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Mismatch negativity and P3a amplitude in young adolescents with first-episode psychosis: a comparison with ADHD

Published online by Cambridge University Press:  25 October 2016

J. Rydkjær ,
J. R. Møllegaard Jepsen ,
A. K. Pagsberg ,
B. Fagerlund ,
B. Y. Glenthøj  and
B. Oranje
J. Rydkjær*
Affiliation:
Center for Clinical Intervention and Neuropsychiatric Schizophrenia Research (CINS) and Center for Neuropsychiatric Schizophrenia Research (CNSR), Mental Health Centre Glostrup, University of Copenhagen, Denmark Child and Adolescent Mental Health Center, Mental Health Services, Capital Region of Denmark, Copenhagen, Denmark
J. R. Møllegaard Jepsen
Affiliation:
Center for Clinical Intervention and Neuropsychiatric Schizophrenia Research (CINS) and Center for Neuropsychiatric Schizophrenia Research (CNSR), Mental Health Centre Glostrup, University of Copenhagen, Denmark Child and Adolescent Mental Health Center, Mental Health Services, Capital Region of Denmark, Copenhagen, Denmark
A. K. Pagsberg
Affiliation:
Child and Adolescent Mental Health Center, Mental Health Services, Capital Region of Denmark, Copenhagen, Denmark Faculty of Health and Medical Sciences, University of Copenhagen, Denmark
B. Fagerlund
Affiliation:
Center for Clinical Intervention and Neuropsychiatric Schizophrenia Research (CINS) and Center for Neuropsychiatric Schizophrenia Research (CNSR), Mental Health Centre Glostrup, University of Copenhagen, Denmark
B. Y. Glenthøj
Affiliation:
Center for Clinical Intervention and Neuropsychiatric Schizophrenia Research (CINS) and Center for Neuropsychiatric Schizophrenia Research (CNSR), Mental Health Centre Glostrup, University of Copenhagen, Denmark Faculty of Health and Medical Sciences, University of Copenhagen, Denmark
B. Oranje
Affiliation:
Center for Clinical Intervention and Neuropsychiatric Schizophrenia Research (CINS) and Center for Neuropsychiatric Schizophrenia Research (CNSR), Mental Health Centre Glostrup, University of Copenhagen, Denmark Faculty of Health and Medical Sciences, University of Copenhagen, Denmark Department of Psychiatry, Brain Center Rudolf Magnus, University Medical Center Utrecht, Utrecht, The Netherlands
*
*Address for correspondence: J. Rydkjær, Ph.D., Center for Neuropsychiatric Schizophrenia Research, Mental Health Centre Glostrup, Ndr. Ringvej 29-67, 2600 Glostrup, Denmark. (Email: jacob.rydkjaer@regionh.dk)
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Abstract

Background

Deficient mismatch negativity (MMN) has been proposed as a candidate biomarker in schizophrenia and may therefore be potentially useful in early identification and intervention in early onset psychosis. In this study we explored whether deficits in the automatic orienting and reorienting responses, measured as MMN and P3a amplitude, are present in young adolescents with first-episode psychosis (FEP) and whether findings are specific to psychosis compared to young adolescents with attention deficit hyperactivity disorder (ADHD).

Method

MMN and P3a amplitude were assessed in young adolescents (age 12–17 years) with either FEP (N = 27) or ADHD (N = 28) and age- and gender-matched healthy controls (N = 43). The MMN paradigm consisted of a four-tone auditory oddball task with deviant stimuli based on frequency, duration and their combination.

Results

Significantly less MMN was found in patients with psychosis compared to healthy controls in response to frequency and duration deviants. MMN amplitudes in the group of patients with ADHD were not significantly different from patients with psychosis or healthy controls. No significant group differences were found on P3a amplitude.

Conclusion

Young adolescents with FEP showed impaired MMN compared to healthy controls while intermediate and overlapping levels of MMN were observed in adolescents with ADHD. The findings suggest that young FEP patients already exhibit pre-attentive deficits that are characteristic of schizophrenia albeit expressed on a continuum shared with other neuropsychiatric disorders.

Keywords

Biomarkerelectrophysiologyneuropsychiatric disorderschizophrenia
Type
Original Articles
Information
Psychological Medicine , Volume 47 , Issue 2 , January 2017 , pp. 377 - 388
Copyright
Copyright © Cambridge University Press 2016 

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References

Addington, J, Heinssen, RK, Robinson, DG, Schooler, NR, Marcy, P, Brunette, MF, Correll, CU, Estroff, S, Mueser, KT, Penn, D, Robinson, JA, Rosenheck, RA, Azrin, ST, Goldstein, AB, Severe, J, Kane, JM (2015). Duration of untreated psychosis in community treatment settings in the United States. Psychiatric Services 66, 753–756. CrossRefGoogle ScholarPubMed
American Psychiatric Association (2013). Diagnostic and Statistical Manual of Mental Disorders, 5th edn. American Psychiatric Association: Arlington, VA.Google Scholar
Arnsten, AF (2009). Toward a new understanding of attention-deficit hyperactivity disorder pathophysiology: an important role for prefrontal cortex dysfunction. CNS Drugs 23, (Suppl. 1), 33–41.Google Scholar
Atkinson, RJ, Michie, PT, Schall, U (2012). Duration mismatch negativity and P3a in first-episode psychosis and individuals at ultra-high risk of psychosis. Biological Psychiatry 71, 98–104.CrossRefGoogle ScholarPubMed
Bech, P, Gram, LF, Dein, E, Jacobsen, O, Vitger, J, Bolwig, TG (1975). Quantitative rating of depressive states. Acta Psychiatrica Scandinavica 51, 161–170.Google Scholar
Brockhaus-Dumke, A, Tendolkar, I, Pukrop, R, Schultze-Lutter, F, Klosterkotter, J, Ruhrmann, S (2005). Impaired mismatch negativity generation in prodromal subjects and patients with schizophrenia. Schizophrenia Research 73, 297–310.CrossRefGoogle ScholarPubMed
Brodsky, K, Willcutt, EG, Davalos, DB, Ross, RG (2014). Neuropsychological functioning in childhood-onset psychosis and attention-deficit/hyperactivity disorder. Journal of Child Psychology and Psychiatry 55, 811–818.Google Scholar
Bruggemann, JM, Stockill, HV, Lenroot, RK, Laurens, KR (2013). Mismatch negativity (MMN) and sensory auditory processing in children aged 9–12 years presenting with putative antecedents of schizophrenia. International Journal of Psychophysiology 89, 374–380.Google Scholar
Catts, SV, Shelley, AM, Ward, PB, Liebert, B, McConaghy, N, Andrews, S, Michie, PT (1995). Brain potential evidence for an auditory sensory memory deficit in schizophrenia. American Journal of Psychiatry 152, 213–219.Google ScholarPubMed
Chang, JP, Lane, HY, Tsai, GE (2014). Attention deficit hyperactivity disorder and N-methyl-D-aspartate (NMDA) dysregulation. Current Pharmaceutical Design 20, 5180–5185.CrossRefGoogle ScholarPubMed
Dominguez, MD, Fisher, HL, Major, B, Chisholm, B, Rahaman, N, Joyce, J, Woolley, J, Lawrence, J, Hinton, M, Marlowe, K, Aitchison, K, Johnson, S, Hodes, M (2013). Duration of untreated psychosis in adolescents: ethnic differences and clinical profiles. Schizophrenia Research 150, 526–532.Google Scholar
Driver, DI, Gogtay, N, Rapoport, JL (2013). Childhood onset schizophrenia and early onset schizophrenia spectrum disorders. Child and Adolescent Psychiatric Clinics of North America 22, 539–555.Google Scholar
DuPaul, GJ, Anastopoulos, AD, Power, TJ, Reid, R, Ikeda, MJ, McGoey, KE (1998). Parent ratings of attention-deficit/hyperactivity disorder symptoms: factor structure and normative data. Journal of Psychopathology and Behavioral Assessment 20, 83–102.CrossRefGoogle Scholar
Friedman, D, Cycowicz, YM, Gaeta, H (2001). The novelty P3: an event-related brain potential (ERP) sign of the brain's evaluation of novelty. Neuroscience & Biobehavioral Reviews 25, 355–373.Google Scholar
Gardner, DM, Murphy, AL, O'Donnell, H, Centorrino, F, Baldessarini, RJ (2010). International consensus study of antipsychotic dosing. American Journal of Psychiatry 167, 686–693.Google Scholar
Giard, MH, Perrin, F, Pernier, J, Bouchet, P (1990). Brain generators implicated in the processing of auditory stimulus deviance: a topographic event-related potential study. Psychophysiology 27, 627–640.Google Scholar
Gomes, H, Duff, M, Flores, A, Halperin, JM (2013). Automatic processing of duration in children with attention-deficit/hyperactivity disorder. Journal of the International Neuropsychological Society 19, 686–694.Google Scholar
Groom, MJ, Jackson, GM, Calton, TG, Andrews, HK, Bates, AT, Liddle, PF, Hollis, C (2008). Cognitive deficits in early-onset schizophrenia spectrum patients and their non-psychotic siblings: a comparison with ADHD. Schizophrenia Research 99, 85–95.Google Scholar
Hamilton, M (1960). A rating scale for depression. Journal of Neurology, Neurosurgery & Psychiatry 23, 56–62.Google Scholar
Hollis, C (2000). Adult outcomes of child- and adolescent-onset schizophrenia: diagnostic stability and predictive validity. American Journal of Psychiatry 157, 1652–1659.Google Scholar
Howes, OD, Kapur, S (2009). The dopamine hypothesis of schizophrenia: version III-the final common pathway. Schizophrenia Bulletin 35, 549–562.Google Scholar
Huttunen, T, Halonen, A, Kaartinen, J, Lyytinen, H (2007). Does mismatch negativity show differences in reading-disabled children compared to normal children and children with attention deficit? Developmental Neuropsychology 31, 453–470.Google Scholar
Huttunen-Scott, T, Kaartinen, J, Tolvanen, A, Lyytinen, H (2008). Mismatch negativity (MMN) elicited by duration deviations in children with reading disorder, attention deficit or both. International Journal of Psychophysiology 69, 69–77.CrossRefGoogle ScholarPubMed
Jahshan, C, Cadenhead, KS, Rissling, AJ, Kirihara, K, Braff, DL, Light, GA (2012). Automatic sensory information processing abnormalities across the illness course of schizophrenia. Psychological Medicine 42, 85–97.Google Scholar
Joa, I, Johannessen, JO, Langeveld, J, Friis, S, Melle, I, Opjordsmoen, S, Simonsen, E, Vaglum, P, McGlashan, T, Larsen, TK (2009). Baseline profiles of adolescent vs. adult-onset first-episode psychosis in an early detection program. Acta Psychiatrica Scandinavica 119, 494–500.Google Scholar
Kaufman, J, Birmaher, B, Brent, D, Rao, U, Flynn, C, Moreci, P, Williamson, D, Ryan, N (1997). Schedule for Affective Disorders and Schizophrenia for School-Age Children-Present and Lifetime Version (K-SADS-PL): initial reliability and validity data. Journal of the American Academy of Child & Adolescent Psychiatry 36, 980–988.Google Scholar
Kay, SR, Fiszbein, A, Opler, LA (1987). The positive and negative syndrome scale (PANSS) for schizophrenia. Schizophrenia Bulletin 13, 261–276.Google Scholar
Kemner, C, Verbaten, MN, Koelega, HS, Buitelaar, JK, van der Gaag, RJ, Camfferman, G, van, EH (1996). Event-related brain potentials in children with attention-deficit and hyperactivity disorder: effects of stimulus deviancy and task relevance in the visual and auditory modality. Biological Psychiatry 40, 522–534.Google Scholar
Keshavan, M, Montrose, DM, Rajarethinam, R, Diwadkar, V, Prasad, K, Sweeney, JA (2008). Psychopathology among offspring of parents with schizophrenia: relationship to premorbid impairments. Schizophrenia Research 103, 114–120.Google Scholar
Kim-Cohen, J, Caspi, A, Moffitt, TE, Harrington, H, Milne, BJ, Poulton, R (2003). Prior juvenile diagnoses in adults with mental disorder: developmental follow-back of a prospective-longitudinal cohort. Archives of General Psychiatry 60, 709–717.Google Scholar
Krausz, M, Muller-Thomsen, T (1993). Schizophrenia with onset in adolescence: an 11-year followup. Schizophrenia Bulletin 19, 831–841.Google Scholar
Light, GA, Braff, DL (2005). Mismatch negativity deficits are associated with poor functioning in schizophrenia patients. Archives of General Psychiatry 62, 127–136.Google Scholar
Light, GA, Naatanen, R (2013). Mismatch negativity is a breakthrough biomarker for understanding and treating psychotic disorders. Proceedings of the National Academy of Sciences USA 110, 15175–15176.Google Scholar
Magno, E, Yeap, S, Thakore, JH, Garavan, H, De, SP, Foxe, JJ (2008). Are auditory-evoked frequency and duration mismatch negativity deficits endophenotypic for schizophrenia? High-density electrical mapping in clinically unaffected first-degree relatives and first-episode and chronic schizophrenia. Biological Psychiatry 64, 385–391.Google Scholar
Murphy, JR, Rawdon, C, Kelleher, I, Twomey, D, Markey, PS, Cannon, M, Roche, RA (2013). Reduced duration mismatch negativity in adolescents with psychotic symptoms: further evidence for mismatch negativity as a possible biomarker for vulnerability to psychosis. BMC Psychiatry 13, 45.Google Scholar
Naatanen, R (1995). The mismatch negativity: a powerful tool for cognitive neuroscience. Ear and Hearing 16, 6–18.Google Scholar
Naatanen, R, Kahkonen, S (2009). Central auditory dysfunction in schizophrenia as revealed by the mismatch negativity (MMN) and its magnetic equivalent MMNm: a review. International Journal of Neuropsychopharmacology 12, 125–135.Google Scholar
Nagai, T, Tada, M, Kirihara, K, Araki, T, Jinde, S, Kasai, K (2013). Mismatch negativity as a ‘translatable’ brain marker toward early intervention for psychosis: a review. Frontiers in Psychiatry 4, 115.Google Scholar
Oades, RD, Dittmann-Balcar, A, Schepker, R, Eggers, C, Zerbin, D (1996). Auditory event-related potentials (ERPs) and mismatch negativity (MMN) in healthy children and those with attention-deficit or tourette/tic symptoms. Biological Psychology 43, 163–185.Google Scholar
Oades, RD, Dittmann-Balcar, A, Zerbin, D, Grzella, I (1997). Impaired attention-dependent augmentation of MMN in nonparanoid vs paranoid schizophrenic patients: a comparison with obsessive-compulsive disorder and healthy subjects. Biological Psychiatry 41, 1196–1210.Google Scholar
Oades, RD, Wild-Wall, N, Juran, SA, Sachsse, J, Oknina, LB, Ropcke, B (2006). Auditory change detection in schizophrenia: sources of activity, related neuropsychological function and symptoms in patients with a first episode in adolescence, and patients 14 years after an adolescent illness-onset. BMC Psychiatry 6, 7.Google Scholar
Okkels, N, Vernal, DL, Jensen, SO, McGrath, JJ, Nielsen, RE (2013). Changes in the diagnosed incidence of early onset schizophrenia over four decades. Acta Psychiatrica Scandinavica 127, 62–68.Google Scholar
Oknina, LB, Wild-Wall, N, Oades, RD, Juran, SA, Ropcke, B, Pfueller, U, Weisbrod, M, Chan, E, Chen, EY (2005). Frontal and temporal sources of mismatch negativity in healthy controls, patients at onset of schizophrenia in adolescence and others at 15 years after onset. Schizophrenia Research 76, 25–41.Google Scholar
Oranje, B, Jensen, K, Wienberg, M, Glenthoj, BY (2008). Divergent effects of increased serotonergic activity on psychophysiological parameters of human attention. International Journal of Neuropsychopharmacology 11, 453–463.Google Scholar
Pedersen, CB, Mors, O, Bertelsen, A, Waltoft, BL, Agerbo, E, McGrath, JJ, Mortensen, PB, Eaton, WW (2014). A comprehensive nationwide study of the incidence rate and lifetime risk for treated mental disorders. JAMA Psychiatry 71, 573–581.Google Scholar
Perez, VB, Swerdlow, NR, Braff, DL, Naatanen, R, Light, GA (2014 a). Using biomarkers to inform diagnosis, guide treatments and track response to interventions in psychotic illnesses. Biomarkers in Medicine 8, 9–14.Google Scholar
Perez, VB, Woods, SW, Roach, BJ, Ford, JM, McGlashan, TH, Srihari, VH, Mathalon, DH (2014 b). Automatic auditory processing deficits in schizophrenia and clinical high-risk patients: forecasting psychosis risk with mismatch negativity. Biological Psychiatry 75, 459–469.Google Scholar
Rissling, AJ, Braff, DL, Swerdlow, NR, Hellemann, G, Rassovsky, Y, Sprock, J, Pela, M, Light, GA (2012). Disentangling early sensory information processing deficits in schizophrenia. Clinical Neurophysiology 123, 1942–1949.Google Scholar
Ross, RG, Heinlein, S, Tregellas, H (2006). High rates of comorbidity are found in childhood-onset schizophrenia. Schizophrenia Research 88, 90–95.CrossRefGoogle ScholarPubMed
Rothenberger, A, Banaschewski, T, Heinrich, H, Moll, GH, Schmidt, MH, van't, KB (2000). Comorbidity in ADHD-children: effects of coexisting conduct disorder or tic disorder on event-related brain potentials in an auditory selective-attention task. European Archives of Psychiatry and Clinical Neuroscience 250, 101–110.Google Scholar
Salisbury, DF, Kuroki, N, Kasai, K, Shenton, ME, McCarley, RW (2007). Progressive and interrelated functional and structural evidence of post-onset brain reduction in schizophrenia. Archives of General Psychiatry 64, 521–529.Google Scholar
Salisbury, DF, Shenton, ME, Griggs, CB, Bonner-Jackson, A, McCarley, RW (2002). Mismatch negativity in chronic schizophrenia and first-episode schizophrenia. Archives of General Psychiatry 59, 686–694.CrossRefGoogle ScholarPubMed
Schreiber, H, Stolz-Born, G, Kornhuber, HH, Born, J (1992). Event-related potential correlates of impaired selective attention in children at high risk for schizophrenia. Biological Psychiatry 32, 634–651.Google Scholar
Shaffer, D, Gould, MS, Brasic, J, Ambrosini, P, Fisher, P, Bird, H, Aluwahlia, S (1983). A children's global assessment scale (CGAS). Archives of General Psychiatry 40, 1228–1231.Google Scholar
Shelley, AM, Ward, PB, Catts, SV, Michie, PT, Andrews, S, McConaghy, N (1991). Mismatch negativity: an index of a preattentive processing deficit in schizophrenia. Biological Psychiatry 30, 1059–1062.Google Scholar
Stone, JM, Bramin, E, Pauls, A, Sumich, A, McGuire, PK (2010). Thalamic neurochemical abnormalities in individuals with prodromal symptoms of schizophrenia – relationship to auditory event-related potentials. Psychiatry Research 183, 174–176.Google Scholar
Sumich, A, Castro, A, Anilkumar, AP, Zachariah, E, Kumari, V (2013). Neurophysiological correlates of excitement in schizophrenia. Progress in Neuro-psychopharmacology & Biological Psychiatry 1, 132–138.Google Scholar
Sumich, A, Kumari, V, Dodd, P, Ettinger, U, Hughes, C, Zachariah, E, Sharma, T (2008). N100 and P300 amplitude to Go and No-Go variants of the auditory oddball in siblings discordant for schizophrenia. Schizophrenia Research 98, 265–277.Google Scholar
Todd, J, Michie, PT, Schall, U, Karayanidis, F, Yabe, H, Naatanen, R (2008). Deviant matters: duration, frequency, and intensity deviants reveal different patterns of mismatch negativity reduction in early and late schizophrenia. Biological Psychiatry 63, 58–64.Google Scholar
Umbricht, D, Krljes, S (2005). Mismatch negativity in schizophrenia: a meta-analysis. Schizophrenia Research 76, 1–23.Google Scholar
Umbricht, DS, Bates, JA, Lieberman, JA, Kane, JM, Javitt, DC (2006). Electrophysiological indices of automatic and controlled auditory information processing in first-episode, recent-onset and chronic schizophrenia. Biological Psychiatry 59, 762–772.Google Scholar
Wienberg, M, Glenthoj, BY, Jensen, KS, Oranje, B (2010). A single high dose of escitalopram increases mismatch negativity without affecting processing negativity or P300 amplitude in healthy volunteers. Journal of Psychopharmacology 24, 1183–1192.Google Scholar
Winsberg, BG, Javitt, DC, Silipo, GS (1997). Electrophysiological indices of information processing in methylphenidate responders. Biological Psychiatry 42, 434–445.Google Scholar
Wynn, JK, Sugar, C, Horan, WP, Kern, R, Green, MF (2010). Mismatch negativity, social cognition, and functioning in schizophrenia patients. Biological Psychiatry 67, 940–947.CrossRefGoogle ScholarPubMed
Zhou, Z, Zhu, H, Chen, L (2013). Effect of aripiprazole on mismatch negativity (MMN) in schizophrenia. PLoS ONE 8, e52186.Google Scholar