Changes in motor preparation affect the sensory consequences of voice production in voice hearers.


Journal

Neuropsychologia
ISSN: 1873-3514
Titre abrégé: Neuropsychologia
Pays: England
ID NLM: 0020713

Informations de publication

Date de publication:
09 2020
Historique:
received: 02 01 2020
revised: 11 05 2020
accepted: 08 06 2020
pubmed: 20 6 2020
medline: 25 6 2021
entrez: 20 6 2020
Statut: ppublish

Résumé

Auditory verbal hallucinations (AVH) are a cardinal symptom of psychosis but are also present in 6-13% of the general population. Alterations in sensory feedback processing are a likely cause of AVH, indicative of changes in the forward model. However, it is unknown whether such alterations are related to anomalies in forming an efference copy during action preparation, selective for voices, and similar along the psychosis continuum. By directly comparing psychotic and nonclinical voice hearers (NCVH), the current study specifies whether and how AVH proneness modulates both the efference copy (Readiness Potential) and sensory feedback processing for voices and tones (N1, P2) with event-related brain potentials (ERPs). Controls with low AVH proneness (n = 15), NCVH (n = 16) and first-episode psychotic patients with AVH (n = 16) engaged in a button-press task with two types of stimuli: self-initiated and externally generated self-voices or tones during EEG recordings. Groups differed in sensory feedback processing of expected and actual feedback: NCVH displayed an atypically enhanced N1 to self-initiated voices, while N1 suppression was reduced in psychotic patients. P2 suppression for voices and tones was strongest in NCVH, but absent for voices in patients. Motor activity preceding the button press was reduced in NCVH and patients, specifically for sensory feedback to self-voice in NCVH. These findings suggest that selective changes in sensory feedback to voice are core to AVH. These changes already show in preparatory motor activity, potentially reflecting changes in forming an efference copy. The results provide partial support for continuum models of psychosis.

Sections du résumé

BACKGROUND
Auditory verbal hallucinations (AVH) are a cardinal symptom of psychosis but are also present in 6-13% of the general population. Alterations in sensory feedback processing are a likely cause of AVH, indicative of changes in the forward model. However, it is unknown whether such alterations are related to anomalies in forming an efference copy during action preparation, selective for voices, and similar along the psychosis continuum. By directly comparing psychotic and nonclinical voice hearers (NCVH), the current study specifies whether and how AVH proneness modulates both the efference copy (Readiness Potential) and sensory feedback processing for voices and tones (N1, P2) with event-related brain potentials (ERPs).
METHODS
Controls with low AVH proneness (n = 15), NCVH (n = 16) and first-episode psychotic patients with AVH (n = 16) engaged in a button-press task with two types of stimuli: self-initiated and externally generated self-voices or tones during EEG recordings.
RESULTS
Groups differed in sensory feedback processing of expected and actual feedback: NCVH displayed an atypically enhanced N1 to self-initiated voices, while N1 suppression was reduced in psychotic patients. P2 suppression for voices and tones was strongest in NCVH, but absent for voices in patients. Motor activity preceding the button press was reduced in NCVH and patients, specifically for sensory feedback to self-voice in NCVH.
CONCLUSIONS
These findings suggest that selective changes in sensory feedback to voice are core to AVH. These changes already show in preparatory motor activity, potentially reflecting changes in forming an efference copy. The results provide partial support for continuum models of psychosis.

Identifiants

pubmed: 32553846
pii: S0028-3932(20)30204-9
doi: 10.1016/j.neuropsychologia.2020.107531
pii:
doi:

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

107531

Informations de copyright

Copyright © 2020 Elsevier Ltd. All rights reserved.

Auteurs

Ana P Pinheiro (AP)

Faculdade de Psicologia, Universidade de Lisboa, Lisboa, Portugal. Electronic address: appinheiro@psicologia.ulisboa.

Michael Schwartze (M)

Faculty of Psychology and Neuroscience, Maastricht University, Maastricht, The Netherlands.

Maria Amorim (M)

Faculdade de Psicologia, Universidade de Lisboa, Lisboa, Portugal.

Ricardo Coentre (R)

Serviço de Psiquiatria e Saúde Mental, Centro Hospitalar Universitário Lisboa Norte EPE, Lisboa, Portugal; Faculdade de Medicina, Universidade de Lisboa, Lisboa, Portugal.

Pedro Levy (P)

Serviço de Psiquiatria e Saúde Mental, Centro Hospitalar Universitário Lisboa Norte EPE, Lisboa, Portugal.

Sonja A Kotz (SA)

Faculty of Psychology and Neuroscience, Maastricht University, Maastricht, The Netherlands.

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