Distinct BOLD activation profiles following central and peripheral oxytocin administration in awake rats

Frontiers in Behavioral Neuroscience

Volumn 9, Issue September, 2015, Pages

  Ferris, Craig F ^a   Yee, Jason R ^a,b   Kenkel, William M ^b   Dumais, Kelly Marie ^c   Moore, Kelsey ^a   Veenema, Alexa H ^c   Kulkarni, Praveen ^a   Perkybile, Allison M ^b   Carter, C Sue ^b  

^a NORTHEASTERN UNIVERSITY   (United States)

^b INDIANA UNIVERSITY   (United States)

^c BOSTON COLLEGE   (United States)

Author keywords

Cerebellum and emotion; Functional magnetic resonance imaging; Nucleus of the solitary tract; Olfaction and emotion; Oxytocin

Indexed keywords

OXYTOCIN; OXYTOCIN RECEPTOR;

ADULT; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; AUTONOMIC NERVOUS SYSTEM; BOLD SIGNAL; BRAIN FUNCTION; BRAIN REGION; BRAIN STEM; CEREBELLUM; CONTROLLED STUDY; FUNCTIONAL MAGNETIC RESONANCE IMAGING; MALE; NONHUMAN; OLFACTORY BULB; RAT; SIGNAL TRANSDUCTION; SOLITARY TRACT NUCLEUS;

EID: 84943189685     PISSN: 16625153     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnbeh.2015.00245     Document Type: Article

References (126)

1. Andari, E., Duhamel, J. R., Zalla, T., Herbrecht, E., Leboyer, M., and Sirigu, A. (2010). Promoting social behavior with oxytocin in high-functioning autism spectrum disorders. Proc. Natl. Acad. Sci. U.S.A. 107, 4389–4394. doi:10.1073/pnas.0910249107
2. Arletti, R., and Bertolini, A. (1985). Oxytocin stimulates lordosis behavior in female rats. Neuropeptides 6, 247–253. doi:10.1016/0143-4179(85)90095-2
3. Ayers, L. W., Missig, G., Schulkin, J., and Rosen, J. B. (2011). Oxytocin reduces background anxiety in a fear-potentiated startle paradigm: peripheral vs central administration. Neuropsychopharmacology. 36, 2488–97. doi:10.1038/npp.2011.138
4. Baldwin, B. A., and Shillito, E. E. (1974). The effects of ablation of the olfactory bulbs on parturition and maternal behaviour in Soay sheep. Anim. Behav. 22, 220–223. doi:10.1016/S0003-3472(74)80072-2
5. 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
6. Bartz, J. A., and Hollander, E. (2008). Oxytocin and experimental therapeutics in autism spectrum disorders. Prog. Brain Res. 170, 451–462. doi:10.1016/S0079-6123(08)00435-4
7. Bartz, J. A., Zaki, J., Bolger, N., Hollander, E., Ludwig, N. N., Kolevzon, A., et al. (2010). Oxytocin selectively improves empathic accuracy. Psychol. Sci. 21, 1426–1428. doi:10.1177/0956797610383439
8. Beery, A. K., Lacey, E. A., and Francis, D. D. (2008). Oxytocin and vasopressin receptor distributions in a solitary and a social species of tuco-tuco (Ctenomys haigi and Ctenomys sociabilis). J. Comp. Neurol. 507, 1847–1859. doi:10.1002/cne.21638
9. Bernard, J. F., and Besson, J. M. (1990). The spino(trigemino)pontoamygdaloid pathway: electrophysiological evidence for an involvement in pain processes. J. Neurophysiol. 63, 473–490
10. Bertsch, K., Gamer, M., Schmidt, B., Schmidinger, I., Walther, S., Kastel, T., et al. (2013). Oxytocin and reduction of social threat hypersensitivity in women with borderline personality disorder. Am. J. Psychiatry 170, 1169–1177. doi:10.1176/appi.ajp.2013.13020263
11. Bowen, M. T., Carson, D. S., Spiro, A., Arnold, J. C., and McGregor, I. S. (2011). Adolescent oxytocin exposure causes persistent reductions in anxiety and alcohol consumption and enhances sociability in rats. PLoS ONE 6:e27237. doi:10.1371/journal.pone.0027237
12. Brevard, M. E., Duong, T. Q., King, J. A., and Ferris, C. F. (2003). Changes in MRI signal intensity during hypercapnic challenge under conscious and anesthetized conditions. Magn. Reson. Imaging 21, 995–1001. doi:10.1016/S0730-725X(03)00204-2
13. Buchheim, A., Heinrichs, M., George, C., Pokorny, D., Koops, E., Henningsen, P., et al. (2009). Oxytocin enhances the experience of attachment security. Psychoneuroendocrinology 34, 1417–1422. doi:10.1016/j.psyneuen.2009.04.002
14. Buijs, R. M., Van der Beek, E. M., Renaud, L. P., Day, T. A., and Jhamandas, J. H. (1990). Oxytocin localization and function in the A1 noradrenergic cell group: ultrastructural and electrophysiological studies. Neuroscience 39, 717–725. doi:10.1016/0306-4522(90)90255-3
15. Calcagnoli, F., Kreutzmann, J. C., de Boer, S. F., Althaus, M., and Koolhaas, J. M. (2015). Acute and repeated intranasal oxytocin administration exerts anti-aggressive and pro-affiliative effects in male rats. Psychoneuroendocrinology 51, 112–121. doi:10.1016/j.psyneuen.2014.09.019
16. Caldwell, J. D., Prange, A. J. Jr., and Pedersen, C. A. (1986). Oxytocin facilitates the sexual receptivity of estrogen-treated female rats. Neuropeptides 7, 175–189. doi:10.1016/0143-4179(86)90093-4
17. Campbell, P., Ophir, A. G., and Phelps, S. M. (2009). Central vasopressin and oxytocin receptor distributions in two species of singing mice. J. Comp. Neurol. 516, 321–333. doi:10.1002/cne.22116
18. Caous, C. A., Smith, R. L., Haapalainen, E. F., and Lindsey, C. J. (2012). Ultrastructural transneuronal degeneration study of axonal elements within the paratrigeminal nucleus in sinoaortic deafferented rats. Einstein (Sao Paulo) 10, 145–150. doi:10.1590/S1679-45082012000200006
19. Carter, C., and Keverne, E. (2002). “The neurobiology of social affiliation and pair bonding,” in Hormones, Brain and Behavior, eds D. Pfaff (San Diego, CA: Academic Press).
20. Cavdar, S., San, T., Aker, R., Sehirli, U., and Onat, F. (2001). Cerebellar connections to the dorsomedial and posterior nuclei of the hypothalamus in the rat. J. Anat. 198, 37–45. doi:10.1017/S0021878200007172
21. Cechetto, D. F., Standaert, D. G., and Saper, C. B. (1985). Spinal and trigeminal dorsal horn projections to the parabrachial nucleus in the rat. J. Comp. Neurol. 240, 153–160. doi:10.1002/cne.902400205
22. Chang, S. W., Barter, J. W., Ebitz, R. B., Watson, K. K., and Platt, M. L. (2012). Inhaled oxytocin amplifies both vicarious reinforcement and self reinforcement in Rhesus macaques (Macaca mulatta). Proc. Natl. Acad. Sci. U.S.A. 109, 959–964. doi:10.1073/pnas.1114621109
23. Churchland, P. S., and Winkielman, P. (2012). Modulating social behavior with oxytocin: how does it work? What does it mean? Horm. Behav. 61, 392–399. doi:10.1016/j.yhbeh.2011.12.003
24. Dantzer, R., Tazi, A., and Bluthe, R. M. (1990). Cerebral lateralization of olfactory-mediated affective processes in rats. Behav. Brain Res. 40, 53–60. doi:10.1016/0166-4328(90)90042-D
25. De Kloet, E. R., Rotteveel, F., Voorhuis, T. A., and Terlou, M. (1985). Topography of binding sites for neurohypophyseal hormones in rat brain. Eur. J. Pharmacol. 110, 113–119. doi:10.1016/0014-2999(85)90036-6de
26. Wied, D., Gaffori, O., Burbach, J. P., Kovacs, G. L., and van Ree, J. M. (1987). Structure activity relationship studies with C-terminal fragments of vasopressin and oxytocin on avoidance behaviors of rats. J. Pharmacol. Exp. Ther. 241, 268–274
27. Dluzen, D. E., Muraoka, S., Engelmann, M., and Landgraf, R. (1998). The effects of infusion of arginine vasopressin, oxytocin, or their antagonists into the olfactory bulb upon social recognition responses in male rats. Peptides 19, 999–1005. doi:10.1016/S0196-9781(98)00047-3
28. Dumais, K. M., Bredewold, R., Mayer, T. E., and Veenema, A. H. (2013). Sex differences in oxytocin receptor binding in forebrain regions: correlations with social interest in brain region- and sex- specific ways. Horm. Behav. 64, 693–701. doi:10.1016/j.yhbeh.2013.08.012
29. Duong, T. Q., Yacoub, E., Adriany, G., Hu, X., Ugurbil, K., and Kim, S. G. (2003). Microvascular BOLD contribution at 4 and 7 T in the human brain: gradient-echo and spin-echo fMRI with suppression of blood effects. Magn. Reson. Med. 49, 1019–1027. doi:10.1002/mrm.10472
30. Eckstein, M., Becker, B., Scheele, D., Scholz, C., Preckel, K., Schlaepfer, T. E., et al. (2014). Oxytocin facilitates the extinction of conditioned fear in humans. Biol. Psychiatry. 78, 194–202. doi:10.1016/j.biopsych
31. Ermisch, A., Barth, T., Ruhle, H. J., Skopkova, J., Hrbas, P., and Landgraf, R. (1985). On the blood-brain barrier to peptides: accumulation of labelled vasopressin, DesGlyNH2-vasopressin and oxytocin by brain regions. Endocrinol. Exp. 19, 29–37
32. 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
33. Febo, M., Segarra, A. C., Tenney, J. R., Brevard, M. E., Duong, T. Q., and Ferris, C. F. (2004). Imaging cocaine-induced changes in the mesocorticolimbic dopaminergic system of conscious rats. J. Neurosci. Methods 139, 167–176. doi:10.1016/j.jneumeth.2004.04.028
34. Feifel, D., Macdonald, K., Nguyen, A., Cobb, P., Warlan, H., Galangue, B., et al. (2010). Adjunctive intranasal oxytocin reduces symptoms in schizophrenia patients. Biol. Psychiatry 68, 678–680. doi:10.1016/j.biopsych.2010.04.039
35. Feldman, R. (2006). From biological rhythms to social rhythms: physiological precursors of mother-infant synchrony. Dev. Psychol. 42, 175–188. doi:10.1037/0012-1649.42.1.175
36. Feldman, R., and Eidelman, A. I. (2007). Maternal postpartum behavior and the emergence of infant-mother and infant-father synchrony in preterm and full-term infants: the role of neonatal vagal tone. Dev. Psychobiol. 49, 290–302. doi:10.1002/dev.20220
37. Feldman, R., Singer, M., and Zagoory, O. (2010). Touch attenuates infants’ physiological reactivity to stress. Dev. Sci. 13, 271–278. doi:10.1111/j.1467-7687.2009.00890.x
38. Ferris, C. F., Smerkers, B., Kulkarni, P., Caffrey, M., Afacan, O., Toddes, S., et al. (2011). Functional magnetic resonance imaging in awake animals. Rev. Neurosci. 22, 665–674. doi:10.1515/RNS.2011.050
39. Fleming, A. S., and Rosenblatt, J. S. (1974). 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, 221–232. doi:10.1037/h0035937
40. Freund-Mercier, M. J., Stoeckel, M. E., Palacios, J. M., Pazos, A., Reichhart, J. M., Porte, A., et al. (1987). Pharmacological characteristics and anatomical distribution of [3H]oxytocin-binding sites in the Wistar rat brain studied by autoradiography. Neuroscience 20, 599–614. doi:10.1016/0306-4522(87)90113-8
41. Gandelman, R., Zarrow, M. X., Denenberg, V. H., and Myers, M. (1971). Olfactory bulb removal eliminates maternal behavior in the mouse. Science 171, 210–211. doi:10.1126/science.171.3967.210
42. Genovese, C. R., Lazar, N. A., and Nichols, T. (2002). Thresholding of statistical maps in functional neuroimaging using the false discovery rate. Neuroimage 15, 870–878. doi:10.1006/nimg.2001.1037
43. Gimpl, G., and Fahrenholz, F. (2001). The oxytocin receptor system: structure, function, and regulation. Physiol. Rev. 81, 629–683
44. Gossen, A., Hahn, A., Westphal, L., Prinz, S., Schultz, R. T., Grunder, G., et al. (2012). Oxytocin plasma concentrations after single intranasal oxytocin administration – a study in healthy men. Neuropeptides 46, 211–215. doi:10.1016/j.npep.2012.07.001
45. Guastella, A. J., Einfeld, S. L., Gray, K. M., Rinehart, N. J., Tonge, B. J., Lambert, T. J., et al. (2010). Intranasal oxytocin improves emotion recognition for youth with autism spectrum disorders. Biol. Psychiatry 67, 692–694. doi:10.1016/j.biopsych.2009.09.020
46. Guastella, A. J., Hickie, I. B., McGuinness, M. M., Otis, M., Woods, E. A., Disinger, H. M., et al. (2013). Recommendations for the standardisation of oxytocin nasal administration and guidelines for its reporting in human research. Psychoneuroendocrinology 38, 612–625. doi:10.1016/j.psyneuen.2012.11.019
47. Haines, D. E., Dietrichs, E., and Sowa, T. E. (1984). Hypothalamo-cerebellar and cerebello-hypothalamic pathways: a review and hypothesis concerning cerebellar circuits which may influence autonomic centers affective behavior. Brain Behav. Evol. 24, 198–220. doi:10.1159/000315995
48. Heath, R. G., Dempesy, C. W., Fontana, C. J., and Myers, W. A. (1978). Cerebellar stimulation: effects on septal region, hippocampus, and amygdala of cats and rats. Biol. Psychiatry 13, 501–529
49. Helena, C. V., Cristancho-Gordo, R., Gonzalez-Iglesias, A. E., Tabak, J., Bertram, R., and Freeman, M. E. (2011). Systemic oxytocin induces a prolactin secretory rhythm via the pelvic nerve in ovariectomized rats. Am. J. Physiol. Regul. Integr. Comp. Physiol. 301, R676–R681. doi:10.1152/ajpregu.00176.2011
50. Herbert, H., Moga, M. M., and Saper, C. B. (1990). Connections of the parabrachial nucleus with the nucleus of the solitary tract and the medullary reticular formation in the rat. J. Comp. Neurol. 293, 540–580. doi:10.1002/cne.902930404
51. Higa, K. T., Mori, E., Viana, F. F., Morris, M., and Michelini, L. C. (2002). Baroreflex control of heart rate by oxytocin in the solitary-vagal complex. Am. J. Physiol. Regul. Integr. Comp. Physiol. 282, R537–R545. doi:10.1152/ajpregu.00806.2000
52. Hollander, E., Bartz, J., Chaplin, W., Phillips, A., Sumner, J., Soorya, L., et al. (2007). Oxytocin increases retention of social cognition in autism. Biol. Psychiatry 61, 498–503. doi:10.1016/j.biopsych.2006.05.030
53. Hollander, E., Novotny, S., Hanratty, M., Yaffe, R., DeCaria, C. M., Aronowitz, B. R., et al. (2003). Oxytocin infusion reduces repetitive behaviors in adults with autistic and Asperger’s disorders. Neuropsychopharmacology 28, 193–198. doi:10.1038/sj.npp.1300021
54. Holley, A., Bellevue, S., Vosberg, D., Wenzel, K., Roorda, S. Jr., and Pfaus, J. G. (2015). The role of oxytocin and vasopressin in conditioned mate guarding behavior in the female rat. Physiol. Behav. 144, 7–14. doi:10.1016/j.physbeh.2015.02.039
55. Hurlemann, R., Patin, A., Onur, O. A., Cohen, M. X., Baumgartner, T., Metzler, S., et al. (2010). Oxytocin enhances amygdala-dependent, socially reinforced learning and emotional empathy in humans. J. Neurosci. 30, 4999–5007. doi:10.1523/JNEUROSCI.5538-09.2010
56. Iannilli, E., Bitter, T., Gudziol, H., Burmeister, H. P., Mentzel, H. J., Chopra, A. P., et al. (2011). Differences in anosmic and normosmic group in bimodal odorant perception: a functional-MRI study. Rhinology 49, 458–463. doi:10.4193/Rhino11.110
57. Insel, T. R., and Young, L. J. (2001). The neurobiology of attachment. Nat. Rev. Neurosci. 2, 129–136. doi:10.1038/35053579
58. Jaarsma, D., Ruigrok, T. J., Caffe, R., Cozzari, C., Levey, A. I., Mugnaini, E., et al. (1997). Cholinergic innervation and receptors in the cerebellum. Prog. Brain Res. 114, 67–96. doi:10.1016/S0079-6123(08)63359-2
59. Kang, Y. S., and Park, J. H. (2000). Brain uptake and the analgesic effect of oxytocin – its usefulness as an analgesic agent. Arch. Pharm. Res. 23, 391–395. doi:10.1007/BF02975453
60. Kim, S. G., and Ogawa, S. (2012). Biophysical and physiological origins of blood oxygenation level-dependent fMRI signals. J. Cereb. Blood Flow Metab. 32, 1188–1206. doi:10.1038/jcbfm.2012.23
61. King, J. A., Garelick, T. S., Brevard, M. E., Chen, W., Messenger, T. L., Duong, T. Q., et al. (2005). Procedure for minimizing stress for fMRI studies in conscious rats. J. Neurosci. Methods 148, 154–160. doi:10.1016/j.jneumeth.2005.04.011
62. Klenerova, V., Krejci, I., Sida, P., Hlinak, Z., and Hynie, S. (2009). Modulary effects of oxytocin and carbetocin on stress-induced changes in rat behavior in the open-field. J. Physiol. Pharmacol. 60, 57–62
63. 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
64. Kondo, M., Sears, T. A., Sadakane, K., and Nisimaru, N. (1998). Vagal afferent projections to lobule VIIa of the rabbit cerebellar vermis related to cardiovascular control. Neurosci. Res. 30, 111–117. doi:10.1016/S0168-0102(97)00112-0
65. Kosfeld, M., Heinrichs, M., Zak, P. J., Fischbacher, U., and Fehr, E. (2005). Oxytocin increases trust in humans. Nature 435, 673–676. doi:10.1038/nature03701
66. Krutki, P., Grottel, K., and Mrowczynski, W. (1999). Divergence of lamina VII and VIII neurones of S1 and S2 segments of the cat’s spinal cord to the cerebellum and the reticular formation. Acta. Neurobiol. Exp. (Wars) 59, 81–88
67. Landgraf, R. (1985). Plasma oxytocin concentrations in man after different routes of administration of synthetic oxytocin. Exp. Clin. Endocrinol. 85, 245–248. doi:10.1055/s-0029-1210444
68. 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
69. Langhof, H., Hoppener, U., and Rubia, F. J. (1973). Climbing fiber responses to splanchnic nerve stimulation. Brain Res. 53, 232–236. doi:10.1016/0006-8993(73)90787-7
70. Larrazolo-Lopez, A., Kendrick, K. M., Aburto-Arciniega, M., Arriaga-Avila, V., Morimoto, S., Frias, M., et al. (2008). Vaginocervical stimulation enhances social recognition memory in rats via oxytocin release in the olfactory bulb. Neuroscience 152, 585–593. doi:10.1016/j.neuroscience.2008.01.024
71. Leng, G., and Ludwig, M. (2015). Intranasal oxytocin: myths and delusions. Biol. Psychiatry. doi:10.1016/j.biopsych.2015.05.003
72. Ludwig, M., Tobin, V. A., Callahan, M. F., Papadaki, E., Becker, A., Engelmann, M., et al. (2013). Intranasal application of vasopressin fails to elicit changes in brain immediate early gene expression, neural activity and behavioural performance of rats. J. Neuroendocrinol. 25, 655–667. doi:10.1111/jne.12046
73. Lukas, M., Bredewold, R., Neumann, I. D., and Veenema, A. H. (2010). Maternal separation interferes with developmental changes in brain vasopressin and oxytocin receptor binding in male rats. Neuropharmacology 58, 78–87. doi:10.1016/j.neuropharm.2009.06.020
74. Lukas, M., Toth, I., Reber, S. O., Slattery, D. A., Veenema, A. H., and Neumann, I. D. (2011). The neuropeptide oxytocin facilitates pro-social behavior and prevents social avoidance in rats and mice. Neuropsychopharmacology 36, 2159–2168. doi:10.1038/npp.2011.95
75. Lundeberg, T., Uvnas-Moberg, K., Agren, G., and Bruzelius, G. (1994). Anti- nociceptive effects of oxytocin in rats and mice. Neurosci. Lett. 170, 153–157. doi:10.1016/0304-3940(94)90262-3
76. Mainland, J. D., Johnson, B. N., Khan, R., Ivry, R. B., and Sobel, N. (2005). Olfactory impairments in patients with unilateral cerebellar lesions are selective to inputs from the contralesional nostril. J. Neurosci. 25, 6362–6371. doi:10.1523/JNEUROSCI.0920-05.2005
77. 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
78. 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
79. Menetrey, D., and Basbaum, A. I. (1987). Spinal and trigeminal projections to the nucleus of the solitary tract: a possible substrate for somatovisceral and viscerovisceral reflex activation. J. Comp. Neurol. 255, 439–450. doi:10.1002/cne.902550310
80. Menetrey, D., and De Pommery, J. (1991). Origins of spinal ascending pathways that reach central areas involved in visceroception and visceronociception in the rat. Eur. J. Neurosci. 3, 249–259. doi:10.1111/j.1460-9568.1991.tb00087.x
81. Mens, W. B., Witter, A., and van Wimersma Greidanus, T. B. (1983). Penetration of neurohypophyseal hormones from plasma into cerebrospinal fluid (CSF): half-times of disappearance of these neuropeptides from CSF. Brain Res. 262, 143–149. doi:10.1016/0006-8993(83)90478-X
82. Meyer, C., Freund-Mercier, M. J., Guerne, Y., and Richard, P. (1987). Relationship between oxytocin release and amplitude of oxytocin cell neurosecretory bursts during suckling in the rat. J. Endocrinol. 114, 263–270. doi:10.1677/joe.0.1140263
83. Missig, G., Ayers, L. W., Schulkin, J., and Rosen, J. B. (2010). Oxytocin reduces background anxiety in a fear-potentiated startle paradigm. Neuropsychopharmacology 35, 2607–2616. doi:10.1038/npp.2010.155
84. Modi, M. E., Connor-Stroud, F., Landgraf, R., Young, L. J., and Parr, L. A. (2014). Aerosolized oxytocin increases cerebrospinal fluid oxytocin in Rhesus macaques. Psychoneuroendocrinology 45, 49–57. doi:10.1016/j.psyneuen.2014.02.011
85. Moody, K. M., Steinman, J. L., Komisaruk, B. R., and Adler, N. T. (1994). Pelvic neurectomy blocks oxytocin-facilitated sexual receptivity in rats. Physiol. Behav. 56, 1057–1060. doi:10.1016/0031-9384(94)90343-3
86. Moore, G. A., and Calkins, S. D. (2004). Infants’ vagal regulation in the still-face paradigm is related to dyadic coordination of mother-infant interaction. Dev. Psychol. 40, 1068–1080. doi:10.1037/0012-1649.40.6.1068
87. Neumann, I. D., Maloumby, R., Beiderbeck, D. I., Lukas, M., and Landgraf, R. (2013). Increased brain and plasma oxytocin after nasal and peripheral administration in rats and mice. Psychoneuroendocrinology 38, 1985–1993. doi:10.1016/j.psyneuen.2013.03.003
88. Newman, P. P., and Paul, D. H. (1966). The representation of some visceral afferents in the anterior lobe of the cerebellum. J. Physiol. 182, 195–208. doi:10.1113/jphysiol.1966.sp007818
89. Newman, P. P., and Paul, D. H. (1967). Analysis of unit activity in the cerebellum. J. Physiol. 191, 53–54
90. Newman, P. P., and Paul, D. H. (1969). The projection of splanchnic afferents on the cerebellum of the cat. J. Physiol. 202, 223–227. doi:10.1113/jphysiol.1969.sp008806
91. Nisimaru, N., and Katayama, S. (1995). Projection of cardiovascular afferents to the lateral nodulus-uvula of the cerebellum in rabbits. Neurosci. Res. 21, 343–350. doi:10.1016/0168-0102(94)00872-D
92. Norris, D. G. (2006). Principles of magnetic resonance assessment of brain function. J. Magn. Reson. Imaging 23, 794–807. doi:10.1002/jmri.20587
93. Numan, M., and Insel, T. (2003). “The neurobiology of parental behaviour,” in Hormones, Brain and Behavior Series, eds G. F. Ball, J. Balthazart and R. J. Nelson (New York, NY: Springer). 8–41
94. Okahara, K., and Nisimaru, N. (1991). Climbing fiber responses evoked in lobule VII of the posterior cerebellum from a vagal nerve in rabbits. Neurosci. Res. 12, 232–239. doi:10.1016/0168-0102(91)90113-D
95. Pedersen, C. A. (1997). Oxytocin control of maternal behavior. Regulation by sex steroids and offspring stimuli. Ann. N. Y. Acad. Sci. 807, 126–145. doi:10.1111/j.1749-6632.1997.tb51916.x
96. Perciavalle, V., Apps, R., Bracha, V., Delgado-Garcia, J. M., Gibson, A. R., Leggio, M., et al. (2013). Consensus paper: current views on the role of cerebellar interpositus nucleus in movement control and emotion. Cerebellum 12, 738–757. doi:10.1007/s12311-013-0464-0
97. Peters, J. H., McDougall, S. J., Kellett, D. O., Jordan, D., Llewellyn-Smith, I. J., and Andresen, M. C. (2008). Oxytocin enhances cranial visceral afferent synaptic transmission to the solitary tract nucleus. J. Neurosci. 28, 11731–11740. doi:10.1523/JNEUROSCI.3419-08.2008
98. Porges, S. (2004). “The vagus: a mediator of behavioral and visceral features associated with autism,” in The Neurobiology of Autism, eds M. Bauman and T. Kemper (Baltimore, MD: Johns Hopkins University Press), 65–78
99. Puglia, M. H., Lillard, T. S., Morris, J. P., and Connelly, J. J. (2015). Epigenetic modification of the oxytocin receptor gene influences the perception of anger and fear in the human brain. Proc. Natl. Acad. Sci. U.S.A. 112, 3308–3313. doi:10.1073/pnas.1422096112
100. Ramos, L., Hicks, C., Kevin, R., Caminer, A., Narlawar, R., Kassiou, M., et al. (2013). Acute prosocial effects of oxytocin and vasopressin when given alone or in combination with 3,4-methylenedioxymethamphetamine in rats: involvement of the V1A receptor. Neuropsychopharmacology 38, 2249–2259. doi:10.1038/npp.2013.125
101. Ricardo, J. A., and Koh, E. T. (1978). Anatomical evidence of direct projections from the nucleus of the solitary tract to the hypothalamus, amygdala, and other forebrain structures in the rat. Brain Res. 153, 1–26. doi:10.1016/0006-8993(78)91125-3
102. Rinaman, L. (1998). Oxytocinergic inputs to the nucleus of the solitary tract and dorsal motor nucleus of the vagus in neonatal rats. J. Comp. Neurol. 399, 101–109. doi:10.1002/(SICI)1096-9861(19980914)399:1<101::AID-CNE8>3.0.CO;2-5
103. 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
104. Rosen, G. J., de Vries, G. J., Goldman, S. L., Goldman, B. D., and Forger, N. G. (2008). Distribution of oxytocin in the brain of a eusocial rodent. Neuroscience 155, 809–817. doi:10.1016/j.neuroscience.2008.05.039
105. Rubia, F. J. (1970). The projection of visceral afferents to the cerebellar cortex of the cat. Pflugers Arch. 320, 97–110. doi:10.1007/BF00588545
106. Rubia, F. J., and Phelps, J. B. (1970). Responses of the cerebellar cortex to cutaneous and visceral afferents. I. Fiber responses. Pflugers Arch. 314, 68–85. doi:10.1007/BF00587047
107. Sanchez-Andrade, G., and Kendrick, K. M. (2009). The main olfactory system and social learning in mammals. Behav. Brain Res. 200, 323–335. doi:10.1016/j.bbr.2008.12.021
108. Sawchenko, P. E., and Swanson, L. W. (1982). Immunohistochemical identification of neurons in the paraventricular nucleus of the hypothalamus that project to the medulla or to the spinal cord in the rat. J. Comp. Neurol. 205, 260–272. doi:10.1002/cne.902050306
109. Slattery, D. A., and Neumann, I. D. (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
110. Snider, R. S., and Maiti, A. (1976). Cerebellar contributions to the Papez circuit. J. Neurosci. Res. 2, 133–146. doi:10.1002/jnr.490020204
111. Song, Z., McCann, K. E., McNeill, J. K., Larkin, T. E. II, Huhman, K. L., and Albers, H. E. (2014). Oxytocin induces social communication by activating arginine-vasopressin V1a receptors and not oxytocin receptors. Psychoneuroendocrinology 50, 14–19. doi:10.1016/j.psyneuen.2014.08.005
112. Striepens, N., Kendrick, K. M., Hanking, V., Landgraf, R., Wullner, U., Maier, W., et al. (2013). Elevated cerebrospinal fluid and blood concentrations of oxytocin following its intranasal administration in humans. Sci. Rep. 3, 3440. doi:10.1038/srep03440
113. Suraev, A. S., Bowen, M. T., Ali, S. O., Hicks, C., Ramos, L., and McGregor, I. S. (2014). Adolescent exposure to oxytocin, but not the selective oxytocin receptor agonist TGOT, increases social behavior and plasma oxytocin in adulthood. Horm. Behav. 65, 488–496. doi:10.1016/j.yhbeh.2014.03.002
114. Tobin, V. A., Hashimoto, H., Wacker, D. W., Takayanagi, Y., Langnaese, K., Caquineau, C., et al. (2010). An intrinsic vasopressin system in the olfactory bulb is involved in social recognition. Nature 464, 413–417. doi:10.1038/nature08826
115. Torvik, A. (1956). Afferent connections to the sensory trigeminal nuclei, the nucleus of the solitary tract and adjacent structures; an experimental study in the rat. J. Comp. Neurol. 106, 51–141. doi:10.1002/cne.901060104
116. Tribollet, E., Barberis, C., Jard, S., Dubois-Dauphin, M., and Dreifuss, J. J. (1988). Localization and pharmacological characterization of high affinity binding sites for vasopressin and oxytocin in the rat brain by light microscopic autoradiography. Brain Res. 442, 105–118. doi:10.1016/0006-8993(88)91437-0
117. Uvnas-Moberg, K., Ahlenius, S., Hillegaart, V., and Alster, P. (1994). High doses of oxytocin cause sedation and low doses cause an anxiolytic-like effect in male rats. Pharmacol. Biochem. Behav. 49, 101–106. doi:10.1016/0091-3057(94)90462-6
118. van Leeuwen, F. W., van Heerikhuize, J., van der Meulen, G., and Wolters, P. (1985). Light microscopic autoradiographic localization of [3H]oxytocin binding sites in the rat brain, pituitary and mammary gland. Brain Res. 359, 320–325. doi:10.1016/0006-8993(85)91443-X
119. Veenema, A. H., and Neumann, I. D. (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
120. Vela, C., Diaz-Cabiale, Z., Parrado, C., Narvaez, M., Covenas, R., and Narvaez, J. A. (2010). Involvement of oxytocin in the nucleus tractus solitarii on central cardiovascular control: interactions with glutamate. J. Physiol. Pharmacol. 61, 59–65
121. Williams, J. R., Carter, C. S., and Insel, T. (1992). Partner preference development in female prairie voles is facilitated by mating or the central infusion of oxytocin. Ann. N. Y. Acad. Sci. 652, 487–489. doi:10.1111/j.1749-6632.1992.tb34393.x
122. 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
123. Witt, D. M., Winslow, J. T., and Insel, T. R. (1992). Enhanced social interactions in rats following chronic, centrally infused oxytocin. Pharmacol. Biochem. Behav. 43, 855–861. doi:10.1016/0091-3057(92)90418-F
124. Yacoub, E., Shmuel, A., Logothetis, N., and Ugurbil, K. (2007). Robust detection of ocular dominance columns in humans using Hahn spin echo BOLD functional MRI at 7 Tesla. Neuroimage 37, 1161–1177. doi:10.1016/j.neuroimage.2007.05.020
125. Zhang, G., and Cai, D. (2011). Circadian intervention of obesity development via resting-stage feeding manipulation or oxytocin treatment. Am. J. Physiol. Endocrinol. Metab. 301, E1004–12. doi:10.1152/ajpendo.00196.2011
126. Zhang, N., Yacoub, E., Zhu, X. H., Ugurbil, K., and Chen, W. (2009). Linearity of blood-oxygenation-level dependent signal at microvasculature. Neuroimage 48, 313–318. doi:10.1016/j.neuroimage.2009.06.071