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RETRACTED - Ventral striatum dysfunction in children and adolescents with reactive attachment disorder: functional MRI study

Published online by Cambridge University Press:  02 January 2018

Shinichiro Takiguchi ,
Takashi X. Fujisawa ,
Sakae Mizushima ,
Daisuke N. Saito ,
Yuko Okamoto ,
Koji Shimada ,
Michiko Koizumi ,
Hirokazu Kumazaki ,
Minyoung Jung  and
Hirotaka Kosaka
...Show all authors
Shinichiro Takiguchi
Affiliation:
Advanced Biomedical Sciences Course, Graduate School of Medical Sciences, and Research Center for Child Mental Development, University of Fukui, Fukui, Japan
Takashi X. Fujisawa
Affiliation:
Division of Developmental Higher Brain Functions, United Graduate School of Child Development, and Research Center for Child Mental Development, University of Fukui, Fukui, Japan
Sakae Mizushima
Affiliation:
Division of Developmental Higher Brain Functions, United Graduate School of Child Development, and Research Center for Child Mental Development, University of Fukui, Fukui, Japan
Daisuke N. Saito
Affiliation:
Division of Developmental Higher Brain Functions, United Graduate School of Child Development, University of Fukui, Research Center for Child Mental Development, University of Fukui, and Biomedical Imaging Research Center, University of Fukui, Fukui, Japan
Yuko Okamoto
Affiliation:
Division of Developmental Higher Brain Functions, United Graduate School of Child Development, University of Fukui, Fukui, Research Center for Child Mental Development, University of Fukui, Fukui
Koji Shimada
Affiliation:
Division of Developmental Higher Brain Functions, United Graduate School of Child Development, University of Fukui, Research Center for Child Mental Development, University of Fukui, and Biomedical Imaging Research Center, University of Fukui, Fukui, Japan
Michiko Koizumi
Affiliation:
Research Center for Child Mental Development, University of Fukui, Fukui, Japan
Hirokazu Kumazaki
Affiliation:
Division of Developmental Higher Brain Functions, United Graduate School of Child Development, and Research Center for Child Mental Development, University of Fukui, Fukui, Japan
Minyoung Jung
Affiliation:
Division of Developmental Higher Brain Functions, United Graduate School of Child Development, and Research Center for Child Mental Development, University of Fukui, Fukui, Japan
Hirotaka Kosaka
Affiliation:
Division of Developmental Higher Brain Functions, United Graduate School of Child Development, University of Fukui, Research Center for Child Mental Development, University of Fukui, and Department of Neuropsychiatry, Faculty of Medical Sciences, University of Fukui, Fukui, Japan
Michio Hiratani
Affiliation:
Research Center for Child Mental Development, University of Fukui, Hiratani Clinic for Developmental Disorders of Children, Fukui, Japan
Yusei Ohshima
Affiliation:
Research Center for Child Mental Development, and Department of Pediatrics, Faculty of Medical Sciences, University of Fukui, Fukui, Japan
Martin H. Teicher
Affiliation:
Developmental Biopsychiatry Research Program, McLean Hospital, Belmont, Massachusetts, Department of Psychiatry, Harvard Medical School, Boston, Massachusetts, USA
Akemi Tomoda*
Affiliation:
Division of Developmental Higher Brain Functions, United Graduate School of Child Development, and Research Center for Child Mental Development, University of Fukui, Fukui
*
Akemi Tomoda, Research Center for Child Mental Development, University of Fukui, 23-3 Matsuoka-Shimoaizuki, Eiheiji-cho, Fukui 910-1193, Japan. Email: atomoda@u-fukui.ac.jp
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Abstract

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Background

Child maltreatment is a major risk factor for psychopathology, including reactive attachment disorder (RAD).

Aims

To examine whether neural activity during reward processing was altered in children and adolescents with RAD.

Method

Sixteen children and adolescents with RAD and 20 typically developing (TD) individuals performed tasks with high and low monetary rewards while undergoing functional magnetic resonance imaging.

Results

Significantly reduced activity in the caudate and nucleus accumbens was observed during the high monetary reward condition in the RAD group compared with the TD group (P=0.015, family-wise error-corrected cluster level). Significant negative correlations between bilateral striatal activity and avoidant attachment were observed in the RAD and TD groups.

Conclusions

Striatal neural reward activity in the RAD group was markedly decreased. The present results suggest that dopaminergic dysfunction occurs in the striatum of children and adolescents with RAD, leading towards potential future risks for psychopathology.

Type
Research Article
Information
BJPsych Open , Volume 1 , Issue 2 , October 2015 , pp. 121 - 128
Creative Commons
Creative Common License - CCCreative Common License - BYCreative Common License - NCCreative Common License - ND
This is an open access article distributed under the terms of the Creative Commons Non-Commercial, No Derivatives (CC BY-NC-ND) licence (http://creativecommons.org/licenses/by-nc-nd/4.0/).
Copyright
Copyright © The Royal College of Psychiatrists 2015

Footnotes

Declaration of interest

None.

References

1 Minnis, H, Macmillan, S, Pritchett, R, Young, D, Wallace, B, Butcher, J, et al. Prevalence of reactive attachment disorder in a deprived population. Br J Psychiatry 2013; 202: 342–6.CrossRefGoogle Scholar
2 Zeanah, CH, Scheeringa, M, Boris, NW, Heller, SS, Smyke, AT, Trapani, J. Reactive attachment disorder in maltreated toddlers. Child Abuse Negl 2004; 28: 877–88.CrossRefGoogle ScholarPubMed
3 Lehmann, S, Havik, OE, Havik, T, Heiervang, ER. Mental disorders in foster children: a study of prevalence, comorbidity and risk factors. Child Adolesc Psychiatry Ment Health 2013; 7: 39.CrossRefGoogle ScholarPubMed
4 American Psychiatric Association. Diagnostic and Statistical Manual of Mental Disorders, 5th edition (DSM-5). APA, 2013.Google Scholar
5 Gleason, MM, Fox, NA, Drury, S, Smyke, A, Egger, HL, Nelson, CA 3rd, et al. Validity of evidence-derived criteria for reactive attachment disorder: indiscriminately social/disinhibited and emotionally withdrawn/inhibited types. J Am Acad Child Adolesc Psychiatry 2011; 50: 216–31.e3.CrossRefGoogle ScholarPubMed
6 Guttmann-Steinmetz, S, Crowell, JA. Attachment and externalizing disorders: a developmental psychopathology perspective. J Am Acad Child Adolesc Psychiatry 2006; 45: 440–51.CrossRefGoogle ScholarPubMed
7 Kay, C, Green, J. Reactive attachment disorder following early maltreatment: systematic evidence beyond the institution. J Abnorm Child Psychol 2013; 41: 571–81.CrossRefGoogle ScholarPubMed
8 Kocovska, E, Puckering, C, Follan, M, Smillie, M, Gorski, C, Barnes, J, et al. Neurodevelopmental problems in maltreated children referred with indiscriminate friendliness. Res Dev Disabil 2012; 33: 1560–5.CrossRefGoogle ScholarPubMed
9 Andersen, SL, Teicher, MH. Desperately driven and no brakes: developmental stress exposure and subsequent risk for substance abuse. Neurosci Biobehav Rev 2009; 33: 516–24.CrossRefGoogle ScholarPubMed
10 Pechtel, P, Woodman, A, Lyons-Ruth, K. Early maternal withdrawal and nonverbal childhood IQ as precursors for substance use disorder in young adulthood: results of a 20-year prospective study. IntJCogn Ther 2012; 5: 316–29.Google ScholarPubMed
11 van der Vegt, EJM, van der Ende, J, Ferdinand, RF, Verhulst, FC, Tiemeier, H. Early childhood adversities and trajectories of psychiatric problems in adoptees: evidence for long lasting effects. J Abnorm Child Psychol 2009; 37: 239–49.CrossRefGoogle ScholarPubMed
12 O'Connor, TG, Rutter, M. Attachment disorder behavior following early severe deprivation: extension and longitudinal follow-up. English and Romanian Adoptees Study Team. J Am Acad Child Adolesc Psychiatry 2000; 39: 703–12.CrossRefGoogle ScholarPubMed
13 Green, J, Goldwyn, R. Annotation: attachment disorganisation and psychopathology: new findings in attachment research and their potential implications for developmental psychopathology in childhood. J Child Psychol Psychiatry 2002; 43: 835–46.CrossRefGoogle ScholarPubMed
14 Dichter, GS, Damiano, CA, Allen, JA. Reward circuitry dysfunction in psychiatric and neurodevelopmental disorders and genetic syndromes: animal models and clinical findings. J Neurodev Disord 2012; 4: 19.CrossRefGoogle ScholarPubMed
15 Shimada, K, Takiguchi, S, Mizushima, S, Fujisawa, TX, Saito, DN, Kosaka, H, et al. Reduced visual cortex grey matter volume in children and adolescents with reactive attachment disorder. Neuroimage Clin 2015; 9:13–9.CrossRefGoogle ScholarPubMed
16 Izuma, K, Saito, DN, Sadato, N. Processing of social and monetary rewards in the human striatum. Neuron 2008; 58: 284–94.CrossRefGoogle ScholarPubMed
17 Haber, SN, Knutson, B. The reward circuit: linking primate anatomy and human imaging. Neuropsychopharmacology 2010; 35:4–26.CrossRefGoogle ScholarPubMed
18 Sheehan, DV, Sheehan, KH, Shytle, RD, Janavs, J, Bannon, Y, Rogers, JE, et al. Reliability and validity of the Mini International Neuropsychiatric Interview for Children and Adolescents (MINI-KID). J Clin Psychiatry 2010; 71: 313–26.CrossRefGoogle ScholarPubMed
19 Suzuki, H, Tomoda, A. Roles of attachment and self-esteem: impact of early life stress on depressive symptoms among Japanese institutionalized children. BMC Psychiatry 2015; 15:8.CrossRefGoogle ScholarPubMed
20 American Psychiatric Association. Diagnostic and Statistical Manual of Mental Disorders, 4th edition (DSM-IV). APA, 1994.Google Scholar
21 Wechsler, D. Wechsler Intelligence Scale for Children-Fourth Edition. Psychological Corporation, 2003.Google Scholar
22 Sanders, B, Becker-Lausen, E. The measurement of psychological maltreatment: early data on the Child Abuse and Trauma Scale. Child Abuse Negl 1995; 19: 315–23.CrossRefGoogle ScholarPubMed
23 Hazan, C, Shaver, P. Romantic love conceptualized as an attachment process. J Pers Soc Psychol 1987; 52: 511–24.CrossRefGoogle ScholarPubMed
24 Achenbach, TM. Manual for the Child Behavior Checklist/4–18 and 1991 Profile. Department of Psychiatry, University of Vermont, 1991.Google Scholar
25 Birleson, P. The validity of depressive disorder in childhood and the development of a self-rating scale: a research report. J Child Psychol Psychiatry 1981; 22: 73–88.CrossRefGoogle Scholar
26 Asukai, N, Kato, H, Kawamura, N, Kim, Y, Yamamoto, K, Kishimoto, J, et al. Reliability and validity of the Japanese-language version of the impact of event scale-revised (IES-R-J): four studies of different traumatic events. J Nerv Ment Dis 2002; 190: 175–82.CrossRefGoogle ScholarPubMed
27 Wakabayashi, A, Baron-Cohen, S, Uchiyama, T, Yoshida, Y, Tojo, Y, Kuroda, M, et al. The autism-spectrum quotient (AQ) children's version in Japan: a cross-cultural comparison. J Autism Dev Disord 2007; 37: 491–500.CrossRefGoogle ScholarPubMed
28 Yamazaki, K. ADHD-RS-IV Japanese Versions. Japanese Guideline for the Diagnosis and Treatment of Attention Deficit Hyperactivity Disorder (ADHD). Jiho, 2003; 48–54.Google Scholar
29 Goodman, R. The strengths and difficulties questionnaire: a research note. J Child Psychol Psychiatry 1997; 38: 581–6.CrossRefGoogle ScholarPubMed
30 Mizuno, K, Yoneda, T, Komi, M, Hirai, T, Watanabe, Y, Tomoda, A. Osmotic release oral system-methylphenidate improves neural activity during low reward processing in children and adolescents with attention-deficit/hyperactivity disorder. Neuroimage Clin 2013; 2: 366–76.CrossRefGoogle ScholarPubMed
31 Edmiston, EE, Wang, F, Mazure, CM, Guiney, J, Sinha, R, Mayes, LC, et al. Corticostriatal-limbic gray matter morphology in adolescents with self-reported exposure to childhood maltreatment. Arch Pediatr Adolesc Med 2011; 165: 1069–77.CrossRefGoogle ScholarPubMed
32 Neubauer, AC, Fink, A. Intelligence and neural efficiency. Neurosci Biobehav Rev 2009; 33: 1004–23.CrossRefGoogle ScholarPubMed
33 Pizzagalli, DA, Holmes, AJ, Dillon, DG, Goetz, EL, Birk, JL, Bogdan, R, et al. Reduced caudate and nucleus accumbens response to rewards in unmedicated individuals with major depressive disorder. Am J Psychiatry 2009; 166: 702–10.CrossRefGoogle ScholarPubMed
34 Strobl, C, Boulesteix, AL, Zeileis, A, Hothorn, T. Bias in random forest variable importance measures: illustrations, sources and a solution. BMC Bioinformatics 2007; 8: 25.CrossRefGoogle ScholarPubMed
35 Tomoda, A, Polcari, A, Anderson, CM, Teicher, MH. Reduced visual cortex gray matter volume and thickness in young adults who witnessed domestic violence during childhood. PLoS One 2012; 7: e52528.CrossRefGoogle ScholarPubMed
36 Mehta, MA, Gore-Langton, E, Golembo, N, Colvert, E, Williams, SC, Sonuga-Barke, E. Hyporesponsive reward anticipation in the basal ganglia following severe institutional deprivation early in life. J Cogn Neurosci 2010; 22: 2316–25.CrossRefGoogle ScholarPubMed
37 Dillon, DG, Holmes, AJ, Birk, JL, Brooks, N, Lyons-Ruth, K, Pizzagalli, DA. Childhood adversity is associated with left basal ganglia dysfunction during reward anticipation in adulthood. Biol Psychiatry 2009; 66: 206–13.CrossRefGoogle ScholarPubMed
38 Boecker, R, Holz, NE, Buchmann, AF, Blomeyer, D, Plichta, MM, Wolf, I, et al. Impact of early life adversity on reward processing in young adults: EEG-fMRI results from a prospective study over 25 years. PLoS One 2014; 9: e104185.CrossRefGoogle ScholarPubMed
39 Hanson, JL, Hariri, AR, Williamson, DE. Blunted ventral striatum development in adolescence reflects emotional neglect and predicts depressive symptoms. Biol Psychiatry 2015; 78: 598–605.CrossRefGoogle ScholarPubMed
40 Dannlowski, U, Stuhrmann, A, Beutelmann, V, Zwanzger, P, Lenzen, T, Grotegerd, D, et al. Limbic scars: long-term consequences of childhood maltreatment revealed by functional and structural magnetic resonance imaging. Biol Psychiatry 2012; 71: 286–93.CrossRefGoogle ScholarPubMed
41 Cohen, RA, Grieve, S, Hoth, KF, Paul, RH, Sweet, L, Tate, D, et al. Early life stress and morphometry of the adult anterior cingulate cortex and caudate nuclei. Biol Psychiatry 2006; 59: 975–82.CrossRefGoogle ScholarPubMed
42 Pessoa, L, Engelmann, JB. Embedding reward signals into perception and cognition. Front Neurosci 2010; 4: 17.CrossRefGoogle ScholarPubMed
43 Aron, A, Fisher, H, Mashek, DJ, Strong, G, Li, H, Brown, LL. Reward, motivation, and emotion systems associated with early-stage intense romantic love. J Neurophysiol 2005; 94: 327–37.CrossRefGoogle ScholarPubMed
44 Vrticka, P, Andersson, F, Grandjean, D, Sander, D, Vuilleumier, P. Individual attachment style modulates human amygdala and striatum activation during social appraisal. PLoS One 2008; 3: e2868.CrossRefGoogle ScholarPubMed
45 Andersen, SL, Tomoda, A, Vincow, ES, Valente, E, Polcari, A, Teicher, MH. Preliminary evidence for sensitive periods in the effect of childhood sexual abuse on regional brain development. J Neuropsychiatry Clin Neurosci 2008; 20: 292–301.CrossRefGoogle ScholarPubMed
46 Pechtel, P, Lyons-Ruth, K, Anderson, CM, Teicher, MH. Sensitive periods of amygdala development: the role of maltreatment in preadolescence. Neuroimage 2014; 97: 236–44.CrossRefGoogle ScholarPubMed
47 Bruce, J, Fisher, PA, Graham, AM, Moore, WE, Peake, SJ, Mannering, AM. Patterns of brain activation in foster children and nonmaltreated children during an inhibitory control task. Dev Psychopathol 2013; 25: 931–41.CrossRefGoogle ScholarPubMed
48 Carrion, VG, Garrett, A, Menon, V, Weems, CF, Reiss, AL. Posttraumatic stress symptoms and brain function during a response-inhibition task: an fMRI study in youth. Depress Anxiety 2008; 25: 514–26.CrossRefGoogle ScholarPubMed
49 Charney, DS. Psychobiological mechanisms of resilience and vulnerability: implications for successful adaptation to extreme stress. Am J Psychiatry 2004; 161: 195–216.CrossRefGoogle ScholarPubMed
50 Kundakovic, M, Gudsnuk, K, Herbstman, JB, Tang, D, Perera, FP, Champagne, FA. DNA methylation of BDNF as a biomarker of early-life adversity. Proc Natl Acad Sci USA 2015; 112: 6807–13.CrossRefGoogle ScholarPubMed
51 Smyke, AT, Zeanah, CH, Gleason, MM, Drury, SS, Fox, NA, Nelson, CA, et al. A randomized controlled trial comparing foster care and institutional care for children with signs of reactive attachment disorder. Am J Psychiatry 2012; 169: 508–14.CrossRefGoogle ScholarPubMed
52 Zeanah, CH, Gleason, MM. Annual research review: attachment disorders in early childhood – clinical presentation, causes, correlates, and treatment. J Child Psychol Psychiatry 2015; 56: 207–22.CrossRefGoogle ScholarPubMed
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