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      Voice-selective prediction alterations in nonclinical voice hearers

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      Scientific Reports
      Nature Publishing Group UK

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          Abstract

          Auditory verbal hallucinations (AVH) are a cardinal symptom of psychosis but also occur in 6–13% of the general population. Voice perception is thought to engage an internal forward model that generates predictions, preparing the auditory cortex for upcoming sensory feedback. Impaired processing of sensory feedback in vocalization seems to underlie the experience of AVH in psychosis, but whether this is the case in nonclinical voice hearers remains unclear. The current study used electroencephalography (EEG) to investigate whether and how hallucination predisposition (HP) modulates the internal forward model in response to self-initiated tones and self-voices. Participants varying in HP (based on the Launay-Slade Hallucination Scale) listened to self-generated and externally generated tones or self-voices. HP did not affect responses to self vs. externally generated tones. However, HP altered the processing of the self-generated voice: increased HP was associated with increased pre-stimulus alpha power and increased N1 response to the self-generated voice. HP did not affect the P2 response to voices. These findings confirm that both prediction and comparison of predicted and perceived feedback to a self-generated voice are altered in individuals with AVH predisposition. Specific alterations in the processing of self-generated vocalizations may establish a core feature of the psychosis continuum.

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          The N1 wave of the human electric and magnetic response to sound: a review and an analysis of the component structure.

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            Speaking modifies voice-evoked activity in the human auditory cortex.

            The voice we most often hear is our own, and proper interaction between speaking and hearing is essential for both acquisition and performance of spoken language. Disturbed audiovocal interactions have been implicated in aphasia, stuttering, and schizophrenic voice hallucinations, but paradigms for a noninvasive assessment of auditory self-monitoring of speaking and its possible dysfunctions are rare. Using magnetoencephalograpy we show here that self-uttered syllables transiently activate the speaker's auditory cortex around 100 ms after voice onset. These phasic responses were delayed by 11 ms in the speech-dominant left hemisphere relative to the right, whereas during listening to a replay of the same utterances the response latencies were symmetric. Moreover, the auditory cortices did not react to rare vowel changes interspersed randomly within a series of repetitively spoken vowels, in contrast to regular change-related responses evoked 100-200 ms after replayed rare vowels. Thus, speaking primes the human auditory cortex at a millisecond time scale, dampening and delaying reactions to self-produced "expected" sounds, more prominently in the speech-dominant hemisphere. Such motor-to-sensory priming of early auditory cortex responses during voicing constitutes one element of speech self-monitoring that could be compromised in central speech disorders.
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              Corollary discharge dysfunction in schizophrenia: can it explain auditory hallucinations?

              Failure of corollary discharge, a mechanism for distinguishing self-generated from externally generated percepts, has been posited to underlie certain positive symptoms of schizophrenia, including auditory hallucinations. Although originally described in the visual system, corollary discharge may exist in the auditory system, whereby signals from motor speech commands prepare auditory cortex for self-generated speech. While associated with sensorimotor systems, it might also apply to inner speech or thought, regarded as our most complex motor act. In this paper, we describe the results of a series of studies in which we have shown that: (1) event-related brain potentials (ERPs) can be used to demonstrate the corollary discharge phenomenon during talking, (2) corollary discharge is abnormal in patients with schizophrenia, (3) EEG gamma band coherence between frontal and temporal lobes is greater during talking than listening and is disrupted by distorted feedback during talking in normals, and (4) patients with schizophrenia do not show this pattern for EEG gamma coherence. While these studies have identified ERPs and EEG gamma coherence indices of the efference copy/corollary discharge system and documented abnormalities in these systems in patients with schizophrenia, we have so far had limited success in establishing a relationship between these neurobiologic indicators of corollary discharge abnormality and reports of hallucinations in patients.
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                Author and article information

                Contributors
                appinheiro@psicologia.ulisboa.pt
                Journal
                Sci Rep
                Sci Rep
                Scientific Reports
                Nature Publishing Group UK (London )
                2045-2322
                3 October 2018
                3 October 2018
                2018
                : 8
                : 14717
                Affiliations
                [1 ]ISNI 0000 0001 2181 4263, GRID grid.9983.b, Faculdade de Psicologia, , Universidade de Lisboa, ; Lisboa, Portugal
                [2 ]ISNI 0000 0001 2159 175X, GRID grid.10328.38, Neuropsychophysiology Lab, School of Psychology, , University of Minho, ; Braga, Portugal
                [3 ]ISNI 0000 0001 0481 6099, GRID grid.5012.6, Faculty of Psychology and Neuroscience, , Maastricht University, ; Maastricht, The Netherlands
                [4 ]ISNI 0000 0001 0041 5028, GRID grid.419524.f, Department of Neuropsychology, , Max-Planck-Institute for Human Cognitive and Brain Sciences, ; Leipzig, Germany
                Author information
                http://orcid.org/0000-0002-7981-3682
                Article
                32614
                10.1038/s41598-018-32614-9
                6170384
                30283058
                4110487a-0cdd-49a9-9fdd-4d3f1299b3f2
                © The Author(s) 2018

                Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.

                History
                : 13 April 2018
                : 3 September 2018
                Funding
                Funded by: Fundação para a Ciência e a Tecnologia - Portuguese Science National Foundation (FCT): PTDC/PSI-PCL/116626/2010, IF/00334/2012, PTDC/MHC-PCN/0101/2014
                Funded by: Fundação para a Ciência e a Tecnologia - Portuguese Science National Foundation (FCT): PTDC/MHC-PCN/0101/2014
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