A role for autonomic cardiac control in the effects of oxytocin on social behavior and psychiatric illness

Frontiers in Neuroscience

Volumn , Issue 7 APR, 2013, Pages

  Quintana, Daniel S ^a   Kemp, Andrew H ^a   Alvares, Gail A ^a   Guastella, Adam J ^a  

^a UNIVERSITY OF SYDNEY   (Australia)

Author keywords

Autonomic nervous system; Heart rate variability; Oxytocin; Social behavior; Social cognition

Indexed keywords

OXYTOCIN; OXYTOCIN RECEPTOR;

AUTONOMIC CARDIAC CONTROL; AUTONOMIC NERVOUS SYSTEM FUNCTION; CARDIOVASCULAR SYSTEM; DRUG EFFECT; ELECTROCARDIOGRAM; EMOTION; HEART FUNCTION; HEART RATE VARIABILITY; HUMAN; MENTAL DISEASE; NONHUMAN; REVIEW; SOCIAL BEHAVIOR; SOCIAL INTERACTION; SURVIVAL;

EID: 84878900942     PISSN: 16624548     EISSN: 1662453X     Source Type: Journal    
DOI: 10.3389/fnins.2013.00048     Document Type: Review

References (116)

1. Allen, M. T., Matthews, K. A., and Kenyon, K. L. (2000). The relationships of resting baroreflex sensitivity, heart rate variability and measures of impulse control in children and adolescents. Int. J. Psychophysiol. 37, 185-194.
2. 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.
3. Averbeck, B. B., Bobin, T., Evans, S., and Shergill, S. S. (2012). Emotion recognition and oxytocin in patients with schizophrenia. Psychol. Med. 42, 259-266.
4. Bahadur, S., and Pathak, K. (2012). Physicochemical and physiological considerations for efficient nose-to-brain targeting. Expert Opin. Drug Deliv. 9, 19-31.
5. Bal, E., Harden, E., Lamb, D., Van Hecke, A. V., Denver, J. W., and Porges, S. W. (2010). Emotion recognition in children with autism spectrum disorders: relations to eye gaze and autonomic state. J. Autism Dev. Disord. 40, 358-370.
6. Baron-Cohen, S., Wheelwright, S., Hill, J., Raste, Y., and Plumb, I. (2001). The "Reading the Mind in the Eyes" Test revised version: a study with normal adults, and adults with Asperger syndrome or high-functioning autism. J. Child Psychol. Psychiatry 42, 241-251.
7. Bartz, J., Simeon, D., Hamilton, H., Kim, S., Crystal, S., Braun, A., et al. (2011a). Oxytocin can hinder trust and cooperation in borderline personality disorder. Soc. Cogn. Affect. Neurosci. 6, 556-563.
8. Bartz, J. A., Zaki, J., Bolger, N., and Ochsner, K. N. (2011b). Social effects of oxytocin in humans: context and person matter. Trends Cogn. Sci. 15, 301-309.
9. Berntson, G. G., Bigger, J. T., Eckberg, D. L., Grossman, P., Kaufmann, P. G., Malik, M., et al. (1997). Heart rate variability: origins, methods, and interpretive caveats. Psychophysiology 34, 623-648.
10. Berntson, G. G., Cacioppo, J. T., and Quigley, K. S. (1991). Autonomic determinism: the modes of autonomic control, the doctrine of autonomic space, and the laws of autonomic constraint. Psychol. Rev. 98, 459-487.
11. Bijleveld, E., Custers, R., and Aarts, H. (2009). The unconscious eye opener: pupil dilation reveals strategic recruitment of resources upon presentation of subliminal reward cues. Psychol. Sci. 20, 1313-1315.
12. Born, J., Lange, T., Kern, W., McGregor, G. P., Bickel, U., and Fehm, H. L. (2002). Sniffing neuropeptides: a transnasal approach to the human brain. Nat. Neurosci. 5, 514-516.
13. Buijs, R. M., Swaab, D. F., Dogterom, J., and van Leeuwen, F. W. (1978). Intra- and extrahypothalamic vasopressin and oxytocin pathways in the rat. Cell Tissue Res. 186, 423-433.
14. Butler, E. A., Egloff, B., Wlhelm, F. H., Smith, N. C., Erickson, E. A., and Gross, J. J. (2003). The social consequences of expressive suppression. Emotion 3, 48.
15. Butler, E. A., Wilhelm, F. H., and Gross, J. J. (2006). Respiratory sinus arrhythmia, emotion, and emotion regulation during social interaction. Psychophysiology 43, 612-622.
16. Cannon, W. B. (1939). The Wisdom of the Body. New York, NY: Norton.
17. Chen, F. S., Kumsta, R., and Heinrichs, M. (2011). Oxytocin and intergroup relations: Goodwill is not a fixed pie. Proc. Natl. Acad. Sci. U.S.A. 108:E45. doi: 10.1073/pnas.1101633108
18. Colton, C. W., and Manderscheid, R. W. (2006). Congruencies in increased mortality rates, years of potential life lost, and causes of death among public mental health clients in eight states. Prev. Chronic Dis. 3, A42.
19. De Dreu, C. K. W. (2012). Oxytocin modulates cooperation within and competition between groups: an integrative review and research agenda. Horm. Behav. 61, 419-428.
20. De Dreu, C. K. W., Greer, L. L., Van Kleef, G. A., Shalvi, S., and Handgraaf, M. J. J. (2011). Oxytocin promotes human ethnocentrism. Proc. Natl. Acad. Sci. U.S.A. 108, 1262-1266.
21. Declerck, C. H., Boone, C., and Kiyonari, T. (2010). Oxytocin and cooperation under conditions of uncertainty: The modulating role of incentives and social information. Horm. Behav. 57, 368-374.
22. Diamond, L. M., and Cribbet, M. R. (2012). Links between adolescent sympathetic and parasympathetic nervous system functioning and interpersonal behavior over time. Int. J. Psychophysiol. doi: 10.1016/j.ijpsycho.2012.08.008. [Epub ahead of print].
23. Diamond, L. M., and Hicks, A. M. (2005). Attachment style, current relationship security, and negative emotions: the mediating role of physiological regulation. J. Soc. Pers. Relat. 22, 499-518.
24. Diamond, L. M., Hicks, A. M., and Otter-Henderson, K. D. (2011). Individual differences in vagal regulation moderate associations between daily affect and daily couple interactions. Pers. Soc. Psychol. Bull. 37, 731-744.
25. Djupesland, P. G. (2013). Nasal drug delivery devices: characteristics and performance in a clinical perspective-a review. Drug Deliv. Transl. Res. 3, 42-62.
26. Domes, G., Heinrichs, M., Michel, A., Berger, C., and Herpertz, S. C. (2007a). Oxytocin improves "mind-reading" in humans. Biol. Psychiatry 61, 731-733.
27. Domes, G., Heinrichs, M., Gläscher, J., Büchel, C., Braus, D. F., and Herpertz, S. C. (2007b). Oxytocin attenuates amygdala responses to emotional faces regardless of valence. Biol. Psychiatry 62, 1187-1190.
28. Fries, A. B. W., Ziegler, T. E., Kurian, J. R., Jacoris, S., and Pollak, S. D. (2005). Early experience in humans is associated with changes in neuropeptides critical for regulating social behavior. Proc. Natl. Acad. Sci. U.S.A. 102, 17237-17240.
29. Gamer, M., Zurowski, B., and Buchel, C. (2010). Different amygdala subregions mediate valence-related and attentional effects of oxytocin in humans. Proc. Natl. Acad. Sci. U.S.A. 107, 9400-9405.
30. Goodwin, R. D., Davidson, K. W., and Keyes, K. (2009). Mental disorders and cardiovascular disease among adults in the United States. J. Psychiatr. Res. 43, 239-246.
31. Green, M. F., Penn, D. L., Bentall, R., Carpenter, W. T., Gaebel, W., Gur, R. C., et al. (2008). Social cognition in schizophrenia: an NIMH workshop on definitions, assessment, and research opportunities. Schizophr. Bull. 34, 1211-1220.
32. Grippo, A. J., Trahanas, D. M., Zimmerman, R. R., Porges, S. W., and Carter, C. S. (2009). Oxytocin protects against negative behavioral and autonomic consequences of long-term social isolation. Psychoneuroendocrinology 34, 1542-1553.
33. 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.
34. Guastella, A. J., Hickie, I. B., McGuinness, M. M., Otis, M., Woods, E. A., Disinger, H. M., et al. (2012). Recommendations for the standardisation of oxytocin nasal administration and guidelines for its reporting in human research. Psychoneuroendocrinology. doi: 10.1016/j.psyneuen.2012.11.019. [Epub ahead of print].
35. Guastella, A. J., Howard, A. L., Dadds, M. R., Mitchell, P., and Carson, D. S. (2009). A randomized controlled trial of intranasal oxytocin as an adjunct to exposure therapy for social anxiety disorder. Psychoneuroendocrinology 34, 917-923.
36. Guastella, A. J., and MacLeod, C. (2012). A critical review of the influence of oxytocin nasal spray on social cognition in humans: evidence and future directions. Horm. Behav. 61, 410-418.
37. Guastella, A. J., Mitchell, P. B., and Dadds, M. R. (2008). Oxytocin increases gaze to the eye region of human faces. Biol. Psychiatry 63, 3-5.
38. Gutkowska, J., Jankowski, M., Lambert, C., Mukaddam-Daher, S., Zingg, H. H., and McCann, S. M. (1997). Oxytocin releases atrial natriuretic peptide by combining with oxytocin receptors in the heart. Proc. Natl. Acad. Sci. U.S.A. 94, 11704-11709.
39. Gutkowska, J., Jankowski, M., Mukaddam-Daher, S., and McCann, S. (2000). Oxytocin is a cardiovascular hormone. Braz. J. Med. Biol. Res. 33, 625-633.
40. Gutkowska, J., Paquette, A., Wang, D., Lavoie, J. M., and Jankowski, M. (2007). Effect of exercise training on cardiac oxytocin and natriuretic peptide systems in ovariectomized rats. Am. J. Physiol. Regul. Integr. Comp. Physiol. 293, R267-R275.
41. Herpertz, S. C., Mueller, B., Qunaibi, M., Lichterfeld, C., Konrad, K., and Herpertz-Dahlmann, B. (2005). Response to emotional stimuli in boys with conduct disorder. Am. J. Psychiatry 162, 1100-1107.
42. 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.
43. Holst, S., Uvnäs-Moberg, K., and Petersson, M. (2002). Postnatal oxytocin treatment and postnatal stroking of rats reduce blood pressure in adulthood. Auton. Neurosci. 99, 85-90.
44. Holt-Lunstad, J., Uchino, B. N., Smith, T. W., and Hicks, A. (2007). On the importance of relationship quality: the impact of ambivalence in friendships on cardiovascular functioning. Ann. Behav. Med. 33, 278-290.
45. Jankowski, M., Hajjar, F., Kawas, S. A., Mukaddam-Daher, S., Hoffman, G., McCann, S. M., et al. (1998). Rat heart: a site of oxytocin production and action. Proc. Natl. Acad. Sci. U.S.A. 95, 14558.
46. Jelinski, M., Hamacher, K., and Coenen, H. H. (2002). C-Terminal18F-fluoroethylamidation exemplified on [Gly-OH9] oxytocin. J. Labelled Comp. Radiopharm. 45, 217-229.
47. Jindal, R. D., Keshavan, M. S., Eklund, K., Stevens, A., Montrose, D. M., and Yeragani, V. K. (2009). Beat-to-beat heart rate and QT interval variability in first episode neuroleptic-naive psychosis. Schizophr. Res. 113, 176-180.
48. Kemp, A. H., and Guastella, A. J. (2011). The role of oxytocin in human affect: a novel hypothesis. Curr. Dir. Psychol. Sci. 20, 222-231.
49. Kemp, A. H., Quintana, D., Kuhnert, R.-L., Griffiths, K., Hickie, I. B., and Guastella, A. J. (2012a). Oxytocin increases heart rate variability in humans at rest: implications for social approach-related motivation and capacity for social engagement. PLoS ONE 7:e44014. doi: 10.1371/journal.pone.0044014
50. Kemp, A. H., Quintana, D., Felmingham, K. L., Matthews, S., and Jelinek, H. F. (2012b). Depression, Comorbid Anxiety Disorders, and Heart Rate Variability in Physically Healthy, Unmedicated Patients: Implications for Cardiovascular Risk. PLoS ONE 7:e30777. doi: 10.1371/journal.pone.0030777
51. Kemp, A. H., Quintana, D., Gray, M. A., Felmingham, K. L., Brown, K., and Gatt, J. M. (2010). Impact of depression and antidepressant treatment on heart rate variability: a review and meta-analysis. Biol. Psychiatry 67, 1067-1074.
52. Kéri, S., Kiss, I., and Kelemen, O. (2009). Sharing secrets: oxytocin and trust in schizophrenia. Soc. Neurosci. 4, 287-293.
53. Kettunen, J., Ravaja, N., Näätänen, P., and Keltikangas-Järvinen, L. (2000). The relationship of respiratory sinus arrhythmia to the co-activation of autonomic and facial responses during the Rorschach test. Psychophysiology 37, 242-250.
54. Kirsch, P., Esslinger, C., Chen, Q., Mier, D., Lis, S., Siddhanti, S., et al. (2005). Oxytocin modulates neural circuitry for social cognition and fear in humans. J. Neurosci. 25, 11489-11493.
55. Koizumi, K., and Kollai, M. (1981). Control of reciprocal and non-reciprocal action of vagal and sympathetic efferents: study of centrally induced reactions. J. Auton. Nerv. Syst. 3, 483-501.
56. Kok, B. E., and Fredrickson, B. L. (2010). Upward spirals of the heart: autonomic flexibility, as indexed by vagal tone, reciprocally and prospectively predicts positive emotions and social connectedness. Biol. Psychol. 85, 432-436.
57. Kollai, M., and Koizumi, K. (1979). Reciprocal and non-reciprocal action of the vagal and sympathetic nerves innervating the heart. J. Auton. Nerv. Syst. 1, 33-52.
58. Kosfeld, M., Heinrichs, M., Zak, P. J., Fischbacher, U., and Fehr, E. (2005). Oxytocin increases trust in humans. Nature 435, 673-676.
59. Kubzansky, L. D., Mendes, W. B., Appleton, A. A., Block, J., and Adler, G. K. (2012). A heartfelt response: oxytocin effects on response to social stress in men and women. Biol. Psychol. 90, 1-9.
60. Labuschagne, I., Phan, K. L., Wood, A., Angstadt, M., Chua, P., Heinrichs, M., et al. (2010). Oxytocin attenuates amygdala reactivity to fear in generalized social anxiety disorder. Neuropsychopharmacology 35, 2403-2413.
61. Laeng, B., and Falkenberg, L. (2007). Women's pupillary responses to sexually significant others during the hormonal cycle. Horm. Behav. 52, 520-530.
62. 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
63. Lang, P. J., Greenwald, M. K., Bradley, M. M., and Hamm, A. O. (1993). Looking at pictures: affective, facial, visceral, and behavioral reactions. Psychophysiology 30, 261-273.
64. Langley, J. N. (1921). The Autonomic Nervous System. Cambridge, England: Heffer and Sons.
65. Leknes, S., Wessberg, J., Ellingsen, D. M., Chelnokova, O., Olausson, H., and Laeng, B. (2012). Oxytocin enhances pupil dilation and sensitivity to "hidden" emotional expressions. Soc. Cogn. Affect. Neurosci. doi:10.1093/scan/nss062. [Epub ahead of print].
66. Liu, Q., Shen, Y., Chen, J., Gao, X., Feng, C., Wang, L., et al. (2012). Nose-to-brain transport pathways of wheat germ agglutinin conjugated peg-pla nanoparticles. Pharm. Res. 29, 546-558.
67. Mack, S. O., Kc, P., Wu, M., Coleman, B. R., Tolentino-Silva, F. P., and Haxhiu, M. A. (2002). Paraventricular oxytocin neurons are involved in neural modulation of breathing. J. Appl. Physiol. 92, 826-834.
68. Marsh, P., Beauchaine, T. P., and Williams, B. (2008). Dissociation of sad facial expressions and autonomic nervous system responding in boys with disruptive behavior disorders. Psychophysiology 45, 100-110.
69. Ming, X., Julu, P. O. O., Brimacombe, M., Connor, S., and Daniels, M. L. (2005). Reduced cardiac parasympathetic activity in children with autism. Brain Dev. 27, 509-516.
70. Modahl, C., Green, L., Fein, D., Morris, M., Waterhouse, L., Feinstein, C., et al. (1998). Plasma oxytocin levels in autistic children. Biol. Psychiatry 43, 270-277.
71. Morris, M., Callahan, M. F., Li, P., and Lucion, A. B. (1995). Central oxytocin mediates stress-induced tachycardia. J. Neuroendocrinol. 7, 455-459.
72. Movius, H. L., and Allen, J. J. B. (2005). Cardiac Vagal Tone, defensiveness, and motivational style. Biol. Psychol. 68, 147-162.
73. Mujica-Parodi, L. R., Yeragani, V., and Malaspina, D. (2005). Nonlinear complexity and spectral analyses of heart rate variability in medicated and unmedicated patients with schizophrenia. Neuropsychobiology 51, 10-15.
74. Mukaddam-Daher, S., Yin, Y. L., Roy, J., Gutkowska, J., and Cardinal, R. (2001). Negative inotropic and chronotropic effects of oxytocin. Hypertension 38, 292-296.
75. Nageotte, J. (1906). The pars intermedia of nervus intermedius of Wrisberg, and the bulbopontine gustatory nucleus in man. Rev. Neurol. Psychiatr. (Edinburgh) 4, 473-488.
76. Norman, G. J., Cacioppo, J. T., Morris, J. S., Malarkey, W. B., Berntson, G. G., and DeVries, A. C. (2011). Oxytocin increases autonomic cardiac control: moderation by loneliness. Biol. Psychol. 86, 174-180.
77. Paton, J. F. R., Boscan, P., Pickering, A. E., and Nalivaiko, E. (2005). The yin and yang of cardiac autonomic control: vago-sympathetic interactions revisited. Brain Res. Rev. 49, 555-565.
78. Pearson, A. A. (1947). The roots of the facial nerve in the human embryos and fetuses. J. Comp. Neurol. 87, 139-159.
79. Pedersen, C. A., Gibson, C. M., Rau, S. W., Salimi, K., Smedley, K. L., Casey, R. L., et al. (2011). Intranasal oxytocin reduces psychotic symptoms and improves Theory of Mind and social perception in schizophrenia. Schizophr. Res. 132, 50-53.
80. Petersson, M., Alster, P., Lundeberg, T., and Uvnäs-Moberg, K. (1996). Oxytocin causes a long-term decrease of blood pressure in female and male rats. Physiol. Behav. 60, 1311-1315.
81. Petersson, M., and Uvnäs-Moberg, K. (2008). Postnatal oxytocin treatment of spontaneously hypertensive male rats decreases blood pressure and body weight in adulthood. Neurosci. Lett. 440, 166-169.
82. Petty, M. A., Lang, R. E., Unger, T., and Ganten, D. (1985). The cardiovascular effects of oxytocin in conscious male rats. Eur. J. Pharmacol. 112, 203-210.
83. Porges, S. (2003). Social engagement and attachment: a phylogenetic perspective. Ann. N.Y. Acad. Sci. 1008, 31-47.
84. Porges, S. W. (1998). Love: an emergent property of the mammalian autonomic nervous system. Psychoneuroendocrinology 23, 837-861.
85. Porges, S. W. (2001). The polyvagal theory: phylogenetic substrates of a social nervous system. Int. J. Psychophysiol. 42, 123-146.
86. Porges, S. W. (2007). A phylogenetic journey through the vague and ambiguous Xth cranial nerve: a commentary on contemporary heart rate variability research. Biol. Psychol. 74, 301-307.
87. Porges, S. W. (2011). The Polyvagal Theory: Neurophysiological Foundations of Emotions, Attachment, Communication, and Self-Regulation. New York, NY: W. W. Norton and Company.
88. Quintana, D. S., Guastella, A. J., McGregor, I. S., Hickie, I. B., and Kemp, A. H. (in press). Heart rate variability predicts alcohol craving in alcohol dependent outpatients: further evidence for HRV as a psychophysiological marker of self-regulation. Drug Alcohol Depend.
89. Quintana, D. S., Guastella, A. J., Outhred, T., Hickie, I. B., and Kemp, A. H. (2012). Heart rate variability is associated with emotion recognition: direct evidence for a relationship between the autonomic nervous system and social cognition. Int. J. Psychophysiol. 86, 168-172.
90. Quintana, D. S., McGregor, I. S., Guastella, A. J., Malhi, G. S., and Kemp, A. H. (2013). A meta-analysis on the impact of alcohol dependence on short-term resting-state heart rate variability: implications for cardiovascular risk. Alcohol Clin. Exp. Res. 37, E23-E29.
91. Ross, C. A., Ruggiero, D. A., Park, D. H., Joh, T. H., Sved, A. F., Fernandez-Pardal, J., et al. (1984). Tonic vasomotor control by the rostral ventrolateral medulla: effect of electrical or chemical stimulation of the area containing C1 adrenaline neurons on arterial pressure, heart rate, and plasma catecholamines and vasopressin. J. Neurosci. 4, 474-494.
92. Sartain, J. B., Barry, J. J., Howat, P. W., McCormack, D. I., and Bryant, M. (2008). Intravenous oxytocin bolus of 2 units is superior to 5 units during elective Caesarean section. Br. J. Anaesth. 101, 822-826.
93. Savaskan, E., Ehrhardt, R., Schulz, A., Walter, M., and Schächinger, H. (2008). Post-learning intranasal oxytocin modulates human memory for facial identity. Psychoneuroendocrinology 33, 368-374.
94. Scheele, D., Striepens, N., Gunturkun, O., Deutschlander, S., Maier, W., Kendrick, K. M., et al. (2012). Oxytocin modulates social distance between males and females. J. Neurosci. 32, 16074-16079.
95. Segerstrom, S. C., and Nes, L. S. (2007). Heart rate variability reflects self-regulatory strength, effort, and fatigue. Psychol. Sci. 18, 275-281.
96. Shamay-Tsoory, S. G. (2010). One hormonal system for love and envy: a reply to tops. Biol. Psychiatry, 67, e7.
97. Simeon, D., Bartz, J., Hamilton, H., Crystal, S., Braun, A., Ketay, S., et al. (2011). Oxytocin administration attenuates stress reactivity in borderline personality disorder: a pilot study. Psychoneuroendocrinology 36, 1418-1421.
98. Simpson, K. R., and Knox, G. E. (2009). Oxytocin as a high-alert medication: implications for perinatal patient safety. MCN Am. J. Matern. Child Nurs. 34, 8-15. quiz: 16-17.
99. Smith, O. A., and DeVito, J. L. (1984). Central neural integration for the control of autonomic responses associated with emotion. Annu. Rev. Neurosci. 7, 43-65.
100. Sofroniew, M. V., and Schrell, U. (1981). Evidence for a direct projection from oxytocin and vasopressin neurons in the hypothalamic paraventricular nucleus to the medulla oblongata: immunohistochemical visualization of both the horseradish peroxidase transported and the peptide produced by the same neurons. Neurosci. Lett. 22, 211-217.
101. Stifter, C. A., Fox, N. A., and Porges, S. W. (1989). Facial expressivity and vagal tone in 5-and 10-month-old infants. Infant Behav. Dev. 12, 127-137.
102. Thayer, J. F. (2009). "Heart rate variability: a neurovisceral integration model," in Encyclopedia of Neuroscience, ed L. R. Squire (Oxford: Academic Press), 1041-1047.
103. Thayer, J. F., Åhs, F., Fredrikson, M., Sollers, J. J. III., and Wager, T. D. (2012). A meta-analysis of heart rate variability and neuroimaging studies: implications for heart rate variability as a marker of stress and health. Neurosci. Biobehav. Rev. 36, 747-756.
104. Thayer, J. F., and Brosschot, J. F. (2005). Psychosomatics and psychopathology: looking up and down from the brain. Psychoneuroendocrinology 30, 1050-1058.
105. Thayer, J. F., Hansen, A. L., Saus-Rose, E., and Johnsen, B. H. (2009). Heart rate variability, prefrontal neural function, and cognitive performance: the neurovisceral integration perspective on self-regulation, adaptation, and health. Ann. Behav. Med. 37, 141-153.
106. Thayer, J. F., and Lane, R. D. (2007). The role of vagal function in the risk for cardiovascular disease and mortality. Biol. Psychol. 74, 224-242.
107. Thayer, J. F., and Sternberg, E. (2006). Beyond heart rate variability: vagal regulation of allostatic systems. Ann. N.Y. Acad. Sci. 1088, 361-372.
108. Thayer, J. F., Yamamoto, S. S., and Brosschot, J. F. (2010). The relationship of autonomic imbalance, heart rate variability and cardiovascular disease risk factors. Int. J. Cardiol. 141, 122-131.
109. Thomas, J. S., Koh, S. H., and Cooper, G. M. (2007). Haemodynamic effects of oxytocin given as i.v. bolus or infusion on women undergoing Caesarean section. Br. J. Anaesth. 98, 116-119.
110. Thorne, R. G., Pronk, G. J., Padmanabhan, V., and Frey, W. H. II. (2004). Delivery of insulin-like growth factor-I to the rat brain and spinal cord along olfactory and trigeminal pathways following intranasal administration. Neuroscience 127, 481-496.
111. Tops, M. (2010). Oxytocin: envy or engagement in others?. Biol. Psychiatry 67, e5-e6.
112. Van Hecke, A. V., Lebow, J., Bal, E., Lamb, D., Harden, E., Kramer, A., et al. (2009). Electroencephalogram and heart rate regulation to familiar and unfamiliar people in children with autism spectrum disorders. Child Dev. 80, 1118-1133.
113. Wiseman, R., and Watt, C. (2010). Judging a book by its cover: the unconscious influence of pupil size on consumer choice. Perception 39, 1417-1419.
114. Woodbury, R. A., and Abreu, B. E. (1944). Influence of oxytocin (pitocin) upon the heart and blood pressure of the chicken, rabbit, cat, dog and turtle. Am. J. Physiol. 142, 114-120.
115. Woodbury, R. A., Hamilton, W. F., Volipitto, P. P., Abreu, B. E., and Harper, H. T. Jr. (1944). Cardiac and blood pressure effects of pitocin (oxytocin) in man. J. Pharmacol. Exp. Therap. 81, 95-100.
116. Zak, P. J., Stanton, A. A., and Ahmadi, S. (2007). Oxytocin increases generosity in humans. PLoS ONE 2:e1128. doi: 10.1371/journal.pone.0001128