Oxytocin promotes functional coupling between paraventricular nucleus and both sympathetic and parasympathetic cardioregulatory nuclei

Hormones and Behavior

Volumn 80, Issue , 2016, Pages 82-91

  Yee, Jason R ^a,b   Kenkel, William M ^a,b   Frijling, Jessie L ^c   Dodhia, Sonam ^d   Onishi, Kenneth G ^e   Tovar, Santiago ^f   Saber, Maha J ^g   Lewis, Gregory F ^h   Liu, Wensheng ⁱ   Porges, Stephen W ^b,h   Carter, C Sue ^b  

^a NORTHEASTERN UNIVERSITY   (United States)

^b INDIANA UNIVERSITY   (United States)

^c UNIVERSITY OF AMSTERDAM   (Netherlands)

^d Columbia University ^*  (United States)

^e UNIVERSITY OF CHICAGO   (United States)

^f UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

^g CASE WESTERN RESERVE UNIVERSITY   (United States)

^h UNIVERSITY OF NORTH CAROLINA   (United States)

ⁱ NORTHWESTERN UNIVERSITY   (United States)

Author keywords

Brainstem; c Fos; Oxytocin; Paraventricular nucleus; Prairie vole; Stress

Indexed keywords

OXYTOCIN; PROTEIN C FOS;

ADULT; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CORTICOSTERONE BLOOD LEVEL; CORTICOSTERONE RELEASE; FEMALE; GROOMING; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; IMMUNOREACTIVITY; MALE; MICROTUS OCHROGASTER; NONHUMAN; OXYTOCIN BLOOD LEVEL; PARASYMPATHETIC FUNCTION; PARAVENTRICULAR THALAMIC NUCLEUS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; REARING; ROSTRAL VENTROLATERAL MEDULLA; SOCIAL BEHAVIOR; SYMPATHETIC FUNCTION; VAGUS NERVE DORSAL NUCLEUS; ADRENERGIC SYSTEM; ANIMAL; AROUSAL; ARVICOLINAE; CHOLINERGIC SYSTEM; HEART; HEART RATE; HYPOPHYSIS ADRENAL SYSTEM; HYPOTHALAMIC PARAVENTRICULAR NUCLEUS; HYPOTHALAMUS HYPOPHYSIS SYSTEM; INNERVATION; NERVE TRACT; PHYSIOLOGY; SYNAPTIC TRANSMISSION;

ANIMALS; AROUSAL; ARVICOLINAE; FEMALE; HEART; HEART RATE; HYPOTHALAMO-HYPOPHYSEAL SYSTEM; NEURAL PATHWAYS; OXYTOCIN; PARASYMPATHETIC NERVOUS SYSTEM; PARAVENTRICULAR HYPOTHALAMIC NUCLEUS; PITUITARY-ADRENAL SYSTEM; SYMPATHETIC NERVOUS SYSTEM; SYNAPTIC TRANSMISSION;

EID: 84958279440     PISSN: 0018506X     EISSN: 10956867     Source Type: Journal    
DOI: 10.1016/j.yhbeh.2016.01.010     Document Type: Article

References (78)

1. Allen Mouse Brain Atlas [Internet] Seattle (WA): Allen Institute for Brain Science. ©2009 2011, Available from: http://mouse.brain-map.org.
2. Amico J.A., Cai H.M., Vollmer R.R. Corticosterone release in oxytocin gene deletion mice following exposure to psychogenic versus non-psychogenic stress. Neurosci. Lett. 2008, 442:262-266.
3. Babygirija R., Yoshimoto S., Gribovskaja-Rupp I., Bülbül M., Ludwig K., Takahashi T. Social interaction attenuates stress responses following chronic stress in maternally separated rats. Brain Res. 2012, 1469:54-62. 10.1016/j.brainres.2012.06.007.
4. Bakermans-Kranenburg M.J., van IJzendoorn M.H. Sniffing around oxytocin: review and meta-analyses of trials in healthy and clinical groups with implications for pharmacotherapy. Transl. Psychiat. 2013, 3.
5. Baribeau D.A., Anagnostou E. Oxytocin and vasopressin: linking pituitary neuropeptides and their receptors to social neurocircuits. Front. Neurosci. 2015, 9:335. 10.3389/fnins.2015.00335.
6. Blume A., Bosch O.J., Miklos S., Torner L., Wales L., Waldherr M., Neumann I.D. Oxytocin reduces anxiety via ERK1/2 activation: local effect within the rat hypothalamic paraventricular nucleus. Eur. J. Neurosci. 2008, 27:1947-1956. 10.1111/j.1460-9568.2008.06184.x.
7. Bowen M.T., McGregor I.S. Oxytocin and vasopressin modulate the social response to threat: a preclinical study. Int. J. Neuropsychopharmacol. 2014, 17:1621-1633.
8. Bowen M.T., Kevin R.C., May M., Staples L.G., Hunt G.E., McGregor I.S. Defensive aggregation (huddling) in Rattus norvegicus toward predator odor: individual differences, social buffering effects and neural correlates. PLoS One 2013, 8.
9. Bülbül M., Babygirija R., Cerjak D., Yoshimoto S., Ludwig K., Takahashi T. Hypothalamic oxytocin attenuates CRF expression via GABA(A) receptors in rats. Brain Res. 2011, 1387:39-45. 10.1016/j.brainres.2011.02.091.
10. Carter C.S. Neuroendocrine perspectives on social attachment and love. Psychoneuroendocrinology 1998, 23:779-818.
11. Carter C.S. Oxytocin pathways and the evolution of human behavior. Annu. Rev. Psychol. 2014, 65:17-39.
12. Carter C.S., DeVries A.C., Getz L.L. Physiological substrates of mammalian monogamy: the prairie vole model. Neurosci. Biobehav. Rev. 1995, 19:303-314.
13. Carter C.S., Grippo A.J., Pournajafi-Nazarloo H., Ruscio M.G., Porges S.W. Oxytocin, vasopressin and sociality. Prog. Brain Res. 2008, 170:331-336.
14. Ceccatelli S., Villar M.J., Goldstein M., Hokfelt T. Expression of c-Fos immunoreactivity in transmitter-characterized neurons after stress. Proc. Natl. Acad. Sci. U. S. A. 1989, 86:9569-9573.
15. Cho M.M., DeVries A.C., Williams J.R., Carter C.S. The effects of oxytocin and vasopressin on partner preferences in male and female prairie voles (Microtus ochrogaster). Behav. Neurosci. 1999, 113:1071-1079.
16. Cullinan W.E., Herman J.P., Battaglia D.F., Akil H., Watson S.J. Pattern and time course of immediate early gene expression in rat brain following acute stress. Neuroscience 1995, 64:477-505.
17. DeVries A.C., DeVries M.B., Taymans S., Carter C.S. Modulation of pair bonding in female prairie voles (Microtus ochrogaster) by corticosterone. Proc. Natl. Acad. Sci. U. S. A. 1995, 92:7744-7748.
18. DeVries A.C., DeVries M.B., Taymans S.E., Carter C.S. The effects of stress on social preferences are sexually dimorphic in prairie voles. Proc. Natl. Acad. Sci. U. S. A. 1996, 93:11980-11984.
19. Engelmann M., Wotjak C.T., Neumann I., Ludwig M., Landgraf R. Behavioral consequences of intracerebral vasopressin and oxytocin: focus on learning and memory. Neurosci. Biobehav. Rev. 1996, 20:341-358.
20. Falke N. Oxytocin stimulates oxytocin release from isolated nerve terminals of rat neural lobes. Neuropeptides 1989, 14:269-274.
21. Ferguson M.L., Katkin E.S. Visceral perception, anhedonia, and emotion. Biol. Psychol. 1996, 42:131-145.
22. Ferguson A.V., Donevan S.D., Papas S., Smith P.M. Circumventricular structures: CNS sensors of circulating peptides and autonomic control centres. Endocrinol. Exp. 1990, 24:19-27.
23. Ferris C.F., Yee J.R., Kenkel W.M., Dumais K.M., Moore K., Veenema A.H., Kulkarni P., Perkybile A.M., Carter C.S. Distinct BOLD activation profiles following central and peripheral oxytocin administration in awake rats. Front. Behav. Neurosci. 2015, 9:245. 10.3389/fnbeh.2015.00245.
24. Geerling J.C., Shin J.-W., Chimenti P.C., Loewy A.D. Paraventricular hypothalamic nucleus: axonal projections to the brainstem. J. Comp. Neurol. 2010, 518:1460-1499. 10.1002/cne.22283.
25. Gibbs D.M. Immunoneutralization of oxytocin attenuates stress-induced corticotropin secretion in the rat. Regul. Pept. 1985, 12:273-277.
26. Gibbs D.M., Vale W., Rivier J., Yen S.S. Oxytocin potentiates the ACTH-releasing activity of CRF(41) but not vasopressin. Life Sci. 1984, 34:2245-2249.
27. Goehler L.E., Gaykema R.P., Nguyen K.T., Lee J.E., Tilders F.J., Maier S.F., Watkins L.R. Interleukin-1beta in immune cells of the abdominal vagus nerve: a link between the immune and nervous systems?. J. Neurosci. 1999, 19:2799-2806.
28. Gordon I., Zagoory-Sharon O., Schneiderman I., Leckman J.F., Weller A., Feldman R. Oxytocin and cortisol in romantically unattached young adults: associations with bonding and psychological distress. Psychophysiology 2008, 45:349-352.
29. Grabowska-Zhang A.M., Sheldon B.C., Hinde C.A. Long-term familiarity promotes joining in neighbour nest defence. Biol. Lett. 2012, 8:544-546.
30. Griffiths S.W., Brockmark S., Hojesjo J., Johnsson J.I. Coping with divided attention: the advantage of familiarity. Proceedings. Biol. Sci./R. Soc. 2004, 271:695-699.
31. Grippo A.J., Gerena D., Huang J., Kumar N., Shah M., Ughreja R., Carter C.S. Social isolation induces behavioral and neuroendocrine disturbances relevant to depression in female and male prairie voles. Psychoneuroendocrinology 2007, 32:966-980. 10.1016/j.psyneuen.2007.07.004.
32. Grippo A.J., Lamb D.G., Carter C.S., Porges S.W. Cardiac regulation in the socially monogamous prairie vole. Physiol. Behav. 2007, 90:386-393.
33. Grippo A.J., Trahanas D.M., Zimmerman R.R., Porges S.W., Carter C.S. Oxytocin protects against negative behavioral and autonomic consequences of long-term social isolation. Psychoneuroendocrinology 2009, 34:1542-1553.
34. Grippo A.J., Pournajafi-Nazarloo H., Sanzenbacher L., Trahanas D.M., McNeal N., Clarke D.A., Porges S.W., Sue Carter C. Peripheral oxytocin administration buffers autonomic but not behavioral responses to environmental stressors in isolated prairie voles. Stress 2011, 15(2). 10.3109/10253890.2011.605486.
35. Gutkowska J., Jankowski M. Oxytocin re-visited: its role in cardiovascular regulation. J. Neuroendocrinol. 2011.
36. Harris J.C., Carter C.S. Therapeutic interventions with oxytocin: current status and concerns. J. Am. Acad. Child Adolesc. Psychiatry 2013, 52:998-1000.
37. Heinrichs M., Baumgartner T., Kirschbaum C., Ehlert U. Social support and oxytocin interact to suppress cortisol and subjective responses to psychosocial stress. Biol. Psychiatry 2003, 54:1389-1398.
38. Herman J.P., Prewitt C.M., Cullinan W.E. Neuronal circuit regulation of the hypothalamo-pituitary-adrenocortical stress axis. Crit. Rev. Neurobiol. 1996, 10:371-394.
39. Hong W., Kennedy A., Burgos-Artizzu X.P., Zelikowsky M., Navonne S.G., Perona P., Anderson D.J. Automated measurement of mouse social behaviors using depth sensing, video tracking, and machine learning. Proc. Natl. Acad. Sci. U. S. A. 2015, 112:E5351-E5360. 10.1073/pnas.1515982112.
40. Insel T.R., Winslow J.T., Wang Z., Young L.J. Oxytocin, vasopressin, and the neuroendocrine basis of pair bond formation. Adv. Exp. Med. Biol. 1998, 449:215-224.
41. Jong T.R.de, Menon R., Bludau A., Grund T., Biermeier V., Klampfl S.M., Jurek B., Bosch O.J., Hellhammer J., Neumann I.D. Salivary oxytocin concentrations in response to running, sexual self-stimulation, breastfeeding and the TSST: the Regensburg Oxytocin Challenge (ROC) study. Psychoneuroendocrinology 2015, 62:381-388. 10.1016/j.psyneuen.2015.08.027.
42. Jurek B., Slattery D.A., Hiraoka Y., Liu Y., Nishimori K., Aguilera G., Neumann I.D., van den Burg E.H. Oxytocin regulates stress-induced crf gene transcription through CREB-regulated transcription coactivator 3. J. Neurosci. 2015, 35:12248-12260. 10.1523/JNEUROSCI.1345-14.2015.
43. Kelly A.M., Goodson J.L. Social functions of individual vasopressin-oxytocin cell groups in vertebrates: what do we really know?. Front. Neuroendocrinol. 2014, 35:512-529. 10.1016/j.yfrne.2014.04.005.
44. Kenkel W.M., Paredes J., Yee J.R., Pournajafi-Nazarloo H., Bales K.L., Carter C.S. Neuroendocrine and behavioural responses to exposure to an infant in male prairie voles. J. Neuroendocrinol. 2012, 24:874-886.
45. Kenkel W.M., Suboc G., Sue Carter C. Autonomic, behavioral and neuroendocrine correlates of paternal behavior in male prairie voles. Physiol. Behav. 2014, 128:252-259.
46. Kojima S., Alberts J.R. Oxytocin mediates the acquisition of filial, odor-guided huddling for maternally-associated odor in preweanling rats. Horm. Behav. 2011, 60:549-558.
47. Komisaruk B.R., Sansone G. Neural pathways mediating vaginal function: the vagus nerves and spinal cord oxytocin. Scand. J. Psychol. 2003, 44:241-250.
48. Lieberwirth C., Wang Z. Social bonding: regulation by neuropeptides. Front. Neurosci. 2014, 8. 10.3389/fnins.2014.00171.
49. Macdonald K., Feifel D. Helping oxytocin deliver: considerations in the development of oxytocin-based therapeutics for brain disorders. Front. Neurosci. 2013, 7:35.
50. Maolood N., Meister B. Protein components of the blood-brain barrier (BBB) in the brainstem area postrema-nucleus tractus solitarius region. J. Chem. Neuroanat. 2009, 37:182-195.
51. Moos F., Freund-Mercier M.J., Guerne Y., Guerne J.M., Stoeckel M.E., Richard P. Release of oxytocin and vasopressin by magnocellular nuclei in vitro: specific facilitatory effect of oxytocin on its own release. J. Endocrinol. 1984, 102:63-72.
52. Norman G.J., Cacioppo J.T., Morris J.S., Malarkey W.B., Berntson G.G., Devries A.C. Oxytocin increases autonomic cardiac control: moderation by loneliness. Biol. Psychol. 2011, 86:174-180.
53. Ohayon S., Avni O., Taylor A.L., Perona P., Roian Egnor S.E. Automated multi-day tracking of marked mice for the analysis of social behaviour. J. Neurosci. Methods 2013, 219:10-19. 10.1016/j.jneumeth.2013.05.013.
54. Pacak K., Palkovits M. Stressor specificity of central neuroendocrine responses: implications for stress-related disorders. Endocr. Rev. 2001, 22:502-548.
55. Perry A., Mankuta D., Shamay-Tsoory S.G. OT promotes closer interpersonal distance among highly empathic individuals. Soc. Cogn. Affect. Neurosci. 2014, 10(1):3-9. (Epub 2014 Feb 7). 10.1093/scan/nsu017.
56. Petersson M., Hulting A.L., Uvnas-Moberg K. Oxytocin causes a sustained decrease in plasma levels of corticosterone in rats. Neurosci. Lett. 1999, 264:41-44.
57. Piñol R.A., Bateman R., Mendelowitz D. Optogenetic approaches to characterize the long-range synaptic pathways from the hypothalamus to brain stem autonomic nuclei. J. Neurosci. Methods 2012, 210:238-246.
58. Piñol R.A., Jameson H., Popratiloff A., Lee N.H., Mendelowitz D. Visualization of oxytocin release that mediates paired pulse facilitation in hypothalamic pathways to brainstem autonomic neurons. PLoS One 2014, 9. 10.1371/journal.pone.0112138.
59. Porges S.W. Social engagement and attachment: a phylogenetic perspective. Ann. N. Y. Acad. Sci. 2003, 1008:31-47.
60. Rudinger J., Kesarev O.V., Poduska K., Pickering B.T., Dyball R.E., Ferguson D.R., Ward W.R. (4-proline, 8-isoleucine)-oxytocin and (4-leucine, 8-isoleucine)-oxytocin, possible intermediates in the evolutionary series of neurophypophysial hormones: synthesis and some pharmacological properties. Experientia 1969, 25:680-682.
61. Ruscio M.G., Sweeny T., Hazelton J., Suppatkul P., Carter C.S. Social environment regulates corticotropin releasing factor, corticosterone and vasopressin in juvenile prairie voles. Horm. Behav. 2007, 51:54-61.
62. Seyfarth R.M., Cheney D.L. The evolutionary origins of friendship. Annu Rev Psychol 2012, 153-177. S.T. Fiske, D.L. Schacter, S.E. Taylor (Eds.).
63. Silk J.B., House B.R. Evolutionary foundations of human prosocial sentiments. Proc. Natl. Acad. Sci. U. S. A. 2011, 108(Suppl. 2):10910-10917.
64. Silk J.B., Alberts S.C., Altman J. Social bonds of female baboons enhance infant survival. Science 2003, 302:1231-1234.
65. Smith A.S., Wang Z. Hypothalamic oxytocin mediates social buffering of the stress response. Biol. Psychiatry 2014, 76:281-288.
66. Smith A.S., Agmo A., Birnie A.K., French J.A. Manipulation of the oxytocin system alters social behavior and attraction in pair-bonding primates, Callithrix penicillata. Horm. Behav. 2010, 57:255-262.
67. Smith A.S., Tabbaa M., Lei K., Eastham P., Butler M.J., Linton L., Altshuler R., Liu Y., Wang Z. Local oxytocin tempers anxiety by activating GABAA receptors in the hypothalamic paraventricular nucleus. Psychoneuroendocrinology 2015, 63:50-58. 10.1016/j.psyneuen.2015.09.017.
68. Stoesz B.M., Hare J.F., Snow W.M. Neurophysiological mechanisms underlying affiliative social behavior: insights from comparative research. Neurosci. Biobehav. Rev. 2013, 37:123-132. 10.1016/j.neubiorev.2012.11.007.
69. Swanson L.W., Sawchenko P.E. Paraventricular nucleus: a site for the integration of neuroendocrine and autonomic mechanisms. Neuroendocrinology 1980, 31:410-417.
70. Tops M., Koole S.L., IJzerman H., Buisman-Pijlman F.T.A. Why social attachment and oxytocin protect against addiction and stress: insights from the dynamics between ventral and dorsal corticostriatal systems. Pharmacol. Biochem. Behav. 2014, 119:39-48.
71. Vivas L., Godino A., Dalmasso C., Caeiro X.E., Macchione A.F., Cambiasso M.J. Neurochemical circuits subserving fluid balance and baroreflex: a role for serotonin, oxytocin, and gonadal steroids. Neurobiology of Body Fluid Homeostasis: Transduction and Integration, Boca Raton (FL) 2014, L.A. De Luca, J.V. Menani, A.K. Johnson (Eds.).
72. Williams J.R., Catania K.C., Carter C.S. Development of partner preferences in female prairie voles (Microtus ochrogaster): the role of social and sexual experience. Horm. Behav. 1992, 26:339-349.
73. Williams J.R., Insel T.R., Harbaugh C.R., Carter C.S. Oxytocin administered centrally facilitates formation of a partner preference in female prairie voles (Microtus ochrogaster). J. Neuroendocrinol. 1994, 6:247-250.
74. Windle R.J., Shanks N., Lightman S.L., Ingram C.D. Central oxytocin administration reduces stress-induced corticosterone release and anxiety behavior in rats. Endocrinology 1997, 138:2829-2834.
75. Windle R.J., Kershaw Y.M., Shanks N., Wood S.A., Lightman S.L., Ingram C.D. Oxytocin attenuates stress-induced c-fos mRNA expression in specific forebrain regions associated with modulation of hypothalamo-pituitary-adrenal activity. J. Neurosci. 2004, 24:2974-2982.
76. Winslow J.T., Shapiro L., Carter C.S., Insel T.R. Oxytocin and complex social behavior: species comparisons. Psychopharmacol. Bull. 1993, 29:409-414.
77. Witt D.M., Carter C.S., Walton D.M. Central and peripheral effects of oxytocin administration in prairie voles (Microtus ochrogaster). Pharmacol. Biochem. Behav. 1990, 37:63-69.
78. Zheng J., Babygirija R., Bülbül M., Cerjak D., Ludwig K., Takahashi T. Hypothalamic oxytocin mediates adaptation mechanism against chronic stress in rats. Am. J. Physiol. Gastrointest. Liver Physiol. 2010, 299:G946-G953. 10.1152/ajpgi.00483.2009.