment in rats. Neuropsychopharmacology 23: 633–644.
Freeman ME. 1988. The ovarian cycle in the rat. The physiology of reproduction, vol 1. Knobil E, Neill JD, editors. New York: Raven Press; pp. 1893–1928.
Frye CA. 2001. The role of neurosteroids and non-genomic effects of progestins and androgens in mediating sexual receptivity of rodents. Brain Res Rev 37: 201–222.
Fuchs RA, Evans KA, Parker MP, See RE. 2004. Differential involvement of orbitofrontal cortex subregions in conditioned cue-induced and cocaine-primed reinstatement of cocaine seeking in rats. J Neurosci 24: 6600–6610.
Gaffori O, Le Moal M. 1979. Disruption of maternal behavior and appearance of cannibalism after ventral mesencephalic tegmentum lesions. Physiol Behav 23: 317–323.
Gammie SC, Nelson RJ. 1999. Maternal aggression is reduced in neuronal nitric oxide synthase-deficient mice. J Neurosci 19: 8027–8035.
Gandelman R, Zarrow MX, Denenberg VH, 1970. Maternal behavior: differences between mother and virgin mice as a function of the testing procedure. Dev Psychobiol 3(3): 207–214.
Gandelman R, Zarrow MX, Denenberg VH. 1972. Reproductive and maternal performance in the mouse following removal of the olfactory bulbs. J Reprod Fertil 28(3): 453–456.
Garland HO, Atherton JC, Baylis C, Morgan MRA, Milne CM. 1987. Hormonal profiles for progesterone, oestradiol, prolactin, plasma renin activity, aldosterone and corticosterone during pregnancy and pseudopregnancy in two strains of rat: correlation with renal studies. J Endocrinol 113: 435–444.
Gibori G, Chatterton RT, Chien JL. 1979. Ovarian and serum concentrations of androgen throughout pregnancy in the rat. Biol Reprod 21: 53–56.
Gibori G, Khan I, Warshaw ML, McLean MP, Puryear TK, et al 1988. Placental-derived regulators and the complex control of luteal cell function. Recent Prog Horm Res 44: 377–425.
Gibori G, Sridaran R. 1981. Sites of androgen and estradiol production in the second half of pregnancy in the rat. Biol Reprod 24: 249–256.
Giordano AL, Johnson AE, Rosenblatt JS. 1990. Haloperidol-induced disruption of retrieval behavior and reversal with apomorphine in lactating rats. Physiol Behav 48(1): 211–214.
Giordano AL, Siegel HI, Rosenblatt JS. 1991. Nuclear estrogen receptor binding in microdissected brain regions of female rats during pregnancy: implications for maternal and sexual behavior. Physiol Behav 50(6): 1263–1267.
Gingrich JA, Hen R. 2000. Commentary The broken mouse: the role of development, plasticity, and environment in the interpretation of phenotypic changes in knockout mice. Curr Opin Neurobiol 10: 146–152.
Gonzalez-Mariscal G, Jimenez P, Beyer C, Rosenblatt JS. 2003. Androgens stimulate specific aspects of maternal nest-building and reduce food intake in rabbits. Horm Behav 43: 312–317.
Gordon JH, Nance DM, Wallis CJ, Gorski RA. 1977. Effects of estrogen on dopamine turnover, glutamic acid decarboxylase activity and lordosis behavior in septal lesioned female rats. Brain Res Bull 2(5): 341–346.
Grattan DR. 2001. The actions of prolactin in the brain during pregnancy and lactation. The maternal brain neurobiological and neuroendocrine adaptation and disorders in pregnancy and postpartum. Progress in Brain Research, vol 133. Russell JA, Douglas AJ, Windle RJ, Ingram CD, editors. Amsterdam, New York, Oxford: Elsevier; pp. 153–173.
Greco B, Lubbers LS, Blaustein JD. 2003. Estrogen receptor beta messenger ribonucleic acid expression in the forebrain of proestrus, pregnant, and lactating female rats. Endocrinology 144: 1869–1875.
Groenewegen HJ, Wright CI, Beijer AV. 1996. The nucleus accumbens: gateway for limbic structures to reach the motor system? Prog Brain Res 107: 485–511.
Groenewegen HJ, Uylings HB. 2000. The prefrontal cortex and the integration of sensory, limbic and autonomic information. Prog Brain Res 126: 3–28.
Groenewegen HJ, van den Heuvel OA, Cath DC, Voorn P, Veltman DJ. 2003. Does an imbalance between the dorsal and ventral striatopallidal systems play in Tourette's syndrome? A neuronal circuit approach. Brain Dev 25(Suppl 1): S3–S14.
Grota LJ, Eik-Nes KB. 1967. Plasma progesterone concentrations during pregnancy and lactation in the rat. J Reprod Fert 13: 83–91.
Gualillo O, Cominos J, Blanco M, Garcia-Caballero T, Kojima M, et al 2001. Grehlin, a novel placental-derived hormone. Endocrinology 142: 788–794.
Gunnersen JM, Crawford RJ, Tregear GW. 1995. Expression of the relaxin gene in rat tissues. Mol Cell Endocrinol 110: 55–64.
Hansen S. 1994. Maternal behavior of female rats with 6-OHDA lesions in the ventral striatum: characterization of the pup retrieval deficit. Physiol Behav 55(4): 615–620.
Hansen S, Bergvall AH, Nyiredi S. 1993. Interaction with pups enhances dopamine release in the ventral striatum of maternal rats: a microdialysis study. Pharmacol Biochem Behav 45(3): 673–676.
Hansen S, Harthon C, Wallin E, Lofberg L, Svensson K. 1991a. The effects of 6-OHDA-induced dopamine depletions in the ventral or dorsal striatum on maternal and sexual behavior in the female rat. Pharmacol Biochem Behav 39(1): 71–77.
Hansen S, Harthon C, Wallin E, Lofberg L, Svensson K. 1991b. Mesotelencephalic dopamine system and reproductive behavior in the female rat: effects of ventral tegmental 6-hydroxydopamine lesions on maternal and sexual responsiveness. Behav Neurosci 105(4): 588–598.
Hard E, Hansen S. 1985. Reduced fearfulness in the lactating rat. Physiol Behav 35(4): 641–643.
Hauser H, Gandelman R. 1985. Lever pressing for pups: evidence for hormonal influence upon maternal behavior of mice. Horm Behav 19(4): 454–468.
Heap RB, Flint APF. 1986. Pregnancy. Hormonal control of reproduction (2nd edition). Austin CR, Short RV, editors. Cambridge England: Cambridge University Press; pp. 153–194.
Heimer L, Zahm DS, Alheid GF. 1995. Basal ganglia. The rat nervous system. Paxinos G, editor. San Diego, New York: Academic Press; pp. 579–629.
Heine PA, Di S, Ross LR, Anderson LL, Jacobson CD. 1997. Relaxin-induced expression of Fos in the forebrain of the late pregnant rat. Neuroendocrinology 66: 38–46.
Hernandez ML, Fernandez-Ruiz JJ, Navarro M, de Miguel R, Cebeira M, et al 1994. Modifications of mesolimbic and nigrostriatal dopaminergic activities after intracerebroventricular administration of prolactin. J Neural Transm Gen Sect 96(1): 63–79.
Hernandez ML, Fernandez-Ruiz JJ, de Miguel R, Ramos JA. 1991. Time-dependent effects of ovarian steroids on tyrosine hydroxylase activity in the limbic forebrain of ♀ rats. Journal of Neural Transmission 83: 77-84.
Hiroi N, White NM. 1991. The lateral nucleus of the amygdala mediates expression of the amphetamine-produced conditioned place preference. J Neurosci 11: 2107–2116.
Hollaway WR, Dollinger MJ, Denenberg VH. 1980. Parturition in the rat: description and assessment. Maternal infleunces and early behavior. Bell RW, Smotherman WP, editors. New York: SP Med. Sci. Books; pp. 1–26.
Hornsby DJ, Wilson BC, Summerlee AJ. 2001. Relaxin and drinking in pregnant rats. Prog Brain Res 133: 229–240.
Hruska RE, Nowak MW. 1988. Estrogen treatment increases the density of D1 dopamine receptors in the rat striatum. Brain Res 442: 349–350.
Hruska RE, Pitman KT. 1982. Distribution and localization of estrogen-sensitive dopamine receptors in the rat brain. J Neurochem 39(5): 1418–1423.
Hu M, Becker JB. 2003. Effects of sex and estrogen on behavioral sensitization to cocaine in rats. J Neurosci 23(2): 693–699.
Hull EM, Lorrain DS, Du J, Matuszewich L, Lumley LA, et al 1999. Hormone-neurotransmitter interactions in the control of sexual behavior. Behav Brain Res 105: 105–116.
Ikemoto S, Panksepp J. 1999. The role of nucleus accumbens dopamine in motivated behavior: a unifying interpretation with special reference to reward-seeking. Brain Res Rev 31: 6–41.
Insel TR. 1986. Postpartum increases in brain oxytocin binding. Neuroendocrinology 44(4): 515–518.
Insel TR. 1990. Regional changes in brain oxytocin receptor post-partm: time-course and relationship to maternal behaviour. J Neuroendocrinol 2: 539–545.
Insel TR, Harbaugh CR. 1989. Lesions of the hypothalamic paraventricular nucleus disrupt the initiation of maternal behavior. Physiol Behav 45(5): 1033–1041.
Isaac WL, Nonneman AJ, Neisewander J, Landers T, Bardo MT. 1989. Prefrontal cortex lesions differentially disrupt cocaine-reinforced conditioned place preference but not conditioned taste aversion. Behav Neurosci 103: 345–355.
Jacobson CD, Terkel J, Gorski RA, Sawyer CH. 1980. Effects of small medial preoptic area lesions on maternal behavior: retrieving and nest building in the rat. Brain Res 194(2): 471–478.
Jirik-Babb P, Manaker S, Tucker AM, Hofer MA. 1984. The role of the accessory and main olfactory systems in maternal behavior of the primiparous rat. Behav Neural Biol 40: 170–178.
Jones HM, Vernon MW, Rush ME. 1987. Androgenic modulation of periovulatory follicle-stimulating hormone release in the rat. Biol Reprod 37: 268–276.
Joyce JN, Van Hartesveldt C. 1984. Estradiol application to one striatum produces postural deviation to systemic apomorphine. Pharmacol Biochem Behav 20: 575–581.
Kalinichev M, Rosenblatt JS, Nakabeppu Y, Morrell JI. 2000. Induction of c-fos-like and fosB-like immunoreactivity reveals forebrain neuronal populations involved differentially in pup-mediated maternal behavior in juvenile and adult rats. J Comp Neurol 416(1): 45–78.
Kalivas PW, Barnes CD. 1994. Limbic motor circuits and neuropsychiatry. Boca Raton: CRC Press.
Kalivas PW, Nakamura M. 1999. Neural systems for behavioral activation and reward. Curr Opin Neurobiol 9: 223–227.
Kaltwasser MT, Crawley JN. 1987. Oxytocin and cholecysokinin induce grooming behavior in the ventral tegmentum of the rat. Brain Res 426: 1–7.
Kanyicska B, Nguyen DN, Arey BJ, Freeman ME. 1990. Hysterectomy-induced alterations in prolactin secretion of lactating rats. Endocrinology 126: 2021–2026.
Kazandjian A, Spyraki C, Papadopoulou Z, Sfikakis A, Varonos DD. 1988. Behavioural and biochemical effects of haloperidol during the oestrous cycle of the rat. Neuropharmacology 27(1): 73–78.
Keating RJ, Tcholakian RK. 1979. In vivo patterns of circulating steroid in adult male rats. I. Variation in testosterone during twenty four and forty eight hour standard and reverse light dark cycles. Endocrinology 104(1): 184–193.
Kelley AE. 2004. Ventral striatal control of appetitive motivation: role in ingestive behavior and reward-related learning. Neurosci Biobehav Rev 27: 765–776.
Kelley AE, Berridge KC. 2002. The neuroscience of natural rewards: relevance to addictive drugs. J Neurosci 22(9): 3306–3311.
Kelly PA, Binart N, Lucas B, Bouchard B, Goffin V. 2001. Implications of multiple phenotypes observed in prolactin receptor knockout mice. Front Neuroendocrinol 22(2): 140–145.
Kenyon P, Cronin P, Keeble S. 1983. Role of the infraorbital nerve in retrieving behavior in lactating rats. Behav Neurosci 97: 255–269.
Kilpatrick IC, Starr MS, Fletcher A, James TA, MacLeod NK. 1980. Evidence for a GABAergic nigrostriatal pathway in the rat. I. Behavioural and biochemical studies. Exp Brain Res 40: 45–54.
Kirkby RJ. 1967. Caudate nucleus lesions and maternal behavior in the rat. Psychonomic Science 9: 601-602.
Kolunie JM, Stern JM. 1995. Maternal aggression in rats: effects of olfactory bulbectomy, ZnSO4-induced anosmia, and vomeronasal organ removal. Horm Behav 29(4): 492–518.
Koob GF, Vaccarino FJ, Amaltric M, Bloom FE. 1987. Positive reinforcement properties of drugs: search for neural substrates. Brain reward systems and abuse. Engel J, Oreland L, editors. New York: Raven Press; pp. 35–50.
Kremarik P, Fruend-Mercier MJ, Stoeckel ME. 1995. Estrogen-sensitive oxytocin binding sites and differentially regulation by progesterone in the telencephalon and the hypothalamus of the rat. J Neuroendocrinol 281-289.
Kritzer MF. 1997. Selective colocalization of immunoreactivity for intracellular gonadal hormone receptors and tyrosine hydroxylase in the ventral tegmental area, substantia nigra, and retrorubral fields in the rat. J Comp Neurol 379(2): 247–260.
Kubota Y, Inagaki S, Kito S, Wu JY. 1987. Dopaminergic axons directly make synapses with GABAergic neurons in the rat neostriatum. Brain Res 406: 147–156.
Lambert RC, Moos FC, Ingram CD, Wakerley JB, Kremarik P, et al 1993. Electrical activity of neurons in the ventrolateral septum and bed nuclei of the stria terminalis in suckled rats: statistical analysis gives evidence for sensitivity to oxytocin and for relation to the milk-ejection reflex. Neuroscience 54(2): 361–376.
Lammers CH, D'Souza U, Qin ZH, Lee SH, Yajima S, Mouradian MM. 1999. Regulation of striatal dopamine receptors by estrogen. Synapse 34(3): 222–227.
Laping NJ, Ramirez VD. 1988. Prolactin-induced yawning behavior requires an intact nigro-striatal dopamine system. Pharmacol Biochem Behav 29: 59–62.
Leckman JF, Herman AE. 2002. Maternal behavior and developmental psychopathology Biol Psychiatry 51: 27–43.
Lee A, Clancy S, Fleming AS. 2000. Mother rats bar-press for pups: effects of lesions of the mpoa and limbic sites on maternal behavior and operant responding for pup-reinforcement. Behav Brain Res 108(2): 215–231.
Lee A, Li M, Watchus J, Fleming AS. 1999. Neuroanatomical basis of maternal memory in postpartum rats: selective role for the nucleus accumbens. Behav Neurosci 113: 523–538.
Lee CK, Kang HS, Lee BJ, Kang HM, Choi WS, et al 1999. Effects of dopamine and melatonin on the regulation of PIT-1 isotype placental growth hormone and lactogen gene expression in the rat placenta. Mol Cells 9: 646–651.
Leon M, Woodside B. 1983. Energetic limits on reproduction: maternal food intake. Physiol Behav 30(6): 945–957.
Levesque D, Gagne B, Barden N, Di Paolo T. 1992. Chronic estradiol treatment increases anterior pituitary but not striatal D2 dopamine receptor mRNA levels in rats. Neurosci Lett 140: 5–8.
Li Y, Hu X-T, Berney TG, Vartanian AJ, Stine CD, et al 1999. Both glutamate receptor antagonists and prefrontal cortex lesions prevent induction of cocaine sensitization and associated neuroadaptions. Synapse 34: 169–180.
Lindblom C, Sodersten P, Eneroth P. 1985. Effects of pup sucking behavior on inhibition of sexual behavior and ovulatory secretion of LH in lactating rats. J Endocrinol 104: 419–425.
Linden A, Uvnas-Moberg K, Eneroth P, Sodersten P. 1989. Stimulation of maternal behaviour in rats with chlocystokinin octapeptide. J Neuroendocrinol 1: 389–392.
Lisciotto CA, Morrell JI. 1993. Circulating gonadal steroid hormones regulate estrogen receptor mRNA in the male rat forebrain. Mol Brain Res 20: 79–90.
Lofstrom A. 1977. Catecholamine turnover alterations in discrete areas of the median eminence of the 4- and 5-day cyclic rat. Brain Res 120(1): 113–131.
Lofstrom A, Eneroth P, Gustaffson JA, Skett P. 1977. Effects of estradiol benzoate on catecholamine levels and turnover in discrete areas of the median eminence and the limbic forebrain, and on serum luteinizing hormone, follicle stimulating hormone and prolactin concentrations in the ovariectomized female rat. Endocrinology 101: 1559–1569.
Lonstein JS. 2002. Effects of dopamine receptor antagonism with haloperidol on nuturing behavior in the biparental prairie vole. Pharmacol Biochem Behav 74: 11–19.
Lonstein JS. 2005. Reduced anxiety in postpartum rats requires recent physical contact with pups, but is independent of suckling or peripheral sources of hormones. Hormones and Behavior, 47(3): 241-255.
Lonstein JS, Blaustein JD. 2004. Immunocytochemical investigation of nuclear progestin receptor expression within dopaminergic neurones of the female rat brain. J Neuroendocrinol 16: 534–543.
Lonstein JS, Dominguez JM, Putnam SK, DeVries GJ, Hull EM. 2003. Intracellular preoptic and striatal monoamines in pregnant and lactating rats: possible role in maternal behavior. Brain Res 970: 149–158.
Lonstein JS, Fleming AS. 2001. Parental behavior in rats and mice. Current protocols in neuroscience. New York: Wiley and Sons; pp. 8.15.1–8.15.26.
Lonstein JS, Gammie SC. 2002. Sensory, hormonal, and neural control of maternal aggression in laboratory rodents. Neurosci Biobehav Rev 26(8): 869–888.
Lorberbaum JP, Newman JD, Dubno JR, Horwitz AR, Nahas Z, et al 1999. Feasibility of using fMRI to study mothers responding to infant cries. Depress Anxiety 10: 99–104.
Lonstein JS, Simmons DA, Stern JM. 1998. Functions of the caudal periqueductal gray in lactating rats: kyphosis, lordosis, maternal aggression and fearfulness. Behav Neurosci 112: 1502–1518.
Lonstein JS, Stern JM. 1997a. Role of the midbrain periaqueductal gray in maternal nurturance and aggression: c-fos and electrolytic lesion studies in lactating rats. J Neurosci 17(9): 3364–3378.
Lonstein JS, Stern JM. 1997b. Somatosensory contributions to c-fos activation within the caudal periaqueductal gray of lactating rats: effects of perioral, rooting, and suckling stimuli from pups. Horm Behav 32: 155–166.
Lonstein JS, Stern JM. 1998. Site and behavioral specificity of periaqueductal gray lesions on postpartum sexual, maternal, and aggressive behaviors in rats. Brain Res 804: 21–35.
Lonstein JS, Simmons DA, Swann JM, Stern JM. 1998. Forebrain expression of c-fos due to active maternal behaviour in lactating rats. Neuroscience 82: 267–281.
Magnusson JE, Fisher K. 2000. The involvement of dopamine in nociception: the role of D(1) and D(2) receptors in the dorsolateral striatum. Brain Res 855(2): 260–266.
Magnusson JE, Fleming AS. 1995. Rat pups are reinforcing to the maternal rat: role of sensory cues. Psychobiology 23: 69–75.
Mann PE, Bridges RS. 2001. Lactogenic hormone regulation of maternal behavior. The maternal brain neurobiological and neuroendocrine adaptation and disorders in pregnancy and postpartum. Progress in Brain Research, vol 133. Russell JA, Douglas AJ, Windle RJ, Ingram CD, editors. Amsterdam, New York, Oxford: Elsevier; pp. 252–262.
Mann PE, Bridges RS. 2002. Prolactin receptor gene expression in the forebrain of pregnant and lactating rats. Mol Brain Res 105: 136–145.
Mann PE, Felicio LF, Bridges RS. 1995. Investigation into the role of cholecystokinin (CCK) in the induction and maintenance of maternal behavior in rats. Horm Behav 29: 392–406.
Mantalenakis SJ, Ketchel MM. 1966. Frequency and extent of delayed implantation in lactating rats and mice. J Reprod Fertil 12: 391–394.
Marinari KT, Moltz H. 1978. Serum prolactin levels and vaginal cyclicity in concaveated and lactating female rats. Physiol Behav 21: 525–528.
Mattheij JAM, Swarts HJM, Verstijnen CPHJ. 1984. The response of plasma prolactin to suckling during normal and prolonged lactation in the rat. Horm Res 20: 261–268.
Mattheij JAM, Swarts HJM, van Mourik S. 1985. Plasma prolactin in rat during suckling without prior separation from pups. Acta Endocrinol 108(4): 468–474.
Matthews J, Gustafsson JA. 2003. Estrogen signaling: a subtle balance between ER alpha and ER beta. Mol Interv 3: 281–292.
Matthews JC, Beveridge MJ, Malandro MS, Rothstein JD, Campbell-Thompson M, et al 1998. Activity and protein localization of multiple glutamate transporters in gestation day 14 vs 20 rat placenta. Am J Physiol 274: C603–C614.
Matthews-Felton T, Corodimas KP, Rosenblatt JS, Morrell JI. 1995. Lateral habenula neurons are necessary for the hormonal onset of maternal behavior and for the display of postpartum estrus in naturally parturient female rats. Behav Neurosci 109(6): 1172–1188.
Matthews-Felton T, Linton LN, Rosenblatt JS, Morrell JI. 1999. Estrogen implants in the lateral habenular nucleus does not stimulate the onset of maternal behavior in female rats. Horm Behav 35: 71–80.
Mattson BJ. 2002. Competing appetitive processes in the lactating, maternal rodent: natural and pharmacological stimuli. PhD thesis Rutgers, Newark NJ: The State University of New Jersey; pp. 1–211.
Mattson BJ, Morrell JI. 2005. Preference for cocaine- versus pup-associated cues differentially engages neurons expressing either Fos or CART in lactating, maternal rat. Neuroscience 135: 315-328.
Mattson BJ, Williams SE, Rosenblatt JS, Morrell JI. 2001. Comparison of two positive reinforcing stimuli: pups and cocaine throughout the postpartum period. Behav Neurosci 115: 683–694.
Mattson BJ, Williams SE, Rosenblatt JS, Morrell JI. 2003. Preferences for cocaine- or pup-asssociated chambers differentiates otherwise behaviorally identical postpartum maternal rats. Psychopharmacology 167: 1–8.
Mayer AD, Rosenblatt JS, 1980. Hormonal interaction with stimulus and situational factors in the initiation of maternal behavior in nonpregnant rats. J Comp Physiol Psychol 94(6): 1040–1059.
McDermott JL. 1993. Effects of estrogen upon dopamine release from the corpus striatum of young and aged female rats. Brain Res 606: 118–125.
McDermott JL, Anderson LI, Dluzen DE. 1997. Interactive effects of tamoxifen and estrogen upon the nigrostriatal dopaminergic system. Neuroendocrinology 66(3): 181–187.
McFarland K, Lapish CC, Kalivas PW. 2003. Prefrontal glutamate release into the core of the nucleus accumbens mediates cocaine-induced reinstatement of drug-seeking behavior. J Neurosci 23: 3531–3537.
McGinnis MY, Gordon JH, Gorski RA. 1980. Time course and localization of the effects of estrogen on glutamic acid decarboxylase activity. J Neurochem 34(4): 785–792.
McKinley MJ, Burns P, Colvill LM, Oldfield BJ, Wade JD, et al 1997. Distribution of Fos immunoreactivity in the lamina terminalis and hypothalamus induced by centrally administered relaxin in conscious rats. J Neuroendocrinol 9: 431–437.
Mermelstein PG, Becker JB, Surmeier DJ. 1996. Estradiol reduces calcium currents in rat neostriatal neurons via a membrane receptor. J Neurosci 16: 595–604.
Miceli MO, Fleming AS, Malsbury CW. 1983. Disruption of maternal behaviour in virgin and postparturient rats following sagittal plane knife cuts in the preoptic area-hypothalamus. Behav Brain Res 9(3): 337–360.
Miranda-Paiva CM, Ribeiro-Barbosa ER, Canteras NS, Felicio LF. 2003. A role for the periaqueductal grey in opioidergic inhibition of maternal behavior. Eur J Neurosci 18: 667–674.
Mittler T, Cho J, Peoples LL, West MO. 1994. Representtion of the body in the lateral striatum of the freely moving rat: single neurons related to licking. Exp Brain Res 98: 163–167.
Moltz H, Geller D, Levin R. 1967. Maternal behavior in totally mammectomized rats. J Comp Physiol Psychol 64: 225–229.
Moltz H, Levin R, Leon M. 1969a. Prolactin in the postpartum rat: synthesis and release in the absence of suckling stimulation. Science 163: 1083–1084.
Moltz H, Levin R, Leon M. 1969b. Differential effect of progesterone on the maternal behavior of primiparous and multiparous rats. J Comp Physiol Psychol 67: 36–40.
Moltz H, Lubin M, Leon M, Numan M. 1970. Hormonal induction of maternal behavior in the ovariectomized nulliparous rat. Physiol Behav 5: 1373–1377.
Moltz H, Robbins D, Parks M. 1966. Caesarean delivery and maternal behavior of primiparous and multiparous rats. J Comp Physiol Psychol 61: 455–460.
Mora S, Dussaubat N, Diaz-Veliz G. 1996. Effects of the estrous cycle and ovarian hormones on behavior indices of anxiety in female rats. Psychoneuroendocrinology 21: 609–620.
Morgan HD, Watchus JA, Milgram NW, Fleming AS. 1999. The long lasting effects of electrical simulation of the medial preoptic area and medial amygdala on maternal behavior in female rats. Behav Brain Res 99(1): 61–73.
Morissette M, Biron D, DiPaolo T. 1990a. Effect of estradiol and progesterone on rat striatl dopamine uptake sites. Brain Res Bull 25: 419–422.
Morissette M, DiPaolo T. 1993. Effect of chronic estradiol and progesterone treatments of ovariectomized rats on brain dopamine uptake sites. J Neurochem 60(5): 1876–1883.
Morissette M, Levesque D, Belanger A, DiPaolo T. 1990b. A physiological dose of estradiol with progesterone affects striatum biogenic amines. Can J Physiol Pharmacol 68: 1520–1526.
Morrell JI, Wagner CK, Malik KF, Lisciotto CA. 1995. Estradiol receptor RNA: neuroanatomy and regulation in three physiological models. Neurobiological effects of sex steroid hormones. Micevych PE, Hammer RP, editors. New York NY: Cambridge University Press; pp. 57–84.
Moss FA. 1924. Study of animal drives. J Exp Psychol 3: 165–185.
Mufson EJ, Cai WJ, Jaffar S, Chen E, Stebbins G, et al 1999. Estrogen receptor immunoreactivity within subregions of the rat forebrain: neuronal distribution and association with perikarya containing choline acetyltranferase. Brain Res 849: 253–274.
Mustafa A, Nyberg F, Bogdanovic N, Islam A, Suliman I, et al. 1995. Prolactin binding sites in rat brain and liver: effects of long-term ovariectomy and ovarian steroids. Neurosci Lett. Nov 24; 200(3): 179–182.
Nicoletti F, Patti F, Ferrara N, Canonico PL, Giammona G, et al 1982. Comparative effects of estrogens and prolactin on nigral and striatal GAD activity. Brain Res 232(1): 238–241.
Nicoletti F, Speciale C, Sortino MA, Panetta MS, Di Giorgio RM, et al 1985. Estrogen effects on nigral glutamic acid decarboxylase activity: a possible role for catecholestrogen. Eur J Pharmacol 115(2–3): 297–300.
Neisewander JL, Baker DA, Fuchs RA, Tran-Nguyen LT, Palmer A, et al 2000. Fos protein expression and cocaine-seeking behavior in rats after exposure to a cocaine self-administration environment. J Neurosci 20: 798–805.
Nissen HW. 1930. A study of maternal behavior in the white rat by means of the obstruction method. J Genetic Psychol 37: 377–393.
Niswender GD, Juengel JL, McGuire WJ, Belfiore CJ, Wiltbank MC. 1994. Luteal function: the estrous cycle and early pregnancy. Biol Reprod 50: 239–247.
Novakova V, Sterc J, Kuchar S, Mozes S, 1993. Maternal behaviour in septal rat females. Physiol Res 42(5): 351–360.
Numan M. 1978. Progesterone inhibition of maternal behavior in the rat. Horm Behav 11: 209–231.
Numan M. 1988. Maternal behavior. The physiologiy of reproductive behavior. Knobil E, Neill J, editors. New York: Raven Press, Ltd.
Numan M. 1994. Maternal behavior. The physiology of reproduction. Knobil E, Neil JD, editors. New York: Raven Press; pp. 223–283.
Numan M. 1990. Long-term effects of preoptic area knife cuts on the maternal behavior of postpartum rats. Behav Neural Biol 53(2): 284–290.
Numan M, Numan MJ. 1996. A lesion and neuroanatomical tract-tracing analysis of the role of the bed nucleus of the stria terminalis in retrieval behavior and other aspects of maternal responsiveness in rats. Dev Psychobiol 29(1): 23–51.
Numan M, Callahan EC. 1980. The connections of the medial preoptic region and maternal behavior in the rat. Physiol Behav 25(5): 653–665.
Numan M, Corodimas KP. 1985. The effects of paraventricular hypothalamic lesions on maternal behavior in rats. Physiol Behav 35(3): 417–425.
Numan M, Corodimas KP, Numan MJ, Factor EM, Piers WD. 1988. Axon-sparing lesions of the preoptic region and substantia innominata disrupt maternal behavior in rats. Behav Neurosci 102(3): 381–396.
Numan M, Insel TR. 2003. The Neurobiology of Parental Behavior. New York: Springer-Verlag.
Numan M, McSparren J, Numan MJ. 1990. Dorsolateral connections of the medial preoptic area and maternal behavior in rats. Behav Neurosci 104: 964–979.
Numan M, Nagle DS. 1983. Preoptic area and substantia nigra interact in the control of maternal behavior in the rat. Behav Neurosci 97(1): 120–139.
Numan M, Numan MJ. 1994. Expression of Fos-like immunoreactivity in the preoptic area of maternally behaving virgin and postpartum rats. Behav Neurosci 108(2): 379–394.
Numan M, Numan MJ. 1995. Importance of pup-related sensory inputs and maternal performance for the expression of Fos-like immunoreactivity in the preoptic area and ventral bed nucleus of the stria terminalis of postpartum rats. Behav Neurosci 109(1): 135–149.
Numan M, Numan MJ. 1997. Projection sites of medial preoptic area and ventral bed nucleus of the stria terminalis neurons that express Fos during maternal behavior in female rats. J Neuroendocrinol 9(5): 369–384.
Numan M, Numan MJ, English JB. 1993. Excitotoxic amino acid injections into the medial amygdala facilitate maternal behavior in virgin female rats. Horm Behav 27: 56–81.
Numan M, Rosenblatt JS, Komisaruk BR. 1977. Medial preoptic area and onset of maternal behavior in the rat. J Comp Physiol Psychol 91(1): 146–164.
Numan M, Roach JK, Del Cerro MC, Guillamon A, Segovia S, et al 1999. Expression of intracellular progesterone receptors in rat brain during different reproductive states, and involvement in maternal behavior. Brain Res 830(2): 358–371.
Numan M, Smith HG. 1984. Maternal behavior in rats: evidence for the involvment of preoptic projections to the ventral tegmental area. Behav Neurosci 98: 712–727.
Ogawa S, Eng V, Taylor J, Lubahn DB, Korach KS, et al 1998. Roles of estrogen receptor-α gene expression in reproduction-related behaviors in female mice. Endocrinology 139: 5070–5081.
Olazabal DE, Ferreira A. 1997. Maternal behavior in rats with kainic acid-induced lesions of the hypothalamic paraventricular nucleus. Physiol Behav 61(5): 779–784.
Olazabal DE, Abercrombie E, Rosenblatt JS, Morrell JI. 2004. The content of dopamine, serotonin, and their metabolites in the neural circuit that mediates maternal behavior in juvenile and adult rats. Brain Res Bull 63: 259–268.
Olazabal DE, Kalinichev M, Morrell JI, Rosenblatt JS. 2002. MPOA Cytotoxic lesions and maternal behavior in the rat: Effects of midpubertal lesions on maternal behavior and the role of ovarian hormones in the maturation of MPOA control of maternal behavior. Horm Behav 41: 126–138.
Osheroff P, Phillips HS. 1991. Autoradiographic localization of relaxin binding sites in the rat brain. Proc Natl Acad Sci 88: 6413–6417.
Ouhtit A, Morel G, Kelly PA. 1993. Visualization of gene expression of short and long forms of prolactin receptor in rat reproductive tissues. Biol Reprod 49: 528–536.
Paladini CA, Celada P, Tepper JM. 1999. Striatal, pallidal, and pars reticulata evoked inhibition of nigrostriatal dopaminergic neurons is mediated by GABAA receptors in vivo. Neuroscience 89: 799–812.
Pare D, Collins DR. 2000. Neuronal correlates of fear in the lateral amygdala: multiple extracellular recordings in conscious cats. J Neurosci 20: 2701–2710.
Park WK, Bari AA, Jey AR, Anderson SM, Spealman RD, et al 2002. Cocaine administered into the medial prefrontal cortex reinstates cocaine-seeking behavior by increasing AMPA receptor-mediated glutamate transmission in the nucleus accumbens. J Neurosci 22: 2916–2925.
Parkinson JA, Crofts HS, McGuigan M, Tomic DL, Everitt BJ, et al 2001. The role of the primate amygdala in conditioned reinforcement. J Neurosci 21: 7770–7780.
Parsons B, Rainbow TC, MacLusky NJ, McEwen BS. 1982. Progestin receptor levels in rat hypothalamus and limbic nuclei. J Neurosci 2: 1446–1452.
Pasqualini C, Olivier V, Guibert B, Frain O, Leviel V. 1995. Acute stimulatory effect of estradiol on striatal dopamine synthesis. J Neurochem 65(4): 1651–1657.
Patchev VK, Schlosser SF, Hassan AH, Almeida OF. 1993. Oxytocin binding sites in rat limbic and hypothalamic structures: site-specific modulation by adrenal and gonadal steroids. Neuroscience 57: 537–543.
Pedersen CA. 1997. Oxytocin control of maternal behavior. Regulation by sex steroids and offspring stimuli. Ann NY Acad Sci 807: 126–145.
Pedersen CA, Ascher JA, Monroe YL, Prange AJ. 1982. Oxytocin induces maternal behavior in virgin female rats. Science 216: 648–650.
Pedersen CA, Boccia ML. 2003. Oxytocin antagonism alters rat dams’ oral grooming and upright posturing over pups. Physiol Behav 80: 233–241.
Pedersen CA, Caldwell JD, Walker C, Ayers G, Mason GA. 1994. Oxytocin activates the postpartum onset of rat maternal behavior in the ventral tegmental and medial preoptic areas. Behav Neurosci 108(6): 1163–1171.
Pennartz CMA, Groenewegen HJ, Lopes Da Silva FH. 1994. The nucleus accumbens as a complex of functionally distinct neuronal ensembles: an integration of behavioural, electronphysiological and anatomical data. Prog Neurobiol 42: 719–761.
Pfaff D, Keiner M. 1973. Atlas of estradiol-concentrating cells in the central nervous system of the female rat. J Comp Neurol 151(2): 121–158.
Pi XJ, Grattan DR. 1999a. Increased expression of both short and long forms of prolactin receptor mRNA in hypothalamic nuclei of lactating rats. J Mol Endocrinol 23: 13–22.
Pi XJ, Grattan DR. 1999b. Expression of prolactin receptor mRNA is increased in the preoptic area of lactating rats. Endocrine 11: 91–98.
Pi XJ, Grattan DR. 1999c. Increased prolactin receptor immunoreactivity in the hypothalamus of lactating rats. J Neuroendocrinol 11(9): 693–705.
Pi X, Voogt JL. 2000. Effect of suckling on prolactin receptor immunoreactivity in the hypothalamus of the rat. Neuroendocrinology 71(5): 308–317.
Pi X, Voogt JS. 2001. Mechanisms for suckling-induced changes in expression of prolactin receptor in the hypothalamus of the lactating rat. Brain Res 891: 197–205.
Pi X, Zhang B, Li J, Voogt JL. 2003. Promoter usage and estrogen regulation of prolactin receptor gene in the brain of the female rat. Neuroendocrinology 77: 187-197.
Piccirillo M, Alpert JE, Cohen DJ, Shaywitz BA. 1980. Effects of 6-hydroxydopamine and amphetamine on rat mothering behavior and offspring development. Pharmacol Biochem Behav 13(3): 391–395.
Pifl C, Giros B, Caron MG. 1993. Dopamine transporter expression confers cytoxicity to low doses of the parkinsonism-inducing neurotoxin 1-methyl-4-phenylpyridinum. J Neurosci 12(10): 4246–4253.
Pryce CR, Dobeli M, Martin RD. 1993. Effects of sex steroids on maternal motivation in the common marmoset (Callithrix jacchus): development and application of an operant system with maternal reinforcement. J Comp Psychol 107(1): 99–115.
Quinones-Jenab V, Jenab S, Ogawa S, Adan RA, Burbach JP, et al 1997. Effects of estrogen on oxytocin receptor messenger ribonucleic acid expression in the uterus, pituitary and forebrain of the female rat. Neuroendocrinology 65: 9–17.
Ramirez VD, Zheng J. 1996. Membrane sex-steroid receptors in the brain. Front Neuroendocrinol 17: 402–439.
Rees SL, Panesar S, Steiner M, Fleming AS. 2004. The effects of adrenalectomy and corticosterone replacement on maternal behavior in the postpartum rat. Horm Behav 46: 411-419.
Rehavi M, Goldin M, Roz N, Weizman A. 1998. Regulation of rat brain vesicular monoamine transporter by chronic treatment with ovarian hormones. Brain Res Mol Brain Res 57(1): 31–37.
Reid MS, O'Connor WT, Herrera-Marschitz M, Ungerstedt U. 1990. The effects of intranigral GABA and dynorpin A injections on striatal dopamine and GABA release: evidence that dopamine provides inhibitory regulation of striatal GABA neurons via D2 receptors. Brain Res 519: 255–260.
Reisbick S, Rosenblatt JS, Mayer AD. 1975. Decline of maternal behavior in the virgin and lactating rat. J Comp Physiol Psychol 89(7): 722–732.
Robbins TW, Everitt BJ. 1999. Motivation and Reward. Fundamental Neuroscience. Zigmond M, et al editors. Academic Press; New York Chp 48 pp. 1245–1278.
Robertson MC, Gillespie B, Friesen HG. 1982. Characterization of the two forms of rat placental lactogens (rPL): rPL-I and rPL-II. Endocrinology 111: 1862–1866.
Rodriguez M, Gonzalez-Hernandez T. 1999. Electrophysiological and morphological evidence for a GABAergic nigrostrial pathway. J Neurosci 19: 4682–4894.
Roky R, Paut-Pagano L, Goffin V, Kitahama K, Valatx JL, et al 1996. Distribution of prolactin receptors in the rat forebrain. Immunohistochemical study. Neuroendocrinology 63: 422–429.
Rosenberg P, Halaris A, Moltz H. 1977. Effects of central norepinephrine depletion on the initiation and maintenance of maternal behavior in the rat. Pharmacol Biochem Behav 6(1): 21–24.
Rosenblatt JS. 1967. Non-hormonal basis of maternal behavior in the rat. Science 156: 1512–1514.
Rosenblatt JS, Siegel HI, Mayer AD. 1979. Progress in the Study of maternal behavior in the rat: Hormonal, Nonhormonal, Sensory, and Developmental Aspects. Advances in the Study of Behavior, vol 10. Rosenblatt JS, Hinde RA, Beer C, Busnel M-C, editors. NY London: Academic Press; pp. 225–311.
Rosenblatt JS. 1995. Hormonal basis of parenting. Handbook of Parenting volume 2 Biology and Ecology of Parenting. Bornstein MH, editor. New Jersey, Hove UK: Lawrence Erlbaum Associates, Publishers Mahwah.
Rosenblatt JS, Ceus K. 1998. Estrogen implants in the medial preoptic area stimulate maternal behavior in male rats. Horm Behav 33: 23–30.
Rosenblatt JS, Olufowobi A, Siegel HI. 1998. Effects of pregnancy hormones on maternal responsiveness, responsiveness to estrogen stimulation of maternal behavior, and lordosis response to estrogen stimulation. Horm Behav 33: 104–114.
Rosenblatt JS, Siegel HI, 1975. Hysterectomy-induced maternal behavior during pregnancy in the rat. J Comp Physiol Psychol 89(7): 685–700.
Rosenblatt JS, Wagner CK, Morrell JI. 1994. Hormonal priming and triggering of maternal behavior in the rat with special reference to the relations between estrogen receptor binding and ER mRNA in specific brain regions. Psychoneuroendocrinology 19: 543–552.
Rosenkranz JA, Grace AA. 2001. Dopamine attenuates prefrontal cortical suppression of sensory inputs to the basolateral amygdala of rats. J Neurosci 21: 4090–4103.
Roth LL, Rosenblatt JS. 1968. Mammary glands of pregnant rats: development stimulated by licking. Science 151: 1403–1404.
Roy EJ, Buyer DR, Licari VA. 1990. Estradiol in the striatum: effects on behavior and dopamine receptors but no evidence for membrane steroid receptors. Brain Res Bull 25: 221–227.
Rubin BS, Bridges RS. 1984. Disruption of ongoing maternal responsiveness in rats by central administration of morphine sulfate. Brain Res 307(1–2): 91–97.
Rush ME, Blake CA. 1982. Serum testosterone concentrations during the 4-day cycle in normal and adrenalectomized rats. Proc Soc Exp Biol Med 169: 216–221.
Russell JA, Leng G, Douglas AJ. 2003. The magnocellular oxytocin system, the fount of maternity: adaptations in pregnancy. Front Neuroendoncrinol 24: 27–61.
Russo SJ, Festa ED, Fabian SJ, Gazi FM, Kraish M, et al 2003. Gonadal hormones differentially modulate cocaine-induced conditioned place preference in male and female rats. Neuroscience 120(2): 523–33.
Sakaguchi K, Tanaka M, Ohkubo T, Doh-ura K, Fujikawa T, et al 1996. Induction of brain prolactin receptor long-form mRNA expression and maternal behavior in pup-contracted male rats: promotion by prolactin administration and suppression by female contact. Neuroendocrinology 63: 559–568.
Sakamoto Y, Suga S, Sakuma Y. 1993. Estrogen-sensitive neurons in the female rat ventral tegmental area: a dual route for the hormone action. J Neurophysiol 70(4): 1469–1475.
Salzberg HC, Lonstein JS, Stern JM. 2002. GABAA receptor regulation of kyphotic nursing and female sexual behavior in the caudal ventrolateral periaqueductal gray of postpartum rats. Neuroscience 114: 675–687.
Sanyal MKJ. 1978. Secretion of progesterone during gestation in the rat. Endocrinology 79: 179–190.
Saper C. 2000. Hypothalamic connections with the cerebral cortex. Prog Brain Res 126: 40–48.
Sar M. 1988. Distribution of progestin-concentrating cells in rat brain: colocalization of [3H]ORG.2058, a synthetic progestin, and antibodies to tyrosine hydroxylase in hypotyhalamus by combined autoradiography and immunocytochemistry. Endocrinology 123: 1110–1118.
Schlinger BA, Arnold AP. 1993. Estrogen síntesis in vivo in the adult zebra finch: additional evidence that circulating estrogens can originate in the brain. Endo 133: 2610–2616.
Schneider JS, Stone MK, Wynne-Edwards KE, Horton TH, Lydon J, et al 2003. Progesterone receptors mediate male aggression toward infants. PNS 100: 2951–2956.
Schroeder BE, Binzak JM, Kelley AM. 1999. A common profile of prefrontal cortical activation following exposure to nicotine or chocolate-associated contextual cues. Neuroscience 105: 535–545.
Schulz H, Kovacs GL, Telegdy G. 1979. Action of posterior pituitary neuropeptides on the nigrostriatal dopaminergic system. Eur J Pharmacol 57: 185–190.
Schumacher M, Coirini H, Frankfurt M, McEwen BS. 1989. Localized actions of progesterone in the hypothalamus involve oxytocin. Proc Natl Acad Sci USA 86: 6798–6801.
Schwartz E, Rowe FA. 1976. Olfactory bulbectomy: influences on maternal behavior in primiparous and multiparous rats. Physiol Behav 17: 879–883.
Sell SL, Scalzitti JM, Thomas ML, Cunningham KA. 2000. Influence of ovarian hormones and estrous cycle on the behavioral response to cocaine in female rats. J Pharm Exp Ther 293: 879–886.
Shaikh AA. 1971. Estrone and estradiol levels in the ovarian venous blood from rats during estrus cycle and pregnancy. Biol Reprod 5: 297–307.
Shearman LP, McReynolds AM, Zhou FC, Meyer JS. 1998. Relationship between 125 RTI-55-labeled cocaine binding sites and the serotonin transporter in rat placenta. Am J Physiol 275: 1621–1629.
Sheehan TP, Cirrito J, Numan MJ, Numan M. 2000. Using c-Fos immunocytochemistry to identify forebrain regions that may inhibit maternal behavior in rats. Behav Neurosci 114(2): 337–352.
Sheehan TP, Numan M. 1997. Microinjection of the tachykinin neuropeptide K into the ventromedial hypothalamus disrupts the hormonal onset of maternal behavior in female rats. J Neuroendocrinol 9(9): 677–687.
Sheehan T, Paul M, Amaral E, Numan MJ, Numan M. 2001.Evidence that the medial amygdala projects to the anterior/ventromedial hypothalamic nuclei to inhibit maternal behavior in rats. Neuroscience. 106(2): 341–356.
Sherwood OD. 1988. Relaxin. The physiology of reproduction, vol 2. Knobil E, Neill JD, editors. New York: Raven Press.
Sherwood OD, Crnekovic VE, Gordon WL, Rutherford JE. 1980. Radioimmunoassay of relaxin throughout pregnancy and during parturition in the rat. Endocrinology 107: 691–698.
Shimizu H, Bray GA 1993. Effects of castration, estrogen replacement and estrus cycle on monoamine metabolism in the nucleus accumbens, measured by microdialysis. Brain Res 621(2): 200–206.
Shingo T, Gregg C, Enwere E, Fujikawa H, Hassam R, et al 2003. Pregnancy-stimulated neurogenesis in the adult female forebrain mediated by prolactin. Science 299: 117–120.
Siegel HI, Rosenblatt JS. 1978. Duration of estrogen stimulation and progesterone inhibition of maternal behavior in pregnancy-terminated rats. Horm Behav 11: 12–19.
Siegel HI, Rosenblatt JS. 1975a. Estrogen-induced maternal behavior in hysterectomized-ovariectomized virgin rats. Physiol Behav 14: 465–471.
Siegel HI, Rosenblatt JS. 1975b. Hormonal basis of hysterectomy-induced maternal behavior during pregnancy in the rat. Horm Behav 6: 211–222.
Silva MR, Bernardi MM, Cruz-Casallas PE, Felicio LF. 2003. Pimozide injections into the nucleus accumbens disrupt maternal behaviour in lactating rats. Pharmacol Toxicol 93: 42–47.
Silva MR, Bernardi MM, Felicio LF. 2001. Effects of dopamine receptor antagonists on ongoing maternal behavior in rats. Pharmacol Biochem Behav 68(3): 461–468.
Simerly RB, Swanson LW. 1986. The organization of neural inputs to the medial preoptic nucleus of the rat. J Comp Neurol 246: 312–342.
Simerly RB, Swanson LW. 1988. Projections of the medial preoptic nucleus: a Phaseolus vulgaris leucoagglutinin anterograde tract tracting study in the rat. J Comp Neurol 270: 209–242.
Simmons R. 1924. The relative effectiveness of certain incentives in animal learning. Comp Psychol Monog 2: 79.
Sinnamon HM. 1993. Preoptic and hypothalamic neurons and the initiation of locomotion in the anesthetized rats. Prog Neurobiol 41: 323–344.
Smith JT, Waddell BJ. 2002. Leptin receptor expression in the rat placenta: changes in ob-ra, ob-rb, and ob-re with gestational age and suppression of glucocorticoids. Biol Reprod 67(4): 1204–1210.
Smith MO, Holland RC. 1975. Effects of lesions of the nucleus accumbens on lactation and postpartum behavior. Physiol Psychol 3: 331–336.
Smith MS, Freeman ME, Neill JD. 1975. The control of progesterone secretion during the estrous cycle and early pseudopregnancy in the rat: prolactin, gonadotrophin, and steroid levels associated with rescue of the corpus luteum of pseudopregnancy. Endocrinology 96: 219–226.
Smith MS, Neill JD. 1977. Inhibition of gonadotrophin secretion during lactation in the rat: relative contribution of suckling and ovarian steroids. Biol Reprod 17: 255–261.
Smith KS, Mattson BJ, Morrell JI. 2002. The MPOA is engaged in the motivation to perform maternal behavior. Abstract, Society for Behavioral Neuroendocrinology.
Sorenson CA, Gordon M. 1975. Effects of 6-hydroxydopamine on shock-elicited aggression, emotionality and maternal behavior in female rats. Pharmacol Biochem Behav 3(3): 331–335.
Spanagel R, Weiss F. 1999. The dopamine hypothesis of reward: past and current status. Trends Neurosci 22: 521–527.
Spielewoy C, Roubert C, Hamon M, Nosten-Bertrand M, Betancur C, et al 2000. Behavioural disturbances associated with hyperdopaminergia in dopamine-transporter knockout mice. Behav Pharmacol 11(3–4): 279–290.
Stack EC, Balakrishnan R, Numan MJ, Numan M. 2002. A functional neuroanatomical investigation of the role of the medial preoptic area in neural circuits regulating maternal behavior. Behav Brain Res 131: 17–36.
Stack EC, Numan M. 2000. The temporal course of expression of c-Fos and Fos B within the medial preoptic area and other brain regions of postpartum female rats during prolonged mother-young interactions. Behav Neurosci 114: 609–622.
Stack EC, Numan MJ, Numan M. 2001. The effects of bilateral lesions of the shell of the nucleus accumbens on maternal behavior in the rat. Soc Neurosci Abst 857.1.
Steele MK, Rowland D, Moltz H. 1979. Initiation of maternal behavior in the rat: possible involvement of limbic norepinephrine. Pharmacol Biochem Behav 11(2): 123–130.
Stern JM. 1989. Maternal behavior: sensory, hormonal, and neural determinants. Psychoneuroendocrinology. Brush FR, Levine S, editors. San Diego: Academic Press; pp. 102–226.
Stern JM. 1996. Somatosensation and maternal care in Norway rats. Parental Care - Evolution, Mechanisms, and Adaptive Significance. Advances in the Study of Behavior, vol. 25. Rosenblatt JS, Snowdon CT, editors. New York: Academic Press.
Stern JM. 1991. Nursing posture is elicited rapidly in maternally naive, haloperidol-treated female and male rats in response to ventral trunk stimulation from active pups. Horm Behav 25(4): 504–517.
Stern JM, Johnson SK. 1989. Perioral somatosensory determinants of nursing behavior in Norway rats (Rattus norvegicus). J Comp Psychol 103(3): 269–280.
Stern JM, Keer SE. 1999. Maternal motivation of lactating rats is disrupted by low dosages of haloperidol. Behav Brain Res 99(2): 231–239.
Stern JM, Keer SE. 2002. Acute hunger of pups elicits increased kyphotic nursing and shorter intervals between nursing bouts: implications for changes in nursing with time postpartum. J Comp Psychol 116: 83–92.
Stern JM, Mackinnon DA. 1976. Postpartum, hormonal, and nonhormonal induction of maternal behavior in rats: effects on T-maze retrieval of pups. Horm Behav 7(3): 305–316.
Stern JM, Mackinnon DA. 1978. Sensory regulation of maternal behavior in rats: effects of pup age. Dev Psychobiol 11(6): 579–586.
Stern JM, Protomastro M. 2000. Effects of low dosages of apomorphine on maternal responsiveness in lactating rats. Pharmacol Biochem Behav 66: 353–359.
Stern JM, Taylor LA. 1991. Haloperidol inhibits maternal retrieval and licking, but enhances nursing behavior and litter weight gains in lactating rats. J Neuroendocrinol 3: 591–596.
Stivers JA, Kaltwasser MT, Hill PS, Hruby VJ, Crawley JN. 1988. Ventral tegmental oxytocin induces grooming. Peptides 9: 223–231.
Sugiyama T, Minoura H, Kawabe N, Tanaka M, Nakashima K, 1994. Preferential expression of long form prolactin receptor mRNA in the rat brain during the oestrous cycle, pregnancy and lactation: hormones involved in its gene expression. J Endocrinol 141(2): 325–333.
Sugiyama T, Minoura H, Toyoda N, Sakaguchi K, Tanaka M, et al 1996. Pup contact induces the expression of long form prolactin receptor mRNA in the brain of female rats: effects of ovariectomy and hypophysectomy on receptor gene expression. J Endocrinol 149(2): 335–340.
Summerlee AJ, Ramsey DG, Poterski RS. 1998. Neutralization of relaxin within the brain affects the timing of birth in rats. Endocrinology 139: 479–484.
Swanson LW. 1988–1989. The neural basis of motivated behavior. Acta Morphologica Neerlando-Scandinavica 26: 165–176.
Swanson LW. 1998. Brain maps: structure of the rat brain, second edition. Amsterdam: Elsevier.
Swanson LW, Mogenson GJ, Simerly RB, Wu M. 1987. Anatomical and electrophysiological evidence for a projection from the medial preoptic area to the ‘mesencephalic and subthalamic locomotor regions’ in the rat. Brain Res 405(1): 108–122.
Takeo T, Sakuma Y. 1995. Diametrically opposite effects of estrogen on the excitability of female rats medial and lateral preoptic neurons with axons to the midbrain locomotor region. Neurosci Res 22: 73–80.
Talamantes F, Ogren L. 1988. The placenta as an endocrine organ: Polypeptides. The physiology of reproduction, vol 2. Knobil E, Neill JD, editors. New York: Raven Press; pp. 2093–2144.
Tansey EM, Aubuthnott GW, Fink G, Whale D. 1983. Oestradiol-17 beta increases the firing rate of antidromically indentified neurones of the rat neostriatum. Neuroendocrinology 37: 106–110.
Taya K, Greenwald GS. 1982. Peripheral blood and ovarian levels of sex steroid in the lactating rat. Endocrinology Japan 29: 453–459.
Taya K, Sasamoto S. 1981. Changes in FSH, LH and prolactin secretion and ovarian follicular development during lactation in the rat. Endocrinology Japan 28: 187–196.
Tepper JM, Martin LP, Anderson DR. 1995. GABAA receptor-mediated inhibition of rat substantia nigra dopaminergic neurons by pars reticulata projection neurons. J Neurosci 15: 3092–3103.
Terkel J, Bridges RS, Sawyer CH. 1979. Effects of transecting lateral neural connections of the medial preoptic area on maternal behavior in the rat: nest building, pup retrieval and prolactin secretion. Brain Res 169: 369–380.
Terkel J, Rosenblatt JS. 1972. Humoral factors underlying maternal behavior at parturition: cross transfusions between freely moving rats. J Comp Physiol Psychol 80: 355–371.
Thoman EB, Levine S. 1970. Effects of adrenalectomy on maternal behavior in rats. Dev Psychobiol 3: 237–244.
Thoman EB, Sproul M, Seeler B, Levine S. 1970. Influence of adrenalectomy in female rats on reproductive processes including effects of the foetus and offspring. J Endocrinol 46: 297–303.
Thompson TL. 1999. Attenuation of dopamine uptake in vivo following priming with estradiol benzoate. Brain Res 834(1–2): 164–167.
Thompson TL, Moss RL. 1994. Estrogen regulation of dopamine release in the nucleus accumbens: genomic- and nongenomic-mediated effects. J Neurochem 62(5): 1750–1756.
Thompson TL, Moss RL. 1997. Modulation of mesolimbic dopaminergic activity over the rat estrous cycle. Neurosci Lett 229(3): 145–148.
Thompson TL, Moore CC, Smith B. 2000. Estrogen priming modualtes autoreceptor-mediated potentiation of dopamine uptake. European Journal of Pharmacology;, 401: 357-363.
Tonegawa S, Nakazawa K, Wilson MA. 2003. Genetic neuroscience of mammalian learning and memory. Philos Trans R Society Lond B Biol Sci 358: 787–795.
Torner L, Toschi N, Nava G, Clapp C, Neumann ID. 2002. Increased hypothalamic expression of prolactin in lactation: involvement in behavioural and neuroendocrine stress responses. Eur J Neurosci 15(8): 1381–1389.
Tribollet E, Audigier S, Dubois-Dauphin M, Dreifuss JJ. 1990. Gonadal steroid regulation oxytocin receptors but not vasopressin receptors in the brain of male and female rats. An autoradiographical study. Brain Res 511: 129–140.
Tucker AM. 1988. Lactation and its hormonal control. The physiology of reproduction, vol 2. Knobil E, Neill JD, editors. New York: Raven Press; pp. 2235–2258.
Tyler JL, Gordon JH, Gorski RA. 1979. Effects of olfactory bulbectomy and estrogen on tyrosine hydroxylase and glutamic acid decarboxylase in the nigrostriatal and mesolimbic dopamine systems of adult female rats. Pharmacol Biochem Behav 11(5): 549–552.
Tzschentke TM. 1998. Measuring reward with the conditioned place preference paradigm: a comprehensive review of drug effects, recent progress and new issues. Prog Neurobiol 56: 613–672.
Van Der Shooter P, Lankhorst RR, De Roo JA, de Greef WJ. 1978. Suckling stimulus, lactation and suppression of ovulation in the rat. Endocrinology 103: 949–956.
Van Hemel SB. 1973. Pup retrieving as a reinforcer in nulliparous mice. J Exper Anal Behav 19: 233–238.
Vernotica EM, Rosenblatt JS, Morrell JI. 1999. Microinfusion of cocaine into the medial preoptic area or nucleus accumbens transiently impairs maternal behavior in the rat. Behav Neurosci 113(2): 377–390.
Voloschin LM, Tramezzani JH. 1984. Relationship of prolactin release in lactating rats to milk ejection, sleep state, and ultrasonic vocalizations by the pups. Endocrinology 114: 618–623.
Voorn P, Vanderschuren LJMJ, Groenewegen HJ, Robbins TW, Pennartz CMA. 2004 Putting a spin on the dorsal–ventral divide of the striatum. Trends Neurosci 27: 468–474.
Wagner CK, Morrell JI. 1995. In situ analysis of estrogen receptor mRNA expression in the brain of female rats during pregnancy. Brain Res Mol Brain Res 33(1): 127–135.
Wagner CK, Morrell JI. 1996. Levels of estrogen receptor immunoreactivity are altered in behaviorally-relevant brain regions in female rats during pregnancy. Brain Res Mol Brain Res 42(2): 328–336.
Wagner CK, Silverman AJ, Morrell JI. 1998. Evidence for estrogen receptor in cell nuclei and axon terminals within the lateral habenula of the rat: regulation during pregnancy. J Comp Neurol 392: 330–342.
Walsh CJ, Fleming AS, Lee A, Magnusson JE. 1996. The effects of olfactory and somatosensory desensitization on Fos-like immunoreactivity in the brains of pup- exposed postpartum rats. Behav Neurosci 110(1): 134–153.
Walsh RJ, Slaby FJ, Posner BI. 1987. A receptor-mediated mechanism for the transport of prolactin from blood to cerebrospinal fluid. Endocrinology 120: 1846–1850.
Wansaw MP, Williams S, Rosenblatt JS, Morrell JI. 2002. Cocaine and pup induced conditioned place preference in the lactating maternal rat. Abstract. Orlando, Florida: Society for Neuroscience.
Wansaw MP, Reiss J, Morrell JI. 2003a. Varying the time dams are deprived of pups has minimal effects on preferences for pup-associated cues in the early, and substantial effects in the late postpartum period. Abstract. New Orleans, Louisiana: Society for Neuroscience.
Wansaw MP, Reiss J, Morrell JI. 2003b. Dynamic changes in motivation to seek either natural or pharmacological rewards occur as the postpartum period progresses in the rat. NIDA Symposium Abstract. New Orleans Louisiana: Society for Neuroscience.
Wayner MJ, Barone FC, Scharoun SL, Guevara-Aguilar R, Aguilar-Baturoni HU. 1983. Limbic connections to the lateral preoptic area: a horseradish peroxidase study in the rat. Neurosci Biobehav Rev 7: 375–384.
Wellman J, Carr D, Graham A, Jones H, Human JL, et al 1997. Preoptic area infusions of morphine disrupt – and naloxone restores – parental-like behavior in juvenile rats. Brain Res Bull 44(2): 183–191.
Wilsoncroft WE. 1969. Babies by bar-press: maternal behavior in the rat. Behav Res Meth Instrum 1: 229–230.
Wise RA. 1998. Drug-activation of brain reward pathways. Drug Alcohol Depend 51: 13–22.
Woodside B, Abizaid A, Walker CD. 2000. Changes in leptin levels during lactation: implications for lactational hyperphagia and anovulation. Horm Behav 37: 353–365.
Woodside B, Popeski N. 1999. 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.
Ying S-Y, Gove S, Fang VS, Greep RO. 1973. Ovulation in the postpartum rat. Endocrinology 92: 108–116.
Young LJ, Muns S, Wang Z, Insel TR. 1997. Changes in oxytocin receptor mRNA in rat brain during pregnancy and the effects of estrogen and interleukin-6. J Neuroendocrinol 9(11): 859–865.
Xiao L, Becker JB. 1998. Effects of estrogen agonists on amphetamine-stimulated striatal dopamine release. Synapse 29: 379–391.
Xiao L, Jackson LR, Becker JB. 2003. The effect of estradiol in the striatum is blocked by ICI 182,780 but not tamoxifen: pharmacological and behavioral evidence. Neuroendocrinology 77: 239–245.
Zaborszky L, Alheid GF, Beinfeld MC, Eiden LE, Heimer L, et al 1985. Cholecystokinin innervation of the ventral striatum: a morphological and radioimmunological study. Neuroscience 14: 427–453.
Zahm DS, Brog JS. 1992. On the significance of subterritories in the “accumbens” part of the rat ventral striatum. Neuroscience 50: 751–767.
Zhou W, Cunningham KA, Thomas ML. 2002. Estrogen regulation of gene expression in the brain: a possible mechanism altering the response to psychostimulants in female rats. Brain Res Mol Brain Res 100(1–2): 75–83.
Zsarnovszky A, Scalise TJ, Horvath TL, Naftolin F. 2000. Estrogen effects on tyrosine hydroxylase-immunoreactive cells in the ventral mesencephalon of the female rat: further evidence for the two cell hypothesis of dopamine function. Brain Res 868(2): 363–366.
Acknowledgments
The authors would like to thank Dr. Jill B. Becker for helpful comments on some sections of this chapter.
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2007 Springer Science+Business Media, LLC
About this entry
Cite this entry
Lonstein, J.S., Morrell, J.I. (2007). Neuroendocrinology and Neurochemistry of Maternal Motivation and Behavior. In: Lajtha, A., Blaustein, J.D. (eds) Handbook of Neurochemistry and Molecular Neurobiology. Springer, New York, NY. https://doi.org/10.1007/978-0-387-30405-2_5
Download citation
DOI: https://doi.org/10.1007/978-0-387-30405-2_5
Published:
Publisher Name: Springer, New York, NY
Print ISBN: 978-0-387-30362-8
Online ISBN: 978-0-387-30405-2
eBook Packages: Biomedical and Life SciencesReference Module Biomedical and Life Sciences