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Aberrant connectivity of areas for decoding degraded speech in patients with auditory verbal hallucinations.

ABSTRACT: Auditory verbal hallucinations (AVH) are a hallmark of psychotic experience. Various mechanisms including misattribution of inner speech and imbalance between bottom-up and top-down factors in auditory perception potentially due to aberrant connectivity between frontal and temporo-parietal areas have been suggested to underlie AVH. Experimental evidence for disturbed connectivity of networks sustaining auditory-verbal processing is, however, sparse. We compared functional resting-state connectivity in 49 psychotic patients with frequent AVH and 49 matched controls. The analysis was seeded from the left middle temporal gyrus (MTG), thalamus, angular gyrus (AG) and inferior frontal gyrus (IFG) as these regions are implicated in extracting meaning from impoverished speech-like sounds. Aberrant connectivity was found for all seeds. Decreased connectivity was observed between the left MTG and its right homotope, between the left AG and the surrounding inferior parietal cortex (IPC) and the left inferior temporal gyrus, between the left thalamus and the right cerebellum, as well as between the left IFG and left IPC, and dorsolateral and ventrolateral prefrontal cortex (DLPFC/VLPFC). Increased connectivity was observed between the left IFG and the supplementary motor area (SMA) and the left insula and between the left thalamus and the left fusiform gyrus/hippocampus. The predisposition to experience AVH might result from decoupling between the speech production system (IFG, insula and SMA) and the self-monitoring system (DLPFC, VLPFC, IPC) leading to misattribution of inner speech. Furthermore, decreased connectivity between nodes involved in speech processing (AG, MTG) and other regions implicated in auditory processing might reflect aberrant top-down influences in AVH.

SUBMITTER: Clos M

PROVIDER: S-EPMC8011946 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Background and objectiveAs a key feature of schizophrenia, auditory verbal hallucination (AVH) is causing concern. Altered dynamic functional connectivity (dFC) patterns involving in auditory related regions were rarely reported in schizophrenia patients with AVH. The goal of this research was to find out the dFC abnormalities of auditory related regions in first-episode, drug-naïve schizophrenia patients with and without AVH using resting state functional magnetic resonance imaging (rs-fMRI).MethodsA total of 107 schizophrenia patients with AVH, 85 schizophrenia patients without AVH (NAVH) underwent rs-fMRI examinations, and 104 healthy controls (HC) were matched. Seed-based dFC of the primary auditory cortex (Heschl's gyrus, HES), auditory association cortex (AAC, including Brodmann's areas 22 and 42), and medial geniculate nucleus (MGN) was conducted to build a whole-brain dFC diagram, then inter group comparison and correlation analysis were performed.ResultsIn comparison to the NAVH and HC groups, the AVH group showed increased dFC from left ACC to the right middle temporal gyrus and right middle occipital gyrus, decreased dFC from left HES to the left superior occipital gyrus, left cuneus gyrus, left precuneus gyrus, decreased dFC from right HES to the posterior cingulate gyrus, and decreased dFC from left MGN to the bilateral calcarine gyrus, bilateral cuneus gyrus, bilateral lingual gyrus. The Auditory Hallucination Rating Scale (AHRS) was significantly positively correlated with the dFC values of cluster 1 (bilateral calcarine gyrus, cuneus gyrus, lingual gyrus, superior occipital gyrus, precuneus gyrus, and posterior cingulate gyrus) using left AAC seed, cluster 2 (right middle temporal gyrus and right middle occipital gyrus) using left AAC seed, cluster 1 (bilateral calcarine gyrus, cuneus gyrus, lingual gyrus, superior occipital gyrus, precuneus gyrus and posterior cingulate gyrus) using right AAC seed and cluster 2 (posterior cingulate gyrus) using right HES seed in the AVH group. In both AVH and NAVH groups, a significantly negative correlation is also found between the dFC values of cluster 2 (posterior cingulate gyrus) using the right HES seed and the PANSS negative sub-scores.ConclusionsThe present findings demonstrate that schizophrenia patients with AVH showed multiple abnormal dFC regions using auditory related cortex and nucleus as seeds, particularly involving the occipital lobe, default mode network (DMN), and middle temporal lobe, implying that the different dFC patterns of auditory related areas could provide a neurological mechanism of AVH in schizophrenia.

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Aberrant connectivity of areas for decoding degraded speech in patients with auditory verbal hallucinations.

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