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01-06-2017 | Original Contribution

Intrinsic functional connectivity of fronto-temporal networks in adolescents with early psychosis

Authors: Cristina Solé-Padullés, Josefina Castro-Fornieles, Elena de la Serna, Vanessa Sánchez-Gistau, Soledad Romero, Olga Puig, Anna Calvo, Nuria Bargalló, Inmaculada Baeza, Gisela Sugranyes

Published in: European Child & Adolescent Psychiatry | Issue 6/2017

Abstract

Adults with psychotic disorders have abnormal connectivity of fronto-temporal networks. However, whether these abnormalities are present in adolescents with early psychosis has not been fully assessed. One-hundred and thirty-nine adolescents aged 12–18 underwent resting-state functional magnetic resonance imaging and diffusion tensor imaging. Following motion correction, data were available for 44 participants with a psychosis risk syndrome, 34 patients with a first episode psychosis (FEP) and 35 healthy controls. Independent component analysis was performed to assess functional networks showing a fronto-temporal scope; this identified a language and a salience network. Mean fractional anisotropy was measured in clusters showing between-group differences in intrinsic functional connectivity (iFC). For the language network, there was a group effect within the right middle/inferior frontal gyrus, explained by reduced iFC in patients with an FEP relative to healthy controls, while in participants with a psychosis risk syndrome values of iFC were intermediate. In this region, values of iFC were positively correlated with mean fractional anisotropy in patients with an FEP. No group differences were observed in the salience network. Reduced iFC of the language network, in association with disrupted white matter microstructure, may characterize FEP during adolescence.

Fu CH, Suckling J, Williams SC, Andrew CM, Vythelingum GN, McGuire PK (2005) Effects of psychotic state and task demand on prefrontal function in schizophrenia: an fMRI study of overt verbal fluency. Am J Psychiatry 162(3):485–494CrossRefPubMed

Plaze M, Bartrés-Faz D, Martinot JL et al (2008) Left superior temporal gyrus activation during sentence perception negatively correlates with auditory hallucination severity in schizophrenia patients. Schizophr Res 87(1–3):109–115

Stephan KE, Friston KJ, Frith CD (2009) Dysconnection in schizophrenia: from abnormal synaptic plasticity to failures of self-monitoring. Schizophr Bull 35(3):509–527CrossRefPubMedPubMedCentral

Fox MD, Raichle ME (2007) Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging. Nat Rev Neurosci 8:700–711CrossRefPubMed

Raichle ME (2010) Two views of brain function. Trends Cogn Sci 14:180–190CrossRefPubMed

Matthews M, Fair DA (2015) Research review: Functional brain connectivity and child psychopathology–overview and methodological considerations for investigators new to the field. Child Psychol Psychiatry 56(4):400–414CrossRef

Pettersson-Yeo W, Allen P, Benetti S, McGuire P, Mechelli A (2011) Dysconnectivity in schizophrenia: where are we now? Neurosci Biobehav Rev 35(5):1110–1124CrossRefPubMed

Gavrilescu M, Rossell S, Stuart GW et al (2010) Reduced connectivity of the auditory cortex in patients with auditory hallucinations: a resting state functional magnetic resonance imaging study. Psychol Med 40:1149–1158CrossRefPubMed

Shinn AK, Baker JT, Cohen BM, Ongür D (2013) Functional connectivity of left Heschl’s gyrus in vulnerability to auditory hallucinations in schizophrenia. Schizophr Res 143:260–268CrossRefPubMed

10.

Calhoun VD, Kiehl KA, Pearlson GD (2008) Modulation of temporally coherent brain networks estimated using ICA at rest and during cognitive tasks. Hum Brain Mapp 29(7):828–838CrossRefPubMedPubMedCentral

11.

Khadka S, Meda SA, Stevens MC et al (2013) Is aberrant functional connectivity a psychosis endophenotype? A resting state functional magnetic resonance imaging study. Biol Psychiatry 74(6):458–466CrossRefPubMedPubMedCentral

12.

Thoma RJ, Chaze C, Lewine JD et al (2016) Functional MRI EVALUATIOn of Multiple Neural Networks Underlying Auditory Verbal Hallucinations in Schizophrenia Spectrum Disorders. Front Psychiatry 29(7):39

13.

Menon V, Uddin LQ (2010) Saliency, switching, attention and control: a network model of insula function. Brain Struct Funct 214:655–667CrossRefPubMedPubMedCentral

14.

Palaniyappan L, White TP, Liddle PF (2012) The concept of salience network dysfunction in schizophrenia: from neuroimaging observations to therapeutic opportunities. Curr Top Med Chem 12(21):2324–2338CrossRefPubMed

15.

Zhou Y, Liang M, Jiang T et al (2007) Functional dysconnectivity of the dorsolateral prefrontal cortex in first-episode schizophrenia using resting-state fMRI. Neurosci Lett 417:297–302CrossRefPubMed

16.

Pu W, Li L, Zhang H et al (2012) Morphological and functional abnormalities of salience network in the early-stage of paranoid schizophrenia. Schizophr Res 141(1):15–21CrossRefPubMed

17.

Manoliu A, Riedl V, Zherdin A, Mühlau M et al (2014) Aberrant dependence of default mode/central executive network interactions on anterior insular salience network activity in schizophrenia. Schizophr Bull 40:428–437CrossRefPubMed

18.

Orliac F, Naveau M, Joliot M et al (2013) Links among resting-state default-mode network, salience network, and symptomatology in schizophrenia. Schizophr Res 148(1–3):74–80CrossRefPubMed

19.

Kraguljac NV, White DM, Hadley JA et al (2015) Abnormalities in large scale functional networks in unmedicated patients with schizophrenia and effects of risperidone. Neuroimage Clin 22(10):146–158

20.

Berman RA, Gotts SJ, McAdams HM et al (2016) Disrupted sensorimotor and social-cognitive networks underlie symptoms in childhood-onset schizophrenia. Brain 139(Pt 1):276–291CrossRefPubMed

21.

Miller TJ, McGlashan TH, Rosen JL et al (2003) 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 29:703–715CrossRefPubMed

22.

Pettersson-Yeo W, Benetti S, Frisciata S et al (2015) Does neuroanatomy account for superior temporal dysfunction in early psychosis? A multimodal MRI investigation. J Psychiatry Neurosci 40:100–107PubMedPubMedCentral

23.

Colibazzi T, Horga G, Wang Z et al (2016) Neural Dysfunction in Cognitive Control Circuits in Persons at Clinical High-Risk for Psychosis. Neuropsychopharmacology 41(5):1241–1250CrossRefPubMed

24.

Yoon YB, Yun JY, Jung WH et al (2015) Altered Fronto-Temporal Functional Connectivity in Individuals at Ultra-High-Risk of Developing Psychosis. PLoS One 10(8):e0135347CrossRefPubMedPubMedCentral

25.

Wotruba D, Michels L, Buechler R et al (2014) Aberrant coupling within and across the default mode, task-positive, and salience network in subjects at risk for psychosis. Schizophr Bull 40:1095–1104CrossRefPubMed

26.

Wang C, Ji F, Hong Z, Poh JS et al (2016) Disrupted salience network functional connectivity and white-matter microstructure in persons at risk for psychosis: findings from the LYRIKS study. Psychol Med 46(13):2771–2783CrossRefPubMedPubMedCentral

27.

Pelletier-Baldelli A, Bernard JA, Mittal VA (2015) Intrinsic Functional Connectivity in Salience and Default Mode Networks and Aberrant Social Processes in Youth at Ultra-High Risk for Psychosis. PLoS One 10(8):e0134936CrossRefPubMedPubMedCentral

28.

Tamnes CK, Agartz I (2016) White Matter Microstructure in Early-Onset Schizophrenia: A Systematic Review of Diffusion Tensor Imaging Studies. J Am Acad Child Adolesc Psychiatry 55(4):269–279CrossRefPubMed

29.

Shergill SS, Kanaan RA, Chitnis XA et al (2007) A diffusion tensor imaging study of fasciculi in schizophrenia. Am J Psychiatry 164(3):467–473CrossRefPubMed

30.

Oh JS, Kubicki M, Rosenberger G et al (2009) Thalamo-frontal white matter alterations in chronic schizophrenia: a quantitative diffusion tractography study. Hum Brain Mapp 30(11):3812–3825CrossRefPubMedPubMedCentral

31.

Benetti S, Pettersson-Yeo W, Allen P et al (2015) Auditory verbal hallucinations and brain dysconnectivity in the perisylvian language network: a multimodal investigation. Schizophr Bull 41(1):192–200CrossRefPubMed

32.

Leroux E, Delcroix N, Dollfus S (2014) Left fronto-temporal dysconnectivity within the language network in schizophrenia: an fMRI and DTI study. Psychiatry Res 223(3):261–267CrossRefPubMed

33.

Taylor SJ, Barker LA, Heavey L, McHale S (2015) The longitudinal development of social and executive functions in late adolescence and early adulthood. Front Behav Neurosci 15:252

34.

Rubia K (2013) Functional brain imaging across development. Eur Child Adolesc Psychiatry 22(12):719–731CrossRefPubMed

35.

Sole-Padulles C, Castro-Fornieles J, De La Serna E et al (2016) Intrinsic connectivity networks from childhood to late adolescence: effects of age and sex. Dev Cogn Neurosci 17:35–44CrossRefPubMed

36.

Gogtay N, Giedd JN, Lusk L et al (2004) Dynamic mapping of human cortical development during childhood through early adulthood. Proc Natl Acad Sci U S A 101(21):8174–8179CrossRefPubMedPubMedCentral

37.

Satterthwaite TD, Baker JT (2015) How can studies of resting-state functional connectivity help us understand psychosis as a disorder of brain development? Curr Opin Neurobiol 30:85–91CrossRefPubMed

38.

Satterthwaite TD, Vandekar SN, Wolf DH et al (2015) Connectome-wide network analysis of youth with Psychosis-Spectrum symptoms. Mol Psychiatry 20(12):1508–1515CrossRefPubMedPubMedCentral

39.

Rapado-Castro M, Bartholomeusz CF, Castro-Fornieles J et al (2015) Gender effects on brain changes in early-onset psychosis. Eur Child Adolesc Psychiatry 24(10):1193–1205CrossRefPubMed

40.

Kay SR, Fiszbein A, Opler LA (1987) The positive and negative syndrome scale (PANSS) for schizophrenia. Schizophr Bull 13:261–276CrossRefPubMed

41.

Cornblatt BA, Lencz T, Smith CW, Correll CU, Auther AM, Nakayama E (2003) The schizophrenia prodrome revisited: a neurodevelopmental perspective. Schizophr Bull 29:633–651CrossRefPubMed

42.

Klosterkötter J, Ruhrmann R, Schultze-Lutter F et al (2005) The European Prediction of Psychosis Study (EPOS): integrating early recognition and intervention in Europe. World Psychiatry 4:161–167PubMedPubMedCentral

43.

American Psychiatric Association (APA) (1994) Diagnostic and statistical manual of mental disorders (DSM-IV). American Psychiatric Association, Washington

44.

Geller B, Zimerman B, Williams M et al (2001) Reliability of the Washington University in St. Louis Kiddie Schedule for Affective Disorders and Schizophrenia (WASH-U-KSADS) mania and rapid cycling sections. J Am Acad Child Adolesc Psychiatry 40:450–455CrossRefPubMed

45.

Wechsler D (2005) The Wechsler intelligence scale for children IV. TEA ediciones, Madrid

46.

Wechsler D (1999) Wechlser Adult Intelligence Scale III. TEA ediciones, Madrid

47.

Chao-Gan Y, Yu-Feng Z (2010) DPARSF: a MATLAB toolbox for “Pipeline” data analysis of resting-state fMRI. Front Syst Neurosci 14(4):13

48.

Power JD, Barnes KA, Snyder AZ, Schlaggar BL, Petersen S (2012) Spurious but systematic correlations in functional connectivity MRI networks arise from subject motion. Neuroimage 59:2142–2154CrossRefPubMed

49.

Yan CG, Cheung B, Kelly C et al (2013) A comprehensive assessment of regional variation in the impact of head micromovements on functional connectomics. Neuroimage 1(76):183–201CrossRef

50.

Erhardt EB, Rachakonda S, Bedrick EJ, Allen EA, Adali T, Calhoun VD (2011) Comparison of multi-subject ICA methods for analysis of fMRI data. Hum Brain Mapp 32(12):2075–2095CrossRefPubMed

51.

Lui S, Li T, Deng W et al (2010) Short-term effects of antipsychotic treatment on cerebral function in drug-naive first-episode schizophrenia revealed by “resting state” functional magnetic resonance imaging. Arch Gen Psychiatry 67:783–792CrossRefPubMed

52.

Woods SW (2003) Chlorpromazine equivalent doses for the newer atypical antipsychotics. J Clin Psych 64:663–667CrossRef

53.

Shirer WR, Ryali S, Rykhlevskaia E, Menon V, Greicius MD (2012) Decoding subject-driven cognitive states with whole-brain connectivity patterns. Cereb Cortex 22:158–165CrossRefPubMed

54.

Friederici AD (2011) The brain basis of language processing: from structure to function. Physiol Rev 91:1357–1392CrossRefPubMed

55.

Seeley WW, Menon V, Schatzberg AF et al (2007) Dissociable intrinsic connectivity networks for salience processing and executive control. J Neurosci 28:2349–2356CrossRef

56.

Knecht S, Deppe M, Drager B et al (2000) Language lateralization in healthy right-handers. Brain 123:74–81CrossRefPubMed

57.

Simonyan K, Fuertinger S (2015) Speech networks at rest and in action: Interactions between functional brain networks controlling speech production. J Neurophysiol 1:2967–2978CrossRef

58.

McAvoy M, Mitra A, Coalson RS et al (2016) Unmasking language lateralization in human brain intrinsic activity. Cereb Cortex 26(4):1733–1746CrossRefPubMed

59.

Soroker N, Kasher A, Giora R et al (2005) Processing of basic speech acts following localized brain damage: a new light on the neuroanatomy of language. Brain Cogn 57:214–217CrossRefPubMed

60.

Lee SY, Bang M, Kim KR et al (2015) Impaired facial emotion recognition in individuals at ultra-high risk for psychosis and with first-episode schizophrenia, and their associations with neurocognitive deficits and self-reported schizotypy. Schizophr Res 165:60–65CrossRefPubMed

61.

Crossley NA, Mechelli A, Fusar-Poli P et al (2009) Superior temporal lobe dysfunction and frontotemporal dysconnectivity in subjects at risk of psychosis and in first-episode psychosis. Hum Brain Mapp 30(12):4129–4137CrossRefPubMed

62.

Carletti F, Woolley JB, Bhattacharyya S et al (2012) Alterations in white matter evident before the onset of psychosis. Schizophr Bull 38:1170–1179CrossRefPubMedPubMedCentral

63.

Fusar-Poli P, Bonoldi I, Yung AR et al (2012) Predicting psychosis: meta-analysis of transition outcomes in individuals at high clinical risk. Arch Gen Psychiatry 69:220–229CrossRefPubMed

64.

Sugranyes G, Kyriakopoulos M, Dima D et al (2012) Multimodal analyses identify linked functional and white matter abnormalities within the working memory network in schizophrenia. Schizophr Res 138:136–142CrossRefPubMedPubMedCentral

65.

Zatorre RJ, Fields RD, Johansen-Berg H (2012) Plasticity in gray and white: neuroimaging changes in brain structure during learning. Nat Neurosci 15(4):528–536CrossRefPubMedPubMedCentral

66.

Eklund A, Nichols TE, Knutsson H (2016) Cluster failure: Why fMRI inferences for spatial extent have inflated false-positive rates. Proc Natl Acad Sci 113(28):7900–7905CrossRefPubMedPubMedCentral

Title: Intrinsic functional connectivity of fronto-temporal networks in adolescents with early psychosis
Authors: Cristina Solé-Padullés
Josefina Castro-Fornieles
Elena de la Serna
Vanessa Sánchez-Gistau
Soledad Romero
Olga Puig
Anna Calvo
Nuria Bargalló
Inmaculada Baeza
Gisela Sugranyes
Publication date: 01-06-2017
Publisher: Springer Berlin Heidelberg
Published in: European Child & Adolescent Psychiatry / Issue 6/2017
Print ISSN: 1018-8827
Electronic ISSN: 1435-165X
DOI: https://doi.org/10.1007/s00787-016-0931-5

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Intrinsic functional connectivity of fronto-temporal networks in adolescents with early psychosis

Abstract

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

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