Translational Neuroscience

, Volume 1, Issue 2, pp 148–159 | Cite as

Recent advances in the neurobiology of attachment behavior

  • Đurđica Šešo-Šimić
  • Goran Sedmak
  • Patrick R. Hof
  • Goran Šimić
Communication
  • 198 Downloads

Abstract

In a biological sense an individual’s life is all about survival and reproduction. Beside the selection of a mate, the mutual commitment of a parent to sustain an infant through a period of dependency is amongst the most important aspects of natural selection. Here we review how the highly conserved circuitry of key midbrain and hypothalamic structures, and limbic and frontal cortical regions support these processes, and at the same time are involved in shaping the offspring’s emotional development and behavior. Many recent studies provided new findings on how attachment behavior and parental bonding is promoted and maintained through genetic and epigenetic influences on synaptic plasticity of mirror neurons and various neuropeptide systems, particularly oxytocinergic, and how these systems serve to link social cues to the brain reward system. Most of this evidence suggests that stress, early parental deprivation and lack of care during the postnatal period leads to profound and lasting changes in the attachment pattern and motivational development with consequent increased vulnerability of the mesocortical and mesolimbic dopamine-associated reward reinforcement pathways to psychosocial stressors, abuse of stimulants and psychopathology later in life.

Keywords

Aggressiveness Attachment behavior Autism Dopamine Emotional development Motivation Oxytocin Mirror neurons Parental bonding Psychopathology 

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References

  1. [1]
    Sameroff A., A unified theory of development: a dialectic integration of nature and nurture, Child Dev., 2010, 81, 6–22PubMedCrossRefGoogle Scholar
  2. [2]
    Adolphs R., Cognitive neuroscience of human social behavior, Nature Neurosci., 2003, 4, 165–178Google Scholar
  3. [3]
    Fagiolini M., Jensen C.L., Champagne F.A., Epigenetic influences on brain development and plasticity, Curr. Opin. Neurobiol., 2009, 19, 207–212PubMedCrossRefGoogle Scholar
  4. [4]
    Rutter M., Clinical implications of attachment concepts: retrospect and prospect, J. Child Psychol. Psychiatr., 1995, 36, 549–571Google Scholar
  5. [5]
    Cassidy J., The nature of child’s ties, In: Handbook of attachment: theory, research and clinical applications (eds. Cassidy J, Shaver PR), New York: Guilford Press, 1999, 3–20Google Scholar
  6. [6]
    Bowlby J., The nature of the child’s tie to his mother, Int. J. Psychoanal., 1958, 39, 350–373PubMedGoogle Scholar
  7. [7]
    Ainsworth M. D., Blehar M., Waters E., Wall S., Patterns of attachment: a psychological study of the Strange Situation, Hillsdale NJ: Lawrence Erlbaum Associates, 1978Google Scholar
  8. [8]
    Weinfield N. S., Sroufe L.A., Egeland B., Carlson E., Individual differences in infant-caregiver attachment, In: Handbook of attachment: theory, research and clinical applications (eds. Cassidy J, Shaver PR), New York and London: Guilford Press, 2008, 78–101Google Scholar
  9. [9]
    Main M., Solomon J., Discovery of an insecure disoriented attachment pattern: procedures, findings and implications for the classification of behavior, In: Affective development in infancy (eds. Brazelton T, Youngman M), Norwood, NJ: Ablex, 1986Google Scholar
  10. [10]
    Prior V., Glaser D., Understanding attachment and attachment disorders: theory, evidence, and practice, Jessica Kingsley Publishers: London and Philadelphia, 2006Google Scholar
  11. [11]
    Karen R., Becoming attached: first relationships and how they shape our capacity to love, New York: Oxford University Press, 1994Google Scholar
  12. [12]
    Marvin R. S., Britner P.A., Normative development: the ontogeny of attachment, In: Handbook of attachment: theory, research and clinical applications (eds. Cassidy J, Shaver PR), New York and London: Guilford Press, 2008, 269–294Google Scholar
  13. [13]
    Kobak R., Madsen S., Disruption in attachment bonds, In: Handbook of attachment: theory, research and clinical applications (eds. Cassidy J, Shaver PR), New York and London: Guilford Press, 2008, 23–47Google Scholar
  14. [14]
    Fraley R. C., Shaver P.R., Adult romantic attachment: theoretical developments, emerging controversies, and unanswered questions, Rev. Gen. Psychol., 2000, 4, 132–154CrossRefGoogle Scholar
  15. [15]
    Rholes W. S., Simpson J.A., Attachment theory: basic concepts and contemporary questions, In: Adult attachment: theory, research, and clinical implications (Rholes WS, Simpson JA, eds), New York: Guilford Press, 2004, 3–14Google Scholar
  16. [16]
    Main M., Kaplan N., Cassidy J., Security in infancy, childhood and adulthood: a move to the level of representation, In: Growing points of attachment theory and research (Bretherton I, Waters E, eds), Chicago: University of Chicago Press, 1985Google Scholar
  17. [17]
    Steele H., Steele M., Fonagy P., Associations among attachment classifications of mothers, fathers, and their infants, Child Dev., 1996, 67, 541–555PubMedCrossRefGoogle Scholar
  18. [18]
    Wise R. A., Bozarth M.A., Brain reward circuitry: four circuit elements „wired” in apparent series, Brain Res. Bull., 1984, 12, 203–208PubMedCrossRefGoogle Scholar
  19. [19]
    Arrias-Carrión O., Pŏppel E., Dopamine, learning, and reward-seeking behavior, Acta Neurobiol. Exp., 2007, 67, 481–488Google Scholar
  20. [20]
    Burgdorf J., Panksepp J., The neurobiology of positive emotions, Neurosci. Biobehav. Rev. 2006, 30, 173–187PubMedCrossRefGoogle Scholar
  21. [21]
    Olds J., Milner P., Positive reinforcement produced by electrical stimulation of septal area and other regions of rat brain, J. Comp. Physiol. Psychol., 1954, 47, 419–427PubMedCrossRefGoogle Scholar
  22. [22]
    Olds M. E., Olds J., Emotional and associative mechanisms in the rat brain, J. Comp. Physiol. Psychol., 1961, 54,120–26CrossRefGoogle Scholar
  23. [23]
    Moan C. E., Heath R.G., Septal stimulation for the initiation of heterosexual activity in a homosexual male, J. Behav. Ther. Exp. Psychiatr., 1972, 3, 23–30CrossRefGoogle Scholar
  24. [24]
    Gardner E. L., Lowinson J.H., Drug craving and positive/negative hedonic brain substrates activated by addicting drugs, Sem. Neurosci., 1993, 5, 359–368CrossRefGoogle Scholar
  25. [25]
    Giros B., Jaber M., Jones S.R., Wightman R.M., Caron M.G., Hyperlocomotion and indifference to cocaine and amphetamine in mice lacking the dopamine transporter, Nature, 379, 606–612Google Scholar
  26. [26]
    Wise R. A., Dopamine, learning and motivation, Nat. Rev. Neurosci., 2004, 5, 483–494PubMedCrossRefGoogle Scholar
  27. [27]
    Lisman J. E., Grace A.A., The hippocampal-VTA loop: controlling the entry of information into long-term memory, Neuron, 2005, 46, 703–713PubMedCrossRefGoogle Scholar
  28. [28]
    Pierce R.C., Kumaresan V., The mesolimbic dopamine system: the final common pathway for the reinforcing effect of drugs of abuse?, Neurosci. Biobehav. Rev. 2006, 30, 215–238PubMedCrossRefGoogle Scholar
  29. [29]
    Rothman R. B., Baumann M.H., Balance between dopamine and serotonin release modulates behavioral effects of amphetaminetype drugs, Ann. N.Y. Acad. Sci., 2006, 1074, 245–260PubMedCrossRefGoogle Scholar
  30. [30]
    Kahlig K. M., Binda F., Khoshbouei H., Amphetamine induces dopamine efflux through a dopamine transporter channel, Proc. Natl. Acad. Sci. USA, 2005, 102, 3495–3500PubMedCrossRefGoogle Scholar
  31. [31]
    Gonzales R. A., Job M.O., Doyon W.M., The role of mesolimbic dopamine in the development and maintenance of ethanol reinforcement, Pharmacol. Ther., 2004, 103, 121–146PubMedCrossRefGoogle Scholar
  32. [32]
    Gardner E. L., Endocannabinoid signaling system and brain reward: emphasis on dopamine, Pharmacol. Biochem. Behav., 2005, 81, 263–284PubMedCrossRefGoogle Scholar
  33. [33]
    Schultz W., Dayan P., Montague P.R., A neural substrate of prediction and reward, Science, 1997, 275, 1593–1599PubMedCrossRefGoogle Scholar
  34. [34]
    Schultz W., Behavioral theories and the neurophysiology of reward, Annu. Rev. Psychol. 2006, 57, 87–115PubMedCrossRefGoogle Scholar
  35. [35]
    Bromm B., Brain images of pain, News Physiol. Sci., 2001, 16, 244–249PubMedGoogle Scholar
  36. [36]
    Kringelbach M. L., Rolls E.T., The functional neuroanatomy of the human orbitofrontal cortex: evidence from neuroimaging and neuropsychology, Prog. Neurobiol., 2004, 72, 341–372PubMedCrossRefGoogle Scholar
  37. [37]
    Hof P. R., Mufson E.J., Morrison J.H., Human orbitofrontal cortex: cytoarchitecture and quantitative immunohistochemical parcellation, J. Comp. Neurol., 1995, 359, 48–68PubMedCrossRefGoogle Scholar
  38. [38]
    Kringelbach M. L., The human orbitofrontal cortex: linking reward to hedonic experience, Nat. Rev. Neurosci., 2005, 6, 691–702PubMedCrossRefGoogle Scholar
  39. [39]
    Gogtay N., Giedd J.N., Lusk L., Hayashi K.M., Greenstein D., Vaituzis A.C., et al., Dynamic mapping of human cortical development during childhood through early adulthood. Proc. Natl. Acad. Sci. USA, 2004, 101, 8174–8179PubMedCrossRefGoogle Scholar
  40. [40]
    Brake W. G., Zhang T.Y., Diorio J., Meaney M.J., Gratton A., Influence of early postnatal rearing conditions on mesocorticolimbic dopamine and behavioral responses to psychostimulants and stressors in adult rats, Eur. J. Neurosci., 2004, 19, 1863–1874PubMedCrossRefGoogle Scholar
  41. [41]
    Anderson M. C., Ochsner K.N., Kuhl B., Cooper J., Robertson E., Gabrieli S.W. et al., Neural systems undelying the suppression of unwanted memories, Science, 2004, 303, 232–235PubMedCrossRefGoogle Scholar
  42. [42]
    Bauer H., Pripfl J., Lamm C., Prainsack C., Taylor N., Functional neuroanatomy of learned helplessness, Neuroimage, 2003, 20, 927–939PubMedCrossRefGoogle Scholar
  43. [43]
    Siegal M., Varley R., Neural systems involved in ‘theory of mind’, Nat. Rev. Neurosci. 2002, 3, 463–471PubMedGoogle Scholar
  44. [44]
    Di Pellegrino G., Fadiga L., Fogassi L., Gallese V., Rizzolatti G., Understanding motor events: a neurophysiological study, Exp. Brain Res., 1992, 91, 176–180PubMedCrossRefGoogle Scholar
  45. [45]
    Rizzolatti G., Fabbri-Destro M., Mirror neurons: from discovery to autism, Exp. Brain Res., 2010, 200, 223–237PubMedCrossRefGoogle Scholar
  46. [46]
    Rizzolatti G., Craighero L., The mirror-neuron system, Annu. Rev. Neurosci., 2004, 27, 169–179PubMedCrossRefGoogle Scholar
  47. [47]
    Fabbri-Destro M., Rizzolatti G., The mirror system in monkeys and humans, Physiology, 2008, 23, 171–179PubMedCrossRefGoogle Scholar
  48. [48]
    Iacoboni M., Imitation, empathy, and mirror neurons, Annu. Rev. Psychol., 2009, 60, 653–670PubMedCrossRefGoogle Scholar
  49. [49]
    Rizzolatti G., Arbib M.A., Language within our grasp, Trends Neurosci., 1998, 21, 188–194PubMedCrossRefGoogle Scholar
  50. [50]
    Fadiga L., Craighero L., Buccino G., Rizzolatti G., Speech listening specifically modulates the excitability of tongue muscles: s TMS study, Eur. J. Neurosci., 2002, 15, 399–402PubMedCrossRefGoogle Scholar
  51. [51]
    Watkins K. E., Strafella A.P., Paus T., Seeing and hearing speech excites the motor system involved in speech production, Neuropsychologia, 2003, 41, 989–994PubMedCrossRefGoogle Scholar
  52. [52]
    Wilson S. M., Saygin A.P., Sereno M.I., Iacoboni M., Listening to speech activates motor areas involved in speech production, Nat. Neurosci., 2004, 7, 701–702PubMedCrossRefGoogle Scholar
  53. [53]
    Carr L., Iacoboni M., Dubeau M.C., Mazziotta J.C., Lenzi G.L., Neural mechanisms of empathy in humans: a relay from neural systems for imitation to limbic areas, Proc. Natl. Acad. Sci. USA, 2003, 100, 5497–5502PubMedCrossRefGoogle Scholar
  54. [54]
    Lenzi D., Trentini C., Pantano P., Macaluso E., Iacoboni M., Lenzi G.I., et al., Neural basis of maternal communication and emotional expression processing during infant preverbal stage, Cereb. Cortex, 2009, 19, 1124–1133PubMedCrossRefGoogle Scholar
  55. [55]
    Williams J. H.G., Whiten A., Suddendorf T., Perrett D.I., Imitation, mirror neurons, and autism, Neurosci. Biobehav. Rev., 2001, 25, 287–295PubMedCrossRefGoogle Scholar
  56. [56]
    Iacoboni M., Dapretto M., The mirror neurons system and the consequences of its dysfunction, Nat. Rev. Neurosci., 2006, 7, 942–951PubMedCrossRefGoogle Scholar
  57. [57]
    Rizzolatti G., Fabbri-Destro M., Cattaneo L., Mirror neurons and their clinical relevance, Nat. Clin. Pract. Neurol., 2009, 5, 24–34PubMedCrossRefGoogle Scholar
  58. [58]
    Dapretto M., Davies M.S., Pfeifer J.H., Scott A.A., Sigman M., Bookheimer S.Y. et al., Understanding emotions in others: mirror neuron dysfunction in children with autism spectrum disorder, Nat. Neurosci., 2006, 9, 28–30PubMedCrossRefGoogle Scholar
  59. [59]
    Darwin C. R., The expression of emotions in man and animals, London: John Murray, 1872CrossRefGoogle Scholar
  60. [60]
    Plutchik R., Outlines of a new theory of emotion, Trans. NY Acad. Sci., 1958, 20, 394–403Google Scholar
  61. [61]
    Russell P. A., A circumplex model of affect, J. Pers. Soc. Psychol., 1971, 39, 1161–1178Google Scholar
  62. [62]
    Kolb B., Whishaw I.Q. (eds.), Fundamentals of human neuropsychology, 6th edition, Worth Publishers, 2008Google Scholar
  63. [63]
    Ekman P., Friesen W.V., Constants across culture in the face and emotion, J. Pers. Soc. Psychol., 1971, 17, 124–129PubMedCrossRefGoogle Scholar
  64. [64]
    Shaffer D. R., Social and personality development, 6th edition, Belmont, CA: Wadsworth, 2009Google Scholar
  65. [65]
    Oster H., Emotion in the infant’s face: insights from the study of infants with facial anomalies, Ann. NY Acad. Sci., 2003, 1000, 197–204PubMedCrossRefGoogle Scholar
  66. [66]
    Feldman R., Weller A., Zagoory-Sharon O., Levine A., Evidence for a neuroendocrinological foundation of human affiliation: plasma oxytocin levels across pregnancy and the postpartum period predict mother-infant bonding, Psychol. Sci., 2007, 18, 965–970PubMedCrossRefGoogle Scholar
  67. [67]
    Baumgartner T., Heinrichs M., Vonlanthen A., Fischbacher U., Fehr E, Oxytocin shapes the neural circuitry of trust and trust adaptation in humans, Neuron, 2008, 58, 639–650PubMedCrossRefGoogle Scholar
  68. [68]
    Guastella A. J., Mitchell P.B., Dadds M.R., Oxytocin increases gaze to the eye region of human faces, Biol. Psychiatry, 2008, 63, 3–5PubMedCrossRefGoogle Scholar
  69. [69]
    Olazábal D. E., Young L.J., Oxytocin receptors in the nucleus accumbens facilitate „spontaneous“ maternal behavior in adult female prarie voles, Neuroscience, 2006, 141, 559–568PubMedCrossRefGoogle Scholar
  70. [70]
    Strathearn L., Fonagy P., Amico J., Montague P.R., Adult attachment predicts maternal brain and oxytocin response to infant cues, Neuropsychopharmacology, 2009, 34, 2655–2666PubMedCrossRefGoogle Scholar
  71. [71]
    Bales K. L., van Westerhuyzen J.A., Lewis-Reese A.D., Grotte N.D., Lanter J.A., Carter C.S., Oxytocin has dose-dependent developmental effects on pair-bonding and alloparental care in female prairie voles, Horm. Behav., 2007, 52, 274–279PubMedCrossRefGoogle Scholar
  72. [72]
    Ahern T.H., Young L.J., The impact of early life family structure on adult social attachment, alloparental behavior, and the neuropeptide systems regulating affiliative behaviors in the monogamous prairie vole (Microtus ochrogaster), Front. Behav. Neurosci., 2009, 3, 1–19CrossRefGoogle Scholar
  73. [73]
    Modahl C., Green L., Fein D., Morris M., Waterhouse L., Feinstein C., et al., Plasma oxytocin levels in autistic children, Biol. Psychiatry, 1998, 43, 270–277PubMedCrossRefGoogle Scholar
  74. [74]
    Hollander E., Bartz J., Chaplin W., Phillips A., Sumner J., Soorya L., et al., Oxytocin increases retention of social cognition in autism, Biol. Psychiatry, 2007, 61, 498–503PubMedCrossRefGoogle Scholar
  75. [75]
    Fries A. B., Ziegler T.E., Kurian J.R., Jacoris S., Pollak S.D., Early experience in humans is associated with changes in neuropeptides critical for regulating social behavior, Proc. Natl. Acad. Sci. USA, 2005, 102, 17237–17240PubMedCrossRefGoogle Scholar
  76. [76]
    Chugani H. T., Behen M.E., Muzik O., Juhász C., Nagy F., Chugani D.C., Local brain functional activity following early deprivations: a study of post-institutionalized Romanian orphans, Neuroimage, 2001, 14, 1290–1301PubMedCrossRefGoogle Scholar
  77. [77]
    Heim C., Young L.J., Newport D.J., Mletzko T., Miller A.H., Nemeroff C.B., Lower CSF oxytocin concentrations in women with a history of childhood abuse, Mol. Psychiatry, 2009, 14, 954–958PubMedCrossRefGoogle Scholar
  78. [78]
    Gordon I., Zagoory-Sharon O., Leckman J.F., Feldman R., Prolactin, oxytocin, and the development of paternal behavior across the first six months of fatherhood, Horm. Behav., 2010, Epub ahead of printGoogle Scholar
  79. [79]
    Nagasawa M, Kikusui T, Onaka T, Ohta M, Dog’s gaze at its owner increases owner’s urinary oxytocin during social interaction, Horm. Behav., 2009, 55, 434–441PubMedCrossRefGoogle Scholar
  80. [80]
    Neumann I. D., The advantage of social living: brain neuropeptides mediate the beneficial consequences of sex and motherhood, Front. Bioendocrinol., 2009, 30, 483–496CrossRefGoogle Scholar
  81. [81]
    Leckman J. F., Herman A.E., Maternal behavior and developmental psychopathology, Biol. Psychiatry, 2002, 51, 27–43PubMedCrossRefGoogle Scholar
  82. [82]
    Gammie S. C., Bethea E.D., Stevenson S.A., Altered maternal profiles in corticotropin-releasing factor receptor 1 deficient mice, BMC Neurosci, 2007, 8, 17 doi:10. 1186/1471-2202-8-17PubMedCrossRefGoogle Scholar
  83. [83]
    Gammie S. C., Seasholtz A.F., Stevenson S.A., Deletion of corticotropinreleasing factor binding protein selectively impairs maternal, but not intermale aggression, Neuroscience, 2008, 157, 502–512PubMedCrossRefGoogle Scholar
  84. [84]
    Hansen N. S., Gammie S.C., Trpc 2 gene impacts on maternal aggression, accessory olfactory bulb anatomy and brain activity, Gene Brain Behav, 2009, 8, 639–649CrossRefGoogle Scholar
  85. [85]
    Caspi A., McClay J., Moffitt T.E., Mill J., Martin J., Craig I.W., et al., Role of genotype in the cycle of violence in maltreated children, Science, 2002, 297, 851–854PubMedCrossRefGoogle Scholar
  86. [86]
    Nelson R. J., Trainor B.C., Neural mechanisms of aggression, Nat. Rev. Neurosci., 2007, 8, 536–546PubMedCrossRefGoogle Scholar
  87. [87]
    Pedersen C. A., Biological aspects of social bonding and the roots of human violence, Ann NY Acad SCI, 2004, 1036, 106–127PubMedCrossRefGoogle Scholar
  88. [88]
    Anderson S. W., Bechara A., Damasio H., Tranel D., Damasio A.R., Impairment of social and moral behavior related to early damage in human prefrontal cortex, Nat. Neurosci., 1999, 2, 1032–1037PubMedCrossRefGoogle Scholar
  89. [89]
    Raine A., Lencz T., Bihrle S., LaCasse L., Coilletti P., Reduced prefrontal grey matter volume and reduced autonomic activity in antisocial personality disorder. Arch. Gen. Psychiatry 2000, 57, 119–127PubMedCrossRefGoogle Scholar
  90. [90]
    Kiehl K. A., Smith A.M., Hare R.D., Mendrek A, Forster B.B., Brink J., et al., Limbic abnormalities in affective processing by criminal psychopats as revealed by functional magnetic resonance imaging, Biol Psychiatry 2001, 50, 677–684PubMedCrossRefGoogle Scholar
  91. [91]
    Le Doux J. E., Emotion circuits in the brain, Annu. Rev. Neurosci., 2000, 24, 155–184CrossRefGoogle Scholar
  92. [92]
    Mueller B. R., Bale T.L., Sex-specific programming of offspring emotionality after stress early in pregnancy, J. Neurosci., 2008, 28, 9055–9065PubMedCrossRefGoogle Scholar
  93. [93]
    Champagne FA, Weaver IC, Diorio J, Dymov S, Szyf M, Meaney MJ, Maternal care associated with methylation of the estrogen receptoralpha1b promoter and estrogen receptor-alpha expression in the medial preoptic area of female offspring, Endocrinology, 2006, 147, 2909–2915PubMedCrossRefGoogle Scholar
  94. [94]
    Weaver I. C., Cervoni N, Champagne FA, D’Alessio AC, Sharma S, Seckl J.R., et al., Epigenetic programming by maternal behavior, Nat. Neurosci., 2004, 7, 847–854PubMedCrossRefGoogle Scholar
  95. [95]
    Oberlander T. F., Weinberg J, Papsdorf M, Grunau R, Misri S, Devlin A.M., Prenatal exposure to maternal depression, neonatal methylation of human glucocorticoid receptor gene (NR 3C1) and infant cortisol stress responses, Epigenetics, 2008, 3, 97–106PubMedCrossRefGoogle Scholar
  96. [96]
    Roth TL, Lubin FD, Funk AJ, Sweatt JD, Lasting epigenetic influence of early-life adversity on the BDNF gene, Biol. Psychiatry, 2009, 65, 760–769PubMedCrossRefGoogle Scholar
  97. [97]
    Champagne DL, Bagot RC, van Hasselt F, Ramakers G, Meaney MJ, de Kloet ER, et al., Maternal care and hippocampal plasticity: evidence for experience-dependent structural plasticity, altered synaptic functioning, and differential responsiveness to glucocorticoids and stress, J. Neurosci., 2008, 28, 6037–6045PubMedCrossRefGoogle Scholar
  98. [98]
    Fischer A, Sananbenesi F, Wang X, Dobbin M, Tsai LH, Recovery of learning and memory is associated with chromatin remodelling, Nature, 2007, 447, 178–182PubMedCrossRefGoogle Scholar
  99. [99]
    Arai JA, Li S, Hartley DM, Feig LA, Transgenerational rescue of a genetic defect in long-term potentiation and memory formation by juvenile enrichment, J. Neurosci., 2009, 29, 1496–1502PubMedCrossRefGoogle Scholar
  100. [100]
    Zhou Z., Hong E.J., Cohen S., Zhao W.N., Ho H.Y., Schmidt L., et al., Brain-specific phosphorylation of MeCP 2 regulates activitydependent BDNF transcription, dendritic growth, and spine maturation, Neuron, 2006, 52, 255–269PubMedCrossRefGoogle Scholar
  101. [101]
    Nelson E. D., Kavalali E.T., Monteggia L.M., Activity-dependent suppression of miniature neurotransmission through the regulation of DNA methylation, J. Neurosci., 2008, 28, 395–406PubMedCrossRefGoogle Scholar
  102. [102]
    Moretti P, Zoghbi H. Y., MeCP2 dysfunction in Rett syndrome and related disorders, Curr. Opin. Genet. Dev., 2006, 16, 276–281PubMedCrossRefGoogle Scholar
  103. [103]
    Adachi M, Autry A. E., Covington H.E., Monteggia L.M., MeCP2-mediated transcription repression in the basolateral amygdala may underlie heightened anxiety in a mouse model of Rett syndrome, J. Neurosci., 2009, 29, 4218–4227PubMedCrossRefGoogle Scholar
  104. [104]
    Leslie K. R., Johnson-Frey S.H., Grafton S.T., Functional imaging of face and hand imitation: towards a motor theory of empathy, Neuroimage, 2004, 21, 601–607PubMedCrossRefGoogle Scholar

Copyright information

© © Versita Warsaw and Springer-Verlag Wien 2010

Authors and Affiliations

  • Đurđica Šešo-Šimić
    • 1
  • Goran Sedmak
    • 2
  • Patrick R. Hof
    • 3
  • Goran Šimić
    • 2
  1. 1.Department of PaediatricsZagreb-East Medical CenterZagrebCroatia
  2. 2.Department of Neuroscience, Croatian Institute for Brain ResearchUniversity of Zagreb School of MedicineZagrebCroatia
  3. 3.Department of NeuroscienceMount Sinai School of MedicineNew YorkUSA

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