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. 2023 Jun;24(5):387-399.
doi: 10.1080/15622975.2022.2112974. Epub 2022 Sep 9.

The decoupling of structural and functional connectivity of auditory networks in individuals at clinical high-risk for psychosis

Mina Langhein  1   2 , Amanda E Lyall  2   3 , Saskia Steinmann  1   2 , Johanna Seitz-Holland  2 , Felix L Nägele  1   2 , Suheyla Cetin-Karayumak  2 , Fan Zhang  4 , Jonas Rauh  1 , Marius Mußmann  1 , Tashrif Billah  2 , Nikos Makris  2   3 , Ofer Pasternak  2   4 , Lauren J O'Donnell  4 , Yogesh Rathi  2   4 , Gregor Leicht  1 , Marek Kubicki  2   3 , Martha E Shenton  2   3   4 , Christoph Mulert  1   5
Affiliations

The decoupling of structural and functional connectivity of auditory networks in individuals at clinical high-risk for psychosis

Mina Langhein et al. World J Biol Psychiatry. 2023 Jun.

Abstract

Objectives: Disrupted auditory networks play an important role in the pathophysiology of psychosis, with abnormalities already observed in individuals at clinical high-risk for psychosis (CHR). Here, we examine structural and functional connectivity of an auditory network in CHR utilising state-of-the-art electroencephalography and diffusion imaging techniques.

Methods: Twenty-six CHR subjects and 13 healthy controls (HC) underwent diffusion MRI and electroencephalography while performing an auditory task. We investigated structural connectivity, measured as fractional anisotropy in the Arcuate Fasciculus (AF), Cingulum Bundle, and Superior Longitudinal Fasciculus-II. Gamma-band lagged-phase synchronisation, a functional connectivity measure, was calculated between cortical regions connected by these tracts.

Results: CHR subjects showed significantly higher structural connectivity in the right AF than HC (p < .001). Although non-significant, functional connectivity between cortical areas connected by the AF was lower in CHR than HC (p = .078). Structural and functional connectivity were correlated in HC (p = .056) but not in CHR (p = .29).

Conclusions: We observe significant differences in structural connectivity of the AF, without a concomitant significant change in functional connectivity in CHR subjects. This may suggest that the CHR state is characterised by a decoupling of structural and functional connectivity, possibly due to abnormal white matter maturation.

Keywords: EEG; MRI; biological psychiatry; imaging; schizophrenia.

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Conflict of interest statement

Declaration of Interest

The authors have declared that there are no conflicts of interest in relation to the subject of this study.

Figures

Figure 1.
Figure 1.
Study Protocol. CHR: Clinical High-Risk; -NP: Non-Psychosis; -P: Psychosis; dACC: dorsal Anterior Cingulate Cortex; DLPFC: Dorsolateral Prefrontal Cortex; HC: Healthy Controls; PAC: Primary Auditory Cortex. DLPFC, PAC and dACC generate the auditory-evoked gamma-band response.
Figure 2.
Figure 2.
Clustering results of the (a) AF, (b) CB and (c) SLF-II of a CHR subject. White matter fiber clustering was used to extract tracts for each subject. AF: Arcuate Fasciculus; CB: Cingulum Bundle; CHR: Clinical High-Risk; SLF-II: Superior Longitudinal Fasciculus II.
Figure 3.
Figure 3.
FA and LPS compared between CHR subjects and HC CHR subjects exhibited significantly increased FA in the right AF compared to HC (CHR: .64 ± .02; HC: .61 ± .03; F(1, 34) = 12.41; p < .001, η2 = .31). The LPS between right PAC and DLPFC, which are connected by the AF, was decreased in CHR subjects compared to HC (CHR: .69 ± .14; HC: .77 ± .12; F(1, 37) = 3.3; p = .078, η2 = .08). AF: Arcuate Fasciculus; CHR: Clinical High-Risk; DLPFC: Dorsolateral Prefrontal Cortex; FA: free-water corrected Fractional Anisotropy; HC: Healthy Controls; LPS: Lagged Phase Synchronization; PAC: Primary Auditory Cortex.
Figure 4.
Figure 4.
Correlation of functional and structural connectivity measures In HC, the FA of the right AF was positively correlated with the LPS between the respective regions, right PAC and DLPFC. This correlation was absent in CHR individuals. AF: Arcuate Fasciculus; CHR: Clinical High-Risk; DLPFC: Dorsolateral Prefrontal Cortex; FA: free-water corrected Fractional Anisotropy; HC: Healthy Controls; LPS: Lagged Phase Synchronization; PAC: Primary Auditory Cortex.
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