Cargando…

The effect of multisensory semantic congruency on unisensory object recognition in schizophrenia

Multisensory, as opposed to unisensory processing of stimuli, has been found to enhance the performance (e.g., reaction time, accuracy, and discrimination) of healthy individuals across various tasks. However, this enhancement is not as pronounced in patients with schizophrenia (SZ), indicating impa...

Descripción completa

Detalles Bibliográficos
Autores principales: Ghaneirad, Erfan, Borgolte, Anna, Sinke, Christopher, Čuš, Anja, Bleich, Stefan, Szycik, Gregor R.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10646423/
https://www.ncbi.nlm.nih.gov/pubmed/38025441
http://dx.doi.org/10.3389/fpsyt.2023.1246879
_version_ 1785134892183453696
author Ghaneirad, Erfan
Borgolte, Anna
Sinke, Christopher
Čuš, Anja
Bleich, Stefan
Szycik, Gregor R.
author_facet Ghaneirad, Erfan
Borgolte, Anna
Sinke, Christopher
Čuš, Anja
Bleich, Stefan
Szycik, Gregor R.
author_sort Ghaneirad, Erfan
collection PubMed
description Multisensory, as opposed to unisensory processing of stimuli, has been found to enhance the performance (e.g., reaction time, accuracy, and discrimination) of healthy individuals across various tasks. However, this enhancement is not as pronounced in patients with schizophrenia (SZ), indicating impaired multisensory integration (MSI) in these individuals. To the best of our knowledge, no study has yet investigated the impact of MSI deficits in the context of working memory, a domain highly reliant on multisensory processing and substantially impaired in schizophrenia. To address this research gap, we employed two adopted versions of the continuous object recognition task to investigate the effect of single-trail multisensory encoding on subsequent object recognition in 21 schizophrenia patients and 21 healthy controls (HC). Participants were tasked with discriminating between initial and repeated presentations. For the initial presentations, half of the stimuli were audiovisual pairings, while the other half were presented unimodal. The task-relevant stimuli were then presented a second time in a unisensory manner (either auditory stimuli in the auditory task or visual stimuli in the visual task). To explore the impact of semantic context on multisensory encoding, half of the audiovisual pairings were selected to be semantically congruent, while the remaining pairs were not semantically related to each other. Consistent with prior studies, our findings demonstrated that the impact of single-trial multisensory presentation during encoding remains discernible during subsequent object recognition. This influence could be distinguished based on the semantic congruity between the auditory and visual stimuli presented during the encoding. This effect was more robust in the auditory task. In the auditory task, when congruent multisensory pairings were encoded, both participant groups demonstrated a multisensory facilitation effect. This effect resulted in improved accuracy and RT performance. Regarding incongruent audiovisual encoding, as expected, HC did not demonstrate an evident multisensory facilitation effect on memory performance. In contrast, SZs exhibited an atypically accelerated reaction time during the subsequent auditory object recognition. Based on the predictive coding model we propose that this observed deviations indicate a reduced semantic modulatory effect and anomalous predictive errors signaling, particularly in the context of conflicting cross-modal sensory inputs in SZ.
format Online
Article
Text
id pubmed-10646423
institution National Center for Biotechnology Information
language English
publishDate 2023
publisher Frontiers Media S.A.
record_format MEDLINE/PubMed
spelling pubmed-106464232023-11-01 The effect of multisensory semantic congruency on unisensory object recognition in schizophrenia Ghaneirad, Erfan Borgolte, Anna Sinke, Christopher Čuš, Anja Bleich, Stefan Szycik, Gregor R. Front Psychiatry Psychiatry Multisensory, as opposed to unisensory processing of stimuli, has been found to enhance the performance (e.g., reaction time, accuracy, and discrimination) of healthy individuals across various tasks. However, this enhancement is not as pronounced in patients with schizophrenia (SZ), indicating impaired multisensory integration (MSI) in these individuals. To the best of our knowledge, no study has yet investigated the impact of MSI deficits in the context of working memory, a domain highly reliant on multisensory processing and substantially impaired in schizophrenia. To address this research gap, we employed two adopted versions of the continuous object recognition task to investigate the effect of single-trail multisensory encoding on subsequent object recognition in 21 schizophrenia patients and 21 healthy controls (HC). Participants were tasked with discriminating between initial and repeated presentations. For the initial presentations, half of the stimuli were audiovisual pairings, while the other half were presented unimodal. The task-relevant stimuli were then presented a second time in a unisensory manner (either auditory stimuli in the auditory task or visual stimuli in the visual task). To explore the impact of semantic context on multisensory encoding, half of the audiovisual pairings were selected to be semantically congruent, while the remaining pairs were not semantically related to each other. Consistent with prior studies, our findings demonstrated that the impact of single-trial multisensory presentation during encoding remains discernible during subsequent object recognition. This influence could be distinguished based on the semantic congruity between the auditory and visual stimuli presented during the encoding. This effect was more robust in the auditory task. In the auditory task, when congruent multisensory pairings were encoded, both participant groups demonstrated a multisensory facilitation effect. This effect resulted in improved accuracy and RT performance. Regarding incongruent audiovisual encoding, as expected, HC did not demonstrate an evident multisensory facilitation effect on memory performance. In contrast, SZs exhibited an atypically accelerated reaction time during the subsequent auditory object recognition. Based on the predictive coding model we propose that this observed deviations indicate a reduced semantic modulatory effect and anomalous predictive errors signaling, particularly in the context of conflicting cross-modal sensory inputs in SZ. Frontiers Media S.A. 2023-11-01 /pmc/articles/PMC10646423/ /pubmed/38025441 http://dx.doi.org/10.3389/fpsyt.2023.1246879 Text en Copyright © 2023 Ghaneirad, Borgolte, Sinke, Čuš, Bleich and Szycik. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Psychiatry
Ghaneirad, Erfan
Borgolte, Anna
Sinke, Christopher
Čuš, Anja
Bleich, Stefan
Szycik, Gregor R.
The effect of multisensory semantic congruency on unisensory object recognition in schizophrenia
title The effect of multisensory semantic congruency on unisensory object recognition in schizophrenia
title_full The effect of multisensory semantic congruency on unisensory object recognition in schizophrenia
title_fullStr The effect of multisensory semantic congruency on unisensory object recognition in schizophrenia
title_full_unstemmed The effect of multisensory semantic congruency on unisensory object recognition in schizophrenia
title_short The effect of multisensory semantic congruency on unisensory object recognition in schizophrenia
title_sort effect of multisensory semantic congruency on unisensory object recognition in schizophrenia
topic Psychiatry
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10646423/
https://www.ncbi.nlm.nih.gov/pubmed/38025441
http://dx.doi.org/10.3389/fpsyt.2023.1246879
work_keys_str_mv AT ghaneiraderfan theeffectofmultisensorysemanticcongruencyonunisensoryobjectrecognitioninschizophrenia
AT borgolteanna theeffectofmultisensorysemanticcongruencyonunisensoryobjectrecognitioninschizophrenia
AT sinkechristopher theeffectofmultisensorysemanticcongruencyonunisensoryobjectrecognitioninschizophrenia
AT cusanja theeffectofmultisensorysemanticcongruencyonunisensoryobjectrecognitioninschizophrenia
AT bleichstefan theeffectofmultisensorysemanticcongruencyonunisensoryobjectrecognitioninschizophrenia
AT szycikgregorr theeffectofmultisensorysemanticcongruencyonunisensoryobjectrecognitioninschizophrenia
AT ghaneiraderfan effectofmultisensorysemanticcongruencyonunisensoryobjectrecognitioninschizophrenia
AT borgolteanna effectofmultisensorysemanticcongruencyonunisensoryobjectrecognitioninschizophrenia
AT sinkechristopher effectofmultisensorysemanticcongruencyonunisensoryobjectrecognitioninschizophrenia
AT cusanja effectofmultisensorysemanticcongruencyonunisensoryobjectrecognitioninschizophrenia
AT bleichstefan effectofmultisensorysemanticcongruencyonunisensoryobjectrecognitioninschizophrenia
AT szycikgregorr effectofmultisensorysemanticcongruencyonunisensoryobjectrecognitioninschizophrenia