Variations in Nucleus Accumbens Dopamine Associated with Individual Differences in Maternal Behavior in the Rat

Journal of Neuroscience

Volumn 24, Issue 17, 2004, Pages 4113-4123

  Champagne, Frances A ^a   Chretien, Pablo ^a   Stevenson, Carl W ^a   Zhang, Tie Yuan ^a   Gratton, Alain ^a   Meaney, Michael J ^a  

^a MCGILL UNIVERSITY   (Canada)

Author keywords

Behavior; Dopamine; Dopamine receptors; Maternal; Nucleus accumbens; Voltammetry

Indexed keywords

DOPAMINE; DOPAMINE RECEPTOR; VANOXERINE;

ANIMAL EXPERIMENT; ARTICLE; AUTORADIOGRAPHY; CONTROLLED STUDY; DOPAMINE UPTAKE; DOPAMINERGIC SYSTEM; FEMALE; GROOMING; IN VIVO STUDY; LACTATION; LICKING; MATERNAL BEHAVIOR; MOTHER CHILD RELATION; MOTIVATION; NEWBORN; NONHUMAN; NUCLEUS ACCUMBENS; POTENTIOMETRY; PRIORITY JOURNAL; RAT;

ANIMALS; ANIMALS, NEWBORN; BEHAVIOR, ANIMAL; BINDING, COMPETITIVE; DOPAMINE; DOPAMINE PLASMA MEMBRANE TRANSPORT PROTEINS; DOPAMINE UPTAKE INHIBITORS; ELECTROCHEMISTRY; ELECTRODES, IMPLANTED; FEMALE; GROOMING; INDIVIDUALITY; LACTATION; MATERNAL BEHAVIOR; MEMBRANE GLYCOPROTEINS; MEMBRANE TRANSPORT PROTEINS; NERVE TISSUE PROTEINS; NUCLEUS ACCUMBENS; RATS; RATS, LONG-EVANS; RECEPTORS, DOPAMINE; TIME FACTORS; TONGUE;

EID: 2442509089     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.5322-03.2004     Document Type: Article

References (91)

1. Andersen PH (1989) The dopamine inhibitor GBR 12909: selectivity and molecular mechanism of action. Eur J Pharmacol 166:493-504.
2. Bakowska JC, Morrell JI (1995) Quantitative autoradiographic analysis of D1 and D2 dopamine receptors in rat brain in early and late pregnancy Brain Res 703:191-200.
3. Baumann MH, Ayestas MA, Sharpe LG, Lewis DB, Rice KC, Rothman RB (2002) Persistent antagonism of methamphetamine-induced dopamine release in rats pretreated with GBR12909 decanoate. J Pharmacol Exp Ther 301:1190-1197.
4. Breton C, Zingg HH (1997) Expression and region-specific regulation of the oxytocin receptor gene in rat brain. Endocrinology 138:1857-1862.
5. Breton C, Pechoux C, Morel G, Zingg HH (1995) Oxytocin receptor messenger ribonucleic acid: characterization, regulation, and cellular localization in the rat pituitary gland. Endocrinology 136:2928-2936.
6. Bridges RS (1996) Biochemical basis of parental behavior in the rat. Adv Study Behav 25:215-242.
7. 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.
8. Caldji C, Tannenbaum B, Sharma S, Francis D, Plotsky P, Meaney MJ (1998) Maternal care during infancy regulates the development of neural systems mediating the expression of fearfulness in the rat. Proc Natl Acad Sci USA 95:5335-5340.
9. Caldji C, Diorio J, Meaney MJ (2003) Variations in maternal care alter GABAA receptor subunit expression in brain regions associated with fear. Neuropsychopharmacology 28:1950-1959.
10. 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.
11. Cass WA, Gerhardt GA (1995) In vivo assessment of dopamine uptake in rat medial prefrontal cortex: comparison with dorsal striatum and nucleus accumbens. J Neurochem 65:201-207.
12. Cass WA, Zahniser NR, Flach KA, Gerhardt GA (1993) Clearance of exogenous dopamine in rat dorsal striatum and nucleus accumbens: role of metabolism and effects of locally applied uptake inhibitors. J Neurochem 61:2269-2278.
13. 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.
14. Champagne F, Francis DD, Mar A, Meaney MJ (2003a) Naturally-occurring variations in maternal care in the rat as a mediating influence for the effects of environment on the development of individual differences in stress reactivity. Physiol Behav 79:359-371.
15. Champagne FA, Weaver ICG, Diorio J, Sharma S, Meaney MJ (2003b) Natural variations in maternal care are associated with estrogen receptor alpha expression and estrogen sensitivity in the MPOA. Endocrinology 144:4720-4724.
16. Chretien P, Pomerleau F, Gratton A (1998) Regional differences in the acute ventral striatal dopamine response to repeated stress. Soc Neurosci Abstr 24:484.
17. Clarke G, Lincoln DW, Merrick LP (1979) Dopaminergic control of oxytocin release in lactating rats. J Endocrinol 83:409-420.
18. Crowley WR, Parker SL, Armstrong WE, Wang W, Grosvenor CE (1991) Excitatory and inhibitory dopaminergic regulation of oxytocin secretion in the lactating rat: evidence for respective mediation by D-1 and D-2 dopamine receptor subtypes. Neuroendocrinology 53:493-502.
19. Cruttwell CJ, Herbison AE, Bicknell RJ (1995) Differential cellular localization of oestrogen receptor immunoreactivity and oxytocin mRNA and immunoreactivity in the rat preoptic area. Neurosci Lett 200:89-92.
20. Denenberg VH, Karas GG (1959) Effects of differential infantile handling upon weight gain and mortality in the rat and mouse. Science 130:629-630.
21. Di Chiara G, Loddo P, Tanda G (1999) Reciprocal changes in prefrontal and limbic dopamine responsiveness to aversive and rewarding stimuli after chronic mild stress: implications for the psychobiology of depression. Biol Psychiatry 46:1624-1633.
22. Doherty MD, Gratton A (1992) High-speed chronoamperometric measurements of mesolimbic and nigrostriatal dopamine release associated with repeated daily stress. Brain Res 586:295-302.
23. Doherty MD, Gratton A (1996) Medial prefrontal cortical D1 receptor modulation of the meso-accumbens dopamine response to stress: an electrochemical study in freely-behaving rats. Brain Res 715:86-97.
24. Doherty MD, Gratton A (1997) NMDA receptors in nucleus accumbens modulate stress-induced dopamine release in nucleus accumbens and ventral tegmental area. Synapse 26:225-234.
25. Doherty MD, Gratton A (1999) Effects of medial prefrontal cortical injections of GABA receptor agonists and antagonists on the local and nucleus accumbens dopamine responses to stress. Synapse 32:288-300.
26. Drago F, Caldwell JD, Pedersen CA, Continella G, Scapagnini U, Prange Jr AJ (1986) Dopamine neurotransmission in the nucleus accumbens may be involved in oxytocin-enhanced grooming behavior of the rat. Pharmacol Biochem Behav 24:1185-1188.
27. Fahrbach SE, Morrell JI, Pfaff DW (1985) Possible role for endogenous oxytocin in estrogen-facilitated maternal behavior in rats. Neuroendocrinology 40:526-532.
28. Fleming AS, Suh EJ, Korsmit M, Rusak B (1994) Activation of Fos-like immunoreactivity in the medial preoptic area and limbic structures by maternal and social interactions in rats. Behav Neurosci 108:724-734.
29. Francis DD, Diorio J, Liu D, Meaney MJ (1999) Non-genomic transmission across generations of maternal behavior and stress responses in the rat. Science 286:1155-1158.
30. Francis DD, Champagne F, Meaney MJ (2000) Variations in maternal behaviour are associated with differences in oxytocin receptor levels in the rat. J Neuroendocrinol 12:1145-1148.
31. Galfori O, Le Moal M (1979) Disruption of maternal behavior and appearance of cannibalism after ventral tegmental lesions. Physiol Behav 23:317-323.
32. Galloway MP, Wolf ME, Roth RH (1986) Regulation of dopamine synthesis in the medial prefrontal cortex is mediated by release modulating autoreceptors: studies in vivo. J Pharmacol Exp Ther 236:689-698.
33. Gangolli EA, Conneely OM, O'Malley BW (1997) Neurotransmitters activate the human estrogen receptor in a neuroblastoma cell line. J Steroid Biochem Mol Biol 61:1-9.
34. Gerhardt GA, Oke AF, Nagy G, Moghaddam B, Adams RN (1984) Nafion-coated electrodes with high selectivity for CNS electrochemistry. Brain Res 290:390-395.
35. Gerhardt GA, Friedemann M, Brodie MS, Vickroy TW, Gratton AP, Hoffer BJ, Rose GM (1989) The effects of cholecystokinin (CCK-8) on dopamine-containing nerve terminals in the caudate nucleus and nucleus accumbens of the anesthetized rat: an in vivo electrochemical study. Brain Res 499:157-163.
36. Giordano B, Johnson AE, Rosenblatt JS (1990) Haloperidol-induced disruption of retrieval behavior and reversal with apomorphine in lactating rats. Physiol Behav 48:211-214.
37. Gratton A, Hoffer BJ, Gerhardt GA (1989) In vivo electrochemical studies of monoamine release in the medial prefrontal cortex of the rat. Neuroscience 29:57-64.
38. Hansen S (1994) Maternal behavior of female rats with 6-OHDA lesions in the ventral striatum: characterization of the pup retrieval deficit. Physiol Behav 55:615-620.
39. Hansen S, Harthon C, Wallin E, Lofberg L, Svensson K (1991) 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 39:71-77.
40. 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 45:673-676.
41. 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.
42. 2 receptors in the nucleus accumbens in mediating reward. J Neurosci 17:8580-8587.
43. Jenkins WJ, Becker JB (2001) Role of the striatum and nucleus accumbens in paced copulatory behavior in the female rat. Behav Brain Res 121:119-128.
44. Kalivas PW, Duffy P (1995) Selective activation of dopamine transmission in the shell of the nucleus accumbens by stress. Brain Res 675:325-328.
45. Keer SE, Stern JM (1999) Dopamine receptor blockade in the nucleus accumbens inhibits maternal retrieval and licking, but enhances nursing behavior in lactating rats. Physiol Behav 67:659-669.
46. Kiyatkin EA, Gratton A (1994) Electrochemical monitoring of extracellular dopamine in nucleus accumbens of rats lever-pressing for food. Brain Res 652:225-234.
47. Kovacs GL, Sarnyai Z, Szabo G (1998) Oxytocin and addiction: a review. Psychoneuroendocrinology 23:945-962.
48. Lee A, Clancy S, Fleming AS (2002) 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 108:215-231.
49. Lee MHS, Williams DI (1974) Changes in licking behaviour of rat mother following handling of young. Anim Behav 22:679-681.
50. Levine S (1957) Infantile experience and resistance to psychological stress. Science 126:405-406.
51. Li M, Fleming AS (2003) Differential involvement of nucleus accumbens shell and core subregions in maternal memory in postpartum female rats. Behav Neurosci 117:426-445.
52. Lin S-H, Miyata S, Weng W, Matsunaga W, Ichikawa J, Furuya K, Nakashima T, Kiyohara T (1998) Comparison of the expression of two immediate early gene proteins, FosB and Fos, in the rat preoptic area, hypothalamus and brainstem during pregnancy, parturition and lactation. Neursci Res 32:333-341.
53. Liu D, Diorio J, Tannenbaum B, Caldji C, Francis D, Freedman A, Sharma S, Pearson D, Plotsky PM, Meaney MJ (1997) Maternal care, hippocampal glucocorticoid receptors, and hypothalamic-pituitary-adrenal responses to stress. Science 277:1659-1662.
54. Liu D, Diorio J, Day JC, Francis DD, Meaney MJ (2000) Maternal care, hippocampal synaptogenesis and cognitive development in rats. Nat Neurosci 3:799-806.
55. Lonstein JS, Stern JM (1997) 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.
56. Lonstein JS, Simmons DA, Swann JM, Stern JM (1998) Forebrain expression of cFos due to active maternal behavior in lactating rats. Neuroscience 82:267-228.
57. Lopez HH, Ettenberg A (2002) Sexually conditioned incentives: attenuation of motivational impact during dopamine receptor antagonism. Pharmacol Biochem Behav 72:65-72.
58. Mitchell JB, Gratton A (1991) Opioid modulation and sensitization of dopamine release elicited by sexually relevant stimuli: a high speed chronoamperometric study in freely behaving rats. Brain Res 551:20-27.
59. Mitchell JB, Gratton A (1992) Partial dopamine depletion of the prefrontal cortex leads to enhanced mesolimbic dopamine release elicited by repeated exposure to naturally reinforcing stimuli. J Neurosci 12:3609-3618.
60. Moghaddam B, Bunney BS (1990) Acute effects of typical and atypical antipsychotic drugs on the release of dopamine from prefrontal cortex, nucleus accumbens, and striatum of the rat: an in vivo microdialysis study. J Neurochem 54:1755-1760.
61. Moos F, Richard P (1979) Effects of dopaminergic antagonist and agonist on oxytocin release induced by various stimuli. Neuroendocrinology 28:138-144.
62. Myers MM, Brunelli SA, Squire JM, Shindeldecker RD, Hofer MA (1989) Maternal behavior of SHR rats and its relationship to offspring blood pressures. Dev Psychobiol 22:29-53.
63. Numan M, Sheehan TP (1997) Neuroanatomical circuitry for mammalian maternal behavior. Ann NY Acad Sci 807:101-125.
64. Numan M, Smith HG (1984) Maternal behavior in rats: evidence for the involvement of preoptic projections to the ventral tegmental area. Behav Neurosci 98:712-727.
65. Parsons LH, Caine SB, Sokoloff P, Schwartz JC, Koob GF, Weiss F (1996) Neurochemical evidence that postsynaptic nucleus accumbens D3 receptor stimulation enhances cocaine reinforcement. J Neurochem 67:1078-1089.
66. 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.
67. Paxinos G, Watson C (1986) The rat brain in stereotaxic coordinates. Sydney: Academy.
68. Pedersen CA, Caldwell JD, Johnson MF, Fort SA, Prange AJ Jr (1985) Oxytocin antiserum delays onset of ovarian steroid-induced maternal behavior. Neuropeptides 6:175-182.
69. 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 108:1163-1171.
70. Pentney RJ, Gratton A (1991) Effects of local delta and mu opioid receptor activation on basal and stimulated dopamine release in striatum and nucleus accumbens of rat: an in vivo electrochemical study. Neuroscience 45:95-102.
71. Pilla M, Perachon S, Sautel F, Garrido F, Mann A, Wermuth CG, Schwartz JC, Everitt BJ, Sokoloff P (1999) Selective inhibition of cocaine-seeking behaviour by a partial dopamine D3 receptor agonist. Nature 400:371-375.
72. Richardson NR, Gratton A (1996) Behavior-relevant changes in nucleus accumbens dopamine transmission elicited by food reinforcement: an electrochemical study in rat. J Neurosci 16:8160-8169.
73. Robbins TW, Everitt BJ (1996) Neurobehavioural mechanisms of reward and motivation. Curr Opin Neuobiol 6:228-236.
74. Sarnyai Z (1998) Oxytocin and neuroadaptation to cocaine. Prog Brain Res 119:449-466.
75. Sarnyai Z, Biro E, Babarczy E, Vecsernyes M, Laczi F, Szabo G, Krivan M, Kovacs GL, Telegdy G (1992) Oxytocin modulates behavioural adaptation to repeated treatment with cocaine in rats. Neuropharmacology 31:593-598.
76. 3H]leucine and horseradish peroxidase. Brain Res 178:17-40.
77. Smith CL, Conneely OM, O'Malley BW (1993) Modulation of the ligand-independent activation of the human estrogen receptor by hormone and antihormone. Proc Natl Acad Sci USA 90:6120-6124.
78. Sokolowski JD, Conlan AN, Salamone JD (1998) A microdialysis study of nucleus accumbens core and shell dopamine during operant responding in the rat. Neuroscience 86:1001-1009.
79. Starke K, Gothert M, Kilbinger H (1989) Modulation of neurotransmitter release by presynaptic autoreceptors. Physiol Rev 69:864-989.
80. Stern JM, Lonstein JS (2001) Neural mediation of nursing and related maternal behaviors. Prog Brain Res 133:263-278.
81. Stern JM, Taylor LA (1991) Haloperidol inhibits maternal retrieval and licking, but facilitates nursing behavior and milk ejection in lactating rats. J Neuroendocrinol 3:591-596.
82. Stivers JA, Kaltwasser MT, Hill PS, Hruby VJ, Crawley JN (1988) Ventral tegmental oxytocin induces grooming. Peptides 9[Suppl 1]:223-231.
83. Szechtman H, Siegel HI, Rosemblatt JS, Komisaruk BR (1977) Tail-pinch facilitates onset of maternal behavior in rats. Physiol Behav 19:807-809.
84. Talmaciu RK, Hoffmann IS, Cubeddu LX (1986) Dopamine autoreceptors modulate dopamine release from the prefrontal cortex. J Neurochem 47:865-870.
85. Vorel SR, Ashby Jr CR, Paul M, Liu X, Hayes R, Hagan JJ, Middlemiss DN, Stemp G, Gardner EL (2002) Dopamine D3 receptor antagonism inhibits cocaine-seeking and cocaine-enhanced brain reward in rats. J Neurosci 22:9595-9603.
86. Wightman RM, Amatore C, Engstrom RC, Hale PD, Kristensen EW, Kuhr WG, May LJ (1988) Real-time characterization of dopamine overflow and uptake in the rat striatum. Neuroscience 25:513-523.
87. Wolterink G, Phillips G, Cador M, Donselaar-Wolterink I, Robbins TW, Everitt BJ (1993) Relative roles of ventral striatal D1 and D2 dopamine receptors in responding with conditioned reinforcement. Psychopharmacology 110:355-364.
88. Young LJ, Wang Z, Donaldson R, Rissman EF (1998) Estrogen receptor alpha is essential for induction of oxytocin receptor by estrogen. NeuroReport 9:933-936.
89. Yuan ZF, Pan JT (1996) Stimulatory effect of central oxytocin on tuberoinfundibular dopaminergic neuron activity and inhibition on prolactin secretion: neurochemical and electrophysiological studies. Endocrinology 137:4120-4125.
90. Zahm DS, Heimer L (1993) Specificity in the efferent projections of the nucleus accumbens in the rat: comparison of the rostral pole projection patterns with those of the core and shell. J Comp Neurol 327:220-232.
91. Zahniser NR, Larson GA, Gerhardt GA (1999) In vivo dopamine clearance rate in rat striatum: regulation by extracellular dopamine concentration and dopamine transporter inhibitors. J Pharmacol Exp Ther 289:266-277.