Oxytocin in the medial prefrontal cortex regulates maternal care, maternal aggression and anxiety during the postpartum period

Frontiers in Behavioral Neuroscience

Volumn 8, Issue AUG, 2014, Pages

  Sabihi, Sara ^a   Dong, Shirley M ^a   Durosko, Nicole E ^a   Leuner, Benedetta ^a  

^a OHIO STATE UNIVERSITY   (United States)

Author keywords

Anxiety; Lactation; Maternal behavior; Medial prefrontal cortex; Oxytocin; Prelimbic

Indexed keywords

OXYTOCIN; OXYTOCIN ANTAGONIST; OXYTOCIN RECEPTOR;

AGGRESSION; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANXIETY; ARTICLE; BEHAVIOR CHANGE; BRAIN REGION; CONTROLLED STUDY; DIESTRUS; FEMALE; HYPOTHALAMIC PARAVENTRICULAR NUCLEUS; LACTATION; LATENT PERIOD; LIMBIC CORTEX; LOCOMOTION; MATERNAL BEHAVIOR; MATERNAL CARE; MOUSE; NONHUMAN; PREFRONTAL CORTEX; PUERPERIUM; RAT; REPRODUCTION; VENTROMEDIAL PREFRONTAL CORTEX;

EID: 84905639626     PISSN: 16625153     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnbeh.2014.00258     Document Type: Article

References (96)

1. Afonso, V. M., Sison, M., Lovic, V., and Fleming, A. S. (2007). Medial prefrontal cortex lesions in the female rat affect sexual and maternal behavior and their sequential organization. Behav. Neurosci. 121, 515-526. doi: 10.1037/0735-7044.121.3.515
2. Bale, T. L., Davis, A. M., Auger, A. P., Dorsa, D. M., and McCarthy, M. M. (2001). CNS region-specific oxytocin receptor expression: importance in regulation of anxiety and sex behavior. J. Neurosci. 21, 2546-2552.
3. Bhatnagar, S., Sun, L. M., Raber, J., Maren, S., Julius, D., and Dallman, M. F. (2004). Changes in anxiety-related behaviors and hypothalamic-pituitary-adrenal activity in mice lacking the 5-HT-3A receptor. Physiol. Behav. 81, 545-555. doi: 10.1016/j.physbeh.2004.01.018
4. Boccia, M. L., and Pedersen, C. A. (2001). Brief vs. long maternal separations in infancy: contrasting relationships with adult maternal behavior and lactation levels of aggression and anxiety. Psychoneuroendocrinology 26, 657-672. doi: 10.1016/s0306-4530(01)00019-1
5. Bosch, O. J. (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
6. Bosch, O. J., and Neumann, I. D. (2008). Brain vasopressin is an important regulator of maternal behavior independent of dams' trait anxiety. Proc. Natl. Acad. Sci. U S A 105, 17139-17144. doi: 10.1073/pnas.0807412105
7. Bosch, O. J., and Neumann, I. D. (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
8. Bosch, O. J., Kromer, S. A., Brunton, P. J., and Neumann, I. D. (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
9. Bosch, O. J., Meddle, S. L., Beiderbeck, D. I., Douglas, A. J., and Neumann, I. D. (2005). Brain oxytocin correlates with maternal aggression: link to anxiety. J. Neurosci. 25, 6807-6815. doi: 10.1523/jneurosci.1342-05.2005
10. Bosch, O. J., Pfortsch, J., Beiderbeck, D. I., Landgraf, R., and Neumann, I. D. (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
11. Caughey, S. D., Klampfl, S. M., Bishop, V. R., Pfoertsch, J., Neumann, I. D., Bosch, O. J., et al. (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
12. Consiglio, A. R., and Lucion, A. B. (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
13. Consiglio, A. R., Borsoi, A., Pereira, G. A., and Lucion, A. B. (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
14. Cruz, A. P., Frei, F., and Graeff, F. G. (1994). Ethopharmacological analysis of rat behavior on the elevated plus-maze. Pharmacol. Biochem. Behav. 49, 171-176. doi: 10.1016/0091-3057(94)90472-3
15. Curley, J. P., Jensen, C. L., Franks, B., and Champagne, F. A. (2012). Variation in maternal and anxiety-like behavior associated with discrete patterns of oxytocin and vasopressin 1a receptor density in the lateral septum. Horm. Behav. 61, 454-461. doi: 10.1016/j.yhbeh.2012.01.013
16. De Almeida, R. M., Giovenardi, M., Charchat, H., and Lucion, A. B. (1998). 8-OH-DPAT in the median raphe nucleus decreases while in the medial septal area it may increase anxiety in female rats. Neurosci. Biobehav. Rev. 23, 259-264. doi: 10.1016/s0149-7634(98)00026-8
17. Erskine, M. S., Denenberg, V. H., and Goldman, B. D. (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
18. Everett, J. W. (1989). Neurobiology of reproduction in the female rat. A fifty-year perspective. Monogr. Endocrinol. 32, 1-133. doi: 10.1007/978-3-642-83797-5
19. Febo, M. (2012). Firing patterns of maternal rat prelimbic neurons during spontaneous contact with pups. Brain Res. Bull. 88, 534-542. doi: 10.1016/j.brainresbull.2012.05.012
20. Febo, M., Felix-Ortiz, A. C., and Johnson, T. R. (2010). Inactivation or inhibition of neuronal activity in the medial prefrontal cortex largely reduces pup retrieval and grouping in maternal rats. Brain Res. 1325, 77-88. doi: 10.1016/j.brainres.2010.02.027
21. Febo, M., Numan, M., and Ferris, C. F. (2005). Functional magnetic resonance imaging shows oxytocin activates brain regions associated with mother-pup bonding during suckling. J. Neurosci. 25, 11637-11644. doi: 10.1523/jneurosci.3604-05.2005
22. Figueira, R. J., Peabody, M. F., and Lonstein, J. S. (2008). Oxytocin receptor activity in the ventrocaudal periaqueductal gray modulates anxiety-related behavior in postpartum rats. Behav. Neurosci. 122, 618-628. doi: 10.1037/0735-7044.122.3.618
23. Fleming, A. S., and Luebke, C. (1981). Timidity prevents the virgin female rat from being a good mother: emotionality differences between nulliparous and parturient females. Physiol. Behav. 27, 863-868. doi: 10.1016/0031-9384(81)90054-8
24. Francis, D. D., Champagne, F. C., and Meaney, M. J. (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
25. Gammie, S. C. (2005). Current models and future directions for understanding the neural circuitries of maternal behaviors in rodents. Behav. Cogn. Neurosci. Rev. 4, 119-135. doi: 10.1177/1534582305281086
26. Gammie, S. C., Negron, A., Newman, S. M., and Rhodes, J. S. (2004). Corticotropin-releasing factor inhibits maternal aggression in mice. Behav. Neurosci. 118, 805-814. doi: 10.1037/0735-7044.118.4.805
27. Gimpl, G., and Fahrenholz, F. (2001). The oxytocin receptor system: structure, function and regulation. Physiol. Rev. 81, 629-683.
28. Giovenardi, M., Padoin, M. J., Cadore, L. P., and Lucion, A. B. (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
29. Gould, B. R., and Zingg, H. H. (2003). Mapping oxytocin receptor gene expression in the mouse brain and mammary gland using an oxytocin receptor-LacZ reporter mouse. Neuroscience 122, 155-167. doi: 10.1016/s0306-4522(03)00283-5
30. Hard, E., and Hansen, S. (1985). Reduced fearfulness in the lactating rat. Physiol. Behav. 35, 641-643. doi: 10.1016/0031-9384(85)90155-6
31. Heidbreder, C. A., and Groenewegen, H. J. (2003). The medial prefrontal cortex in the rat: evidence for a dorso-ventral distinction based upon functional and anatomical characteristics. Neurosci. Biobehav. Rev. 27, 555-579. doi: 10.1016/j.neubiorev.2003.09.003
32. Hilakivi, L. A., and Lister, R. G. (1990). Correlations between behavior of mice in Porsolt's swim test and in tests of anxiety, locomotion and exploration. Behav. Neural Biol. 53, 153-159. doi: 10.1016/0163-1047(90)90356-b
33. Insel, T. R. (1990). Regional changes in brain oxytocin receptors post-partum: time-course and relationship to maternal behaviour. J. Neuroendocrinol. 2, 539-545. doi: 10.1111/j.1365-2826.1990.tb00445.x
34. Insel, T. R., and Shapiro, L. E. (1992). Oxytocin receptor distribution reflects social organization in monogamous and polygamous voles. Proc. Natl. Acad. Sci. U S A 89, 5981-5985. doi: 10.1073/pnas.89.13.5981
35. Insel, T. R., and Young, L. J. (2001). The neurobiology of attachment. Nat. Rev. Neurosci. 2, 129-136. doi: 10.1038/35053579
36. Johns, J. M., Nelson, C. J., Meter, K. E., Lubin, D. A., Couch, C. D., Ayers, A., et al. (1998). Dose-dependent effects of multiple acute cocaine injections on maternal behavior and aggression in Sprague-Dawley rats. Dev. Neurosci. 20, 525-532. doi: 10.1159/000017353
37. Johns, J. M., Noonan, L. R., Zimmerman, L. I., Li, L., and Pedersen, C. A. (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
38. Jurek, B., Slattery, D. A., Maloumby, R., Hillerer, K., Koszinowski, S., Neumann, I. D., et al. (2012). Differential contribution of hypothalamic MAPK activity to anxiety-like behaviour in virgin and lactating rats. PLoS One7:e37060. doi: 10.1371/journal.pone.0037060
39. Knobloch, H. S., Charlet, A., Hoffmann, L. C., Eliava, M., Khrulev, S., Cetin, A. H., 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
40. Kovács, G. L., Buijs, R. M., Bohus, B., and van Wimersma Greidanus, T. B. (1982). Microinjection of arginine8-vasopressin antiserum into the dorsal hippocampus attenuates passive avoidance behavior in rats. Physiol. Behav.28, 45-48. doi: 10.1016/0031-9384(82)90099-3
41. Kovács, G. L., Vécsei, L., Medve, L., and Telegdy, G. (1980). Effect on memory processes of anti-vasopressin serum microinjected into the dorsal raphe nucleus: the role of catecholaminergic neurotransmission. Exp. Brain Res. 38, 357-361. doi: 10.1007/bf00236656
42. Landgraf, R., and Neumann, I. D. (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
43. Landgraf, R., Neumann, I., Russell, J. A., and Pittman, Q. J. (1992). Push-pull perfusion and microdialysis studies of central oxytocin and vasopressin release in freely moving rats during pregnancy, parturition and lactation. Ann. N Y Acad. Sci. 652, 326-339. doi: 10.1111/j.1749-6632.1992.tb34364.x
44. Lapiz-Bluhm, M. D., Bondi, C. O., Doyen, J., Rodriguez, G. A., Bédard-Arana, T., and Morilak, D. A. (2008). Behavioural assays to model cognitive and affective dimensions of depression and anxiety in rats. J. Neuroendocrinol. 20, 1115-1137. doi: 10.1111/j.1365-2826.2008.01772.x
45. Leuner, B., Caponiti, J. M., and Gould, E. (2012). Oxytocin stimulates adult neurogenesis even under conditions of stress and elevated glucocorticooids. Hippocampus 22, 861-868. doi: 10.1002/hipo.20947
46. Liu, W., Pappas, G. D., and Carter, C. S. (2005). Oxytocin receptors in brain cortical regions are reduced in haploinsufficient (+/-) reeler mice. Neurol. Res. 27, 339-345. doi: 10.1179/016164105x35602
47. Lonstein, J. S. (2005a). Reduced anxiety in postpartum rats requires recent physical interactions with pups, but is independent of suckling and peripheral sources of hormones. Horm. Behav. 47, 241-255. doi: 10.1016/j.yhbeh.2004.11.001
48. Lonstein, J. S. (2005b). Resolving apparent contradictions concerning the relationships among fear or anxiety and aggression during lactation: theoretical comment on D'Anna, Stevenson and Gammie (2005). Behav. Neurosci. 119, 1165-1168. doi: 10.1037/0735-7044.119.4.1165
49. Lonstein, J. S. (2007). Regulation of anxiety during the postpartum period. Front. Neuroendocrinol. 28, 115-141. doi: 10.1016/j.yfrne.2007.05.002
50. Lonstein, J. S., and Gammie, S. C. (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
51. Lonstein, J. S., Simmons, D. A., and Stern, J. M. (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
52. Lubin, D. A., Elliott, J. C., Black, M. C., and Johns, J. M. (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
53. Macbeth, A. H., and Luine, V. N. (2010). Changes in anxiety and cognition due to reproductive experience: a review of data from rodent and human mothers. Neurosci. Biobehav. Rev. 34, 452-467. doi: 10.1016/j.neubiorev.2009.08.011
54. Macdonald, K. S. (2012). Sex, receptors and attachment: a review of individual factors influencing response to oxytocin. Front. Neurosci. 6:194. doi: 10.3389/fnins.2012.00194
55. Manning, M., Misicka, A., Olma, A., Bankowski, K., Stoev, S., Chini, B., et al. (2012). Oxytocin and vasopressin agonists and antagonists as research tools and potential therapeutics. J. Neuroendocrinol. 24, 609-628. doi: 10.1111/j.1365-2826.2012.02303.x
56. Marcondes, F. K., Miguel, K. J., Melo, L. L., and Spadari-Bratfisch, R. C. (2001). Estrous cycle influences the response of female rats in the elevated plus-maze test. Physiol. Behav. 74, 435-440. doi: 10.1016/s0031-9384(01)00593-5
57. McCarthy, M. M., McDonald, C. H., Brooks, P. J., and 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
58. Mora, S., Dussaubat, N., and Díaz-Veliz, G. (1996). Effects of the estrous cycle and ovarian hormones on behavioral indices of anxiety in female rats. Psychoneuroendocrinology 21, 609-620. doi: 10.1016/s0306-4530(96)00015-7
59. Nephew, B. C., Caffrey, M. K., Felix-Ortiz, A. C., Ferris, C. F., and Febo, M. (2009). Blood oxygen level-dependent signal responses in corticolimbic 'emotions' circuitry of lactating rats facing intruder threat to pups. Eur. J. Neurosci. 30, 934-945. doi: 10.1111/j.1460-9568.2009.06875.x
60. Neumann, I., Russell, J. A., and 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
61. Neumann, I. D., and 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
62. Neumann, I. D., Torner, L., and Wigger, A. (2000a). 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
63. Neumann, I. D., Toschi, N., Ohl, F., Torner, L., and Kromer, S. A. (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
64. Neumann, I. D., Wigger, A., Torner, L., Holsboer, F., and Landgraf, R. (2000b). Brain oxytocin inhibits basal and stress-induced activity of the hypothalamo-pituitary-adrenal axis in male and female rats: partial action within the paraventricular nucleus. J. Neuroendocrinol. 12, 235-243. doi: 10.1046/j.1365-2826.2000.00442.x
65. Ninan, I. (2011). Oxytocin suppresses basal glutamatergic transmission but facilitates activity-dependent synaptic potentiation in the medial prefrontal cortex. J. Neurochem. 119, 324-331. doi: 10.1111/j.1471-4159.2011.07430.x
66. Numan, M., and Woodside, B. (2010). Maternity: neural mechanisms, motivational processes and physiological adaptations. Behav. Neurosci. 124, 715-741. doi: 10.1037/a0021548
67. Numan, M., Stolzenberg, D. S., Dellevigne, A. A., Correnti, C. M., and Numan, M. J. (2009). Temporary inactivation of ventral tegmental area neurons with either muscimol or baclofen reversibly disrupts maternal behavior in rats through different underlying mechanisms. Behav. Neurosci. 123, 740-751. doi: 10.1037/a0016204
68. Nyuyki, K. D., Waldherr, M., Baeuml, S., and Neumann, I. D. (2011). Yes, I am ready now: differential effects of paced versus unpaced mating on anxiety and central oxytocin release in female rats. PLoS One 6:e23599. doi: 10.1371/journal.pone.0023599
69. Paxinos, G., and Watson, C. (1998). The Rat Brain in Stereotaxic Coordinates. San Diego, CA: Academic Press.
70. Pedersen, C. A., and Prange, A. J. Jr. (1979). Induction of maternal behavior in virgin rats after intracerebroventricular administration of oxytocin. Proc. Natl. Acad. Sci. U S A 76, 6661-6665. doi: 10.1073/pnas.76.12.6661
71. Pedersen, C. A., Caldwell, J. D., Walker, C., Ayers, G., and Mason, G. A. (1994). Oxytocin activates the postpartum onset of rat maternal behavior in the ventral tegmental and medial preoptic areas. Behav. Neurosci. 108, 1163-1171. doi: 10.1037//0735-7044.108.6.1163
72. Pedersen, C. A., Vadlamudi, S. V., Boccia, M. L., and Amico, J. A. (2006). Maternal behavior deficits in nulliparous oxytocin knockout mice. Genes Brain Behav. 5, 274-281. doi: 10.1111/j.1601-183x.2005.00162.x
73. Pellow, S., Chopin, P., File, S. E., and Briley, M. (1985). Validation of open: closed arm entries in an elevated plus-maze as a measure of anxiety in the rat. J. Neurosci. Methods 14, 149-167. doi: 10.1016/0165-0270(85)90031-7
74. Pereira, M., and Morrell, J. I. (2011). Functional mapping of the neural circuitry of rat maternal motivation: effects of site-specific transient neural inactivation. J. Neuroendocrinol. 23, 1020-1035. doi: 10.1111/j.1365-2826.2011.02200.x
75. Peters, J., Kalivas, P. W., and Quirk, G. J. (2009). Extinction circuits for fear and addiction overlap in prefrontal cortex. Learn. Mem. 16, 279-288. doi: 10.1101/lm.1041309
76. Porges, S. W. (2003). Social engagement and attachment: a phylogenetic perspective. Ann. N Y Acad. Sci. 1008, 31-47. doi: 10.1196/annals.1301.004
77. Prut, L., and Belzung, C. (2003). The open field as a paradigm to measure the effects of drugs on anxiety-like behaviors: a review. Eur. J. Pharmacol. 463, 3-33. doi: 10.1016/s0014-2999(03)01272-x
78. Ring, R. H., Malberg, J. E., Potestio, L., Ping, J., Boikess, S., Luo, B., et al. (2006). Anxiolytic-like activity of oxytocin in male mice: behavioral and autonomic evidence, therapeutic implications. Psychopharmacology (Berl)185, 218-225. doi: 10.1007/s00213-005-0293-z
79. Rosenblatt, J. S. (1967). Nonhormonal basis of maternal behavior in the rat. Science 156, 1512-1514. doi: 10.1126/science.156.3781.1512
80. Rotzinger, S., Lovejoy, D. A., and Tan, L. A. (2010). Behavioral effects of neuropeptides in rodent models of depression and anxiety. Peptides 31, 736-756. doi: 10.1016/j.peptides.2009.12.015
81. Sabihi, S., Durosko, N. E., Dong, S. M., and Leuner, B. (2014). Oxytocin in the prelimbic medial prefrontal cortex reduces anxiety-like behavior in female and male rats. Psychoneuroendocrinology 45, 31-42. doi: 10.1016/j.psyneuen.2014.03.009
82. Saltzman, W., and Maestripieri, D. (2011). The neuroendocrinology of primate maternal behavior. Prog. Neuropsychopharmacol. Biol. Psychiatry 35, 1192-1204. doi: 10.1016/j.pnpbp.2010.09.017
83. Shah, A. A., and Treit, D. (2003). Excitotoxic lesions of the medial prefrontal cortex attenuate fear responses in the elevated-plus maze, social interaction and shock probe burying tests. Brain Res. 969, 183-194. doi: 10.1016/s0006-8993(03)02299-6
84. Shahrokh, D. K., Zhang, T. Y., Diorio, J., Gratton, A., and Meaney, M. J. (2010). Oxytocin-dopamine interactions mediate variations in maternal behavior in the rat. Endocrinology 151, 2276-2286. doi: 10.1210/en.2009-1271
85. Smeltzer, M. D., Curtis, J. T., Aragona, B. J., and Wang, Z. (2006). Dopamine, oxytocin and vasopressin receptor binding in the medial prefrontal cortex of monogamous and promiscuous voles. Neurosci. Lett. 394, 146-151. doi: 10.1016/j.neulet.2005.10.019
86. Sofroniew, M. V. (1983). Morphology of vasopressin and oxytocin neurones and their central and vascular projections. Prog. Brain Res. 60, 101-114. doi: 10.1016/s0079-6123(08)64378-2
87. Stern, C. A., Do Monte, F. H., Gazarini, L., Carobrez, A. P., and Bertoglio, L. J. (2010). Activity in prelimbic cortex is required for adjusting the anxiety response level during the elevated plus-maze retest. Neuroscience 170, 214-222. doi: 10.1016/j.neuroscience.2010.06.080
88. Troisi, A., and D'Amato, F. R. (1994). "Mechanisms of primate infant abuse: the maternal anxiety hypothesis, " inInfanticide and Parental Care, eds F. S. vom Saal and S. Parmigiani (Rome, Italy: Harwood Academic), 199-210.
89. Turner, S. M., Beidel, D. C., Roberson-Nay, R., and Tervo, K. (2003). Parenting behaviors in parents with anxiety disorders. Behav. Res. Ther. 41, 541-554. doi: 10.1016/s0005-7967(02)00028-1
90. van Leengoed, E., Kerker, E., and Swanson, H. H. (1987). Inhibition of post-partum maternal behaviour in the rat by injecting an oxytocin antagonist into the cerebral ventricles. J. Endocrinol. 112, 275-282. doi: 10.1677/joe.0.1120275
91. Vertes, R. P. (2004). Differential projections of the infralimbic and prelimbic cortex in the rat. Synapse 51, 32-58. doi: 10.1002/syn.10279
92. Waldherr, M., and Neumann, I. D. (2007). Centrally released oxytocin mediates mating-induced anxiety in male rats. Proc. Natl. Acad. Sci. U S A 104, 16681-16684. doi: 10.1073/pnas.0705860104
93. Walf, A. A., and Frye, C. A. (2007). The use of the elevated plus maze as an assay of anxiety-related behavior in rodents. Nat. Protoc. 2, 322-328. doi: 10.1038/nprot.2007.44
94. Windle, R. J., Shanks, N., Lightman, S. L., and Ingram, C. D. (1997). Central oxytocin administration reduces stress-induced corticosterone release and anxiety behavior in rats. Endocrinology 138, 2829-2834. doi: 10.1210/en.138.7.2829
95. Young, K. A., Liu, Y., Gobrogge, K. L., Wang, H., and Wang, Z. (2014). Oxytocin reverses amphetamine-induced deficits in social bonding: evidence for an interaction with nucleus accumbens dopamine. J. Neurosci. 34, 8499-8506. doi: 10.1523/JNEUROSCI.4275-13.2014
96. Yu, G. Z., Kaba, H., Okutani, F., Takahashi, S., and Higuchi, T. (1996). The olfactory bulb: a critical site of action for oxytocin in the induction of maternal behaviour in the rat. Neuroscience 72, 1083-1088. doi: 10.1016/0306-4522(95)00600-1