Reduced visual cortex grey matter volume in children and adolescents with reactive attachment disorder

NeuroImage: Clinical

Volumn 9, Issue , 2015, Pages 13-19

  Shimada, Koji ^a   Takiguchi, Shinichiro ^a   Mizushima, Sakae ^a   Fujisawa, Takashi X ^a   Saito, Daisuke N ^a   Kosaka, Hirotaka ^a   Okazawa, Hidehiko ^a   Tomoda, Akemi ^a  

^a UNIVERSITY OF FUKUI   (Japan)

Author keywords

Child maltreatment; Emotional regulation impairments; Grey matter volume; Reactive attachment disorder; Visual cortex; Voxel based morphometry

Indexed keywords

ADOLESCENT; ARTICLE; BRAIN ANALYSIS; BRAIN SIZE; CHILD; CLINICAL ARTICLE; CONTROLLED CLINICAL TRIAL; CONTROLLED STUDY; FEMALE; GRAY MATTER; HUMAN; MALE; NEUROIMAGING; NUCLEAR MAGNETIC RESONANCE IMAGING; OCCIPITAL CORTEX; PRIORITY JOURNAL; PSYCHOLOGIC TEST; PSYCHOSOCIAL DISORDER; STRENGTH AND DIFFICULTIES QUESTIONNAIRE; STRIATE CORTEX; TEMPORAL CORTEX; THALAMUS; VISUAL CORTEX; VOXEL BASED MORPHOMETRY; WECHSLER INTELLIGENCE SCALE; BRAIN; HEMISPHERIC DOMINANCE; MENTAL STRESS; PATHOLOGY;

ADOLESCENT; BRAIN; CHILD; FEMALE; FUNCTIONAL LATERALITY; GRAY MATTER; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; REACTIVE ATTACHMENT DISORDER; STRESS, PSYCHOLOGICAL; VISUAL CORTEX;

EID: 84938822211     PISSN: None     EISSN: 22131582     Source Type: Journal    
DOI: 10.1016/j.nicl.2015.07.001     Document Type: Article

References (78)

1. Edwards V.J., Holden G.W., Felitti V.J., and Anda R.F. Relationship between multiple forms of childhood maltreatment and adult mental health in community respondents: results from the adverse childhood experiences study Am. J. Psychiatry 160 8 2003 1453 1460 10.1176/appi.ajp.160.8.1453 12900308
2. Gilbert R., Widom C.S., Browne K., Fergusson D., Webb E., and Janson S. Burden and consequences of child maltreatment in high-income countries Lancet 373 9657 2009 68 81 10.1016/S0140-6736(08)61706-7 19056114
3. American Psychiatric Association Diagnostic and Statistical Manual of Mental Disorders fifth edition (DSM-v) 2013 American Psychiatric Association Washington, DC
4. Lehmann S., Havik O.E., Havik T., and Heiervang E.R. Mental disorders in foster children: a study of prevalence, comorbidity and risk factors Child Adolesc. Psychiatry Ment. Health 7 1 2013 39 10.1186/1753-2000-7-39 24256809
5. Zeanah C.H., Scheeringa M., Boris N.W., Heller S.S., Smyke A.T., and Trapani J. Reactive attachment disorder in maltreated toddlers Child Abus. Negl. 28 8 2004 877 888 10.1016/j.chiabu.2004.01.010 15350771
6. Minnis H., Macmillan S., Pritchett R., Young D., Wallace B., Butcher J., Sim F., Baynham K., Davidson C., and Gillberg C. Prevalence of reactive attachment disorder in a deprived population Br. J. Psychiatry 202 5 2013 342 346 10.1192/bjp.bp.112.114074 23580380
7. Pritchett R., Pritchett J., Marshall E., Davidson C., and Minnis H. Reactive attachment disorder in the general population: a hidden ESSENCE disorder. Scientific World J. 2013 2013 818157
8. Zeanah C.H., and Gleason M.M. Annual research review: attachment disorders in early childhood - clinical presentation, causes, correlates, and treatment J. Child Psychol. Psychiatry 56 3 2015 207 222 10.1111/jcpp.12347 25359236
9. Zilberstein K. Clarifying core characteristics of attachment disorders: a review of current research and theory Am. J. Orthopsychiatr. 76 1 2006 55 64 10.1037/0002-9432.76.1.55 16569127
10. Minnis H., Green J., O'Connor T.G., Liew A., Glaser D., Taylor E., Follan M., Young D., Barnes J., Gillberg C., Pelosi A., Arthur J., Burston A., Connolly B., and Sadiq F.A. An exploratory study of the association between reactive attachment disorder and attachment narratives in early school-age children J. Child Psychol. Psychiatry 50 8 2009 931 942 10.1111/j.1469-7610.2009.02075.x 19344386
11. Minnis H., Reekie J., Young D., O'Connor T.O.M., Ronald A., Gray A., and Plomin R. Genetic, environmental and gender influences on attachment disorder behaviours Br. J. Psychiatry 190 2007 490 495 10.1192/bjp.bp.105.019745 17541108
12. Vervoort E., De Schipper J.C., Bosmans G., and Verschueren K. Screening symptoms of reactive attachment disorder: evidence for measurement invariance and convergent validity Int. J. Methods Psychiatr. Res. 22 3 2013 256 265 10.1002/mpr.1395 24022942
13. American Psychiatric Association Diagnostic and Statistical Manual of Mental Disorders third edition 1980 American Psychiatric Association Washington, DC
14. Bowlby J. Attachment and Loss, Volume Two: Separation, Anxiety and Anger 1973 Basic Books New York
15. Bowlby J. The making and breaking of affectional bonds: I. Aetiology and psychopathology in the light of attachment theory Br. J. Psychiatry 130 1977 201 210 10.1192/bjp.130.3.201 843768
16. Hart H., and Rubia K. Neuroimaging of child abuse: a critical review Front. Hum. Neurosci. 6 2012 52 10.3389/fnhum.2012.00052 22457645
17. Lim L., Radua J., and Rubia K. Gray matter abnormalities in childhood maltreatment: a voxel-wise meta-analysis Am. J. Psychiatry 171 8 2014 854 863 10.1176/appi.ajp.2014.13101427 24781447
18. McCrory E., De Brito S.A., and Viding E. The impact of childhood maltreatment: a review of neurobiological and genetic factors Front. Psychiatry 2 2011 48 10.3389/fpsyt.2011.00048 21847382
19. Teicher M.H., and Samson J.A. Childhood maltreatment and psychopathology: a case for ecophenotypic variants as clinically and neurobiologically distinct subtypes Am. J. Psychiatry 170 10 2013 1114 1133 10.1176/appi.ajp.2013.12070957 23982148
20. Liao M., Yang F., Zhang Y., He Z., Song M., Jiang T., Li Z., Lu S., Wu W., Su L., and Li L. Childhood maltreatment is associated with larger left thalamic gray matter volume in adolescents with generalized anxiety disorder PLOS One 8 8 2013 e71898 10.1371/journal.pone.0071898 23951265
21. Tomoda A., Navalta C.P., Polcari A., Sadato N., and Teicher M.H. Childhood sexual abuse is associated with reduced gray matter volume in visual cortex of young women Biol. Psychiatry 66 7 2009 642 648 10.1016/j.biopsych.2009.04.021 19560122
22. Tomoda A., Polcari A., Anderson C.M., and Teicher M.H. Reduced visual cortex gray matter volume and thickness in young adults who witnessed domestic violence during childhood PLOS One 7 12 2012 e52528 10.1371/journal.pone.0052528 23300699
23. Tomoda A., Sheu Y.-S., Rabi K., Suzuki H., Navalta C.P., Polcari A., and Teicher M.H. Exposure to parental verbal abuse is associated with increased gray matter volume in superior temporal gyrus Neuroimage 54 Suppl. 1 2011 S280 S286 10.1016/j.neuroimage.2010.05.027 20483374
24. Carrion V.G., Weems C.F., Watson C., Eliez S., Menon V., and Reiss A.L. Converging evidence for abnormalities of the prefrontal cortex and evaluation of midsagittal structures in pediatric posttraumatic stress disorder: an MRI study Psychiatry Res 172 3 2009 10.1016/j.pscychresns.2008.07.008 19349151
25. De Brito S.A., Viding E., Sebastian C.L., Kelly P.A., Mechelli A., Maris H., and McCrory E.J. Reduced orbitofrontal and temporal grey matter in a community sample of maltreated children J. Child Psychol. Psychiatry 54 1 2013 105 112 10.1111/j.1469-7610.2012.02597.x 22880630
26. Tomoda A., Suzuki H., Rabi K., Sheu Y.-S., Polcari A., and Teicher M.H. Reduced prefrontal cortical gray matter volume in young adults exposed to harsh corporal punishment Neuroimage 47 Suppl. 2 2009 T66 T71 10.1016/j.neuroimage.2009.03.005 19285558
27. van Harmelen A.-L., van Tol M.-J., van der Wee N.J.A., Veltman D.J., Aleman A., Spinhoven P., van Buchem M.A., Zitman F.G., Penninx B.W.J.H., and Elzinga B.M. Reduced medial prefrontal cortex volume in adults reporting childhood emotional maltreatment Biol. Psychiatry 68 9 2010 832 838 10.1016/j.biopsych.2010.06.011 20692648
28. Dannlowski U., Stuhrmann A., Beutelmann V., Zwanzger P., Lenzen T., Grotegerd D., Domschke K., Hohoff C., Ohrmann P., Bauer J., Lindner C., Postert C., Konrad C., Arolt V., Heindel W., Suslow T., and Kugel H. Limbic scars: long-term consequences of childhood maltreatment revealed by functional and structural magnetic resonance imaging Biol. Psychiatry 71 4 2012 286 293 10.1016/j.biopsych.2011.10.021 22112927
29. Hanson J.L., Nacewicz B.M., Sutterer M.J., Cayo A.A., Schaefer S.M., Rudolph K.D., Shirtcliff E.A., Pollak S.D., and Davidson R.J. Behavioral problems after early life stress: contributions of the hippocampus and amygdala Biol. Psychiatry 77 4 2015 314 323 10.1016/j.biopsych.2014.04.020 24993057
30. Teicher M.H., Anderson C.M., and Polcari A. Childhood maltreatment is associated with reduced volume in the hippocampal subfields CA3, dentate gyrus, and subiculum Proc. Natl. Acad. Sci. U. S. A. 109 9 2012 E563 E572 10.1073/pnas.1115396109 22331913
31. Edmiston E.E., Wang F., Mazure C.M., Guiney J., Sinha R., Mayes L.C., and Blumberg H.P. Corticostriatal-limbic gray matter morphology in adolescents with self-reported exposure to childhood maltreatment Arch. Pediatr. Adolesc. Med. 165 12 2011 1069 1077 10.1001/archpediatrics.2011.565 22147775
32. Mehta M.A., Golembo N.I., Nosarti C., Colvert E., Mota A., Williams S.C.R., Rutter M., and Sonuga-Barke E.J.S. Amygdala, hippocampal and corpus callosum size following severe early institutional deprivation: the English and Romanian Adoptees Study Pilot J. Child Psychol. Psychiatry 50 8 2009 943 951 10.1111/j.1469-7610.2009.02084.x 19457047
33. Tottenham N., Hare T.A., Quinn B.T., McCarry T.W., Nurse M., Gilhooly T., Millner A., Galvan A., Davidson M.C., Eigsti I.-M., Thomas K.M., Freed P.J., Booma E.S., Gunnar M.R., Altemus M., Aronson J., and Casey B.J. Prolonged institutional rearing is associated with atypically large amygdala volume and difficulties in emotion regulation Dev. Sci. 13 1 2010 46 61 10.1111/j.1467-7687.2009.00852.x 20121862
34. Sheehan D.V., Sheehan K.H., Shytle R.D., Janavs J., Bannon Y., Rogers J.E., Milo K.M., Stock S.L., and Wilkinson B. Reliability and validity of the Mini International neuropsychiatric interview for children and adolescents (MINI-KID) J. Clin. Psychiatry 71 3 2010 313 326 10.4088/JCP.09m05305whi 20331933
35. Orvaschel H., and Puig-Antich J. Schedule for Affective Disorders and Schizophrenia for School-Age Children - Epidemiologic Version (K-SADS-E) fifth edition 1994 Nova Southeastern University Fort Lauderdale, FL
36. Suzuki H., and Tomoda A. Roles of attachment and self-esteem: impact of early life stress on depressive symptoms among Japanese institutionalized children B.M.C. Psychiatry 15 2015 8 10.1186/s12888-015-0385-1 25651759
37. Wechsler D. Wechsler Intelligence Scale for Children third edition 1991 Psychological Corporation San Antonio, TX
38. Wechsler D. Wechsler Intelligence Scale for Children fourth edition 2003 Psychological Corporation San Antonio, TX
39. Wechsler D. Wechsler Adult Intelligence Scale third edition 1997 Psychological Corporation San Antonio, TX
40. Oldfield R.C. The assessment and analysis of handedness: the Edinburgh Inventory Neuropsychologia 9 1 1971 97 113 10.1016/0028-3932(71)90067-4 5146491
41. Birleson P. The validity of depressive disorder in childhood and the development of a self-rating scale: a research report J. Child Psychol. Psychiatry 22 1 1981 73 88 10.1111/j.1469-7610.1981.tb00533.x 7451588
42. Briere J. Trauma Symptom Checklist for Children (TSCC) 1996 Psychological Assessment Resources Odessa, FL
43. Goodman A., Lamping D.L., and Ploubidis G.B. When to use broader internalising and externalising subscales instead of the hypothesised five subscales on the Strengths and Difficulties Questionnaire (SDQ): data from British parents, teachers and children J. Abnorm. Child Psychol. 38 8 2010 1179 1191 10.1007/s10802-010-9434-x 20623175
44. Goodman R. The strengths and difficulties questionnaire: a research note J. Child Psychol. Psychiatry 38 5 1997 581 586 10.1111/j.1469-7610.1997.tb01545.x 9255702
45. Arendt K., Hougaard E., and Thastum M. Psychometric properties of the child and parent versions of Spence children's Anxiety Scale in a Danish community and clinical sample J. Anxiety Disord. 28 8 2014 947 956 10.1016/j.janxdis.2014.09.021 25445085
46. Kočovská E., Puckering C., Follan M., Smillie M., Gorski C., Barnes J., Wilson P., Young D., Lidstone E., Pritchett R., Hockaday H., and Minnis H. Neurodevelopmental problems in maltreated children referred with indiscriminate friendliness Res. Dev. Disabil. 33 5 2012 1560 1565 10.1016/j.ridd.2012.02.016 22522215
47. DuPaul G.J., Power T.J., Anastopoulos A., and Reid D. ADHD Rating Scale-IV: Checklists, Norms, and Clinical Interpretation 1998 Guilford Press New York
48. Gleason M.M., Fox N.A., Drury S., Smyke A., Egger H.L., Nelson C.A. III, Gregas M.C., and Zeanah C.H. Validity of evidence-derived criteria for reactive attachment disorder: indiscriminately social/disinhibited and emotionally withdrawn/inhibited types J. Am. Acad. Child Adolesc. Psychiatry 50 3 2011 216 231.e3 10.1016/j.jaac.2010.12.012 21334562
49. Baron-Cohen S., Hoekstra R.A., Knickmeyer R., and Wheelwright S. The autism-spectrum quotient (AQ) - adolescent version J. Autism Dev. Disord. 36 3 2006 343 350 10.1007/s10803-006-0073-6 16552625
50. Ashburner J., and Friston K.J. Voxel-based morphometry: the methods Neuroimage 11 6 Pt 1 2000 805 821 10.1006/nimg.2000.0582 10860804
51. Ashburner J. A fast diffeomorphic image registration algorithm Neuroimage 38 1 2007 95 113 10.1016/j.neuroimage.2007.07.007 17761438
52. Ridgway G.R., Omar R., Ourselin S., Hill D.L., Warren J.D., and Fox N.C. Issues with threshold masking in voxel-based morphometry of atrophied brains Neuroimage 44 1 2009 99 111 10.1016/j.neuroimage.2008.08.045 18848632
53. Hayasaka S., Phan K.L., Liberzon I., Worsley K.J., and Nichols T.E. Nonstationary cluster-size inference with random field and permutation methods Neuroimage 22 2 2004 676 687 10.1016/j.neuroimage.2004.01.041 15193596
54. Rorden C., Karnath H.-O., and Bonilha L. Improving lesion-symptom mapping J. Cogn. Neurosci. 19 7 2007 1081 1088 10.1162/jocn.2007.19.7.1081 17583985
55. Fennema-Notestine C., Stein M.B., Kennedy C.M., Archibald S.L., and Jernigan T.L. Brain morphometry in female victims of intimate partner violence with and without posttraumatic stress disorder Biol. Psychiatry 52 11 2002 1089 1101 10.1016/S0006-3223(02)01413-0 12460692
56. Hubel D.H., and Wiesel T.N. Early exploration of the visual cortex Neuron 20 3 1998 401 412 10.1016/S0896-6273(00)80984-8 9539118
57. Amaral D.G., Behniea H., and Kelly J.L. Topographic organization of projections from the amygdala to the visual cortex in the macaque monkey Neuroscience 118 4 2003 1099 1120 10.1016/S0306-4522(02)01001-1 12732254
58. Catani M., Jones D.K., Donato R., and ffytche D.H. Occipito-temporal connections in the human brain Brain 126 9 2003 2093 2107 10.1093/brain/awg203 12821517
59. Adolphs R. Emotional vision Nat. Neurosci. 7 11 2004 1167 1168 10.1038/nn1104-1167 15508009
60. Vuilleumier P. How brains beware: neural mechanisms of emotional attention Trends Cogn. Sci. (Regul. Ed.) 9 12 2005 585 594 10.1016/j.tics.2005.10.011 16289871
61. Lim S.-L., Padmala S., and Pessoa L. Segregating the significant from the mundane on a moment-to-moment basis via direct and indirect amygdala contributions Proc. Natl. Acad. Sci. U. S. A. 106 39 2009 16841 16846 10.1073/pnas.0904551106 19805383
62. Pessoa L., and Adolphs R. Emotion processing and the amygdala: from a 'low road' to 'many roads' of evaluating biological significance Nat. Rev. Neurosci. 11 11 2010 773 783 10.1038/nrn2920 20959860
63. Choi J., Jeong B., Polcari A., Rohan M.L., and Teicher M.H. Reduced fractional anisotropy in the visual limbic pathway of young adults witnessing domestic violence in childhood Neuroimage 59 2 2012 1071 1079 10.1016/j.neuroimage.2011.09.033 21985907
64. Huang H., Gundapuneedi T., and Rao U. White matter disruptions in adolescents exposed to childhood maltreatment and vulnerability to psychopathology Neuropsychopharmacology 37 12 2012 2693 2701 10.1038/npp.2012.133 22850736
65. Koizumi M., and Takagishi H. The relationship between child maltreatment and emotion recognition PLOS One 9 1 2014 e86093 10.1371/journal.pone.0086093 24465891
66. Prete G., Laeng B., Fabri M., Foschi N., and Tommasi L. Right hemisphere or valence hypothesis, or both? The processing of hybrid faces in the intact and callosotomized brain Neuropsychologia 68 2015 94 106 10.1016/j.neuropsychologia.2015.01.002 25575451
67. Ahern G.L., and Schwartz G.E. Differential lateralization for positive and negative emotion in the human brain: EEG spectral analysis Neuropsychologia 23 6 1985 745 755 10.1016/0028-3932(85)90081-8 4080136
68. Davidson R.J., Ekman P., Saron C.D., Senulis J.A., and Friesen W.V. Approach-withdrawal and cerebral asymmetry: emotional expression and brain physiology I J. Pers. Soc. Psychol. 58 2 1990 330 341 10.1037/0022-3514.58.2.330 2319445
69. Silberman E.K., and Weingartner H. Hemispheric lateralization of functions related to emotion Brain Cogn. 5 3 1986 322 353 10.1016/0278-2626(86)90035-7 3530287
70. Jansari A., Rodway P., and Goncalves S. Identifying facial emotions: valence specific effects and an exploration of the effects of viewer gender Brain Cogn. 76 3 2011 415 423 10.1016/j.bandc.2011.03.009 21514027
71. Calvo M.G., and Beltrán D. Brain lateralization of holistic versus analytic processing of emotional facial expressions Neuroimage 92 2014 237 247 10.1016/j.neuroimage.2014.01.048 24495810
72. Li L., Wu M., Liao Y., Ouyang L., Du M., Lei D., Chen L., Yao L., Huang X., and Gong Q. Grey matter reduction associated with posttraumatic stress disorder and traumatic stress Neurosci. Biobehav. Rev. 43 2014 163 172 10.1016/j.neubiorev.2014.04.003 24769403
73. Proal E., Reiss P.T., Klein R.G., and et al. Brain gray matter deficits at 33-year follow-up in adults with attention-deficit/hyperactivity disorder established in childhood Arch. Gen. Psychiatry 68 11 2011 1122 1134 10.1001/archgenpsychiatry.2011.117 22065528
74. Castellanos F.X., and Proal E. Large-scale brain systems in ADHD: beyond the prefrontal-striatal model Trends Cogn. Sci. (Regul. Ed.) 16 1 2012 17 26 10.1016/j.tics.2011.11.007 22169776
75. De Bellis M.D., Woolley D.P., and Hooper S.R. Neuropsychological findings in pediatric maltreatment: relationship of PTSD, dissociative symptoms, and abuse/neglect indices to neurocognitive outcomes Child Maltreat. 18 3 2013 171 183 10.1177/1077559513497420 23886642
76. Smyke A.T., Zeanah C.H., Gleason M.M., Drury S.S., Fox N.A., Nelson C.A., and Guthrie D. A randomized controlled trial comparing foster care and institutional care for children with signs of reactive attachment disorder Am. J. Psychiatry 169 5 2012 508 514 10.1176/appi.ajp.2011.11050748 22764361
77. Blakemore S.-J., Burnett S., and Dahl R.E. The role of puberty in the developing adolescent brain Hum. Brain Mapp. 31 6 2010 926 933 10.1002/hbm.21052 20496383
78. Kay C., and Green J. Reactive attachment disorder following early maltreatment: systematic evidence beyond the institution J. Abnorm. Child Psychol. 41 4 2013 571 581 10.1007/s10802-012-9705-9 23250477