Auditory prediction errors and auditory white matter microstructure associated with psychotic-like experiences in healthy individuals
Our sensory systems actively predict sensory information based on previously learnt patterns, which are continuously updated with information from the actual sensory input via prediction errors. Individuals with schizophrenia consistently show reduced auditory prediction errors as well as altered fractional anisotropy (indicative of white matter changes) in the arcuate fasciculus and the auditory interhemispheric pathway, both of which are auditory white matter pathways associated with prediction errors. However, it is not clear if healthy individuals with psychotic-like experiences exhibit similar deficits. Participants underwent electroencephalography (EEG) recordings while listening to a classical two-tone duration deviant oddball paradigm (n = 103) and a stochastic oddball paradigm (n = 89). A subset of participants (n = 89) also underwent diffusion-weighted magnetic resonance imaging (MRI). Fractional anisotropy (FA), was extracted from the arcuate fasciculi and the auditory interhemispheric pathway. While prediction errors evoked by the classical oddball paradigm failed to reveal significant effects, the stochastic oddball paradigm elicited significant clusters at the typical mismatch negativity time window. Furthermore, we observed that FA of the arcuate fasciculi and auditory interhemispheric pathway significantly improved predictive models of psychotic-like experiences in healthy individuals over and above predictions made by auditory prediction error responses alone. Specifically, we observed that decreasing FA in the auditory interhemispheric pathway and reducing ability to learn stochastic irregularities are associated with increasing CAPE + scores. To the extent that these associations have previously been reported in patients with schizophrenia, the findings from this study suggest that both, auditory prediction errors and white matter changes in the auditory interhemispheric pathway, may have the potential to be translated into early screening markers for psychosis.
KeywordsMMN P300 Prodromal Diffusion-weighted imaging (DWI) Schizophrenia Electroencephalography (EEG) Schizotypy
We thank John McGrath for helpful discussions; David Lloyd, Elise Rowe for support in EEG data acquisition. Aiman Al-Najjar and Nicole Atcheson for assisting in MRI data collection, and all participants for their time. M.I.G. was supported by a UQ Fellowship (2016000071), a UQ Foundation Research Excellence Award (2016001844), and the ARC Centre of Excellence for Integrative Brain Function (ARC CE140100007). R.R. was supported through a UQ International Research Scholarship.
- Fitzsimmons J, Schneiderman JS, Whitford TJ, Swisher T, Niznikiewicz MA, Pelavin PE, Terry DP, Mesholam-Gately RI, Seidman LJ, Goldstein JM, Kubicki M (2014) Cingulum bundle diffusivity and delusions of reference in first episode and chronic schizophrenia. Psychiatry Res 224:124–132PubMedPubMedCentralCrossRefGoogle Scholar
- Friedman JI, Tang C, Carpenter D, Buchsbaum M, Schmeidler J, Flanagan L, Golembo S, Kanellopoulou I, Ng J, Hof PR, Harvey PD, Tsopelas ND, Stewart D, Davis KL (2008) Diffusion tensor imaging findings in first-episode and chronic schizophrenia patients. Am J Psychiatry 165:1024–1032PubMedCrossRefPubMedCentralGoogle Scholar
- Mossaheb N, Becker J, Schaefer MR, Klier CM, Schloegelhofer M, Papageorgiou K, Amminger GP (2012) The community assessment of psychic experience (CAPE) questionnaire as a screening-instrument in the detection of individuals at ultra-high risk for psychosis. Schizophr Res 141:210–214PubMedCrossRefPubMedCentralGoogle Scholar
- Oestreich LK, Pasternak O, Shenton ME, Kubicki M, Gong X, McCarthy-Jones S, Whitford TJ (2016) Abnormal white matter microstructure and increased extracellular free-water in the cingulum bundle associated with delusions in chronic schizophrenia. NeuroImage Clin 12:405–414PubMedPubMedCentralCrossRefGoogle Scholar
- Peters BD, de Haan L, Dekker N, Blaas J, Becker HE, Dingemans PM, Akkerman EM, Majoie CB, van Amelsvoort T, den Heeten GJ, Linszen DH (2008) White matter fibertracking in first-episode schizophrenia, schizoaffective patients and subjects at ultra-high risk of psychosis. Neuropsychobiology 58:19–28PubMedCrossRefPubMedCentralGoogle Scholar
- Rissling AJ, Park SH, Young JW, Rissling MB, Sugar CA, Sprock J, Mathias DJ, Pela M, Sharp RF, Braff DL, Light GA (2013) Demand and modality of directed attention modulate “pre-attentive” sensory processes in schizophrenia patients and nonpsychiatric controls. Schizophr Res 146:326–335PubMedPubMedCentralCrossRefGoogle Scholar
- Smith SM, Jenkinson M, Woolrich MW, Beckmann CF, Behrens TE, Johansen-Berg H, Bannister PR, De Luca M, Drobnjak I, Flitney DE, Niazy RK, Saunders J, Vickers J, Zhang Y, De Stefano N, Brady JM, Matthews PM (2004) Advances in functional and structural MR image analysis and implementation as FSL. Neuroimage 23(Suppl 1):S208–219PubMedCrossRefPubMedCentralGoogle Scholar
- Solis-Vivanco R, Mondragon-Maya A, Leon-Ortiz P, Rodriguez-Agudelo Y, Cadenhead KS, de la Fuente-Sandoval C (2014) Mismatch Negativity reduction in the left cortical regions in first-episode psychosis and in individuals at ultra high-risk for psychosis. Schizophr Res 158:58–63PubMedCrossRefPubMedCentralGoogle Scholar
- Whitford TJ, Lee SW, Oh JS, de Luis-Garcia R, Savadjiev P, Alvarado JL, Westin CF, Niznikiewicz M, Nestor PG, McCarley RW, Kubicki M, Shenton ME (2014) Localized abnormalities in the cingulum bundle in patients with schizophrenia: a diffusion tensor tractography study. NeuroImage Clin 5:93–99PubMedPubMedCentralCrossRefGoogle Scholar
- Wigand M, Kubicki M, Clemm von Hohenberg C, Leicht G, Karch S, Eckbo R, Pelavin PE, Hawley K, Rujescu D, Bouix S, Shenton ME, Mulert C (2015) Auditory verbal hallucinations and the interhemispheric auditory pathway in chronic schizophrenia. World J Biol Psychiatry 16:31–44PubMedCrossRefPubMedCentralGoogle Scholar