Aerosolized oxytocin increases cerebrospinal fluid oxytocin in rhesus macaques

Psychoneuroendocrinology

Volumn 45, Issue , 2014, Pages 49-57

  Modi, Meera E ^a,b   Connor Stroud, Fawn ^b   Landgraf, Rainer ^c   Young, Larry J ^a,b   Parr, Lisa A ^a,b  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b EMORY UNIVERSITY   (United States)

^c MAX PLANCK INSTITUTE OF PSYCHIATRY   (Germany)

Author keywords

Autism; Intranasal; Oxytocin; Rhesus monkey; Social cognition; Vasopressin

Indexed keywords

OXYTOCIN; VASOPRESSIN; AEROSOL; NOSE SPRAY;

ADULT; ANIMAL EXPERIMENT; ARTICLE; CEREBROSPINAL FLUID LEVEL; CONTROLLED STUDY; DRUG EFFICACY; LUMBAR SPINE; MALE; NONHUMAN; OXYTOCIN BLOOD LEVEL; PRIORITY JOURNAL; RHESUS MONKEY; VASOPRESSIN BLOOD LEVEL; AEROSOL; ANIMAL; BIOAVAILABILITY; BLOOD; CEREBROSPINAL FLUID; COMPARATIVE STUDY; DRUG EFFECTS; INTRANASAL DRUG ADMINISTRATION; INTRAVENOUS DRUG ADMINISTRATION; TIME; UPREGULATION;

ADMINISTRATION, INTRANASAL; ADMINISTRATION, INTRAVENOUS; AEROSOLS; ANIMALS; BIOLOGICAL AVAILABILITY; MACACA MULATTA; MALE; NASAL SPRAYS; OXYTOCIN; TIME FACTORS; UP-REGULATION;

EID: 84900470253     PISSN: 03064530     EISSN: 18733360     Source Type: Journal    
DOI: 10.1016/j.psyneuen.2014.02.011     Document Type: Article

References (44)

1. Altner H., Altner-Kolnberger I. Freeze-fracture and tracer experiments on the permeability of the zonulae occludentes in the olfactory mucosa of vertebrates. Cell Tissue Res. 1974, 154:51-59.
2. Anagnostou E., Soorya L., Chaplin W., Bartz J., Halpern D., Wasserman S., Wang A.T., Pepa L., Tanel N., Kushki A., Hollander E. Intranasal oxytocin versus placebo in the treatment of adults with autism spectrum disorders: a randomized controlled trial. Mol. Autism 2012, 3:16.
3. Andari E., Duhamel J.R., Zalla T., Herbrecht E., Leboyer M., Sirigu A. Promoting social behavior with oxytocin in high-functioning autism spectrum disorders. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:4389-4394.
4. Bartz J.A., Hollander E. Oxytocin and experimental therapeutics in autism spectrum disorders. Prog. Brain Res. 2008, 170:451-462.
5. Born J., Lange T., Kern W., McGregor G.P., Bickel U., Fehm H.L. Sniffing neuropeptides: a transnasal approach to the human brain. Nat. Neurosci. 2002, 5:514-516.
6. Burri A., Heinrichs M., Schedlowski M., Kruger T.H. The acute effects of intranasal oxytocin administration on endocrine and sexual function in males. Psychoneuroendocrinology 2008, 33:591-600.
7. Chang S.W., Barter J.W., Ebitz R.B., Watson K.K., Platt M.L. Inhaled oxytocin amplifies both vicarious reinforcement and self reinforcement in rhesus macaques (Macaca mulatta). Proc. Natl. Acad. Sci. U. S. A. 2012, 109:959-964.
8. Churchland P.S., Winkielman P. Modulating social behavior with oxytocin: how does it work? What does it mean?. Horm. Behav. 2011, 61:392-399.
9. Dhuria S.V., Hanson L.R., Frey W.H. Intranasal drug targeting of hypocretin-1 (orexin-A) to the central nervous system. J. Pharm. Sci. 2009, 98:2501-2515.
10. Domes G., Lischke A., Berger C., Grossmann A., Hauenstein K., Heinrichs M., Herpertz S.C. Effects of intranasal oxytocin on emotional face processing in women. Psychoneuroendocrinology 2010, 35:83-93.
11. Donaldson Z.R., Young L.J. Oxytocin, vasopressin, and the neurogenetics of sociality. Science 2008, 322:900-904.
12. Ebitz R.B., Watson K.K., Platt M.L. Oxytocin blunts social vigilance in the rhesus macaque. Proc. Natl. Acad. Sci. U. S. A. 2013, 110:11630-11635.
13. Ermisch A., Barth T., Ruhle H.J., Skopkova J., Hrbas P., Landgraf R. On the blood-brain barrier to peptides: accumulation of labelled vasopressin, DesGlyNH2-vasopressin and oxytocin by brain regions. Endocrinol. Exp. 1985, 19:29-37.
14. Frank D.O., Kimbell J.S., Pawar S., Rhee J.S. Effects of anatomy and particle size on nasal sprays and nebulizers 2011, 146:313-319. Otolaryngol. Head Neck Surg.
15. Freeman S.M., Inoue K., Smith A.L., Goodman M.M., Young L.J. The neuroanatomical distribution of oxytocin receptor binding and mRNA in the rhesus macaque (Macaca mulatta). Psychoneuroendocrinology 2014, In press.
16. Freund-Mercier M.J., Stoeckel M.E. Somatodendritic autoreceptors on oxytocin neurones. Adv. Exp. Med. Biol. 1995, 395:185-194.
17. Guastella A.J., Einfeld S.L., Gray K.M., Rinehart N.J., Tonge B.J., Lambert T.J., Hickie I.B. Intranasal oxytocin improves emotion recognition for youth with autism spectrum disorders. Biol. Psychiatry 2010, 67:692-694.
18. Guastella A.J., Hickie I.B., McGuinness M.M., Otis M., Woods E.A., Disinger H.M., Chan H.K., Chen T.F., Banati R.B. Recommendations for the standardisation of oxytocin nasal administration and guidelines for its reporting in human research. Psychoneuroendocrinology 2013, 38:612-625.
19. Guastella A.J., MacLeod C. A critical review of the influence of oxytocin nasal spray on social cognition in humans: evidence and future directions. Horm. Behav. 2012, 61:410-418.
20. Guastella A.J., Mitchell P.B., Dadds M.R. Oxytocin increases gaze to the eye region of human faces. Biol. Psychiatry 2008, 63:3-5.
21. Harkema J.R. Comparative pathology of the nasal mucosa in laboratory animals exposed to inhaled irritants. Environ. Health Perspect. 1990, 85:231-238.
22. Hollander E., Bartz J., Chaplin W., Phillips A., Sumner J., Soorya L., Anagnostou E., Wasserman S. Oxytocin increases retention of social cognition in autism. Biol. Psychiatry 2007, 61:498-503.
23. Hollander E., Novotny S., Hanratty M., Yaffe R., DeCaria C.M., Aronowitz B.R., Mosovich S. Oxytocin infusion reduces repetitive behaviors in adults with autistic and Asperger's disorders. Neuropsychopharmacology 2003, 28:193-198.
24. Klein J.T., Shepherd S.V., Platt M.L. Social attention and the brain. Curr. Biol. 2009, 19:R958-R962.
25. Kosfeld M., Heinrichs M., Zak P.J., Fischbacher U., Fehr E. Oxytocin increases trust in humans. Nature 2005, 435:673-676.
26. Landgraf R. Plasma oxytocin concentrations in man after different routes of administration of synthetic oxytocin. Exp. Clin. Endocrinol. 1985, 85:245-248.
27. Landgraf R., Neumann I.D. Vasopressin and oxytocin release within the brain: a dynamic concept of multiple and variable modes of neuropeptide communication. Front. Neuroendocrinol. 2004, 25:150-176.
28. Landis M.S., Boyden T., Pegg S. Nasal-to-CNS drug delivery: where are we now and where are we heading? An industrial perspective. Ther. Deliv. 2012, 3:195-208.
29. Lochhead J.J., Thorne R.G. Intranasal delivery of biologics to the central nervous system 2011, 64:614-628. Adv. Drug Deliv. Rev.
30. Mens W.B., Witter A., van Wilmersma Greidanus T.B. Penetration of neurophyophyseal hormones from plasma into cerebrospinal fluid: half-times of disappearance of these neuropeptides from CSF. Brain Res. 1983, 262:143-149.
31. Modi M.E., Young L.J. The oxytocin system in drug discovery for autism: animal models and novel therapeutic strategies. Horm. Behav. 2012, 61:340-350.
32. Neumann I., Koehler E., Landgraf R., Summy-Long J. An oxytocin receptor antagonist infused into the supraoptic nucleus attenuates intranuclear and peripheral release of oxytocin during suckling in conscious rats. Endocrinology 1994, 134:141-148.
33. Neumann I., Ludwig M., Engelmann M., Pittman Q.J., Landgraf R. Simultaneous microdialysis in blood and brain: oxytocin and vasopressin release in response to central and peripheral osmotic stimulation and suckling in the rat. Neuroendocrinology 1993, 58:637-645.
34. Neumann I., Maloumby R., Beiderbeck D.I., Lukas M., Landgraf R. Increased brain and plasma oxytocin after nasal and peripheral administration in rats and mice. Psychoneuroendocrinology 2013, 38:1985-1993.
35. Neumann I.D., Landgraf R. Balance of brain oxytocin and vasopressin: implications for anxiety, depression, and social behaviors. Trends Neurosci. 2012, 35:649-659.
36. Neumann I.D., Torner L., Toschi N., Veenema A.H. Oxytocin actions within the supraoptic and paraventricular nuclei: differential effects on peripheral and intranuclear vasopressin release. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2006, 291:R29-R36.
37. Parr L.A., Modi M.E., Siebert E., Young L.J. Intranasal oxytocin selectively attenuates rhesus monkeys' attention to negative facial expressions. Psychoneuroendocrinology 2013, 38:1748-1756.
38. Ross H.E., Young L.J. Oxytocin and the neural mechanisms regulating social cognition and affiliative behavior. Front. Neuroendocrinol. 2009, 30:534-547.
39. Rimmele U., Hediger K., Heinrichs M., Klaver P. Oxytocin makes a face in memory familiar. J. Neuroscience. 2009, 29(11):38-42.
40. Savaskan E., Ehrhardt R., Schulz A., Walter M., Schachinger H. Post-learning intranasal oxytocin modulates human memory for facial identity. Psychoneuroendocrinology 2008, 33:368-374.
41. Suman J.D., Laube B.L., Dalby R. Comparison of nasal deposition and clearance of aerosol generated by nebulizer and an aqueous spray pump. Pharm. Res. 1999, 16:1648-1652.
42. Striepens N., Kendrick K.M., Hanking V., Landgraf R., Wullner U., Maier W., Hurlemann R. Elevated cerebrospinal fluid and blood concentrations of oxytocin following its intranasal administration in humans. Sci. Rep. 2013, 3:3440.
43. Tachibana M., Kagitani-Shimono K., Mohri I., Yamamoto T., Sanefuji W., Nakamura A., Oishi M., Kimura T., Onaka T., Ozono K., Taniike M. Long-term administration of intranasal oxytocin is a safe and promising therapy for early adolescent boys with autism spectrum disorders. Journal of Child and. Adolescent Psychopharmacol. 2013, 23:123-127.
44. Young L.J., Flanagan-Cato L.M. Editorial comment: oxytocin, vasopressin and social behavior. Horm. Behav. 2012, 61:227-229.