Altered auditory processing in frontal and left temporal cortex in 22q11.2 deletion syndrome: A group at high genetic risk for schizophrenia

Psychiatry Research - Neuroimaging

Volumn 212, Issue 2, 2013, Pages 141-149

  Rihs, Tonia A ^a   Tomescu, Miralena I ^a   Britz, Juliane ^a   Rochas, Vincent ^a   Custo, Anna ^a   Schneider, Maude ^a   Debbané, Martin ^a   Eliez, Stephan ^a   Michel, Christoph M ^a,b  

^a UNIVERSITY OF GENEVA   (Switzerland)

^b UNIVERSITY HOSPITAL   (Switzerland)

Author keywords

22q11.2 deletion; EEG source imaging; N100 components; P50 auditory sensory gating; Psychosis; Velo cardio facial syndrome (VCFS)

Indexed keywords

ADOLESCENT; ADULT; ANTERIOR CINGULATE; ARTICLE; AUDITORY CORTEX; AUDITORY STIMULATION; CHROMOSOME DELETION 22Q11; CLINICAL ARTICLE; CONTROLLED STUDY; ELECTRODE; ELECTROENCEPHALOGRAM; EVOKED AUDITORY RESPONSE; FEMALE; FRONTAL CORTEX; GENETIC RISK; HUMAN; MALE; MIDDLE FRONTAL GYRUS; PRIORITY JOURNAL; SCHIZOPHRENIA; TEMPORAL CORTEX;

ACOUSTIC STIMULATION; ADOLESCENT; BRAIN MAPPING; CASE-CONTROL STUDIES; DIGEORGE SYNDROME; DISEASE PROGRESSION; ELECTROENCEPHALOGRAPHY; EVOKED POTENTIALS, AUDITORY; FEMALE; FRONTAL LOBE; FUNCTIONAL LATERALITY; HUMANS; MALE; SCHIZOPHRENIA; TEMPORAL LOBE; YOUNG ADULT;

EID: 84876811357     PISSN: 09254927     EISSN: 18727506     Source Type: Journal    
DOI: 10.1016/j.pscychresns.2012.09.002     Document Type: Article

References (86)

1. Baker K.D., Skuse D.H. Adolescents and young adults with 22q11 deletion syndrome: psychopathology in an at-risk group. British Journal of Psychiatry 2005, 186:115-120.
2. Barbas H., Ghashghaei H., Dombrowski S.M., Rempel-Clower N.L. Medial prefrontal cortices are unified by common connections with superior temporal cortices and distinguished by input from memory-related areas in the rhesus monkey. Journal of Comparative Neurology 1999, 410:343-367.
3. Baudena P., Halgren E., Heit G., Clarke J.M. Intracerebral potentials to rare target and distractor auditory and visual stimuli. III. Frontal cortex. Electroencephalography and Clinical Neurophysiology 1995, 94:251-264.
4. Bearden C.E., van Erp T.G., Dutton R.A., Tran H., Zimmermann L., Sun D., Geaga J.A., Simon T.J., Glahn D.C., Cannon T.D., Emanuel B.S., Toga A.W., Thompson P.M. Mapping cortical thickness in children with 22q11.2 deletions. Cerebral Cortex 2007, 17:1889-1898.
5. Boutros N.N., Korzyukov O., Jansen B., Feingold A., Bell M. Sensory gating deficits during the mid-latency phase of information processing in medicated schizophrenia patients. Psychiatry Research 2004, 126:203-215.
6. Brockhaus-Dumke A., Schultze-Lutter F., Mueller R., Tendolkar I., Bechdolf A., Pukrop R., Klosterkoetter J., Ruhrmann S. Sensory gating in schizophrenia: P50 and N100 gating in antipsychotic-free subjects at risk, first-episode, and chronic patients. Biological Psychiatry 2008, 64:376-384.
7. Brunet D., Murray M.M., Michel C.M. Spatiotemporal analysis of multichannel EEG: CARTOOL. Computational Intelligence and Neuroscience 2011, 2011:813-870.
8. Cadenhead K.S., Light G.A., Shafer K.M., Braff D.L. P50 suppression in individuals at risk for schizophrenia: the convergence of clinical, familial, and vulnerability marker risk assessment. Biological Psychiatry 2005, 57:1504-1509.
9. Calkins M.E., Dobie D.J., Cadenhead K.S., Olincy A., Freedman R., Green M.F., Greenwood T.A., Gur R.E., Gur R.C., Light G.A., Mintz J., Nuechterlein K.H., Radant A.D., Schork N.J., Seidman L.J., Siever L.J., Silverman J.M., Stone W.S., Swerdlow N.R., Tsuang D.W., Tsuang M.T., Turetsky B.I., Braff D.L. The Consortium on the Genetics of Endophenotypes in Schizophrenia: model recruitment, assessment, and endophenotyping methods for a multisite collaboration. Schizophrenia Bulletin 2007, 33:33-48.
10. Chow E.W., Ho A., Wei C., Voormolen E.H., Crawley A.P., Bassett A.S. Association of schizophrenia in 22q11.2 deletion syndrome and gray matter volumetric deficits in the superior temporal gyrus. American Journal of Psychiatry 2011, 168:522-529.
11. Cleghorn J.M., Garnett E.S., Nahmias C., Brown G.M., Kaplan R.D., Szechtman H., Szechtman B., Franco S., Dermer S.W., Cook P. Regional brain metabolism during auditory hallucinations in chronic schizophrenia. British Journal of Psychiatry 1990, 157:562-570.
12. Clementz B.A., Blumenfeld L.D. Multichannel electroencephalographic assessment of auditory evoked response suppression in schizophrenia. Experimental Brain Research 2001, 139:377-390.
13. Debbané M., Glaser B., David M.K., Feinstein C., Eliez S. Psychotic symptoms in children and adolescents with 22q11.2 deletion syndrome: Neuropsychological and behavioral implications. Schizophrenia Research 2006, 84:187-193.
14. Dien J., Tucker D.M., Potts G.F., Hartry-Speiser A.L. Localization of auditory evoked potentials related to selective intermodal attention. Journal of Cognitive Neuroscience 1997, 9:99-823.
15. Fletcher P., McKenna P.J., Friston K.J., Frith C.D., Dolan R.J. Abnormal cingulate modulation of fronto-temporal connectivity in schizophrenia. Neuroimage 1999, 9:337-342.
16. Ford J.M., Mathalon D.H., Kalba S., Marsh L., Pfefferbaum A. N1 and P300 abnormalities in patients with schizophrenia, epilepsy, and epilepsy with schizophrenialike features. Biological Psychiatry 2001, 49:848-860.
17. Fornito A., Yucel M., Dean B., Wood S.J., Pantelis C. Anatomical abnormalities of the anterior cingulate cortex in schizophrenia: bridging the gap between neuroimaging and neuropathology. Schizophrenia Bulletin 2009, 35:973-993.
18. Fornito A., Yung A.R., Wood S.J., Phillips L.J., Nelson B., Cotton S., Velakoulis D., McGorry P.D., Pantelis C., Yucel M. Anatomic abnormalities of the anterior cingulate cortex before psychosis onset: an MRI study of ultra-high-risk individuals. Biological Psychiatry 2008, 64:758-765.
19. Foxe J.J., Yeap S., Snyder A.C., Kelly S.P., Thakore J.H., Molholm S. The N1 auditory evoked potential component as an endophenotype for schizophrenia: high-density electrical mapping in clinically unaffected first-degree relatives, first-episode, and chronic schizophrenia patients. European Archives of Psychiatry and Clinical Neuroscience 2011, 261:331-339.
20. Frodl T., Meisenzahl E.M., Gallinat J., Hegerl U., Moller H.J. Markers from event-related potential subcomponents and reaction time for information processing dysfunction in schizophrenia. European Archives of Psychiatry and Clinical Neuroscience 1998, 248:307-313.
21. Gallinat J., Mulert C., Bajbouj M., Herrmann W.M., Schunter J., Senkowski D., Moukhtieva R., Kronfeldt D., Winterer G. Frontal and temporal dysfunction of auditory stimulus processing in schizophrenia. Neuroimage 2002, 17:110-127.
22. Giard M.H., Perrin F., Echallier J.F., Thevenet M., Froment J.C., Pernier J. Dissociation of temporal and frontal components in the human auditory N1 wave: a scalp current density and dipole model analysis. Electroencephalography and Clinical Neurophysiology 1994, 92:238-252.
23. Goghari V.M., Sponheim S.R., MacDonald A.W. The functional neuroanatomy of symptom dimensions in schizophrenia: a qualitative and quantitative review of a persistent question. Neuroscience and Biobehavioral Reviews 2010, 34:468-486.
24. Goldman A.L., Pezawas L., Mattay V.S., Fischl B., Verchinski B.A., Chen Q., Weinberger D.R., Meyer-Lindenberg A. Widespread reductions of cortical thickness in schizophrenia and spectrum disorders and evidence of heritability. Archives of General Psychiatry 2009, 66:467-477.
25. Gomes H., Dunn M., Ritter W., Kurtzberg D., Brattson A., Kreuzer J.A., Vaughan H.G. Spatiotemporal maturation of the central and lateral N1 components to tones. Developmental Brain Research 2001, 129:147-155.
26. Grave de Peralta Menendez R., Gonzalez Andino S., Lantz G., Michel C.M., Landis T. Noninvasive localization of electromagnetic epileptic activity. I. Method descriptions and simulations. Brain Topography 2001, 14:131-137.
27. Greenwood T.A., Lazzeroni L.C., Murray S.S., Cadenhead K.S., Calkins M.E., Dobie D.J., Green M.F., Gur R.E., Gur R.C., Hardiman G., Kelsoe J.R., Leonard S., Light G.A., Nuechterlein K.H., Olincy A., Radant A.D., Schork N.J., Seidman L.J., Siever L.J., Silverman J.M., Stone W.S., Swerdlow N.R., Tsuang D.W., Tsuang M.T., Turetsky B.I., Freedman R., Braff D.L. Analysis of 94 candidate genes and 12 endophenotypes for schizophrenia from the Consortium on the Genetics of Schizophrenia. American Journal of Psychiatry 2011, 168:930-946.
28. Grossberg S. How hallucinations may arise from brain mechanisms of learning, attention, and volition. Journal of the International Neuropsychological Society 2000, 6:583-592.
29. Halgren E., Baudena P., Clarke J.M., Heit G., Marinkovic K., Devaux B., Vignal J.P., Biraben A. Intracerebral potentials to rare target and distractor auditory and visual stimuli. II. Medial, lateral and posterior temporal lobe. Electroencephalography and Clinical Neurophysiology 1995, 94:229-250.
30. Hansen J.C., Hillyard S.A. Endogenous brain potentials associated with selective auditory attention. Electroencephalography and Clinical Neurophysiology 1980, 49:277-290.
31. Honea R., Crow T.J., Passingham D., Mackay C.E. Regional deficits in brain volume in schizophrenia: a meta-analysis of voxel-based morphometry studies. American Journal of Psychiatry 2005, 162:2233-2245.
32. Hubl D., Koenig T., Strik W.K., Garcia L.M., Dierks T. Competition for neuronal resources: how hallucinations make themselves heard. British Journal of Psychiatry 2007, 190:57-62.
33. Javitt D.C. Sensory processing in schizophrenia: neither simple nor intact. Schizophrenia Bulletin 2009, 35:1059-1064.
34. Jerger K., Biggins C., Fein G. P50 suppression is not affected by attentional manipulations. Biological Psychiatry 1992, 31:365-377.
35. Karayiorgou, M., Simon, T.J., Gogos, J.A., 2010. 22q11.2 microdeletions: linking DNA structural variation to brain dysfunction and schizophrenia. Nature Reviews Neuroscience 11, 402-416.
36. Kates W.R., Antshel K.M., Faraone S.V., Fremont W.P., Higgins A.M., Shprintzen R.J., Botti J.A., Kelchner L., McCarthy C. Neuroanatomic predictors to prodromal psychosis in velocardiofacial syndrome (22q11.2 deletion syndrome): a longitudinal study. Biological Psychiatry 2011, 69:945-952.
37. Kurthen M., Trautner P., Rosburg T., Grunwald T., Dietl T., Kuhn K.U., Schaller C., Elger C.E., Urbach H., Elisevich K., Boutros N.N. Towards a functional topography of sensory gating areas: invasive P50 recording and electrical stimulation mapping in epilepsy surgery candidates. Psychiatry Research 2007, 155:121-133.
38. Laurent A., Garcia-Larrea L., d'Amato T., Bosson J.L., Saoud M., Marie-Cardine M., Maugiere F., Dalery J. Auditory event-related potentials and clinical scores in unmedicated schizophrenic patients. Psychiatry Research 1999, 86:229-238.
39. Lehmann D., Skrandies W. Reference-free identification of components of checkerboard-evoked multichannel potential fields. Electroencephalography and Clinical Neurophysiology 1980, 48:609-621.
40. Lewis-Hanna L.L., Hunter M.D., Farrow T.F., Wilkinson I.D., Woodruff P.W. Enhanced cortical effects of auditory stimulation and auditory attention in healthy individuals prone to auditory hallucinations during partial wakefulness. Neuroimage 2011, 57:1154-1161.
41. Lijffijt M., Lane S.D., Meier S.L., Boutros N.N., Burroughs S., Steinberg J.L., Moeller F.G., Swann A.C. P50, N100, and P200 sensory gating: relationships with behavioral inhibition, attention, and working memory. Psychophysiology 2009, 46:1059-1068.
42. Luck S.J., Mathalon D.H., O'Donnell B.F., Hamalainen M.S., Spencer K.M., Javitt D.C., Uhlhaas P.J. A roadmap for the development and validation of event-related potential biomarkers in schizophrenia research. Biological Psychiatry 2011, 70:28-34.
43. Mayhew S.D., Dirckx S.G., Niazy R.K., Iannetti G.D., Wise R.G. EEG signatures of auditory activity correlate with simultaneously recorded fMRI responses in humans. Neuroimage 2010, 49:849-864.
44. McCallum W.C., Curry S.H. The form and distribution of auditory evoked potentials and CNVs when stimuli and responses are lateralized. Progress in Brain Research 1980, 54:767-775.
45. McGlashan T.H., Addington J., Cannon T., Heinimaa M., McGorry P., O'Brien M., Penn D., Perkins D., Salokangas R.K., Walsh B., Woods S.W., Yung A. Recruitment and treatment practices for help-seeking "prodromal" patients. Schizophrenia Bulletin 2007, 33:715-726.
46. McGorry P.D., Yung A.R., Phillips L.J., Yuen H.P., Francey S., Cosgrave E.M., Germano D., Bravin J., McDonald T., Blair A., Adlard S., Jackson H. Randomized controlled trial of interventions designed to reduce the risk of progression to first-episode psychosis in a clinical sample with subthreshold symptoms. Archives of General Psychiatry 2002, 59:921-928.
47. Michel C.M., Murray M.M., Lantz G., Gonzalez S., Spinelli L., Grave de Peralta R. EEG source imaging. Clinical Neurophysiology 2004, 115:2195-2222.
48. Michel C.M., Murray M.M. Towards the utilization of EEG as a brain imaging tool. Neuroimage 2012, 61(2):371-385.
49. Minzenberg M.J., Laird A.R., Thelen S., Carter C.S., Glahn D.C. Meta-analysis of 41 functional neuroimaging studies of executive function in schizophrenia. Archives of General Psychiatry 2009, 66:811-822.
50. Morosan P., Rademacher J., Schleicher A., Amunts K., Schormann T., Zilles K. Human primary auditory cortex: cytoarchitectonic subdivisions and mapping into a spatial reference system. Neuroimage 2001, 13:684-701.
51. Morrison A.P., French P., Parker S., Roberts M., Stevens H., Bentall R.P., Lewis S.W. Three-year follow-up of a randomized controlled trial of cognitive therapy for the prevention of psychosis in people at ultrahigh risk. Schizophrenia Bulletin 2007, 33:682-687.
52. Mulert C., Gallinat J., Pascual-Marqui R., Dorn H., Frick K., Schlattmann P., Mientus S., Herrmann W.M., Winterer G. Reduced event-related current density in the anterior cingulate cortex in schizophrenia. Neuroimage 2001, 13:589-600.
53. Murray M.M., Brunet D., Michel C.M. Topographic ERP analyses: a step-by-step tutorial review. Brain Topography 2008, 20:249-264.
54. Myles-Worsley M., Ord L., Blailes F., Ngiralmau H., Freedman R. P50 sensory gating in adolescents from a pacific island isolate with elevated risk for schizophrenia. Biological Psychiatry 2004, 55:663-667.
55. Naatanen R., Picton T. The N1 wave of the human electric and magnetic response to sound: a review and an analysis of the component structure. Psychophysiology 1987, 24:375-425.
56. O'Donnell B.F., Vohs J.L., Hetrick W.P., Carroll C.A., Shekhar A. Auditory event-related potential abnormalities in bipolar disorder and schizophrenia. International Journal of Psychophysiology 2004, 53:45-55.
57. Ogura C., Nageishi Y., Matsubayashi M., Omura F., Kishimoto A., Shimokochi M. Abnormalities in event-related potentials, N100, P200, P300 and slow wave in schizophrenia. Japanese Journal of Psychiatry and Neurology 1991, 45:57-65.
58. Olincy A., Braff D.L., Adler L.E., Cadenhead K.S., Calkins M.E., Dobie D.J., Green M.F., Greenwood T.A., Gur R.E., Gur R.C., Light G.A., Mintz J., Nuechterlein K.H., Radant A.D., Schork N.J., Seidman L.J., Siever L.J., Silverman J.M., Stone W.S., Swerdlow N.R., Tsuang D.W., Tsuang M.T., Turetsky B.I., Wagner B.D., Freedman R. Inhibition of the P50 cerebral evoked response to repeated auditory stimuli: results from the Consortium on Genetics of Schizophrenia. Schizophrenia Research 2010, 119:175-182.
59. Orr J.M., Weissman D.H. Anterior cingulate cortex makes two contributions to minimizing distraction. Cerebral Cortex 2009, 19:703-711.
60. Pearlson G.D. Superior temporal gyrus and planum temporale in schizophrenia: a selective review. Progress in Neuro-Psychopharmacology and Biological Psychiatry 1997, 21:1203-1229.
61. Philip N., Bassett A. Cognitive, behavioural and psychiatric phenotype in 22q11.2 deletion syndrome. Behavior Genetics 2011, 41:403-412.
62. Picton T.W., Alain C., Woods D.L., John M.S., Scherg M., Valdes-Sosa P., Bosch-Bayard J., Trujillo N.J. Intracerebral sources of human auditory-evoked potentials. Audiology and Neurotology 1999, 4:64-79.
63. Ponton C.W., Eggermont J.J., Kwong B., Don M. Maturation of human central auditory system activity: evidence from multi-channel evoked potentials. Clinical Neurophysiology 2000, 111:220-236.
64. Potts G.F., Dien J., Hartry-Speiser A.L., McDougal L.M., Tucker D.M. Dense sensor array topography of the event-related potential to task-relevant auditory stimuli. Electroencephalography and Clinical Neurophysiology 1998, 106:444-456.
65. Preston G.A., Weinberger D.R. Intermediate phenotypes in schizophrenia: a selective review. Dialogues in Clinical Neuroscience 2005, 7:165-179.
66. Romanos M., Ehlis A.C., Baehne C.G., Jacob C., Renner T.J., Storch A., Briegel W., Walitza S., Lesch K.P., Fallgatter A.J. Reduced NoGo-anteriorisation during continuous performance test in deletion syndrome 22q11.2. Journal of Psychiatric Research 2010, 44:768-774.
67. Rosburg T., Boutros N.N., Ford J.M. Reduced auditory evoked potential component N100 in schizophrenia-a critical review. Psychiatry Research 2008, 161:259-274.
68. Roth W.T., Horvath T.B., Pfefferbaum A., Kopell B.S. Event-related potentials in schizophrenics. Electroencephalography and Clinical Neurophysiology 1980, 48:127-139.
69. Salisbury D.F., Collins K.C., McCarley R.W. Reductions in the N1 and P2 auditory event-related potentials in first-hospitalized and chronic schizophrenia. Schizophrenia Bulletin 2010, 36:991-1000.
70. Schaer M., Debbane M., Bach Cuadra M., Ottet M.C., Glaser B., Thiran J.P., Eliez S. Deviant trajectories of cortical maturation in 22q11.2 deletion syndrome (22q11 DS): a cross-sectional and longitudinal study. Schizophrenia Research 2009, 115:182-190.
71. Scherg M., Vajsar J., Picton T.W. A source analysis of the late human auditory evoked potentials. Journal of Cognitive Neuroscience 1989, 1:336-355.
72. Schultz C.C., Koch K., Wagner G., Nenadic I., Schachtzabel C., Gullmar D., Reichenbach J.R., Sauer H., Schlosser R.G. Reduced anterior cingulate cognitive activation is associated with prefrontal-temporal cortical thinning in schizophrenia. Biological Psychiatry 2012, 71(2):146-153.
73. Shelley A.M., Silipo G., Javitt D.C. Diminished responsiveness of ERPs in schizophrenic subjects to changes in auditory stimulation parameters: implications for theories of cortical dysfunction. Schizophrenia Research 1999, 37:65-79.
74. Shergill S.S., Brammer M.J., Williams S.C., Murray R.M., McGuire P.K. Mapping auditory hallucinations in schizophrenia using functional magnetic resonance imaging. Archives of General Psychiatry 2000, 57:1033-1038.
75. Shin K.S., Jung W.H., Kim J.S., Jang J.H., Hwang J.Y., Chung C.K., Kwon J.S. Neuromagnetic auditory response and its relation to cortical thickness in ultra-high-risk for psychosis. Schizophrenia Research 2012, 140:93-98.
76. Simons C.J., Sambeth A., Krabbendam L., Pfeifer S., van Os J., Riedel W.J. Auditory P300 and N100 components as intermediate phenotypes for psychotic disorder: familial liability and reliability. Clinical Neurophysiology 2011, 122:1984-1990.
77. Spinelli L., Andino S.G., Lantz G., Seeck M., Michel C.M. Electromagnetic inverse solutions in anatomically constrained spherical head models. Brain Topography 2000, 13:115-125.
78. Steinschneider M., Arezzo J., Vaughan H.G. Phase-locked cortical responses to a human speech sound and low-frequency tones in the monkey. Brain Research 1980, 198:75-84.
79. Strik W.K., Dierks T., Boning J., Osterheider M., Caspari A., Korber J. Disorders of smooth pursuit eye movement and auditory N100 in schizophrenic patients. Psychiatry Research 1992, 41:227-235.
80. Turetsky B.I., Bilker W.B., Siegel S.J., Kohler C.G., Gur R.E. Profile of auditory information-processing deficits in schizophrenia. Psychiatry Research 2009, 165:27-37.
81. Turetsky B.I., Calkins M.E., Light G.A., Olincy A., Radant A.D., Swerdlow N.R. Neurophysiological endophenotypes of schizophrenia: the viability of selected candidate measures. Schizophrenia Bulletin 2007, 33:69-94.
82. Tzourio N., Massioui F.E., Crivello F., Joliot M., Renault B., Mazoyer B. Functional anatomy of human auditory attention studied with PET. Neuroimage 1997, 5:63-77.
83. van Lutterveld R., Oranje B., Kemner C., Abramovic L., Willems A.E., Boks M.P., Glenthoj B.Y., Kahn R.S., Sommer I.E. Increased psychophysiological parameters of attention in non-psychotic individuals with auditory verbal hallucinations. Schizophrenia Research 2010, 121:153-159.
84. Vorstman J.A., Turetsky B.I., Sijmens-Morcus M.E., de Sain M.G., Dorland B., Sprong M., Rappaport E.F., Beemer F.A., Emanuel B.S., Kahn R.S., van Engeland H., Kemner C. Proline affects brain function in 22q11 DS children with the low activity COMT 158 allele. Neuropsychopharmacology 2009, 34:739-746.
85. Wood C.C., Wolpaw J.R. Scalp distribution of human auditory evoked potentials. II. Evidence for overlapping sources and involvement of auditory cortex. Electroencephalography and Clinical Neurophysiology 1982, 54:25-38.
86. Woodruff P.W. Auditory hallucinations: Insights and questions from neuroimaging. Cognitive Neuropsychiatry 2004, 9:73-91.