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Auditory prediction errors and auditory white matter microstructure associated with psychotic-like experiences in healthy individuals

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Abstract

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.

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Acknowledgements

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.

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  1. UQ Centre for Clinical Research, The University of Queensland, Brisbane, Australia

    L. K. L. Oestreich

  2. Centre for Advanced Imaging, The University of Queensland, Brisbane, Australia

    L. K. L. Oestreich & M. I. Garrido

  3. Royal Brisbane and Women’s Hospital, Brisbane, Australia

    L. K. L. Oestreich

  4. Queensland Brain Institute, The University of Queensland, Brisbane, Australia

    R. Randeniya & M. I. Garrido

  5. Melbourne School of Psychological Sciences, The University of Melbourne, Melbourne, Australia

    M. I. Garrido

  6. ARC Centre for Integrative Brain Function, Clayton, Australia

    R. Randeniya & M. I. Garrido

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Oestreich, L.K.L., Randeniya, R. & Garrido, M.I. Auditory prediction errors and auditory white matter microstructure associated with psychotic-like experiences in healthy individuals. Brain Struct Funct 224, 3277–3289 (2019). https://doi.org/10.1007/s00429-019-01972-z

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