Visual attention for social information and salivary oxytocin levels in preschool children with autism spectrum disorders: An eye-tracking study

Frontiers in Neuroscience

Volumn 8, Issue SEP, 2014, Pages

  Fujisawa, Takashi X ^a,b,c,d,e   Tanaka, Shiho ^a   Saito, Daisuke N ^a,b,c,d,e   Kosaka, Hirotaka ^a,b,c,d,e   Tomoda, Akemi ^a,b  

^a UNIVERSITY OF FUKUI   (Japan)

^b OSAKA UNIVERSITY   (Japan)

^c KANAZAWA UNIVERSITY   (Japan)

^d HAMAMATSU UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^e Chiba University   (Japan)

Author keywords

Autism spectrum disorder (ASD); Eye tracking; Oxytocin (OT); Preschool children; Visual attention

Indexed keywords

OXYTOCIN;

ARTICLE; ATTENTION; AUTISM; CHILD; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; EYE TRACKING; FEMALE; GAZE; GEOMETRY; HUMAN; INFORMATION; JAPANESE (PEOPLE); MAJOR CLINICAL STUDY; MALE; MOTION; PRESCHOOL CHILD; RECOGNITION; RISK FACTOR; SALIVA; SEX DIFFERENCE; SOCIAL INFORMATION; STANDING; VISUAL ATTENTION;

EID: 84907945360     PISSN: 16624548     EISSN: 1662453X     Source Type: Journal    
DOI: 10.3389/fnins.2014.00295     Document Type: Article

References (54)

1. American Psychiatric Association (APA). (2013). Diagnostic and Statistical Manual of Mental Disorders: DSM-V, 5th Edn. Washington, DC: American Psychiatric Association.
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. doi: 10.1073/pnas.0910249107
3. Baumgartner, T., Heinrichs, M., Vonlanthen, A., Fischbacher, U., and Fehr, E. (2008). Oxytocin shapes the neural circuitry of trust and trust adaptation in humans. Neuron 58, 639-650. doi: 10.1016/j.neuron.2008.04.009
4. Bower, T. G. R. (1989). The Rational Infant: Learning in Infancy. New York, NY: W. H. Freeman & Co Ltd.
5. Carter, C. S. (1998). Neuroendocrine perspectives on social attachment and love. Psychoneuroendocrinology 23, 779-818. doi: 10.1016/S0306-4530(98)00055-9
6. Carter, C. S., Pournajafi-Nazarloo, H., Kramer, K. M., Ziegler, T. E., White-Traut, R., Bello, D., et al. (2007). Behavioral associations and potential as a salivary biomarker. Ann. N.Y. Acad. Sci. 1098, 312-322. doi: 10.1196/annals.1384.006
7. Centelles, L., Assaiante, C., Etchegoyhen, K., Bouvard, M., and Schmitz, C. (2012). Understanding social interaction in children with autism spectrum disorders: does whole-body motion mean anything to them? Encephale 38, 232-240. doi: 10.1016/j.encep.2011.08.005
8. Chevallier, C., Kohls, G., Troiani, V., Brodkin, E. S., and Schultz, R. T. (2012). The social motivation theory of autism. Trends Cogn. Sci. 16, 231-239. doi: 10.1016/j.tics.2012.02.007
9. Doi, H., Fujisawa, T. X., Kanai, C., Ohta, H., Yokoi, H., Iwanami, A., et al. (2013). Recognition of facial expressions and prosodic cues with graded emotional intensities in adults with Asperger syndrome. J. Autism Dev. Disord. 43, 2099-2113. doi: 10.1007/s10803-013-1760-8
10. Domes, G., Heinrichs, M., Gläscher, J., Büchel, C., Braus, D. F., and Herpertz, S. C. (2007a). Oxytocin attenuates amygdala responses to emotional faces regardless of valence. Biol. Psychiatry 62, 1187-1190. doi: 10.1016/j.biopsych.2007.03.025
11. Domes, G., Heinrichs, M., Michel, A., Berger, C., and Herpertz, S. C. (2007b). Oxytocin improves "mind-reading" in humans. Biol. Psychiatry 61, 731-733. doi: 10.1016/j.biopsych.2006.07.015
12. Donaldson, Z. R., and Young, L. J. (2008). Oxytocin, vasopressin, and the neurogenetics of sociality. Science 322, 900-904. doi: 10.1126/science.1158668
13. Feldman, R., Gordon, I., Influs, M., Gutbir, T., and Ebstein, R. P. (2013). Parental oxytocin and early caregiving jointly shape children's oxytocin response and social reciprocity. Neuropsychopharmacology 38, 1154-1162. doi: 10.1038/npp.2013.22
14. Feldman, R., Gordon, I., and Zagoory-Sharon, O. (2011). Maternal and paternal plasma, salivary, and urinary oxytocin and parent-infant synchrony: considering stress and affiliation components of human bonding. Dev. Sci. 14, 752-761. doi: 10.1111/j.1467-7687.2010.01021.x
15. Ferguson, J. N., Young, L. J., Hearn, E. F., Matzuk, M. M., Insel, T. R., and Winslow, J. T. (2000). Social amnesia in mice lacking the oxytocin gene. Nat. Genet. 25, 284-288. doi: 10.1038/77040
16. Gordon, I., Vander Wyk, B. C., Bennett, R. H., Cordeaux, C., and Lucas, M. V., Eilbott, J. A. et al. (2013). Oxytocin enhances brain function in children with autism. Proc. Natl. Acad. Sci. U.S.A. 110, 20953-20958. doi: 10.1073/pnas.1312857110
17. 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
18. 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. doi: 10.1016/j.biopsych.2007.06.026
19. Guillon, Q., Hadjikhani, N., Baduel, S., and Rogé, B. (2014). Visual social attention in autism spectrum disorder: insights from eye tracking studies. Neurosci. Biobehav. Rev. 42, 279-297. doi: 10.1016/j.neubiorev.2014.03.013
20. Higashida, H., Yokoyama, S., Huang, J. J., Liu, L., Ma, W. J., Akther, S., et al. (2012). Social memory, amnesia, and autism: brain oxytocin secretion is regulated by NAD+ metabolites and single nucleotide polymorphisms of CD38. Neurochem. Int. 61, 828-838. doi: 10.1016/j.neuint.2012.01.030
21. Hill, E. L., and Frith, U. (2003). Understanding autism: insights from mind and brain. Philos. Trans. R. Soc. Lond. B Biol. Sci. 358, 281-289. doi: 10.1098/rstb.2002.1209
22. Iizuka, C., Yamashita, Y., Nagamitsu, S., Yamashita, T., Araki, Y., Ohya, T., et al. (2010). Comparison of the strengths and difficulties questionnaire (SDQ) scores between children with high-functioning autism spectrum disorder (HFASD) and attention-deficit/hyperactivity disorder (AD/HD). Brain Dev. 32, 609-612. doi: 10.1016/j.braindev.2009.09.009
23. Ikuzawa, M., Matsushita, H., and Nakazawa, A. (eds.). (2002). Guides for the Use of the Kyoto Scale of Psychological Development 2001 (Japanese). Kyoto: Kyoto International Social Welfare Exchange Center.
24. Insel, T. R. (2010). The challenge of translation in social neuroscience: a review of oxytocin, vasopressin, and affiliative behavior. Neuron 65, 768-779. doi: 10.1016/j.neuron.2010.03.005
25. Israel, S., Lerer, E., Shalev, I., Uzefovsky, F., Riebold, M., Laiba, E., et al. (2009). The oxytocin receptor (OXTR) contributes to prosocial fund allocations in the dictator game and the social value orientations task. PLoS ONE 4:e5535. doi: 10.1371/journal.pone.0005535
26. Jones, W., and Klin, A. (2013). Attention to eyes is present but in decline in 2-6-month-old infants later diagnosed with autism. Nature 504, 427-431. doi: 10.1038/nature12715
27. Kéri, S., Kiss, I., and Kelemen, O. (2009). Sharing secrets: oxytocin and trust in schizophrenia. Soc. Neurosci. 4, 287-293. doi: 10.1080/17470910802319710
28. 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. doi: 10.1523/JNEUROSCI.3984-05.2005
29. Klin, A., Jones, W., Schultz, R., and Volkmar, F. (2003). The enactive mind, or from action to cognition: lessons from autism. Philos. Trans. R. Soc. Lond. B Biol. Sci. 358, 345-360. doi: 10.1098/rstb.2002.1202
30. Klin, A., Jones, W., Schultz, R., Volkmar, F., and Cohen,. D. (2002a). Defining and quantifying the social phenotype in autism. Am. J. Psychiatry 159, 895-908. doi: 10.1176/appi.ajp.159.6.895
31. Klin, A., Jones, W., Schultz, R., Volkmar, F. R., and Cohen, D. J. (2002b). Visual fixation patterns during viewing of naturalistic social situations as predictors of social competence in individuals with autism, Arch. Gen. Psychiatry 59, 809-816. doi: 10.1001/archpsyc.59.9.809
32. Klin, A., Lin, D. J., Gorrindo, P., Ramsay, G., and Jones, W. (2009). Two-year-olds with autism orient to non-social contingencies rather than biological motion. Nature 459, 257-261. doi: 10.1038/nature07868
33. Kosaka, H., Munesue, T., Ishitobi, M., Asano, M., Omori, M., Sato, M., et al. (2012). Long-term oxytocin administration improves social behaviors in a girl with autistic disorder. BMC Psychiatry 12:110. doi: 10.1186/1471-244X-12-110
34. 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
35. 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
36. Matsuishi, T., Nagano, M., Araki, Y., Tanaka, Y., Iwasaki, M., Yamashita, Y., et al. (2008). Scale properties of the strengths and difficulties questionnaire (SDQ): a study of infant and school children in community samples. Brain Dev. 30, 410-415. doi: 10.1016/j.braindev.2007.12.003
37. 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. doi: 10.1016/S0006-3223(97)00439-3
38. Munesue, T., Yokoyama, S., Nakamura, K., Anitha, A., Yamada, K., Hayashi, K., et al. (2010). Two genetic variants of CD38 in subjects with autism spectrum disorder and controls. Neurosci. Res. 67, 181-191. doi: 10.1016/j.neures.2010.03.004
39. Nakano, T., Tanaka, K., Endo, Y., Yamane, Y., Yamamoto, T., Nakano, Y., et al. (2010). Atypical gaze patterns in children and adults with autism spectrum disorders dissociated from developmental changes in gaze behaviour. Proc. Biol. Sci. 277, 2935-2943. doi: 10.1098/rspb.2010.0587
40. Paparella, T., Goods, K. S., Freeman, S., and Kasari, C. (2011). The emergence of nonverbal joint attention and requesting skills in young children with autism. J. Commun. Disord. 44, 569-583. doi: 10.1016/j.jcomdis.2011.08.002
41. Pierce, K., Conant, D., Hazin, R., Stoner, R., and Desmond, J. (2011). Preference for geometric patterns early in life as a risk factor for autism. Arch. Gen. Psychiatry 68, 101-109. doi: 10.1001/archgenpsychiatry.2010.113
42. Redcay, E., Dodell-Feder, D., Mavros, P. L., Kleiner, M., Pearrow, M. J., Triantafyllou, C., et al. (2013). Atypical brain activation patterns during a face-to-face joint attention game in adults with autism spectrum disorder. Hum. Brain Mapp. 34, 2511-2523. doi: 10.1002/hbm.22086
43. Rimmele, U., Hediger, K., Heinrichs, M., and Klaver, P. (2009). Oxytocin makes a face in memory familiar. J. Neurosci. 29, 38-42. doi: 10.1523/JNEUROSCI.4260-08.2009
44. Sasson, N. J., and Touchstone, E. W. (2014). Visual attention to competing social and object images by preschool children with autism spectrum disorder. J. Autism Dev. Disord. 44, 584-592. doi: 10.1007/s10803-013-1910-z
45. Skuse, D. H., and Gallagher, L. (2009). Dopaminergic-neuropeptide interactions in the social brain. Trends Cogn. Sci. 13, 27-35. doi: 10.1016/j.tics.2008.09.007
46. Stavropoulos, K. K., and Carver, L. J. (2013). Research review: social motivation and oxytocin in autism-implications for joint attention development and intervention. J. Child Psychol. Psychiatry 54, 603-618. doi: 10.1111/jcpp.12061
47. Taylor, B., Jck, H., and MacLaughlin, D. (2013). Prevalence and incidence rates of autism in the UK: time trend from 2004-2010 in children aged 8 years. BMJ Open 3:e003219. doi: 10.1136/bmjopen-2013-003219
48. Tsujii, M., Yukihiro, T., Adachi, J., Ichikawa, H., Inoue, M., Uchiyama, T., et al. (2006). Reliability and validity of the infant part of the PARS (PDD-autism society japan rating scale) (Japanese). Rinshou Seishin Igaku 35, 1119-1126.
49. Warreyn, P., Roeyers, H., Van Wetswinkel, U., and De Groote, I. (2007). Temporal coordination of joint attention behavior in preschoolers with autism spectrum disorder. J. Autism Dev. Disord. 37, 501-512. doi: 10.1007/s10803-006-0184-0
50. Watanabe, T., Abe, O., Kuwabara, H., Yahata, N., Takano, Y., Iwashiro, N., et al. (2014). Mitigation of sociocommunicational deficits of autism through oxytocin-induced recovery of medial prefrontal activity: a randomized trial. JAMA Psychiatry 71, 166-175. doi: 10.1001/jamapsychiatry
51. White-Traut, R., Watanabe, K., Pournajafi-Nazarloo, H., Schwertz, D., Bell, A., and Carter, C. S. (2009). Detection of salivary oxytocin levels in lactating women. Dev. Psychobiol. 51, 367-373. doi: 10.1002/dev.20376
52. Young, L. J., and Wang, Z. (2004). The neurobiology of pair bonding. Nat. Neurosci. 7, 1048-1054. doi: 10.1038/nn1327
53. Zak, P. J., Kurzban, R., and Matzner, W. T. (2005). Oxytocin is associated with human trustworthiness. Horm. Behav. 48, 522-527. doi: 10.1016/j.yhbeh.2005.07.009
54. 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