Maternal aggression in rodents: Brain oxytocin and vasopressin mediate pup defence

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 368, Issue 1631, 2013, Pages

  Bosch, Oliver J ^a  

^a UNIVERSITY OF REGENSBURG   (Germany)

Author keywords

Central amygdala; HAB LAB; Intracerebroventricular; Paraventricular nucleus; Receptor agonist antagonist

Indexed keywords

AGGRESSION; BRAIN; FEMALE BEHAVIOR; LACTATION; MATERNAL CARE; NEUROLOGY; PEPTIDE; RODENT;

ARGIPRESSIN; OXYTOCIN;

AGGRESSION; AMYGDALOID NUCLEUS; ANIMAL; CENTRAL NUCLEUS (AMYGDALA); FEMALE; HAB/LAB; INTRACEREBROVENTRICULAR DRUG ADMINISTRATION; LACTATION; MALE; MATERNAL BEHAVIOR; MOUSE; NEWBORN; PARAVENTRICULAR NUCLEUS; PHYSIOLOGY; PREGNANCY; RAT; RECEPTOR AGONIST/ANTAGONIST; REVIEW;

CENTRAL AMYGDALA; HAB/LAB; INTRACEREBROVENTRICULAR; PARAVENTRICULAR NUCLEUS; RECEPTOR AGONIST/ANTAGONIST;

AGGRESSION; AMYGDALA; ANIMALS; ANIMALS, NEWBORN; ARGININE VASOPRESSIN; FEMALE; LACTATION; MALE; MATERNAL BEHAVIOR; MICE; OXYTOCIN; PREGNANCY; RATS;

EID: 84886506900     PISSN: 09628436     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rstb.2013.0085     Document Type: Review

References (130)

1. Peters LC, Sist TC, Kristal MB. 1991 Maintenance and decline of the suppression of infanticide in mother rats. Physiol. Behav. 50, 451-456. (doi:10.1016/0031-9384(91)90093-4)
2. Peters LC, Kristal MB. 1983 Suppression of infanticide in mother rats. J. Comp. Psychol. 97, 167-177. (doi:10.1037/0735-7036.97.2.167)
3. Bosch OJ, Meddle SL, Beiderbeck DI, Douglas AJ, Neumann ID. 2005 Brain oxytocin correlates with maternal aggression: link to anxiety. J. Neurosci. 25, 6807-6815. (doi:10.1523/JNEUROSCI.1342-05.2005)
4. Flannelly KJ, Flannelly L. 1987 Time course of postpartum aggression in rats (Rattus norvegicus). J. Comp. Physiol. Psychol. 101, 101-103. (doi:10.1037/0735-7036.101.1.101)
5. Lonstein JS, Gammie SC. 2002 Sensory, hormonal, and neural control of maternal aggression in laboratory rodents. Neurosci. Biobehav. Rev. 26, 869-888. (doi:10.1016/S0149-7634(02)00087-8)
6. Erskine MS, Barfield RJ, Goldman BD. 1978 Intraspecific fighting during late pregnancy and lactation in rats and effects of litter removal. Behav. Biol. 23, 206-218. (doi:10.1016/S0091-6773(78) 91814-X)
7. O'Connell LA, Hofmann HA. 2012 Evolution of a vertebrate social decision-making network. Science 336, 1154-1157. (doi:10.1126/science.1218889)
8. Numan M, Insel TR. 2003 The neurobiology of parental behaviour. New York, NY: Springer.
9. Rosenblatt JS, Mayer AD. 1995 An analysis of approach/withdrawal processes in the initiation of maternal behavior in the laboratory rat. In Handbook of behavioral neurobiology (eds KE Hood, G Greenberg, E Tobach), pp. 229-298. New York, NY: Plenum Press.
10. Svare B, Gandelman R. 1976 Suckling stimulation induces aggression in virgin female mice. Nature 260, 606-608. (doi:10.1038/260606a0)
11. Svare B, Mann M, Samuels O. 1980 Mice: suckling stimulation but not lactation important for maternal aggression. Behav. Neural. Biol. 29, 453-462. (doi:10.1016/S0163-1047(80)92654-0)
12. Svare B, Gandelman R. 1976 Postpartum aggression in mice: the influence of suckling stimulation. Horm. Behav. 7, 407-416. (doi:10.1016/0018-506X(76)90012-X)
13. Neumann I, Ludwig M, Engelmann M, Pittman QJ, Landgraf R. 1993 Simultaneous microdialysis in blood and brain: oxytocin and vasopressin release in response to central and peripheral osmotic stimulation and suckling in the rat. Neuroendocrinology 58, 637-645. (doi:10.1159/000126604)
14. Neumann I, Landgraf R. 1989 Septal and hippocampal release of oxytocin, but not vasopressin, in the conscious lactating rat during suckling. J. Neuroendocrinol. 1, 305-308. (doi:10.1111/j.1365-2826.1989.tb00120.x)
15. Neumann I, Russell JA, Landgraf R. 1993 Oxytocin and vasopressin release within the supraoptic and paraventricular nuclei of pregnant, parturient and lactating rats: a microdialysis study. Neuroscience 53, 65-75. (doi:10.1016/0306-4522(93)90285-N)
16. Gandelman R, Simon NG. 1980 Postpartum fighting in the rat: nipple development and the presence of young. Behav. Neural. Biol. 28, 350-360. (doi:10.1016/S0163-1047(80)92357-2)
17. Deschamps S, Woodside B, Walker CD. 2003 Pups presence eliminates the stress hyporesponsiveness of early lactating females to a psychological stress representing a threat to the pups. J. Neuroendocrinol. 15, 486-497. (doi:10.1046/j. 1365-2826.2003.01022.x)
18. Bridges RS. 1975 Long-term effects of pregnancy and parturition upon maternal responsiveness in the rat. Physiol. Behav. 14, 245-249. (doi:10.1016/ 0031-9384(75)90028-1)
19. Moltz H, Geller D, Levin R. 1967 Maternal behavior in the totally mammectomized rat. J. Comp. Physiol. Psychol. 64, 225-229. (doi:10.1037/h0088025)
20. Mayer AD, Carter L, Jorge WA, Mota MJ, Tannu S, Rosenblatt JS. 1987 Mammary stimulation and maternal aggression in rodents: thelectomy fails to reduce pre-or postpartum aggression in rats. Horm. Behav. 21, 501-510. (doi:10.1016/0018-506X(87)90008-0)
21. Stern JM, Kolunie JM. 1993 Maternal aggression of rats is impaired by cutaneous anesthesia of the ventral trunk, but not by nipple removal. Physiol. Behav. 54, 861-868. (doi:10.1016/0031-9384(93) 90293-O)
22. Hahn-Holbrook J, Holt-Lunstad J, Holbrook C, Coyne SM, Lawson ET. 2011 Maternal defense: breast feeding increases aggression by reducing stress. Psychol. Sci. 22, 1288-1295. (doi:10.1177/0956797611420729)
23. Caughey SD, Klampfl SM, Bishop VR, Pfoertsch J, Neumann ID, Bosch OJ, Meddle SL. 2011 Changes in the intensity of maternal aggression and central oxytocin and vasopressin V1a receptors across the peripartum period in the rat. J. Neuroendocrinol. 23, 1113-1124. (doi:10.1111/j.1365-2826.2011.02224.x)
24. Svare B, Betteridge C, Katz D, Samuels O. 1981 Some situational and experiential determinants of maternal aggression in mice. Physiol. Behav. 26, 253-258. (doi:10.1016/0031-9384(81)90020-2)
25. Gandelman R. 1972 Mice: postpartum aggression elicited by the presence of an intruder. Horm. Behav. 3, 23-28. (doi:10.1016/0018-506X(72) 90003-7)
26. St John RD, Corning PA. 1973 Maternal aggression in mice. Behav. Biol. 9, 635-639. (doi:10.1016/ S0091-6773(73)80058-6)
27. Svare B, Gandelman R. 1976 A longitudinal analysis of maternal aggression in Rockland-Swiss albino mice. Dev. Psychobiol. 9, 437-446. (doi:10.1002/ dev.420090506)
28. Albert DJ, Walsh ML. 1995 Aggression in the lactating female rat: the normal decline is not dependent on the physical development of the pups. Physiol. Behav. 58, 477-481. (doi:10.1016/ 0031-9384(95)00033-F)
29. Giovenardi M, Consiglio AR, Barros HM, Lucion AB. 2000 Pup age and aggressive behavior in lactating rats. Braz. J. Med. Biol. Res. 33, 1083-1088. (doi:10.1590/S0100-879X2000000900015)
30. Deviterne D, Desor D, Krafft B. 1990 Maternal behavior variations and adaptations, and pup development within litters of various sizes in Wistar rat. Dev. Psychobiol. 23, 349-360. (doi:10.1002/ dev.420230406)
31. Hrdy SB. 1979 Infanticide among animals: a review, classification, and examination of the implications for the reproductive strategies of females. Ethol. Sociobiol. 1, 13-40. (doi:10.1016/0162-3095(79)90004-9)
32. Jakubowski M, Terkel J. 1985 Transition from pup killing to parental behavior in male and virgin female albino rats. Physiol. Behav. 34, 683-686. (doi:10.1016/0031-9384(85)90364-6)
33. Huck UW, Soltis RL, Coopersmith CB. 1982 Infanticide in male laboratory mice: effects of social status, prior sexual experience, and basis for discrimination between related and unrelated young. Anim. Behav. 30, 1158-1165. (doi:10.1016/ S0003-3472(82)80206-6)
34. Neumann ID, Toschi N, Ohl F, Torner L, Kromer SA. 2001 Maternal defence as an emotional stressor in female rats: correlation of neuroendocrine and behavioural parameters and involvement of brain oxytocin. Eur. J. Neurosci. 13, 1016-1024. (doi:10.1046/j.0953-816x.2001.01460.x)
35. Erskine MS, Denenberg VH, Goldman BD. 1978 Aggression in the lactating rat: effects of intruder age and test arena. Behav. Biol. 23, 52-66. (doi:10.1016/S0091-6773(78)91148-3)
36. Flannelly KJ, Flannelly L. 1985 Opponents' size influences maternal aggression. Psychol. Rep. 57, 883-886. (doi:10.2466/pr0.1985.57.3.883)
37. Rosenson LM, Asheroff AK. 1975 Maternal aggression in CD-l mice: influence of the hormonal condition of the intruder. Behav. Biol. 15, 219-224. (doi:10.1016/S0091-6773(75) 91603-X)
38. Haney M, DeBold JF, Miczek KA. 1989 Maternal aggression in mice and rats towards male and female conspecifics. Aggress. Behav. 15, 443-453. (doi:10.1002/1098-2337(1989)15:6,443::AIDAB2480150605.3.0. CO;2-U)
39. Bosch OJ, Klampfl SM, Caughey SD, Meddle SL. In preparation. Hypothalamic and limbic vasopressin and oxytocin release facilitates maternal aggression in the lactating rat.
40. Bosch OJ, Kromer SA, Brunton PJ, Neumann ID. 2004 Release of oxytocin in the hypothalamic paraventricular nucleus, but not central amygdala or lateral septum in lactating residents and virgin intruders during maternal defence. Neuroscience 124, 439-448. (doi:10.1016/j.neuroscience.2003.11.028)
41. Bosch OJ, Neumann ID. 2010 Vasopressin released within the central amygdala promotes maternal aggression. Eur. J. Neurosci. 31, 883-891. (doi:10.1111/j.1460-9568.2010.07115.x)
42. Bosch OJ, Sartori SB, Singewald N, Neumann ID. 2007 Extracellular amino acid levels in the paraventricular nucleus and the central amygdala in high-and low-anxiety dams rats during maternal aggression: regulation by oxytocin. Stress 10, 261-270. (doi:10.1080/10253890701223197)
43. Neumann ID. 2009 The advantage of social living: brain neuropeptides mediate the beneficial consequences of sex and motherhood. Front. Neuroendocrinol. 30, 483-496. (doi:10.1016/j.yfrne.2009.04.012)
44. Bosch OJ, Neumann ID. 2012 Both oxytocin and vasopressin are mediators of maternal care and aggression in rodents: from central release to sites of action. Horm. Behav. 61, 293-303. (doi:10.1016/ j.yhbeh.2011.11.002)
45. Goodson JL. 2008 Nonapeptides and the evolutionary patterning of sociality. Prog. Brain Res. 170, 3-15. (doi:10.1016/S0079-6123(08)00401-9)
46. Veenema AH, Neumann ID. 2008 Central vasopressin and oxytocin release: regulation of complex social behaviours. Prog. Brain Res. 170, 261-276. (doi:10.1016/S0079-6123(08)00422-6)
47. Neumann ID, Landgraf R. 2012 Balance of brain oxytocin and vasopressin: implications for anxiety, depression, and social behaviors. Trends Neurosci. 35, 649-659. (doi:10.1016/j.tins.2012.08.004)
48. Kendrick KM, Keverne EB, Chapman C, Baldwin BA. 1988 Intracranial dialysis measurement of oxytocin, monoamine and uric acid release from the olfactory bulb and substantia nigra of sheep during parturition, suckling, separation from lambs and eating. Brain Res. 439, 1-10. (doi:10.1016/0006-8993(88)91455-2)
49. Landgraf R, Neumann I, Pittman QJ. 1991 Septal and hippocampal release of vasopressin and oxytocin during late pregnancy and parturition in the rat. Neuroendocrinology 54, 378-383. (doi:10.1159/000125917)
50. Moos F, Freund-Mercier MJ, Guerne Y, Guerne JM, Stoeckel ME, Richard P. 1984 Release of oxytocin and vasopressin by magnocellular nuclei in vitro: specific facilitatory effect of oxytocin on its own release. J. Endocrinol. 102, 63-72. (doi:10.1677/ joe.0.1020063)
51. Moos F, Ingram CD, Wakerley JB, Guerne Y, Freund-Mercier MJ, Richard P. 1991 Oxytocin in the bed nucleus of the stria terminalis and lateral septum facilitates bursting of hypothalamic oxytocin neurons in suckled rats. J. Neuroendocrinol. 3, 163-171. (doi:10.1111/j.1365-2826.1991.tb00259.x)
52. Moos F, Poulain DA, Rodriguez F, Guerne Y, Vincent JD, Richard P. 1989 Release of oxytocin within the supraoptic nucleus during the milk ejection reflex in rats. Exp. Brain Res. 76, 593-602. (doi:10.1007/ BF00248916)
53. van den Burg EH, Neumann ID. 2011 Bridging the gap between GPCR activation and behaviour: oxytocin and prolactin signalling in the hypothalamus. J. Mol. Neurosci. 43, 200-208. (doi:10.1007/s12031-010-9452-8)
54. Caldwell HK, Lee HJ, Macbeth AH, Young 3rd WS. 2008 Vasopressin: behavioral roles of an 'original' neuropeptide. Prog. Neurobiol. 84, 1-24. (doi:10.1016/j.pneurobio.2007.10.007)
55. Walker CD, Toufexis DJ, Burlet A. 2001 Hypothalamic and limbic expression of CRF and vasopressin during lactation: implications for the control of ACTH secretion and stress hyporesponsiveness. Prog. Brain Res. 133, 99-110. (doi:10.1016/S0079-6123(01)33008-X)
56. Stoop R. 2012 Neuromodulation by oxytocin and vasopressin. Neuron 76, 142-159. (doi:10.1016/j. neuron.2012.09.025)
57. Lonstein JS. 2007 Regulation of anxiety during the postpartum period. Front. Neuroendocrinol. 28, 115-141. (doi:10.1016/j.yfrne.2007.05.002)
58. Bosch OJ. 2011 Maternal nurturing is dependent on her innate anxiety: the behavioral roles of brain oxytocin and vasopressin. Horm. Behav. 59, 202-212. (doi:10.1016/j.yhbeh.2010.11.012)
59. Altshuler LL, Hendrick V, Cohen LS. 2000 An update on mood and anxiety disorders during pregnancy and the postpartum period. Prim. Care Companion J. Clin. Psychiatry 2, 217-222. (doi:10.4088/PCC. v02n0604)
60. Fleming A, Ruble D, Flett G, Van Wagner V. 1990 Adjustment in first-time mothers: changes in mood and mood content during the early postpartum months. Dev. Psychol. 26, 137-143. (doi:10.1037/ 0012-1649.26.1.137)
61. Groer MW. 2005 Differences between exclusive breastfeeders, formula-feeders, and controls: a study of stress, mood, and endocrine variables. Biol. Res. Nurs. 7, 106-117. (doi:10.1177/1099800405280936)
62. Breitkopf CR, Primeau LA, Levine RE, Olson GL, Wu ZH, Berenson AB. 2006 Anxiety symptoms during pregnancy and postpartum. J. Psychosom. Obstet. Gynaecol. 27, 157-162. (doi:10.1080/01674820500523521)
63. Maestripieri D, D'Amato FR. 1991 Anxiety and maternal aggression in house mice (Mus musculus): a look at interindividual variability. J. Comp. Psychol. 105, 295-301. (doi:10.1037/0735-7036.105.3.295)
64. Parmigiani S, Palanza P, Rogers J, Ferrari PF. 1999 Selection, evolution of behavior and animal models in behavioral neuroscience. Neurosci. Biobehav. Rev. 23, 957-969. (doi:10.1016/S0149-7634(99) 00029-9)
65. Johns JM, Noonan LR, Zimmerman LI, Li L, Pedersen CA. 1994 Effects of chronic and acute cocaine treatment on the onset of maternal behavior and aggression in Sprague-Dawley rats. Behav. Neurosci. 108, 107-112. (doi:10.1037/0735-7044.108.1.107)
66. Lonstein JS, Simmons DA, Stern JM. 1998 Functions of the caudal periaqueductal gray in lactating rats: kyphosis, lordosis, maternal aggression, and fearfulness. Behav. Neurosci. 112, 1502-1518. (doi:10.1037/0735-7044.112.6.1502)
67. Fernandez-Guasti A, Ferreira A, Picazo O. 2001 Diazepam, but not buspirone, induces similar anxiolytic-like actions in lactating and ovariectomized Wistar rats. Pharmacol. Biochem. Behav. 70, 85-93. (doi:10.1016/S0091-3057(01) 00586-X)
68. Ferreira A, Picazo O, Uriarte N, Pereira M, Fernandez-Guasti A. 2000 Inhibitory effect of buspirone and diazepam, but not of 8-OH-DPAT, on maternal behavior and aggression. Pharmacol. Biochem. Behav. 66, 389-396. (doi:10.1016/S0091-3057(00)00211-2)
69. Liebsch G, Montkowski A, Holsboer F, Landgraf R. 1998 Behavioural profiles of two Wistar rat lines selectively bred for high or low anxiety-related behaviour. Behav. Brain Res. 94, 301-310. (doi:10.1016/S0166-4328(97)00198-8)
70. Landgraf R, Wigger A. 2002 High vs low anxietyrelated behavior rats: an animal model of extremes in trait anxiety. Behav. Genet. 32, 301-314. (doi:10.1023/A:1020258104318)
71. Landgraf R et al. 2007 Candidate genes of anxiety-related behavior in HAB/LAB rats and mice: focus on vasopressin and glyoxalase-I. Neurosci. Biobehav. Rev. 31, 89-102. (doi:10.1016/j. neubiorev.2006.07.003)
72. Neumann ID, Veenema AH, Beiderbeck DI. 2010 Aggression and anxiety: social context and neurobiological links. Front. Behav. Neurosci. 4, 12-72. (doi:10.3389/Fnbeh.2010.00012)
73. Neumann ID, Kromer SA, Bosch OJ. 2005 Effects of psycho-social stress during pregnancy on neuroendocrine and behavioural parameters in lactation depend on the genetically determined stress vulnerability. Psychoneuroendocrinology 30, 791-806. (doi:10.1016/j.psyneuen.2005.03.008)
74. Bosch OJ, Neumann ID. 2008 Brain vasopressin is an important regulator of maternal behavior independent of dams' trait anxiety. Proc. Natl Acad. Sci. USA 105, 17 139-17 144. (doi:10.1073/pnas.0807412105)
75. Kessler MS, Bosch OJ, Bunck M, Landgraf R, Neumann ID. 2011 Maternal care differs in mice bred for high vs. low trait anxiety: impact of brain vasopressin and cross-fostering. Soc. Neurosci. 6, 156-168. (doi:10.1080/17470919.2010.495567)
76. Nyberg JM, Vekovischeva O, Sandnabba NK. 2003 Anxiety profiles of mice selectively bred for intermale aggression. Behav. Genet. 33, 503-511. (doi:10.1023/A:1025718531997)
77. Beiderbeck DI, Neumann ID, Veenema AH. 2007 Differences in intermale aggression are accompanied by opposite vasopressin release patterns within the septum in rats bred for low and high anxiety. Eur. J. Neurosci. 26, 3597-3605. (doi:10.1111/j. 1460-9568.2007.05974.x)
78. Veenema AH, Torner L, Blume A, Beiderbeck DI, Neumann ID. 2007 Low inborn anxiety correlates with high intermale aggression: link to ACTH response and neuronal activation of the hypothalamic paraventricular nucleus. Horm. Behav. 51, 11-19. (doi:10.1016/j.yhbeh.2006.07.004)
79. Bale TL, Davis AM, Auger AP, Dorsa DM, McCarthy MM. 2001 CNS region-specific oxytocin receptor expression: importance in regulation of anxiety and sex behavior. J. Neurosci. 21, 2546-2552.
80. Blume A, Bosch OJ, Miklos S, Torner L, Wales L, Waldherr M, Neumann ID. 2008 Oxytocin reduces anxiety via ERK1/2 activation: local effect within the rat hypothalamic paraventricular nucleus. Eur. J. Neurosci. 27, 1947-1956. (doi:10.1111/j. 1460-9568.2008.06184.x)
81. McCarthy MM, McDonald CH, Brooks PJ, Goldman D. 1996 An anxiolytic action of oxytocin is enhanced by estrogen in the mouse. Physiol. Behav. 60, 1209-1215. (doi:10.1016/S0031-9384(96)00212-0)
82. Neumann ID, Torner L, Wigger A. 2000 Brain oxytocin: differential inhibition of neuroendocrine stress responses and anxiety-related behaviour in virgin, pregnant and lactating rats. Neuroscience 95, 567-575. (doi:10.1016/S0306-4522(99)00433-9)
83. Ring RH et al. 2006 Anxiolytic-like activity of oxytocin in male mice: behavioral and autonomic evidence, therapeutic implications. Psychopharmacology 185, 218-225. (doi:10.1007/ s00213-005-0293-z)
84. Jurek B, Slattery DA, Maloumby R, Hillerer K, Koszinowski S, Neumann ID, van den Burg EH. 2012 Differential contribution of hypothalamic MAPK activity to anxiety-like behaviour in virgin and lactating rats. PLoS ONE 7, e37060. (doi:10.1371/ journal.pone.0037060)
85. Campbell A. 2013 The evolutionary psychology of women's aggression. Phil. Trans. R. Soc. B 368, 20130078. (doi:10.1098/rstb.2013.0078)
86. Windle RJ, Shanks N, Lightman SL, Ingram CD. 1997 Central oxytocin administration reduces stressinduced corticosterone release and anxiety behavior in rats. Endocrinology 138, 2829-2834. (doi:10.1210/en.138.7.2829)
87. Manning M et al. 1989 Solid-phase synthesis of 16 potent (selective and nonselective) in vivo antagonists of oxytocin. J. Med. Chem. 32, 382-391. (doi:10.1021/jm00122a016)
88. Slattery DA, Neumann ID. 2010 Chronic icv oxytocin attenuates the pathological high anxiety state of selectively bred Wistar rats. Neuropharmacology 58, 56-61. (doi:10.1016/j.neuropharm.2009.06.038)
89. Waldherr M, Neumann ID. 2007 Centrally released oxytocin mediates mating-induced anxiolysis in male rats. Proc. Natl Acad. Sci. USA 104, 16 681-16 684. (doi:10.1073/pnas.0705860104)
90. Huber D, Veinante P, Stoop R. 2005 Vasopressin and oxytocin excite distinct neuronal populations in the central amygdala. Science 308, 245-248. (doi:10.1126/science.1105636)
91. Viviani D, Charlet A, van den Burg E, Robinet C, Hurni N, Abatis M, Magara F, Stoop R. 2011 Oxytocin selectively gates fear responses through distinct outputs from the central amygdala. Science 333, 104-107. (doi:10.1126/science.1201043)
92. Knobloch HS et al. 2012 Evoked axonal oxytocin release in the central amygdala attenuates fear response. Neuron 73, 553-566. (doi:10.1016/j. neuron.2011.11.030)
93. Murgatroyd C, Wigger A, Frank E, Singewald N, Bunck M, Holsboer F, Landgraf R, Spengler D. 2004 Impaired repression at a vasopressin promoter polymorphism underlies overexpression of vasopressin in a rat model of trait anxiety. J. Neurosci. 24, 7762-7770. (doi:10.1523/ JNEUROSCI.1614-04.2004)
94. Landgraf R, Gerstberger R, Montkowski A, Probst JC, Wotjak CT, Holsboer F, Engelmann M. 1995 V1 vasopressin receptor antisense oligodeoxynucleotide into septum reduces vasopressin binding, social discrimination abilities, and anxiety-related behavior in rats. J. Neurosci. 15, 4250-4258.
95. Ring RH. 2005 The central vasopressinergic system: examining the opportunities for psychiatric drug development. Curr. Pharm. Des. 11, 205-225. (doi:10.2174/1381612053382241)
96. Wigger A et al. 2004 Alterations in central neuropeptide expression, release, and receptor binding in rats bred for high anxiety: critical role of vasopressin. Neuropsychopharmacology 29, 1-14. (doi:10.1038/sj.npp.1300290)
97. Keck ME, Wigger A, Welt T, Muller MB, Gesing A, Reul JM, Holsboer F, Landgraf R, Neumann ID. 2002 Vasopressin mediates the response of the combined dexamethasone/CRH test in hyper-anxious rats: implications for pathogenesis of affective disorders. Neuropsychopharmacology 26, 94-105. (doi:10.1016/S0893-133X(01)00351-7)
98. Kruszynski M, Lammek B, Manning M, Seto J, Haldar J, Sawyer WH. 1980 [1-beta-Mercaptobeta, beta-cyclopentamethylenepropionic acid),2-(Omethyl) tyrosine]argine-vasopressin and [1-betamercapto-beta, beta-cyclopentamethylenepropionic acid)]argine-vasopressine, two highly potent antagonists of the vasopressor response to argininevasopressin. J. Med. Chem. 23, 364-368. (doi:10.1021/jm00178a003)
99. Pedersen CA, Ascher JA, Monroe YL, Prange Jr AJ. 1982 Oxytocin induces maternal behavior in virgin female rats. Science 216, 648-650. (doi:10.1126/ science.7071605)
100. Pedersen CA, Prange Jr AJ. 1979 Induction of maternal behavior in virgin rats after intracerebroventricular administration of oxytocin. Proc. Natl Acad. Sci. USA 76, 6661-6665. (doi:10.1073/pnas.76.12.6661)
101. Young 3rd WS et al. 1998 Targeted reduction of oxytocin expression provides insights into its physiological roles. Adv. Exp. Med. Biol. 449, 231-240. (doi:10.1007/978-1-4615-4871-3_30)
102. Giovenardi M, Padoin MJ, Cadore LP, Lucion AB. 1998 Hypothalamic paraventricular nucleus modulates maternal aggression in rats: effects of ibotenic acid lesion and oxytocin antisense. Physiol. Behav. 63, 351-359. (doi:10.1016/S0031-9384(97)00434-4)
103. Lubin DA, Elliott JC, Black MC, Johns JM. 2003 An oxytocin antagonist infused into the central nucleus of the amygdala increases maternal aggressive behavior. Behav. Neurosci. 117, 195-201. (doi:10.1037/0735-7044.117.2.195)
104. Consiglio AR, Borsoi A, Pereira GA, Lucion AB. 2005 Effects of oxytocin microinjected into the central amygdaloid nucleus and bed nucleus of stria terminalis on maternal aggressive behavior in rats. Physiol. Behav. 85, 354-362. (doi:10.1016/j. physbeh.2005.05.002)
105. Wotjak CT, Landgraf R, Engelmann M. 2008 Listening to neuropeptides by microdialysis: echoes and new sounds? Pharmacol. Biochem. Behav. 90, 125-134. (doi:10.1016/j.pbb.2008.03.017)
106. Landgraf R, Kubota M, Holsboer F, Wotjak CT. 1995 Release of vasopressin and oxytocin within the brain and into blood: microdialysis and antisense targeting. In Neurohypophysis: recent progress of vasopressin and oxytocin research (eds T Saito, K Kurokawa, S Yoshida), pp. 243-256. Amsterdam, The Netherlands: Elsevier.
107. Consiglio AR, Lucion AB. 1996 Lesion of hypothalamic paraventricular nucleus and maternal aggressive behavior in female rats. Physiol. Behav. 59, 591-596. (doi:10.1016/0031-9384(95)02117-5)
108. Leng G, Onaka T, Caquineau C, Sabatier N, Tobin VA, Takayanagi Y. 2008 Oxytocin and appetite. Prog. Brain Res. 170, 137-151. (doi:10.1016/S0079-6123(08)00413-5)
109. Ferris CF, Foote KB, Meltser HM, Plenby MG, Smith KL, Insel TR. 1992 Oxytocin in the amygdala facilitates maternal aggression. Ann. NY Acad. Sci. 652, 456-457. (doi:10.1111/j.1749-6632.1992. tb34382.x)
110. Landgraf R, Neumann ID. 2004 Vasopressin and oxytocin release within the brain: a dynamic concept of multiple and variable modes of neuropeptide communication. Front. Neuroendocrinol. 25, 150-176. (doi:10.1016/j.yfrne.2004.05.001)
111. Bosch OJ, Pfortsch J, Beiderbeck DI, Landgraf R, Neumann ID. 2010 Maternal behaviour is associated with vasopressin release in the medial preoptic area and bed nucleus of the stria terminalis in the rat. J. Neuroendocrinol. 22, 420-429. (doi:10.1111/j. 1365-2826.2010.01984.x)
112. Meddle SL, Bishop VR, Gkoumassi E, van Leeuwen FW, Douglas AJ. 2007 Dynamic changes in oxytocin receptor expression and activation at parturition in the rat brain. Endocrinology 148, 5095-5104. (doi:10.1210/en.2007-0615)
113. 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. (doi:10.1046/j. 1365-2826.2000.00599.x)
114. Gammie SC, Nelson RJ. 2001 cFOS and pCREB activation and maternal aggression in mice. Brain Res. 898, 232-241. (doi:10.1016/S0006-8993(01) 02189-8)
115. Klampfl SM, Neumann ID, Bosch OJ. 2013 Reduced brain CRF receptor activation is required for adequate maternal care and maternal aggression in lactating rats. Eur. J. Neurosci. 38, 2742-2750. (doi:10.1111/ejn.12274)
116. Gammie SC, Negron A, Newman SM, Rhodes JS. 2004 Corticotropin-releasing factor inhibits maternal aggression in mice. Behav. Neurosci. 118, 805-814. (doi:10.1037/0735-7044.118.4.805)
117. Windle RJ, Kershaw YM, Shanks N, Wood SA, Lightman SL, Ingram CD. 2004 Oxytocin attenuates stress-induced c-fos mRNA expression in specific forebrain regions associated with modulation of hypothalamo-pituitaryadrenal activity. J. Neurosci. 24, 2974-2982. (doi:10.1523/JNEUROSCI.3432-03.2004)
118. Wersinger SR, Caldwell HK, Martinez L, Gold P, Hu SB, Young 3rd WS. 2007 Vasopressin 1a receptor knockout mice have a subtle olfactory deficit but normal aggression. Genes Brain Behav. 6, 540-551. (doi:10.1111/j.1601-183X.2006.00281.x)
119. Wersinger SR, Caldwell HK, Christiansen M, Young 3rd WS. 2007 Disruption of the vasopressin 1b receptor gene impairs the attack component of aggressive behavior in mice. Genes Brain Behav. 6, 653-660. (doi:10.1111/j.1601-183X.2006.00294.x)
120. Bosch OJ, Neumann ID. 2007 Brain vasopressin regulates maternal behavior and aggression. In Ann. Meet. Soc. Neurosci., 3-7 November, San Diego, CA. Program no. 84.14. (Online).
121. Nephew BC, Bridges RS. 2008 Central actions of arginine vasopressin and a V1a receptor antagonist on maternal aggression, maternal behavior, and grooming in lactating rats. Pharmacol. Biochem. Behav. 91, 77-83. (doi:10.1016/j.pbb.2008.06.013)
122. Nephew BC, Byrnes EM, Bridges RS. 2010 Vasopressin mediates enhanced offspring protection in multiparous rats. Neuropharmacology 58, 102-106. (doi:10.1016/j.neuropharm.2009.06.032)
123. Wersinger SR, Ginns EI, O'Carroll AM, Lolait SJ, Young 3rd WS. 2002 Vasopressin V1b receptor knockout reduces aggressive behavior in male mice. Mol. Psychiatry 7, 975-984. (doi:10.1038/sj.mp.4001195)
124. Hernando F, Schoots O, Lolait SJ, Burbach JP. 2001 Immunohistochemical localization of the vasopressin V1b receptor in the rat brain and pituitary gland: anatomical support for its involvement in the central effects of vasopressin. Endocrinology 142, 1659-1668. (doi:10.1210/en.142.4.1659)
125. Wotjak CT, Kubota M, Liebsch G, Montkowski A, Holsboer F, Neumann I, Landgraf R. 1996 Release of vasopressin within the rat paraventricular nucleus in response to emotional stress: a novel mechanism of regulating adrenocorticotropic hormone secretion? J. Neurosci. 16, 7725-7732.
126. Douglas AJ, Meddle SL, Kroemer S, Muesch W, Bosch OJ, Neumann ID. 2007 Social stress induces hypothalamo-pituitary-adrenal axis responses in lactating rats bred for high trait anxiety. Eur. J. Neurosci. 25, 1599-1603. (doi:10.1111/j. 1460-9568.2007.05380.x)
127. LeDoux J. 2007 The amygdala. Curr. Biol. 17, R868-R874. (doi:10.1016/j.cub.2007.08.005)
128. Roozendaal B, Schoorlemmer GH, Koolhaas JM, Bohus B. 1993 Cardiac, neuroendocrine, and behavioral effects of central amygdaloid vasopressinergic and oxytocinergic mechanisms under stress-free conditions in rats. Brain Res. Bull. 32, 573-579. (doi:10.1016/0361-9230(93)90157-7)
129. Willcox BJ, Poulin P, Veale WL, Pittman QJ. 1992 Vasopressin-induced motor effects: localization of a sensitive site in the amygdala. Brain Res. 596, 58-64. (doi:10.1016/0006-8993 (92)91532-J)
130. Veenema AH, Beiderbeck DI, Lukas M, Neumann ID. 2010 Distinct correlations of vasopressin release within the lateral septum and the bed nucleus of the stria terminalis with the display of intermale aggression. Horm. Behav. 58, 273-281. (doi:10.1016/j.yhbeh.2010.03.006)