Abstract
Individuals at clinical high risk (CHR) for psychosis exhibit a reduced P300 oddball response, which indicates deficits in attention and working memory processes. Previous studies have mainly researched these responses in the temporal domain; hence, non-phase-locked or induced neural activities may have been ignored. Event-related potential (ERP) and time–frequency (TF) information, combined with clinical and cognitive profiles, may provide an insight into the pathophysiology and psychopathology of the CHR stage. The 104 CHR individuals who completed cognitive assessments and ERP tests were recruited and followed up between 2016 and 2018. Individuals with CHR were classified by three clinical subtypes demonstrated before, specifically 32 from Cluster-1 (characterized by extensive negative symptoms and cognitive deficits, at the highest risk for conversion to psychosis), 34 from Cluster-2 (characterized by thought and behavioral disorganization, with moderate cognitive impairment), and 38 from Cluster-3 (characterized by the mildest symptoms and cognitive deficits). Electroencephalograms were recorded during the auditory oddball paradigm. The P300 ERPs were analyzed in the temporal domain. The event-related spectral perturbation (ERSP) and inter-trial coherence (ITC) were acquired by TF analysis. A reduced P300 response to target tones was noted in Cluster-1 relative to the other two clusters. Moreover, the P300 amplitude of Cluster-1 was associated with speed of processing (SoP) scores. Furthermore, the P300 amplitude of Cluster-3 was significantly correlated with verbal and visual learning scores. In the TF analysis, decreased delta ERSP and ITC were observed in Cluster-1; delta ITC was associated with SoP scores in Cluster-3. The results indicate relatively disrupted oddball responses in a certain CHR subtype and a close affinity between these electrophysiological indexes and attention, working memory, and declarative memory within different CHR clusters. These findings suggest that the auditory oddball response is a potential neurophysiological marker for distinct clinical subtypes of CHR.
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References
Addington J, Addington D, Abidi S, Raedler T, Remington G (2017) Canadian treatment guidelines for individuals at clinical high risk of psychosis. Can J Psychiatry 62:656–661
Alday PM, Kretzschmar F (2019) Speed-accuracy tradeoffs in brain and behavior: testing the independence of P300 and N400 related processes in behavioral responses to sentence categorization. Front Hum Neurosci 13:285
Almeida PR, Vieira JB, Silveira C, Ferreira-Santos F, Chaves PL, Barbosa F, Marques-Teixeira J (2011) Exploring the dynamics of P300 amplitude in patients with schizophrenia. Int J Psychophysiol 81:159–168
Başar-Eroglu C, Başar E, Demiralp T, Schürmann M (1992) P300-response: possible psychophysiological correlates in delta and theta frequency channels. A review. Int J Psychophysiol 13:161–179
Başar E, Güntekin B, Tülay E, Yener GG (2010) Evoked and event related coherence of Alzheimer patients manifest differentiation of sensory-cognitive networks. Brain Res 1357:79–90
Bledowski C, Prvulovic D, Hoechstetter K, Scherg M, Wibral M, Goebel R, Linden DE (2004) Localizing P300 generators in visual target and distractor processing: a combined event-related potential and functional magnetic resonance imaging study. J Neurosci 24:9353–9360
Cohen MX (2014) Analyzing neural time series data: theory and practice. MIT press, Cambridge
Cui H, Giuliano AJ, Zhang T, Xu L, Wei Y, Tang Y, Qian Z, Stone LM, Li H, Whitfield-Gabrieli S, Niznikiewicz M, Keshavan MS, Shenton ME, Wang J, Stone WS (2020) Cognitive dysfunction in a psychotropic medication-naïve, clinical high-risk sample from the shanghai-at-risk-for-psychosis (SHARP) study: associations with clinical outcomes. Schizophr Res 226:138–146
Delorme A, Makeig S (2004) EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis. J Neurosci Methods 134:9–21
Doege K, Bates AT, White TP, Das D, Boks MP, Liddle PF (2009) Reduced event-related low frequency EEG activity in schizophrenia during an auditory oddball task. Psychophysiology 46:566–577
Ethridge LE, Hamm JP, Pearlson GD, Tamminga CA, Sweeney JA, Keshavan MS, Clementz BA (2015) Event-related potential and time–frequency endophenotypes for schizophrenia and psychotic bipolar disorder. Biol Psychiat 77:127–136
Ford JM, Roach BJ, Hoffman RS, Mathalon DH (2008) The dependence of P300 amplitude on gamma synchrony breaks down in schizophrenia. Brain Res 1235:133–142
Fusar-Poli P, Salazar de Pablo G, Correll CU, Meyer-Lindenberg A, Millan MJ, Borgwardt S, Galderisi S, Bechdolf A, Pfennig A, Kessing LV, van Amelsvoort T, Nieman DH, Domschke K, Krebs MO, Koutsouleris N, McGuire P, Do KQ, Arango C (2020) Prevention of psychosis: advances in detection, prognosis, and intervention. JAMA Psychiat 77:755–765
Goldstein A, Spencer KM, Donchin E (2002) The influence of stimulus deviance and novelty on the P300 and novelty P3. Psychophysiology 39:781–790
Hamilton HK, Roach BJ, Bachman PM, Belger A, Carrion RE, Duncan E, Johannesen JK, Light GA, Niznikiewicz MA, Addington J, Bearden CE, Cadenhead KS, Cornblatt BA, McGlashan TH, Perkins DO, Seidman LJ, Tsuang MT, Walker EF, Woods SW, Cannon TD, Mathalon DH (2019) Association between P300 responses to auditory oddball stimuli and clinical outcomes in the psychosis risk syndrome. JAMA Psychiat 76:1187–1197
Hamilton HK, Woods SW, Roach BJ, Llerena K, McGlashan TH, Srihari VH, Ford JM, Mathalon DH (2019) Auditory and visual oddball stimulus processing deficits in schizophrenia and the psychosis risk syndrome: forecasting psychosis risk with P300. Schizophr Bull 45:1068–1080
Jones SH, Thornicroft G, Coffey M, Dunn G (1995) A brief mental health outcome scale-reliability and validity of the global assessment of functioning (GAF). Br J Psychiatry 166:654–659
Kayser J, Tenke CE, Kroppmann CJ, Alschuler DM, Fekri S, Ben-David S, Corcoran CM, Bruder GE (2014) Auditory event-related potentials and α oscillations in the psychosis prodrome: neuronal generator patterns during a novelty oddball task. Int J Psychophysiol 91:104–120
Kim M, Lee TH, Kim JH, Hong H, Lee TY, Lee Y, Salisbury DF, Kwon JS (2018) Decomposing p300 into correlates of genetic risk and current symptoms in schizophrenia: an inter-trial variability analysis. Schizophr Res 192:232–239
Klimesch W (1999) EEG alpha and theta oscillations reflect cognitive and memory performance: a review and analysis. Brain Res Brain Res Rev 29:169–195
Knowles EE, David AS, Reichenberg A (2010) Processing speed deficits in schizophrenia: reexamining the evidence. Am J Psychiatry 167:828–835
Kochunov P, Coyle TR, Rowland LM, Jahanshad N, Thompson PM, Kelly S, Du X, Sampath H, Bruce H, Chiappelli J, Ryan M, Fisseha F, Savransky A, Adhikari B, Chen S, Paciga SA, Whelan CD, Xie Z, Hyde CL, Chen X, Schubert CR, O’Donnell P, Hong LE (2017) Association of white matter with core cognitive deficits in patients with schizophrenia. JAMA Psychiat 74:958–966
Lieberman JA, Small SA, Girgis RR (2019) Early detection and preventive intervention in schizophrenia: from fantasy to reality. Am J Psychiatry 176:794–810
Lopez-Calderon J, Luck SJ (2014) ERPLAB: an open-source toolbox for the analysis of event-related potentials. Front Hum Neurosci 8:213
Luck SJ, Kappenman ES (2013) The oxford handbook of event-related potential components. Oxford University Press, Oxford
Makeig S, Westerfield M, Jung TP, Enghoff S, Townsend J, Courchesne E, Sejnowski TJ (2002) Dynamic brain sources of visual evoked responses. Science 295:690–694
Miller TJ, McGlashan TH, Rosen JL, Somjee L, Markovich PJ, Stein K, Woods SW (2002) Prospective diagnosis of the initial prodrome for schizophrenia based on the structured interview for prodromal syndromes: preliminary evidence of interrater reliability and predictive validity. Am J Psychiatry 159:863–865
Ozgürdal S, Gudlowski Y, Witthaus H, Kawohl W, Uhl I, Hauser M, Gorynia I, Gallinat J, Heinze M, Heinz A, Juckel G (2008) Reduction of auditory event-related P300 amplitude in subjects with at-risk mental state for schizophrenia. Schizophr Res 105:272–278
Polich J (2007) Updating P300: an integrative theory of P3a and P3b. Clin Neurophysiol 118:2128–2148
Ramyead A, Roach B, Hamilton H, Addington J, Psychiatry DMJB (2019) O33. EEG alpha event-related desynchronization deficits predict conversion to psychosis in individuals with the psychosis risk syndrome. Biol Psychiatry 85(10):S119
Rolf V, Piotr J, Edmund WJ (2005) Evidence for an integrative role of p3b in linking reaction to perception. J Psychophysiol 19:165–181
Rolls ET, Loh M, Deco G, Winterer G (2008) Computational models of schizophrenia and dopamine modulation in the prefrontal cortex. Nat Rev Neurosci 9:696–709
Roth A, Roesch-Ely D, Bender S, Weisbrod M, Kaiser S (2007) Increased event-related potential latency and amplitude variability in schizophrenia detected through wavelet-based single trial analysis. Int J Psychophysiol 66:244–254
Seidman LJ, Shapiro DI, Stone WS, Woodberry KA, Ronzio A, Cornblatt BA, Addington J, Bearden CE, Cadenhead KS, Cannon TD, Mathalon DH, McGlashan TH, Perkins DO, Tsuang MT, Walker EF, Woods SW (2016) Association of neurocognition with transition to psychosis: baseline functioning in the second phase of the North American prodrome longitudinal study. JAMA Psychiat 73:1239–1248
Shi C, He Y, Cheung EF, Yu X, Chan RC (2013) An ecologically valid performance-based social functioning assessment battery for schizophrenia. Psychiatry Res 210:787–793
Shi C, Kang L, Yao S, Ma Y, Li T, Liang Y, Cheng Z, Xu Y, Shi J, Xu X, Zhang C, Franklin DR, Heaton RK, Jin H, Yu X (2015) The matrics consensus cognitive battery (MCCB): co-norming and standardization in china. Schizophr Res 169:109–115
Shin YW, Krishnan G, Hetrick WP, Brenner CA, Shekhar A, Malloy FW, O’Donnell BF (2010) Increased temporal variability of auditory event-related potentials in schizophrenia and schizotypal personality disorder. Schizophr Res 124:110–118
Turetsky BI, Dress EM, Braff DL, Calkins ME, Green MF, Greenwood TA, Gur RE, Gur RC, Lazzeroni LC, Nuechterlein KH, Radant AD, Seidman LJ, Siever LJ, Silverman JM, Sprock J, Stone WS, Sugar CA, Swerdlow NR, Tsuang DW, Tsuang MT, Light G (2015) The utility of P300 as a schizophrenia endophenotype and predictive biomarker: clinical and socio-demographic modulators in cogs-2. Schizophr Res 163:53–62
van Os J, Guloksuz S (2017) A critique of the “ultra-high risk” and “transition” paradigm. World Psychiatry 16:200–206
van Tricht MJ, Nieman DH, Koelman JH, van der Meer JN, Bour LJ, de Haan L, Linszen DH (2010) Reduced parietal P300 amplitude is associated with an increased risk for a first psychotic episode. Biol Psychiat 68:642–648
von Stein A, Chiang C, König P (2000) Top-down processing mediated by interareal synchronization. Proc Natl Acad Sci USA 97:14748–14753
Wu G, Gan R, Li Z, Xu L, Tang X, Wei Y, Hu Y, Cui H, Li H, Tang Y, Hui L, Liu X, Li C, Wang J, Zhang T (2019) Real-world effectiveness and safety of antipsychotics in individuals at clinical high-risk for psychosis: study protocol for a prospective observational study (shanghai at risk for psychosis-phase 2). Neuropsychiatr Dis Treat 15:3541–3548
Zhang T, Li H, Woodberry KA, Seidman LJ, Zheng L, Li H, Zhao S, Tang Y, Guo Q, Lu X, Zhuo K, Qian Z, Chow A, Li C, Jiang K, Xiao Z, Wang J (2014) Prodromal psychosis detection in a counseling center population in China: an epidemiological and clinical study. Schizophr Res 152:391–399
Zhang T, Tang X, Li H, Woodberry KA, Kline ER, Xu L, Cui H, Tang Y, Wei Y, Li C, Hui L, Niznikiewicz MA, Shenton ME, Keshavan MS, Stone WS, Wang J (2020) Clinical subtypes that predict conversion to psychosis: a canonical correlation analysis study from the Shanghai at risk for psychosis program. Aust N Z J Psychiatry 54:482–495
Zheng L, Wang J, Zhang T, Li H, Li C, Jiang K (2012) Reliability and validity of the Chinese version of scale of psychosis-risk symptoms. Chin Ment Health J 26:571–576
Zheng W, Zhang QE, Cai DB, Ng CH, Ungvari GS, Ning YP, Xiang YT (2018) Neurocognitive dysfunction in subjects at clinical high risk for psychosis: a meta-analysis. J Psychiatr Res 103:38–45
Acknowledgements
This study was supported by National Natural Science Foundation of China (81671329, 81671332, 81901832), Science and Technology Commission of Shanghai Municipality (19441907800, 19ZR1445200, 17411953100, 19410710800, 19411969100, 19411950800), Shanghai Clinical Research Center for Mental Health (19MC1911100) and The Clinical Research Center at Shanghai Mental Health Center (CRC2018ZD01, CRC2018ZD04), Project of the Key Discipline Construction, Shanghai 3-Year Public Health Action Plan (GWV-10.1-XK18).
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Wu, G., Tang, X., Gan, R. et al. Temporal and time–frequency features of auditory oddball response in distinct subtypes of patients at clinical high risk for psychosis. Eur Arch Psychiatry Clin Neurosci 272, 449–459 (2022). https://doi.org/10.1007/s00406-021-01316-1
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DOI: https://doi.org/10.1007/s00406-021-01316-1