Altered cortico-striatal connectivity in offspring of schizophrenia patients relative to offspring of bipolar patients and controls

PLoS ONE

Volumn 11, Issue 2, 2016, Pages

  Solé Padullés, Cristina ^a   Castro Fornieles, Josefina ^a,b,c,d   De La Serna, Elena ^d   Romero, Soledad ^a,b,d   Calvo, Anna ^a,b,e   Sánchez Gistau, Vanessa ^a,b,d   Padrós Fornieles, Marta ^b   Baeza, Inmaculada ^a,b,d   Bargalló, Núria ^b,d   Frangou, Sophia ^f   Sugranyes, Gisela ^a,b  

^a INSTITUT D INVESTIGACIONS BIOMÈDIQUES AUGUST PI I SUNYER IDIBAPS   (Spain)

^b HOSPITAL CLÍNIC   (Spain)

^c UNIVERSITY OF BARCELONA   (Spain)

^d CENTRO DE INVESTIGACIÓN BIOMÉDICA EN RED DE SALUD MENTAL CIBERSAM   (Spain)

^e BIOMATERIALES Y NANOMEDICINA CIBER BBN   (Spain)

^f MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADOLESCENT; ADULT; ARTICLE; BASAL GANGLION; BIPOLAR DISORDER; BRAIN SIZE; CAUDATE NUCLEUS; CHILD; COGNITION ASSESSMENT; CONNECTOME; CONTROLLED STUDY; DEFAULT MODE NETWORK; DISEASE ASSOCIATION; EXECUTIVE FUNCTION; FEMALE; GRAY MATTER; HUMAN; IMAGE ANALYSIS; IMAGE PROCESSING; INDEPENDENT COMPONENT ANALYSIS; MAJOR CLINICAL STUDY; MALE; NUCLEAR MAGNETIC RESONANCE IMAGING; PROGENY; RESTING STATE NETWORK; RISK ASSESSMENT; RISK FACTOR; SALIENCE NETWORK; SCHIZOPHRENIA; VOXEL BASED MORPHOMETRY; CASE CONTROL STUDY; CLUSTER ANALYSIS; COGNITION; CORPUS STRIATUM; DEMOGRAPHY; MIDDLE AGED; NEOCORTEX; NERVE CELL NETWORK; PATHOLOGY; PATHOPHYSIOLOGY; REGRESSION ANALYSIS; REST; YOUNG ADULT;

ADOLESCENT; ADULT; BASAL GANGLIA; BIPOLAR DISORDER; CASE-CONTROL STUDIES; CHILD; CLUSTER ANALYSIS; COGNITION; CORPUS STRIATUM; DEMOGRAPHY; FEMALE; GRAY MATTER; HUMANS; MALE; MIDDLE AGED; NEOCORTEX; NERVE NET; REGRESSION ANALYSIS; REST; SCHIZOPHRENIA; YOUNG ADULT;

EID: 84960517015     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0148045     Document Type: Article

References (65)

1. Chai XJ, Whitfield-Gabrieli S, Shinn AK, Gabrieli JD, Nieto Castañón A, McCarthy JM, et al. Abnormal medial prefrontal cortex resting-state connectivity in bipolar disorder and schizophrenia. Neuropsychopharmacology. 2011 Sep; 36(10): 2009-2017. doi: 10.1038/npp.2011.88 PMID: 21654735
2. Lichtenstein P, Yip BH, Björk C, Pawitan Y, Cannon TD, Sullivan PF, et al. Common genetic determinants of schizophrenia and bipolar disorder in Swedish families: A population-based study. Lancet. 2009 Jan 17; 373(9659): 234-239. doi: 10.1016/S0140-6736(09)60072-6 PMID: 19150704
3. Keshavan MS, Morris DW, Sweeney JA, Pearlson G, Thaker G, Seidman LJ, et al. A dimensional approach to the psychosis spectrum between bipolar disorder and schizophrenia: The Schizo-Bipolar Scale. Schizophr Res. 2011 Dec; 133(1-3): 250-254. doi: 10.1016/j.schres.2011.09.005 PMID: 21996268
4. Bora E, Pantelis C. Meta-analysis of Cognitive Impairment in First-Episode Bipolar Disorder: Comparison With First-Episode Schizophrenia and Healthy Controls. Schizophr Bull. 2015 Sep; 41(5): 1095-1104. doi: 10.1093/schbul/sbu198 PMID: 25616505
5. Ellison-Wright I, Bullmore E. Anatomy of bipolar disorder and schizophrenia: A meta-analysis. Schizophr Res. 2010 Mar; 117(1): 1-12. doi: 10.1016/j.schres.2009.12.022 PMID: 20071149
6. Delvecchio G, Sugranyes G, Frangou S. Evidence of diagnostic specificity in the neural correlates of facial affect processing in bipolar disorder and schizophrenia: A meta-analysis of functional imaging studies. Psychol Med. 2013 Mar; 43(3): 553-569. doi: 10.1017/S0033291712001432 PMID: 22874625
7. Frangou S. A systems neuroscience perspective of schizophrenia and bipolar disorder. Schizophr Bull. 2014 May; 40(3): 523-531. doi: 10.1093/schbul/sbu017 PMID: 24609453
8. Biswal BB, Van Kylen J, Hyde JS. Simultaneous assessment of flow and BOLD signals in resting-state functional connectivity maps. NMR Biomed. 1997 Jun-Aug; 10(4-5): 165-170. PMID: 9430343
9. Fornito A, Harrison BJ. Brain connectivity and mental illness. Front Psychiatry. 2012 Jul 27; 3: 72. doi: 10.3389/fpsyt.2012.00072 PMID: 22866039
10. Strakowski SM, Adler CM, Almeida J, Altshuler LL, Blumberg HP, Chang KD, et al. The functional neuroanatomy of bipolar disorder: A consensus model. Bipolar Disord. 2012 Jun; 14(4): 313-325. doi: 10. 1111/j.1399-5618.2012.01022.x PMID: 22631617
11. Khadka S, Meda SA, Stevens MC, Glahn DC, Calhoun VD, Sweeney JA, et al. Is aberrant functional connectivity a psychosis endophenotype? A resting state functional magnetic resonance imaging study. Biol Psychiatry. 2013 Sep 15; 74(6): 458-466. doi: 10.1016/j.biopsych.2013.04.024 PMID: 23746539
12. Baker JT, Holmes AJ, Masters GA, Yeo BT, Krienen F, Buckner RL, et al. Disruption of cortical association networks in schizophrenia and psychotic bipolar disorder. JAMA Psychiatry. 2014 Feb; 71(2): 109-118. doi: 10.1001/jamapsychiatry.2013.3469 PMID: 24306091
13. Buckner RL, Andrews-Hanna JR, Schacter DL. The brain's default network: Anatomy, function, and relevance to disease. Ann N Y Acad Sci. 2008 Mar; 1124: 1-38. doi: 10.1196/annals.1440.011 PMID: 18400922
14. Raichle ME, MacLeod AM, Snyder AZ, Powers WJ, Gusnard DA, Shulman GL. A default mode of brain function. Proc Natl Acad Sci U S A. 2001 Jan 16; 98(2): 676-682. PMID: 11209064
15. Orliac F, Naveau M, Joliot M, Delcroix N, Razafimandimby A, Brazo P, et al. Links among resting-state default-mode network, salience network, and symptomatology in schizophrenia. Schizophr Res. 2013 Aug; 148(1-3): 74-80. doi: 10.1016/j.schres.2013.05.007 PMID: 23727217
16. Tang J, Liao Y, Song M, Gao JH, Zhou B, Tan C, et al. Aberrant default mode functional connectivity in early onset schizophrenia. PLoS One. 2013 Jul 29; 8(7): E71061. doi: 10.1371/journal.pone.0071061 PMID: 23923052
17. Lois G, Linke J, Wessa M. Altered functional connectivity between emotional and cognitive resting state networks in euthymic bipolar I disorder patients. PLoS One. 2014 Oct 24; 9(10): E107829. doi: 10. 1371/journal.pone.0107829 eCollection 2014. PMID: 25343370
18. Magioncalda P, Martino M, Conio B, Escelsior A, Piaggio N, Presta A, et al. Functional connectivity and neuronal variability of resting state activity in bipolar disorder-reduction and decoupling in anterior cortical midline structures. Hum Brain Mapp. 2015 Feb; 36(2): 666-682. doi: 10.1002/hbm.22655 PMID: 25307723
19. Seeley WW, Menon V, Schatzberg AF, Keller J, Glover GH, Kenna H, et al. Dissociable intrinsic connectivity networks for salience processing and executive control. J Neurosci. 2007 Feb 28; 27(9): 2349-2356. PMID: 17329432
20. Menon V. Large-scale brain networks and psychopathology: A unifying triple network model. Trends Cogn Sci. 2011 Oct; 15(10): 483-506. doi: 10.1016/j.tics.2011.08.003 PMID: 21908230
21. Tu PC, Lee YC, Chen YS, Li CT, Su TP. Schizophrenia and the brain's control network: Aberrant withinand between-network connectivity of the frontoparietal network in schizophrenia. Schizophr Res. 2013 Jul; 147(2-3): 339-347. doi: 10.1016/j.schres.2013.04.011 PMID: 23706416
22. Wu M, Lu LH, Passarotti AM, Wegbreit E, Fitzgerald J, Pavuluri MN (2013). Altered affective, executive and sensorimotor resting state networks in patients with pediatric mania. Journal of Psychiatry & Neuroscience 38, 232-240.
23. Argyelan M, Ikuta T, DeRosse P, Braga RJ, Burdick KE, John M, Kingsley PB, et al. Resting-state fMRI connectivity impairment in schizophrenia and bipolar disorder. Schizophr Bull. 2014 Jan; 40(1): 100-110. doi: 10.1093/schbul/sbt092 PMID: 23851068
24. Lui S, Yao L, Xiao Y, Keedy SK, Reilly JL, Keefe RS, et al. Resting-state brain function in schizophrenia and psychotic bipolar probands and their first-degree relatives. Psychol Med. 2015 Jan; 45(1): 97-108. doi: 10.1017/S003329171400110X PMID: 25066779
25. Jang JH, Jung WH, Choi JS, Choi CH, Kang DH, Shin NY, et al. Reduced prefrontal functional connectivity in the default mode network is related to greater psychopathology in subjects with high genetic loading for schizophrenia. Schizophr Res. 2011 Apr; 127(1-3): 58-65. doi: 10.1016/j.schres.2010.12. 022 PMID: 21277171
26. van Buuren M, Vink M, Kahn RS. Default-mode network dysfunction and self-referential processing in healthy siblings of schizophrenia patients. Schizophr Res. 2012 Dec; 142(1-3): 237-243. doi: 10.1016/j.schres.2012.09.017 PMID: 23099059
27. Jukuri T, Kiviniemi V, Nikkinen J, Miettunen J, Mäki P, Jääskeläinen E, et al. Default mode network in young people with familial risk for psychosis-The Oulu Brain and Mind study. Schizophr Res. 2013 Feb; 143(2-3): 239-245. doi: 10.1016/j.schres.2012.11.020 PMID: 23245776
28. Meda SA, Gill A, Stevens MC, Lorenzoni RP, Glahn DC, Calhoun VD, et al. Differences in resting-state functional magnetic resonance imaging functional network connectivity between schizophrenia and psychotic bipolar probands and their unaffected first-degree relatives. Biol Psychiatry. 2012 May 15; 71 (10): 881-889. doi: 10.1016/j.biopsych.2012.01.025 PMID: 22401986
29. Jukuri T, Kiviniemi V, Nikkinen J, Miettunen J, Mäki P, Mukkala S, et al. Central executive network in young people with familial risk for psychosis-The Oulu Brain and Mind Study. Schizophr Res. 2015 Feb; 161(2-3): 177-183. doi: 10.1016/j.schres.2014.11.003 PMID: 25468181
30. Singh MK, Chang KD, Kelley RG, Saggar M, Reiss AL, Gotlib IH. Early signs of anomalous neural functional connectivity in healthy offspring of parents with bipolar disorder. Bipolar Disord. 2014 Nov; 16 (7): 678-689. doi: 10.1111/bdi.12221 PMID: 24938878
31. Fornito A, Harrison BJ, Goodby E, Dean A, Ooi C, Nathan PJ, et al. Functional dysconnectivity of corticostriatal circuitry as a risk phenotype for psychosis. JAMA Psychiatry. 2013 Nov; 70(11): 1143-1151. doi: 10.1001/jamapsychiatry.2013.1976 PMID: 24005188
32. Power JD, Fair DA, Schlaggar BL, Petersen SE. The development of human functional brain networks. Neuron. 2010 Sep 9; 67(5): 735-748. doi: 10.1016/j.neuron.2010.08.017 PMID: 20826306
33. Supekar K, Uddin LQ, Prater K, Amin H, Greicius MD, Menon V. Development of functional and structural connectivity within the default mode network in young children. Neuroimage. 2010 Aug 1; 52 (1): 290-301. doi: 10.1016/j.neuroimage.2010.04.009 PMID: 20385244
34. Ordaz SJ, Foran W, Velanova K, Luna B. Longitudinal growth curves of brain function underlying inhibitory control through adolescence. J Neurosci. 2013 Nov 13; 33(46): 18109-18124. doi: 10.1523/JNEUROSCI.1741-13.2013 PMID: 24227721
35. Porter JN, Roy AK, Benson B, Carlisi C, Collins PF, Leibenluft E, et al. Age-related changes in the intrinsic functional connectivity of the human ventral vs. dorsal striatum from childhood to middle age. Dev Cogn Neurosci. 2015 Feb; 11: 83-95. doi: 10.1016/j.dcn.2014.08.011 PMID: 25257972
36. Maziade M, Rouleau N, Mérette C, Cellard C, Battaglia M, Marino C, et al. Verbal and visual memory impairments among young offspring and healthy adult relatives of patients with schizophrenia and bipolar disorder: Selective generational patterns indicate different developmental trajectories. Schizophr Bull. 2011 Nov; 37(6): 1218-28. doi: 10.1093/schbul/sbq026 PMID: 20410238
37. Diwadkar VA, Goradia D, Hosanagar A, Mermon D, Montrose DM, Birmaher B, et al. Working memory and attention deficits in adolescent offspring of schizophrenia or bipolar patients: Comparing vulnerability markers. Prog Neuropsychopharmacol Biol Psychiatry. 2011 Jul 1; 35(5): 1349-54. doi: 10.1016/j. pnpbp.2011.04.009 PMID: 21549798
38. American Psychiatric Association (APA). Diagnostic and Statistical Manual of Mental Disorders (DSMIV); American Psychiatric Association; Washington, DC 1994.
39. Sanchez-Gistau V, Romero S, Moreno D, de la Serna E, Baeza I, Sugranyes G, et al. Psychiatric disorders in child and adolescent offspring of patients with schizophrenia and bipolar disorder: A controlled study. Schizophr Res. 2015 Oct; 168(1-2): 197-203. doi: 10.1016/j.schres.2015.08.034 PMID: 26363969
40. Hollingshead AB, Redlich FC. Social Class and Mental Illness. Wiley: New York; 1958.
41. First MB, Spitzer RL, Gibbon M, Williams JBW. Structured Clinical Interview for DSM-IV-TR Axis I Disorders, Research Version, Patient Edition. (SCID-I/P) New York: Biometrics Research, New York State Psychiatric Institute; 2002.
42. Geller B, Zimerman B, Williams M, Bolhofner K, Craney JL, DelBello MP, et al. Reliability of the Washington University in St. Louis Kiddie Schedule for Affective Disorders and Schizophrenia (WASH-UKSADS) mania and rapid cycling sections. J Am Acad Child Adolesc Psychiatry. 2001 Apr; 40(4): 450-455. PMID: 11314571
43. Miller TJ, McGlashan TH, Rosen JL, Cadenhead K, Cannon T, Ventura J, et al. Prodromal assessment with the structured interview for prodromal syndromes and the scale of prodromal symptoms: Predictive validity, interrater reliability, and training to reliability. Schizophr Bull. 2003; 29(4): 703-715. PMID: 14989408
44. Young RC, Biggs JT, Ziegler VE, Meyer DA (1978). A rating scale for mania: Reliability, validity and sensitivity. The British Journal of Psychiatry 133, 429-435. PMID: 728692
45. Hamilton M. Development of a rating scale for primary depressive illness. Br J Soc Clin Psychol. 1967 Dec; 6(4): 278-296. PMID: 6080235
46. Busner J, Targum SD. The clinical global impressions scale: Applying a research tool in clinical practice. Psychiatry (Edgmont). 2007 Jul; 4(7): 28-37.
47. Wechsler D. The Wechsler intelligence scale for children III. Paidós: Buenos Aires; 1994.
48. Wechsler D. Wechlser Adult Intelligence Scale III. TEA ediciones: Madrid; 1999.
49. Burgund ED, Kang HC, Kelly JE, Buckner RL, Snyder AZ, Petersen SE, et al. The feasibility of a common stereotactic space for children and adults in fMRI studies of development. Neuroimage. 2002 Sep; 17(1): 184-200. PMID: 12482076
50. Erhardt EB, Rachakonda S, Bedrick EJ, Allen EA, Adali T, Calhoun VD. Comparison of multi-subject ICA methods for analysis of fMRI data. Hum Brain Mapp. 2011 Dec; 32(12): 2075-2095. doi: 10.1002/hbm.21170 PMID: 21162045
51. Shirer WR, Ryali S, Rykhlevskaia E, Menon V, Greicius MD. Decoding subject-driven cognitive states with whole-brain connectivity patterns. Cereb Cortex. 2012 Jan; 22(1): 158-165. doi: 10.1093/cercor/bhr099 PMID: 21616982
52. Taki Y, Thyreau B, Kinomura S, Sato K, Goto R, Kawashima R et al. Correlations among brain gray matter volumes, age, gender, and hemisphere in healthy individuals. PLoS One. 2011; 6(7): E22734. doi: 10.1371/journal.pone.0022734 PMID: 21818377
53. Fischl B, Sereno MI, Dale AM. Cortical surface-based analysis. II: Inflation, flattening, and a surfacebased coordinate system. Neuroimage. 1999 Feb; 9(2): 195-207. PMID: 9931269
54. Nakao T, Radua J, Rubia K, Mataix-Cols D. Gray matter volume abnormalities in ADHD: Voxel-based meta-analysis exploring the effects of age and stimulant medication. Am J Psychiatry. 2011 Nov; 168 (11): 1154-1163. doi: 10.1176/appi.ajp.2011.11020281 PMID: 21865529
55. Farr OM, Zhang S, Hu S, Matuskey D, Abdelghany O, Malison RT, et al. The effects of methylphenidate on resting-state striatal, thalamic and global functional connectivity in healthy adults. Int J Neuropsychopharmacol. 2014 Aug; 17(8): 1177-1191. doi: 10.1017/S1461145714000674 PMID: 24825078
56. Tandon N, Bolo NR, Sanghavi K, Mathew IT, Francis AN, Stanley JA, et al. Brain metabolite alterations in young adults at familial high risk for schizophrenia using proton magnetic resonance spectroscopy. Schizophr Res. 2013 Aug; 148(1-3): 59-66. doi: 10.1016/j.schres.2013.05.024 PMID: 23791389
57. Huttunen J, Heinimaa M, Svirskis T, Nyman M, Kajander J, Forsback S, et al. Striatal dopamine synthesis in first-degree relatives of patients with schizophrenia. Biol Psychiatry. 2008 Jan 1; 63(1): 114-117. PMID: 17655830
58. Fusar-Poli P, Howes OD, Allen P, Broome M, Valli I, Asselin MC, et al. Abnormal prefrontal activation directly related to pre-synaptic striatal dopamine dysfunction in people at clinical high risk for psychosis. Mol Psychiatry. 2011 Jan; 16(1): 67-75. doi: 10.1038/mp.2009.108 PMID: 19949389
59. Laird AR, Fox PM, Eickhoff SB, Turner JA, Ray KL, McKay DR, et al. Behavioral interpretations of intrinsic connectivity networks. J Cogn Neurosci. 2011 Dec; 23(12): 4022-4037. doi: 10.1162/jocn-a-00077 PMID: 21671731
60. Diwadkar VA, Pruitt P, Goradia D, Murphy E, Bakshi N, Keshavan MS, et al. Fronto-parietal hypo-activation during working memory independent of structural abnormalities: Conjoint fMRI and sMRI analyses in adolescent offspring of schizophrenia patients. Neuroimage. 2011 Sep 1; 58(1): 234-241. doi: 10.1016/j.neuroimage.2011.06.033 PMID: 21729757
61. Sato JR, Salum GA, Gadelha A, Picon FA, Pan PM, Vieira G, et al. Age effects on the default mode and control networks in typically developing children. J Psychiatr Res. 2014 Nov; 58: 89-95. doi: 10.1016/j. jpsychires.2014.07.004 PMID: 25085608
62. Heinze K, Reniers RL, Nelson B, Yung AR, Lin A, Harrison BJ, et al. Discrete alterations of brain network structural covariance in individuals at ultra-high risk for psychosis. Biol Psychiatry. 2015 Jun 1; 77 (11): 989-996. doi: 10.1016/j.biopsych.2014.10.023 PMID: 25524754
63. Rasic D, Hajek T, Alda M, Uher R. Risk of mental illness in offspring of parents with schizophrenia, bipolar disorder, and major depressive disorder: A meta-analysis of family high-risk studies. Schizophr Bull. 2014 Jan; 40(1): 28-38. doi: 10.1093/schbul/sbt114 PMID: 23960245
64. Jones PB. Adult mental health disorders and their age at onset. Br J Psychiatry Suppl. 2013 Jan; 54: S5-10. doi: 10.1192/bjp.bp.112.119164 PMID: 23288502
65. Insel TR. Rethinking schizophrenia. Nature. 2010 Nov 11; 468(7321): 187-93. doi: 10.1038/nature09552 PMID: 21068826