Auditory hallucinations across the psychosis spectrum: Evidence of dysconnectivity involving cerebellar and temporal lobe regions

Melissa Hwang, Youkyung S Roh, Jessica Talero, Bruce M Cohen, Justin T Baker, Roscoe O Brady, Dost Öngür, Ann K Shinn, Melissa Hwang, Youkyung S Roh, Jessica Talero, Bruce M Cohen, Justin T Baker, Roscoe O Brady, Dost Öngür, Ann K Shinn

Abstract

Background: Auditory hallucinations (AH) are typically associated with schizophrenia (SZ), but they are also prevalent in bipolar disorder (BD). Despite the large body of research on the neural correlates of AH in SZ, the pathophysiology underlying AH remains unclear. Few studies have examined the neural substrates associated with propensity for AH in BD. Investigating AH across the psychosis spectrum has the potential to inform about the neural signature associated with the trait of AH, irrespective of psychiatric diagnosis.

Methods: We compared resting state functional magnetic resonance imaging data in psychosis patients with (n = 90 AH; 68 SZ, 22 BD) and without (n = 55 NAH; 16 SZ, 39 BD) lifetime AH. We performed region of interest (ROI)-to-ROI functional connectivity (FC) analysis using 91 cortical, 15 subcortical, and 26 cerebellar atlas-defined regions. The primary aim was to identify FC differences between patients with and without lifetime AH. We secondarily examined differences between AH and NAH within each diagnosis.

Results: Compared to the NAH group, patients with AH showed higher FC between cerebellum and frontal (left precentral gyrus), temporal [right middle temporal gyrus (MTG), left inferior temporal gyrus (ITG), left temporal fusiform gyrus)], parietal (bilateral superior parietal lobules), and subcortical (left accumbens, left palldium) brain areas. AH also showed lower FC between temporal lobe regions (between right ITG and right MTG and bilateral superior temporal gyri) relative to NAH.

Conclusions: Our findings suggest that dysconnectivity involving the cerebellum and temporal lobe regions may be common neurofunctional elements associated with AH propensity across the psychosis spectrum. We also found dysconnectivity patterns that were unique to lifetime AH within SZ or bipolar psychosis, suggesting both common and distinct mechanisms underlying AH pathophysiology in these disorders.

Keywords: Auditory hallucinations; Bipolar disorder; Cerebellum; Functional connectivity; Resting state functional magnetic resonance imaging; Schizophrenia.

Conflict of interest statement

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Copyright © 2021. Published by Elsevier Inc.

Figures

Fig. 1
Fig. 1
ROI-to-ROI functional connectivity of patients with (AH) and without lifetime auditory hallucinations (NAH) across the psychosis spectrum. Compared to NAH patients, AH patients showed multiple regions (cerebral cortical and subcortical) that were functional hyperconnected to cerebellar regions, and hypoconnectivity between temporal lobe areas. Results were adjusted for motion, diagnosis, lifetime hallucinations in other modalities, negative symptom severity, mania severity, depression severity, and antipsychotic exposure as measured by chlorpromazine equivalents. The significance threshold was set at p < 0.05, two-sided, false discovery rate (FDR)-corrected for multiple comparisons.
Fig. 2
Fig. 2
Cerebello-cerebral cortical functional connectivity associated with lifetime AH across the psychosis spectrum. Compared to NAH patients, AH patients showed higher functional connectivity between cerebellum and regions in frontal, temporal, and parietal areas. The bar graphs show the Fisher-transformed Pearson’s correlation between example ROI-pairs, with healthy control data presented in dashed lines as a point of reference. The data show patients with AH to have increased connectivity relative to both NAH and also healthy controls.
Fig. 3
Fig. 3
Cerebello-subcortical functional connectivity associated with lifetime AH across the psychosis spectrum. Compared to NAH patients, AH patients showed higher functional connectivity between cerebellum and left nucleus accumbens and left pallidum. The bar graphs show the Fisher-transformed Pearson’s correlation between the two significant ROI-to-ROI findings, with healthy control data presented in dashed lines as a point of reference.
Fig. 4
Fig. 4
Functional connectivity between temporal lobe regions in association with lifetime AH across the psychosis spectrum. Compared to NAH patients, AH patients showed lower functional connectivity between temporal lobe areas within the right hemisphere as well as between hemispheres. The bar graphs show the Fisher-transformed Pearson’s correlation between example ROI-pairs, with healthy control data presented in dashed lines as a point of reference.
Fig. 5
Fig. 5
Functional connectivity of AH vs. NAH within each diagnostic category. (A) Schizophrenia AH vs. schizophrenia NAH. (B) Bipolar psychosis AH vs. bipolar psychosis NAH. (See supplementary materials for Fisher-transformed correlation coefficients.)

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