Multivariate pattern classification reveals differential brain activation during emotional processing in individuals with psychosis proneness

NeuroImage

Volumn 59, Issue 3, 2012, Pages 3033-3041

  Modinos, Gemma ^a,b   Pettersson Yeo, William ^a   Allen, Paul ^a   McGuire, Philip K ^a   Aleman, André ^b   Mechelli, Andrea ^a  

^a KING'S COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

Author keywords

Emotion; FMRI; Machine learning; Multivariate; Psychosis proneness; Support Vector Machine

Indexed keywords

ACCURACY; ADULT; AMYGDALOID NUCLEUS; ANTERIOR CINGULATE; ARTICLE; BRAIN FUNCTION; CONTROLLED STUDY; DISEASE PREDISPOSITION; EMOTION; FEMALE; HUMAN; HUMAN EXPERIMENT; INSULA; INTERMETHOD COMPARISON; MALE; MEDIAL PREFRONTAL CORTEX; MULTIVARIATE ANALYSIS; NORMAL HUMAN; PREFRONTAL CORTEX; PRIORITY JOURNAL; PSYCHOSIS; STIMULUS RESPONSE; SUPPORT VECTOR MACHINE; UNIVARIATE ANALYSIS; VISUAL STIMULATION;

AFFECT; ARTIFICIAL INTELLIGENCE; BRAIN; DISEASE SUSCEPTIBILITY; EMOTIONS; FEMALE; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; LINEAR MODELS; MAGNETIC RESONANCE IMAGING; MALE; MODELS, NEUROLOGICAL; MULTIVARIATE ANALYSIS; NERVE NET; PATTERN RECOGNITION, AUTOMATED; PHOTIC STIMULATION; PSYCHOMOTOR PERFORMANCE; PSYCHOTIC DISORDERS; RISK ASSESSMENT; SCHIZOPHRENIA; SUPPORT VECTOR MACHINES; YOUNG ADULT;

EID: 84855449460     PISSN: 10538119     EISSN: 10959572     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2011.10.048     Document Type: Article

References (82)

1. Addington J., Penn D., Woods S.W., Addington D., Perkins D.O. Facial affect recognition in individuals at clinical high risk for psychosis. Br. J. Psychiatry 2008, 192:67-68.
2. Aleman A., Kahn R.S. Strange feelings: do amygdala abnormalities dysregulate the emotional brain in schizophrenia?. Prog. Neurobiol. 2005, 77:283-298.
3. Anticevic, A., Van Snellenberg, J.X., Cohen, R.E., Repovs, G., Dowd, E.C., Barch, D.M., in press. Amygdala recruitment in schizophrenia in response to aversive emotional material: a meta-analysis of neuroimaging studies. Schizophr. Bull. doi:. doi:10.1093/schbul/sbq131.
4. Baas D., Aleman A., Kahn R.S. Lateralization of amygdala activation: a systematic review of functional neuroimaging studies. Brain Res. Brain Res. Rev. 2004, 45:96-103.
5. Beck A.T., Steer R.A., Ball R., Ranieri W.F. Comparison of Beck depression inventories-IA and -II in psychiatric outpatients. J. Pers. Assess. 1996, 67:588-597.
6. Berenbaum H., Boden T.M., Baker J.P., Dizen M., Thompson R.J. Emotional correlates of the different dimensions of schizotypal personality disorder. J. Abnorm. Psychol. 2006, 115:359-368.
7. Borgwardt S.J., Riecher-Rössler A., Dazzan P., Chitnis X., Aston J., Drewe M., Gschwandtner U., Haller S., Pflüger M., Rechsteiner E., D'Souza M., Stieglitz R.D., Radü E.W., McGuire P.K. Regional gray matter volume abnormalities in the at risk mental state. Biol. Psychiatry 2007, 61:1148-1156.
8. Boser B., Guyon I., Vapnik V. A training algorithm for optimal margin classifiers. Fifth Annual Workshop on Computational Learning Theory 1992, 144-152. ACM Press, Baltimore.
9. Brunet-Gouet E., Decety J. Social brain dysfunctions in schizophrenia: a review of neuroimaging studies. Psychiatry Res. 2006, 148:75-92.
10. Bush G., Luu P., Posner M.I. Cognitive and emotional influences in anterior cingulate cortex. Trends Cogn. Sci. 2000, 4:215-222.
11. Cannon T., Cadenhead K., Cornblatt B., Woods S.W., Addington J., Walker E., Seidman L.J., Perkins D., Tsuang M., McGlashan T., Heinssen R. Prediction of psychosis in ultra high risk youth: a multi-site longitudinal study in North America. Arch. Gen. Psychiatry 2008, 65:28-37.
12. Chapman L.J., Chapman J.P., Kwapil T.R., Eckblad M., Zinser M.C. Putatively psychosis-prone subjects 10years later. J. Abnorm. Psychol. 1994, 103:171-183.
13. Cohen A.S., Minor K.S. Emotional experience in patients with schizophrenia revisited: meta-analysis of laboratory studies. Schizophr. Bull. 2010, 36:143-150.
14. Costafreda S.G., Fu C.H., Picchioni M., Toulopoulou T., McDonald C., Kravariti E., Walshe M., Prata D., Murray R.M., McGuire P.K. Pattern of neural responses to verbal fluency shows diagnostic specificity for schizophrenia and bipolar disorder. BMC Psychiatry 2011, 11:18.
15. Damasio A.R., Grabowski T.J., Bechara A., Damasio H., Ponto L.L.B., Parvizi J., Hichwa R.D. Subcortical and cortical brain activity during the feeling of self-generated emotions. Nat. Neurosci. 2000, 3:1049-1056.
16. Davatzikos C., Shen D., Gur R.C., Wu X., Liu D., Fan Y., Hughett P., Turetsky B.I., Gur R.E. Whole-brain morphometric study of schizophrenia revealing a spatially complex set of focal abnormalities. Arch. Gen. Psychiatry 2005, 62:1218-1227.
17. Davidson R.J., Irwin W. The functional neuroanatomy of emotion and affective style. Trends Cogn. Sci. 1999, 3:11-21.
18. Eack S.M., Mermon D.E., Montrose D.M., Miewald J., Gur R.E., Gur R.C., Sweeney J.A., Keshavan M.S. Social cognition deficits among individuals at familial high risk for schizophrenia. Schizophr. Bull. 2010, 36:1081-1088.
19. Fernyhough C., Jones S.R., Whittle C., Waterhouse J., Bentall R.P. Theory of mind, schizotypy, and persecutory ideation in young adults. Cogn. Neuropsychiatry 2008, 13:233-249.
20. Friston K.J., Holmes A.P., Worsley K.J., Poline J.-P., Frith C.D., Frackowiak R.S.J. Statistical parametric maps in functional imaging: a general linear approach. Hum. Brain Mapp. 1995, 2:189-210.
21. Gooding D.C., Tallent K.A., Matts C.W. Clinical status of at-risk individuals 5years later: further validation of the psychometric high-risk strategy. J. Abnorm. Psychol. 2005, 114:170-175.
22. Hanssen M., Bak M., Bijl R., Vollebergh W., Van Os J. The incidence and outcome of subclinical psychotic experiences in the general population. Br. J. Clin. Psychol. 2005, 44:181-191.
23. Henry J.D., Rendell P.G., Green M.J., McDonald S., O'Donnell M. Emotion regulation in schizophrenia: affective, social, and clinical correlates of suppression and reappraisal. J. Abnorm. Psychol. 2008, 117:473-478.
24. Henry J.D., Green M.J., Restuccia C., de Lucia A., Rendell P.G., McDonald S., Grisham J.R. Emotion dysregulation and schizotypy. Psychiatry Res. 2009, 166:116-124.
25. Horan W.P., Blanchard J.J., Clark L.A., Green M.F. Affective traits in schizophrenia and schizotypy. Schizophr. Bull. 2008, 34:856-874.
26. Horan W.P., Reise S.P., Subotnik K.L., Ventura J., Nuechterlein K.H. The validity of psychosis proneness scales as vulnerability indicators in recent-onset schizophrenia patients. Schizophr. Res. 2008, 100:224-236.
27. Houston J.E., Shevlin M., Adamson G., Murphy J. A person-centred approach to modelling population experiences of trauma and mental illness. Soc. Psychiatry Psychiatr. Epidemiol. 2010, 46:149-157.
28. Hulshoff Pol H.E., Schnack H.G., Mandl R.C., van Haren N.E., Koning H., Collins D.L., Evans A.C., Kahn R.S. Focal gray matter density changes in schizophrenia. Arch. Gen. Psychiatry 2001, 58:1118-1125.
29. Jahshan C.S., Sergi M.J. Theory of mind, neurocognition, and functional status in schizotypy. Schizophr. Res. 2007, 89:278-286.
30. Janssen I., Versmissen D., Campo J.A., Myin-Germeys I., van Os J., Krabbendam L. Attribution style and psychosis: evidence for an externalizing bias in patients but not in individuals at high risk. Psychol. Med. 2006, 36:771-778.
31. Kee K.S., Green M.F., Mintz J., Brekke J.S. Is emotion processing a predictor of functional outcome in schizophrenia?. Schizophr. Bull. 2003, 29:487-497.
32. Kerns J.G. Positive schizotypy and emotion processing. J. Abnorm. Psychol. 2005, 114:392-401.
33. Keshavan M.S., Dick E., Mankowski I., Harenski K., Montrose D.M., Diwadkar V., DeBellis M. Decreased left amygdala and hippocampal volumes in young offspring at risk for schizophrenia. Schizophr. Res. 2002, 58:173-183.
34. Kohler C.G., Bilker W., Hagendoorn M., Gur R.E., Gur R.C. Emotion recognition deficit in schizophrenia: association with symptomatology and cognition. Biol. Psychiatry 2000, 48:127-136.
35. Konings M., Bak M., Hanssen M., van Os J., Krabbendam L. Validity and reliability of the CAPE: a self-report instrument for the measurement of psychotic experiences in the general population. Acta Psychiatr. Scand. 2006, 114:55-61.
36. Lang P.J., Bradley M.M., Cuthbert B.N. International Affective Picture System (IAPS): Technical Manual and Affective Ratings 1997, NIMH Center for the study of emotion and attention, University of Florida, Gainsville, FL.
37. Lang P.J., Bradley M.M., Cuthbert B.N. International Affective Picture System (IAPS): affective ratings of pictures and instruction manual. Technical Report A-8 2008, University of Florida, Gainesville, FL.
38. Langdon R., Coltheart M. Mentalising, schizotypy, and schizophrenia. Cognition 1999, 71:43-71.
39. Langdon R., Coltheart M. Visual perspective-taking and schizotypy: evidence for a simulation-based account of mentalizing in normal adults. Cognition 2001, 82:1-26.
40. Langdon R., Coltheart M. Recognition of metaphor and irony in young adults: the impact of schizotypal personality traits. Psychiatry Res. 2004, 125:9-20.
41. Lao Z., Shen D., Xue Z., Karacali B., Resnick S.M., Davatzikos C. Morphological classification of brains via high-dimensional shape transformations and machine learning methods. NeuroImage 2004, 21:46-57.
42. Lawrie S.M., Whalley H.C., Job D.E., Johnstone E.C. Structural and functional abnormalities of the amygdala in schizophrenia. Ann. N. Y. Acad. Sci. 2003, 985:445-460.
43. LeDoux J.E. The Emotional Brain 1996, Simon and Schuster, New York.
44. Li H., Chan R.C., McAlonan G.M., Gong Q.Y. Facial emotion processing in schizophrenia: a meta-analysis of functional neuroimaging data. Schizophr. Bull. 2010, 36:1029-1039.
45. Mason O., Startup M., Halpin S., Schall U., Conrad A., Carr V. Risk factors for transition to first episode psychosis among individuals with "at-risk mental states". Schizophr. Res. 2004, 71:227-237.
46. Mendrek A., Mancini-Marië A., Fahim C., Stip E. Sex differences in the cerebral function associated with processing of aversive stimuli by schizophrenia patients. Aust. N. Z. J. Psychiatry 2007, 41:136-141.
47. Modinos G., Mechelli A., Ormel J., Groenewold N.A., Aleman A., McGuire P.K. Schizotypy and brain structure: a voxel-based morphometry study. Psychol. Med. 2010, 40:1423-1431.
48. Modinos G., Ormel J., Aleman A. Altered activation and functional connectivity of neural systems supporting cognitive control of emotion in psychosis proneness. Schizophr. Res. 2010, 118:88-97.
49. Mohanty A., Heller W., Koven N.S., Fisher J.E., Herrington J.D., Miller G.A. Specificity of emotion-related effects on attentional processing in schizotypy. Schizophr. Res. 2008, 103:129-137.
50. Mourão-Miranda J., Bokde A.L., Born C., Hampel H., Stetter M. Classifying brain states and determining the discriminating activation patterns: Support Vector Machine on functional MRI data. NeuroImage 2005, 28:980-995.
51. Mourão-Miranda J., Friston K.J., Brammer M. Dynamic discrimination analysis: a spatial-temporal SVM. NeuroImage 2007, 36:88-99.
52. Pantelis C., Velakoulis D., McGorry P.D., Wood S.J., Suckling J., Phillips L.J., Yung A.R., Bullmore E.T., Brewer W., Soulsby B., Desmond P., McGuire P.K. Neuroanatomical abnormalities before and after onset of psychosis: a cross sectional and longitudinal MRI comparison. Lancet 2003, 361:281-288.
53. Paradiso S., Andreasen N.C., Crespo-Facorro B., O'Leary D.S., Watkins G.L., Boles Ponto L.L., Hichwa R.D. Emotions in unmedicated patients with schizophrenia during evaluation with positron emission tomography. Am. J. Psychiatry 2003, 160:1775-1783.
54. Phan K.L., Wager T., Taylor S.F., Liberzon I. Functional neuroanatomy of emotion: a meta-analysis of emotion activation studies in PET and fMRI. NeuroImage 2002, 16:331-348.
55. Phillips L.K., Seidman L.J. Emotion processing in persons at risk for schizophrenia. Schizophr. Bull. 2008, 34:888-903.
56. Phillips M.L., Drevets W.C., Rauch S.L., Lane R. Neurobiology of emotion perception I: the neural basis of normal emotion perception. Biol. Psychiatry 2003, 54:504-514.
57. Phillips M.L., Drevets W.C., Rauch S.L., Lane R. Neurobiology of emotion perception II: implications for major psychiatric disorders. Biol. Psychiatry 2003, 54:515-528.
58. Poulton R., Caspi A., Moffitt T.E., Cannon M., Murray R., Harrington H. Children's self-reported psychotic symptoms and adult schizophreniform disorder: a 15-year longitudinal study. Arch. Gen. Psychiatry 2000, 57:1053-1058.
59. Premkumar, P., Ettinger, U., Inchley-Mort, S., Sumich, A., Williams, S.C., Kuipers, E., Kumari, V., in press. Neural processing of social rejection: the role of schizotypal personality traits. Hum. Brain Mapp. doi:. doi:10.1002/hbm.21243.
60. Reiman E.M., Lane R.D., Ahern G.L., Schwartz G.E., Davidson R.J., Friston K.J., Yun L.S., Chen K. Neuroanatomical correlates of externally and internally generated human emotion. Am. J. Psychiatry 1997, 154:918-925.
61. Rolls E.T. The functions of the orbitofrontal cortex. Brain Cogn. 2004, 55:11-29.
62. Rolls E.T., Grabenhorst F. The orbitofrontal cortex and beyond: from affect to decision-making. Prog. Neurobiol. 2008, 86:216-244.
63. Rossler W., Riecher-Rossler A., Angst J., Murray R., Gamma A., Eich D., van Os J., Gross V.A. Psychotic experiences in the general population: a twenty-year prospective community study. Schizophr. Res. 2007, 92:1-14.
64. Saze T., Hirao K., Namiki C., Fukuyama H., Hayashi T., Murai T. Insular volume reduction in schizophrenia. Eur. Arch. Psychiatry Clin. Neurosci. 2007, 257:473-479.
65. Sergerie K., Chochol C., Armony J.L. The role of the amygdala in emotional processing: a quantitative meta-analysis of functional neuroimaging studies. Neurosci. Biobehav. Rev. 2008, 32:811-830.
66. Smieskova R., Fusar-Poli P., Allen P., Bendfeldt K., Stieglitz R.D., Drewe J., Radue E.W., McGuire P.K., Riecher-Rössler A., Borgwardt S.J. Neuroimaging predictors of transition to psychosis-a systematic review and meta-analysis. Neurosci. Biobehav. Rev. 2010, 34:1207-1222.
67. Stefanis N.C., Hanssen M., Smirnis N.K., Avramopoulos D.A., Evdokimidis I.K., Stefanis C.N., Verdoux H., van Os J. Evidence that three dimensions of psychosis have a distribution in the general population. Psychol. Med. 2002, 32:347-358.
68. Sun D., van Erp T.G., Thompson P.M., Bearden C.E., Daley M., Kushan L., Hardt M.E., Nuechterlein K.H., Toga A.W., Cannon T.D. Elucidating a magnetic resonance imaging-based neuroanatomic biomarker for psychosis: classification analysis using probabilistic brain atlas and machine learning algorithms. Biol. Psychiatry 2009, 66:1055-1060.
69. Takahashi H., Koeda M., Oda K., Matsuda T., Matsushima E., Matsuura M., Asai K., Okubo Y. An fMRI study of differential neural response to affective pictures in schizophrenia. NeuroImage 2004, 22:1247-1254.
70. Taylor S.E., Liberzon I., Decker L.R., Koeppe R.A. A functional anatomic study of emotion in schizophrenia. Schizophr. Res. 2002, 58:159-172.
71. Taylor S.E., Phan K.L., Britton J.C., Liberzon I. Neural response to emotional salience in schizophrenia. Neuropsychopharmacology 2005, 30:984-995.
72. Thaker G., Moran M., Adami H., Cassady S. Psychosis proneness scales in schizophrenia spectrum personality disorders: familial vs. nonfamilial samples. Psychiatry Res. 1993, 46:47-57.
73. van 't Wout M., Aleman A., Kessels R.P., Larøi F., Kahn R.S. Emotional processing in a non-clinical psychosis prone-sample. Schizophr. Res. 2004, 68:271-281.
74. van Os J., Linscott R.J., Myin-Germeys I., Delespaul P., Krabbendam L. A systematic review and meta-analysis of the psychosis continuum: evidence for a psychosis proneness-persistence-impairment model of psychotic disorder. Psychol. Med. 2009, 39:179-195.
75. Vapnik V. The Nature of Statistical Learning Theory 1995, Springer-Verlag, New York.
76. Vollema M.G., van den Bosch R.J. The multidimensionality of schizotypy. Schizophr. Bull. 1995, 21:19-31.
77. Wager T.D., Phan K.L., Liberzon I., Taylor S.F. Valence, gender, and lateralization of functional brain anatomy in emotion: a meta-analysis of findings from neuroimaging. NeuroImage 2003, 19:513-531.
78. Whalley H.C., McKirdy J., Romaniuk L., Sussmann J., Johnstone E.C., Wan H.I., McIntosh A.M., Lawrie S.M., Hall J. Functional imaging of emotional memory in bipolar disorder and schizophrenia. Bipolar Disord. 2009, 11:840-856.
79. Wright I.C., Rabe-Hesketh S., Woodruff P.W., David A.S., Murray R.M., Bullmore E.T. Meta-analysis of regional brain volumes in schizophrenia. Am. J. Psychiatry 2000, 157:16-25.
80. Wylie K.P., Tregellas J.R. The role of the insula in schizophrenia. Schizophr. Res. 2010, 123:93-104.
81. Yung A.R., Phillips L.J., Yuen H.P., Francey S.M., McFarlane C.A., Hallgren M., McGorry P.D. Psychosis prediction: 12-month follow up of a high-risk ("prodromal") group. Schizophr. Res. 2003, 60:21-32.
82. Yung A.R., Phillips L.J., Yuen H.P., McGorry P.D. Risk factors for psychosis in an ultra high-risk group: psychopathology and clinical features. Schizophr. Res. 2004, 67:131-142.