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fMRI fluctuations within the language network are correlated with severity of hallucinatory symptoms in schizophrenia

Although schizophrenia (SZ) represents a complex multiform psychiatric disorder, one of its most striking symptoms are auditory verbal hallucinations (AVH). While the neurophysiological origin of this pervasive symptom has been extensively studied, there is so far no consensus conclusion on the neur...

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Autores principales: Spironelli, Chiara, Marino, Marco, Mantini, Dante, Montalti, Riccardo, Craven, Alexander R., Ersland, Lars, Angrilli, Alessandro, Hugdahl, Kenneth
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10616281/
https://www.ncbi.nlm.nih.gov/pubmed/37903802
http://dx.doi.org/10.1038/s41537-023-00401-9
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author Spironelli, Chiara
Marino, Marco
Mantini, Dante
Montalti, Riccardo
Craven, Alexander R.
Ersland, Lars
Angrilli, Alessandro
Hugdahl, Kenneth
author_facet Spironelli, Chiara
Marino, Marco
Mantini, Dante
Montalti, Riccardo
Craven, Alexander R.
Ersland, Lars
Angrilli, Alessandro
Hugdahl, Kenneth
author_sort Spironelli, Chiara
collection PubMed
description Although schizophrenia (SZ) represents a complex multiform psychiatric disorder, one of its most striking symptoms are auditory verbal hallucinations (AVH). While the neurophysiological origin of this pervasive symptom has been extensively studied, there is so far no consensus conclusion on the neural correlates of the vulnerability to hallucinate. With a network-based fMRI approach, following the hypothesis of altered hemispheric dominance (Crow, 1997), we expected that LN alterations might result in self-other distinction impairments in SZ patients, and lead to the distressing subjective experiences of hearing voices. We used the independent component analysis of resting-state fMRI data, to first analyze LN connectivity in three groups of participants: SZ patients with and without hallucinations (AVH/D+ and AVH/D–, respectively), and a matched healthy control (HC) group. Then, we assessed the fMRI fluctuations using additional analyses based on fractional Amplitude of Low Frequency-Fluctuations (fALFF), both at the network- and region of interest (ROI)-level. Specific LN nodes were recruited in the right hemisphere (insula and Broca homologous area) for AVH/D+ , but not for HC and AVH/D–, consistent with a left hemisphere deficit in AVH patients. The fALFF analysis at the ROI level showed a negative correlation between fALFF Slow-4 and P1 Delusions PANSS subscale and a positive correlation between the fALFF Slow-5 and P3 Hallucination PANSS subscale for AVH/D+ only. These effects were not a consequence of structural differences between groups, as morphometric analysis did not evidence any group differences. Given the role of language as an emerging property resulting from the integration of many high-level cognitive processes and the underlying cortical areas, our results suggest that LN features from fMRI connectivity and fluctuations can be a marker of neurophysiological features characterizing SZ patients depending on their vulnerability to hallucinate.
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spelling pubmed-106162812023-11-01 fMRI fluctuations within the language network are correlated with severity of hallucinatory symptoms in schizophrenia Spironelli, Chiara Marino, Marco Mantini, Dante Montalti, Riccardo Craven, Alexander R. Ersland, Lars Angrilli, Alessandro Hugdahl, Kenneth Schizophrenia (Heidelb) Article Although schizophrenia (SZ) represents a complex multiform psychiatric disorder, one of its most striking symptoms are auditory verbal hallucinations (AVH). While the neurophysiological origin of this pervasive symptom has been extensively studied, there is so far no consensus conclusion on the neural correlates of the vulnerability to hallucinate. With a network-based fMRI approach, following the hypothesis of altered hemispheric dominance (Crow, 1997), we expected that LN alterations might result in self-other distinction impairments in SZ patients, and lead to the distressing subjective experiences of hearing voices. We used the independent component analysis of resting-state fMRI data, to first analyze LN connectivity in three groups of participants: SZ patients with and without hallucinations (AVH/D+ and AVH/D–, respectively), and a matched healthy control (HC) group. Then, we assessed the fMRI fluctuations using additional analyses based on fractional Amplitude of Low Frequency-Fluctuations (fALFF), both at the network- and region of interest (ROI)-level. Specific LN nodes were recruited in the right hemisphere (insula and Broca homologous area) for AVH/D+ , but not for HC and AVH/D–, consistent with a left hemisphere deficit in AVH patients. The fALFF analysis at the ROI level showed a negative correlation between fALFF Slow-4 and P1 Delusions PANSS subscale and a positive correlation between the fALFF Slow-5 and P3 Hallucination PANSS subscale for AVH/D+ only. These effects were not a consequence of structural differences between groups, as morphometric analysis did not evidence any group differences. Given the role of language as an emerging property resulting from the integration of many high-level cognitive processes and the underlying cortical areas, our results suggest that LN features from fMRI connectivity and fluctuations can be a marker of neurophysiological features characterizing SZ patients depending on their vulnerability to hallucinate. Nature Publishing Group UK 2023-10-30 /pmc/articles/PMC10616281/ /pubmed/37903802 http://dx.doi.org/10.1038/s41537-023-00401-9 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/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/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Spironelli, Chiara
Marino, Marco
Mantini, Dante
Montalti, Riccardo
Craven, Alexander R.
Ersland, Lars
Angrilli, Alessandro
Hugdahl, Kenneth
fMRI fluctuations within the language network are correlated with severity of hallucinatory symptoms in schizophrenia
title fMRI fluctuations within the language network are correlated with severity of hallucinatory symptoms in schizophrenia
title_full fMRI fluctuations within the language network are correlated with severity of hallucinatory symptoms in schizophrenia
title_fullStr fMRI fluctuations within the language network are correlated with severity of hallucinatory symptoms in schizophrenia
title_full_unstemmed fMRI fluctuations within the language network are correlated with severity of hallucinatory symptoms in schizophrenia
title_short fMRI fluctuations within the language network are correlated with severity of hallucinatory symptoms in schizophrenia
title_sort fmri fluctuations within the language network are correlated with severity of hallucinatory symptoms in schizophrenia
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10616281/
https://www.ncbi.nlm.nih.gov/pubmed/37903802
http://dx.doi.org/10.1038/s41537-023-00401-9
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