Genetic imaging of the association of oxytocin receptor gene (OXTR) polymorphisms with positive maternal parenting

Frontiers in Behavioral Neuroscience

Volumn 8, Issue FEB, 2014, Pages

  Michalska, Kalina J ^a,b,c   Decety, Jean ^a   Liu, Chunyu ^a   Chen, Qi ^a   Martz, Meghan E ^d   Jacob, Suma ^e   Hipwell, Alison E ^f   Lee, Steve S ^g   Chronis Tuscano, Andrea ^c   Waldman, Irwin D ^h   Lahey, Benjamin B ^a  

^a UNIVERSITY OF CHICAGO   (United States)

^b NATIONAL INSTITUTE OF MENTAL HEALTH   (United States)

^c UNIVERSITY OF MARYLAND   (United States)

^d UNIVERSITY OF MICHIGAN   (United States)

^e UNIVERSITY OF MINNESOTA   (United States)

^f UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^g UNIVERSITY OF CALIFORNIA   (United States)

^h EMORY UNIVERSITY   (United States)

Author keywords

Functional magnetic resonance imaging; Maternal parenting oxytocin receptor gene

Indexed keywords

OXYTOCIN RECEPTOR;

ANTERIOR CINGULATE; ARTICLE; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; FUNCTIONAL NEUROIMAGING; GENETIC ASSOCIATION; HEMODYNAMICS; HIPPOCAMPUS; HUMAN; MATERNAL BEHAVIOR; MOTHER CHILD RELATION; ORBITAL CORTEX; OXYTOCIN RECEPTOR GENE; REWARD; SINGLE NUCLEOTIDE POLYMORPHISM; SOCIAL BEHAVIOR;

EID: 84898739141     PISSN: 16625153     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnbeh.2014.00021     Document Type: Article

References (61)

1. Bakermans-Kranenburg, M. J., and van Ijzendoorn, M. H. (2008). Oxytocin receptor (OXTR) and serotonin transporter (5-HTT) genes associated with observed parenting. Soc. Cogn. Affect. Neurosci. 3, 128-134. doi: 10.1093/scan/nsn004
2. Bartels, A., and Zeki, S. (2004). The neural correlates of maternal and romantic love. Neuroimage 21, 1155-1166. doi: 10.1016/j.neuroimage.2003.11.003
3. Bartz, J. A. and Hollander, E. (2006). The neuroscience of affiliation: forging links between basic and clinical research on neuropeptides and social behavior. Horm. Behav. 50, 518-528. doi: 10.1016/j.yhbeh.2006.06.018
4. Bell, R. Q., and Chapman, M. (1986). Child effects in studies using experimental or brief longitudinal approaches to socialization. Dev. Psychol. 22, 595-603. doi: 10.1037/0012-1649.22.5.595
5. Brunton, P. J., and Russell, J. A. (2008). The expectant brain: adapting for motherhood. Nat. Rev. Neurosci. 1, 11-25. doi: 10.1038/nrn2280
6. Bush, G., Luu, P., and Posner, M. I. (2000). Cognitive and emotional influences in anterior cingulate cortex. Trends Cogn. Sci. 4, 215-222. doi: 10.1016/S1364-6613(00)01483-2
7. Campbell, A. (2008). Attachment, aggression and affiliation: the role of oxytocin in female social behavior. Biol. Psychol. 77, 1-10 doi: 10.1016/j.biopsycho.2007.09.001
8. Carter, C. S. (1998). Neuroendocrine perspectives on social attachment and love. Psychoneuroendocrinology 23, 779-818. doi: 10.1016/S0306-4530(98)00055-9
9. Chronis, A. M., Lahey, B. B., Pelham, W. E., Williams, S. H., Baumann, B. L., Kipp, H., et al. (2007). Maternal depression and early positive parenting predict future conduct problems in young children with attention-deficit/hyperactivity disorder. Dev. Psychol. 43, 70-82. doi: 10.1037/0012-1649.43.1.70
10. Chronis-Tuscano, A., Molina, B. S. G., Pelham, W. E., Applegate, B., Dahlke, A., Overmyer, M., et al. (2010). Very early predictors of adolescent depression and suicide attempts in children with attention-deficit/hyperactivity disorder. Arch. Gen. Psychiatry 67, 1044-1051. doi: 10.1001/archgenpsychiatry.2010.127
11. Clarke, G. M., and Cardon, L. R. (2010). Aspects of observing and claiming allele flips in association studies. Genet. Epidemiol. 34, 266-274. doi: 10.1002/gepi.20458
12. Cohen, H., Kaplan, Z., Kozlovsky, N., Gidron, Y., Matar, M. A., and Zohar, J. (2010). Hippocampal microinfusion of oxytocin attenuates the behavioural response to stress by means of dynamic interplay with the glucocorticoid-catecholamine responses. J. Neuroendocrinol. 22, 889-904. doi: 10.1111/j.1365-2826.2010.02003.x
13. Costa, B., Pini, S., Gabelloni, P., Abelli, M., Lari, L., Cardini, A., et al. (2009). Oxytocin receptor polymorphisms and adult attachment style in patients with depression. Psychoneuroendocrinology, 34, 1506-1514. doi: 10.1016/j.psyneuen.2009.05.006
14. DNAGenotek. (2010). Oragene DNA Self-Collection Kit. Ottawa, ON: DNAGenotek, Inc.
15. Francis, D. D., Young, L. J., Meaney, M. J., and Insel, T. R. (2002). Naturally occurring differences in maternal care are associated with the expression of oxytocin and vasopressin (V1a) receptors: gender differences. J. Endocrinol. 14, 349-353. doi: 10.1046/j.0007-1331.2002.00776.x
16. Glascher, J. (2009). Visualization of group inference data in functional neuroimaging. Neuroinformatics 7, 73-82. doi: 10.1007/s12021-008-9042-x
17. Inoue, T., Kimura, T., Azuma, C., Inazawa, J., Takemura, M., Kikuchi, T., et al. (1994). Structural organization of the human oxytocin receptor gene. J. Biol. Chem. 269, 32451-32456.
18. 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
19. 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 ONE4:e5535. doi: 10.1371/journal.pone.0005535
20. Kerns, J. G., Cohen, J. D., MacDonald, A. W., Cho, R. Y., Stenger, V. A., and Carter, C. S. (2004). Anterior cingulate conflict monitoring and adjustments in control. Science 303, 1023-1026. doi: 10.1126/science.1089910
21. Knobloch, H. S., Charlet, A., Hoffman, 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
22. Lahey, B. B., Conger, R. D., Atkeson, B. M., and Treiber, F. A. (1984). Parenting behavior and emotional status of physically abusive mothers. J. Consult. Clin. Psychol. 52, 1062-1071. doi: 10.1037/0022-006X.52.6.1062
23. Lahey, B. B., Pelham, W. E., Loney, J., Lee, S. S., and Willcutt, E. (2005). Instability of the DSM-IV subtypes of ADHD from preschool through elementary school. Arch. Gen. Psychiatry 62, 896-902. doi: 10.1001/archpsyc.62.8.896
24. Lahey, B. B., Rathouz, P. J., Lee, S. S., Chronis-Tuscano, A., Pelham, W. E., Waldman, I. D., et al. (2011). Interactions between early parenting and a polymorphism of the child's dopamine transporter gene in predicting future child conduct disorder symptoms. J. Abnorm. Psychol. 120, 33-45. doi: 10.1037/a0021133
25. 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
26. Lee, H. J., Macbeth, A. H., and Pagani, J. H. (2009). Oxytocin: the great facilitator of life. Prog. Neurobiol. 88, 127-151. doi: 10.1016/j.pneurobio.2009.04.001
27. Lee, S. S., Chronis-Tuscano, A., Keenan, K., Pelham, W. E., Loney, J., Van Hulle, C. A., et al. (2010). Association of maternal dopamine transporter genotype with negative parenting: evidence for gene x environment interaction with child disruptive behavior. Mol. Psychiatry 15, 548-558. doi: 10.1038/mp.2008.102
28. Leibenluft, E., Gobbini, M. I., Harrison, T., and Haxby, J. V. (2004). Mothers' neural activation in response to pictures of their children and other children. Biol. Psychiatry 56, 225-232. doi: 10.1016/j.biopsych.2004.05.017
29. Levine, A., Zagoory-Sharon, O., Feldman, R., and Weller, A. (2007). Oxytocin during pregnancy and early postpartum: individual patterns and maternal-fetal attachment. Peptides 28, 1162-1169. doi: 10.1016/j.peptides.2007.04.016
30. Lim, M. M., and Young, L. J. (2006). Neuropeptidergic regulation of affiliative behavior and social bonding in animals. Horm. Behav. 50, 506-517. doi: 10.1016/j.yhbeh.2006.06.028
31. Lorberbaum, J. P., Newman, J. D., Horwitz, A. R., Dubno, J. R., Lydiard, R. B., Hamner, M. B., et al. (2002). A potential role for thalamocingulate circuitry in human maternal behavior. Biol. Psychiatry 51, 431-445. doi: 10.1016/S0006-3223(01)01284-7
32. Lucht, M. J., Barnow, S., Sonnenfeld, C., Rosenberger, A., Grabe, H. J., Schroeder, W., et al. (2009). Associations between the oxytocin receptor gene (OXTR) and affect, loneliness and intelligence in normal subjects. Prog. Neuropsychopharmacol. Biol. Psychiatry 33, 860-866. doi: 10.1016/j.pnpbp.2009.04.004
33. Ludwig, M., and Leng, G. (2006). Dendritic peptide release and peptide-dependent behaviours. Nat. Rev. Neurosci. 7, 126-136. doi: 10.1038/nrn1845
34. Marsh, A. A., Finger, E. C., Mitchell, D. G. V., Reid, M. E., Sims, C., Kosson, D. S., et al. (2008). Reduced amygdala response to fearful expressions in children and adolescents with callous-unemotional traits and disruptive behavior disorders. Am. J. Psychiatry 165, 712-720. doi: 10.1176/appi.ajp.2007.07071145
35. Nelder, J., and Wedderburn, R. (1972). Generalized linear models. J. R. Statist. Soc. A 135, 370-384.
36. Nitschke, J. B., Nelson, E. E., Rusch, B. D., Fox, A. S., Oakes, T. R., and Davidson, R. J. (2004). Orbitofrontal cortex tracks positive mood in mothers viewing pictures of their newborn infants. Neuroimage 21, 583-592. doi: 10.1016/j.neuroimage.2003.10.005
37. Numan, M., and Insel, T. R. (2003). Neurobiology of Parental Behavior. New York, NY: Springer.
38. Numan, M., and Woodside, B. (2010). Maternity: neural mechanisms, motivational processes, and physiological adaptations. Behav. Neurosci. 124, 715-741. doi: 10.1037/a0021548
39. Olazabal, D. E., and Young, L. J. (2006). Oxytocin receptors in the nucleus accumbens facilitate "spontaneous" maternal behavior in adult female prairie voles. Neuroscience 141, 559-568. doi: 10.1016/j.neuroscience.2006.04.017
40. Parsons, C. E., Stark, E. A., Young, K. S., Stein, A., and Kringelbach, M. L. (2013). Understanding the human parental brain: a critical role of the orbitofrontal cortex. Soc. Neurosci. 8, 525-543. doi: 10.1080/17470919.2013.842610
41. Ragnauth, A. K., Devidze, N., Moy, V., Finley, K., Goodwillie, A., Kow, L. M., et al. (2005). Female oxytocin gene-knockout mice, in a semi-natural environment, display exaggerated aggressive behavior. Gene. Brain Behav. 4, 229-239. doi: 10.1111/j.1601-183X.2005.00118.x
42. Riem, M. M. E., Bakermans-Kranenburg, M. J., Pieper, S., Tops, M., Boksem, M. A. S., Vermeiren, R. R. J. M., et al. (2011a). Oxytocin modulates amygdala, insula, and inferior frontal gyrus responses to infant crying: a randomized controlled trial. Biol. Psychiatry 70, 291-297. doi: 10.1016/j.biopsych.2011.02.006
43. Riem, M. M. E., Pieper, S., Out, D., Bakermans-Kranenburg, M. J., and van Ijzendoorn, M. H. (2011b). Oxytocin receptor gene and depressive symptoms associated with physiological reactivity to infant crying. Soc. Cogn. Affect. Neurosci. 6, 294-300. doi: 10.1093/scan/nsq035
44. Robinson, E. A., and Eyberg, S. M. (1981). The dyadic parent-child interaction coding system: standardization and validation. J. Consult. Clin. Psychol. 49, 245-250. doi: 10.1037/0022-006X.49.2.245
45. Rodrigues, S. M., Saslow, L. R., Garcia, N., John, O. P., and Keltner, D. (2009). Oxytocin receptor genetic variation relates to empathy and stress reactivity in humans. Proc. Natl. Acad. Sci. U.S.A. 106, 21437-21441. doi: 10.1073/pnas.0909579106
46. Rolls, E. T. (2000). The orbitofrontal cortex and reward. Cereb. Cortex 10, 284-294. doi: 10.1093/cercor/10.3.284
47. Ross, H. E., Cole, C. D., Smith, Y., Neumann, I. D., Landgraf, R., Murphy, A. Z., et al. (2009). Characterization of the oxytocin system regulating affiliative behavior in female prairie voles. Neuroscience 162, 892-903. doi: 10.1016/j.neuroscience.2009.05.055
48. Ross, H. E., and Young, L. J. (2009). Oxytocin and the neural mechanisms regulating social cognition and affiliative behavior. Front. Neuroendocrinol. 30, 534-547. doi: 10.1016/j.yfrne.2009.05.004
49. Saphire-Bernstein, S., Way, B. M., Kim, H. S., Sherman, D. K., and Taylor, S. E. (2011). Oxytocin receptor gene (OXTR) is related to psychological resources. Proc. Natl. Acad. Sci. U.S.A. 108, 15118-15122. doi: 10.1073/pnas.1113137108
50. Stoop, R. (2012). Neuromodulation by oxytocin and vasopressin. Neuron76, 142-159. doi: 10.1016/j.neuron.2012.09.025
51. Swain, J. E. (2011). The human parental brain: in vivo neuroimaging. Prog. Neuropsychopharmacol. Biol. Psychiatry 35, 1242-1254. doi: 10.1016/j.pnpbp.2010.10.017
52. Swain, J. E., Leckman, J. F., Mayes, L. C., Feldman, R., Constable, R. T., and Schultz, R. T. (2004). Neural substrates and psychology of human parent-infant attachment in the postpartum. Biol. Psychiatry 55, 153S. Available online at: http://ac.els-cdn.com.proxy-um.researchport.umd.edu/S0006322304002446/1-s2.0-S0006322304002446-main.pdf?_tid=b496afc0-82e6-11e3-bc85-00000aab0f01&acdnat=1390341493_c129ae5a265d822778872839cb6d4bfe
53. Swain, J. E., Lorberbaum, J. P., Kose, S., and Strathearn, L. (2007). Brain basis of early parent-infant interactions: psychology, physiology, and in vivo functional neuroimaging studies. J. Child Psychol. Psychiatry 48, 262-287. doi: 10.1111/j.1469-7610.2007.01731.x
54. Swain, J. E., Tasgin, E., Mayes, L. C., Feldman, R., Constable, R. T., and Leckman, J. F. (2008). Maternal brain response to own baby cry is affected by cesarean section delivery. J. Child Psychol. Psychiatry 49, 1042-1052. doi: 10.1111/j.1469-7610.2008.01963.x
55. Takayanagi, Y., Yoshida, M., Bielsky, I. F., Ross, H. E., Kawamata, M., Onaka, T., et al. (2005). Pervasive social deficits, but normal parturition, in oxytocin receptor-deficient mice. Proc. Natl. Acad. Sci. U.S.A. 102, 16096-16101. doi: 10.1073/pnas.0505312102
56. Tost, H., Kolachana, B., Hakimi, S., Lemaitre, H., Verchinski, B. A., Mattay, V. S., et al. (2010). A common allele in the oxytocin receptor gene (OXTR) impacts prosocial temperament and human hypothalamic-limbic structure and function. Proc. Natl. Acad. Sci. U.S.A. 107, 13936-13941. doi: 10.1073/pnas.1003296107
57. van den Burg, E. H., and Neumann, I. D. (2011). Bridging the gap between GPCR activation and behaviour: Oxytocin and prolactin signalling in the hypothalamus. J. Mol. Neurosci. 43, 200-208. doi: 10.1007/s12031-010-9452-8
58. Volkow, N. D., Tomasi, D., Wang, G. J., Fowler, J. S., Telang, F., Goldstein, R. Z., et al. (2011). Positive emotionality is associated with baseline metabolism in orbitofrontal cortex and in regions of the default network. Mol. Psychiatry 16, 818-825. doi: 10.1038/mp.2011.30
59. Webster-Stratton, C. (1998). Preventing conduct problems in head start children: strengthening parenting competencies. J. Consult. Clin. Psychol. 66, 715-730.
60. Wegman, H. L., and Stetler, C. (2009). A meta-analytic review of the effects of childhood abuse on medical outcomes in adulthood. Psychosom. Med. 71, 805-812. doi: 10.1097/PSY.0b013e3181bb2b46
61. Worsley, K. J., Marrett, S., Neelin, P., Vandal, A. C., Friston, K. J., and Evans, A. C. (1996). A unified statistical approach for determining significant signals in images of cerebral activation. Hum. Brain Mapp. 4, 58-73. doi: 10.1002/(SICI)1097-0193(1996)4:1<58::AID-HBM4>3.0.CO;2-O