Interaction of language, auditory and memory brain networks in auditory verbal hallucinations

Ćurčić‐Blake, Branislava; Ford, Judith M.; Hubl, Daniela; Orlov, Natasza; Sommer, Iris; Waters, Flavie; Allen, Paul; Jardri, Renaud; Woodruff, Peter; David, Olivier; Mulert, Christoph; Woodward, Todd S.; Alemán, André

doi:10.1016/j.pneurobio.2016.11.002

Cited by 181 publications

(169 citation statements)

References 196 publications

(296 reference statements)

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“…Moreover, previous data highlight that these distributed neuronal interactions are dynamically configured on the base of anatomical pathways 7–9 . Alterations of both, the connectome and gamma rhythmic activity, are suggested by the interhemispheric miscommunication theory 10 to constitute a pathophysiological mechanism underlying altered perception as it is observed, for instance, in schizophrenia patients 11 with auditory verbal hallucinations (AVH) 12–15 .…”

Section: Introductionmentioning

confidence: 99%

The role of functional and structural interhemispheric auditory connectivity for language lateralization - A combined EEG and DTI study

Steinmann

Amselberg

Cheng

et al. 2018

Sci Rep

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Interhemispheric connectivity between auditory areas is highly relevant for normal auditory perception and alterations are a major factor for the development of auditory verbal hallucinations. Surprisingly, there is no combined EEG-DTI study directly addressing the role of functional and structural connectivity in the same group of subjects. Accordingly, nothing is known about the relationship between functional connectivity such as gamma-band synchrony, structural integrity of the interhemispheric auditory pathways (IAPs) and language lateralization as well as whether the gamma-band synchrony is configured on the backbone of IAPs. By applying multimodal imaging of 64-channel EEG and DTI tractography, we investigated in 27 healthy volunteers the functional gamma-band synchrony between either bilateral primary or secondary auditory cortices from eLORETA source-estimation during dichotic listening, as well as the correspondent IAPs from which fractional anisotropy (FA) values were extracted. Correlation and regression analyses revealed highest values for gamma-band synchrony, followed by FA for secondary auditory cortices, which were both significantly related to a reduced language lateralization. There was no such association between the white-matter microstructure and gamma-band synchrony, suggesting that structural connectivity might also be relevant for other (minor) aspects of information transfer in addition to gamma-band synchrony, which are not detected in the present coupling analyses. The combination of multimodal EEG-DTI imaging provides converging evidence of neural correlates by showing that both stronger pathways and increased gamma-band synchrony within one cohort of subjects are related to a reduced leftward-lateralization for language.

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Section: Introductionmentioning

confidence: 99%

The role of functional and structural interhemispheric auditory connectivity for language lateralization - A combined EEG and DTI study

Steinmann

Amselberg

Cheng

et al. 2018

Sci Rep

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“…However, our choice to restrict analyses to the part of the matrix containing cortex stays justified in the context of target definition for neuromodulation tools. Again, the consideration that hallucinations may result from neural dysconnectivity (e.g., Ćurčić‐Blake et al, ) favors ICA over more conventional activation‐based approaches, such as GLM. Here, the ICA decomposition of time‐series provides a direct equivalent of functional connectivity components, which is more in line with the process we want to capture.…”

Section: Discussionmentioning

confidence: 99%

fMRI capture of auditory hallucinations: Validation of the two‐steps method

Leroy

Foucher

Pins

et al. 2017

Human Brain Mapping

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Our purpose was to validate a reliable method to capture brain activity concomitant with hallucinatory events, which constitute frequent and disabling experiences in schizophrenia. Capturing hallucinations using functional magnetic resonance imaging (fMRI) remains very challenging. We previously developed a method based on a two-steps strategy including (1) multivariate data-driven analysis of per-hallucinatory fMRI recording and (2) selection of the components of interest based on a post-fMRI interview. However, two tests still need to be conducted to rule out critical pitfalls of conventional fMRI capture methods before this two-steps strategy can be adopted in hallucination research: replication of these findings on an independent sample and assessment of the reliability of the hallucination-related patterns at the subject level. To do so, we recruited a sample of 45 schizophrenia patients suffering from frequent hallucinations, 20 schizophrenia patients without hallucinations and 20 matched healthy volunteers; all participants underwent four different experiments. The main findings are (1) high accuracy in reporting unexpected sensory stimuli in an MRI setting; (2) good detection concordance between hypothesis-driven and data-driven analysis methods (as used in the two-steps strategy) when controlled unexpected sensory stimuli are presented; (3) good agreement of the two-steps method with the online button-press approach to capture hallucinatory events; (4) high spatial consistency of hallucinatory-related networks detected using the two-steps method on two independent samples. By validating the two-steps method, we advance toward the possible transfer of such technology to new image-based therapies for hallucinations. Hum Brain Mapp 38:4966-4979, 2017. © 2017 Wiley Periodicals, Inc.

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“…Component 1 was characterized by activations in bilateral temporal pole (Brodmann Area (BA) 38), superior temporal gyrus (STG; BA 22), supplementary motor area (SMA; BA 6)/dorsal anterior cingulate cortex (dACC; BA 24), visual cortex (BA 17), left precentral gyrus (BA 6), bilateral insula, thalamus, and cerebellum. This network included regions described as part of the auditory network described in Ćurčić‐Blake et al ()'s review on AVHs in schizophrenia, and regions comprising the somatosensory network from Yeo et al () resting‐state fMRI parcellation analysis, and was labelled the Auditory‐Motor Network . Component 2 was characterized by activations in left posterior middle temporal gyrus (BA 21), inferior frontal gyrus (IFG; BAs 44, 45), orbitofrontal cortex (BA 47), dorsolateral prefrontal cortex (BA 46), and bilateral visual cortex (BAs 17, 18, 19).…”

Section: Resultsmentioning

confidence: 99%

“…Studies examining functional brain activity during the experience of hallucinations have reported activation of language and auditory regions (e.g., Broca's area, middle/superior temporal gyri; Allen et al, ; Jardri, Pouchet, Pins, & Thomas, ), findings which are supported by network‐based connectivity analyses (Hoffman, Pittman, Constable, Bhagwagar, & Hampson, ; Thoma et al, ). Trait studies, in which functional brain activity is compared between patients with and without a history of AVHs, have also demonstrated hypercoupling/coordinated hyperactivity within auditory/language networks in AVH patients at rest (Alderson‐Day et al, ; Shinn, Baker, Cohen, & Öngür, ); however, findings of task‐based trait studies are less consistent (Ćurčić‐Blake et al, ), with some reporting hypoactivity (Kompus, Westerhausen, & Hugdahl, ), suggesting interference between AVHs and external auditory processing (Hugdahl, ), and others reporting hyperactivity in similar regions (Hoffman, Fernandez, Pittman, & Hampson, ; Lavigne et al, ). These equivocal findings are likely due to differences in the tasks and statistical analysis techniques employed.…”

Section: Introductionmentioning

confidence: 99%

Hallucination‐ and speech‐specific hypercoupling in frontotemporal auditory and language networks in schizophrenia using combined task‐based fMRI data: An fBIRN study

Lavigne

Woodward

2017

Human Brain Mapping

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Hypercoupling of activity in speech-perception-specific brain networks has been proposed to play a role in the generation of auditory-verbal hallucinations (AVHs) in schizophrenia; however, it is unclear whether this hypercoupling extends to nonverbal auditory perception. We investigated this by comparing schizophrenia patients with and without AVHs, and healthy controls, on task-based functional magnetic resonance imaging (fMRI) data combining verbal speech perception (SP), inner verbal thought generation (VTG), and nonverbal auditory oddball detection (AO). Data from two previously published fMRI studies were simultaneously analyzed using group constrained principal component analysis for fMRI (group fMRI-CPCA), which allowed for comparison of task-related functional brain networks across groups and tasks while holding the brain networks under study constant, leading to determination of the degree to which networks are common to verbal and nonverbal perception conditions, and which show coordinated hyperactivity in hallucinations. Three functional brain networks emerged: (a) auditory-motor, (b) language processing, and (c) default-mode (DMN) networks. Combining the AO and sentence tasks allowed the auditory-motor and language networks to separately emerge, whereas they were aggregated when individual tasks were analyzed. AVH patients showed greater coordinated activity (deactivity for DMN regions) than non-AVH patients during SP in all networks, but this did not extend to VTG or AO. This suggests that the hypercoupling in AVH patients in speech-perception-related brain networks is specific to perceived speech, and does not extend to perceived nonspeech or inner verbal thought generation.

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Interaction of language, auditory and memory brain networks in auditory verbal hallucinations

Cited by 181 publications

References 196 publications

The role of functional and structural interhemispheric auditory connectivity for language lateralization - A combined EEG and DTI study

The role of functional and structural interhemispheric auditory connectivity for language lateralization - A combined EEG and DTI study

fMRI capture of auditory hallucinations: Validation of the two‐steps method

Hallucination‐ and speech‐specific hypercoupling in frontotemporal auditory and language networks in schizophrenia using combined task‐based fMRI data: An fBIRN study

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