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. 2024 Feb 15;45(3):e26614.
doi: 10.1002/hbm.26614.

Low-frequency rTMS induces modifications in cortical structural connectivity - functional connectivity coupling in schizophrenia patients with auditory verbal hallucinations

Yuanjun Xie  1   2 , Chenxi Li  1 , Muzhen Guan  3 , Tian Zhang  1 , Chaozong Ma  1 , Zhongheng Wang  4 , Zhujing Ma  1 , Huaning Wang  4 , Peng Fang  1   5
Affiliations

Low-frequency rTMS induces modifications in cortical structural connectivity - functional connectivity coupling in schizophrenia patients with auditory verbal hallucinations

Yuanjun Xie et al. Hum Brain Mapp. .

Abstract

Auditory verbal hallucinations (AVH) are distinctive clinical manifestations of schizophrenia. While low-frequency repetitive transcranial magnetic stimulation (rTMS) has demonstrated potential in mitigating AVH, the precise mechanisms by which it operates remain obscure. This study aimed to investigate alternations in structural connectivity and functional connectivity (SC-FC) coupling among schizophrenia patients with AVH prior to and following treatment with 1 Hz rTMS that specifically targets the left temporoparietal junction. Initially, patients exhibited significantly reduced macroscopic whole brain level SC-FC coupling compared to healthy controls. Notably, SC-FC coupling increased significantly across multiple networks, including the somatomotor, dorsal attention, ventral attention, frontoparietal control, and default mode networks, following rTMS treatment. Significant alternations in SC-FC coupling were noted in critical nodes comprising the somatomotor network and the default mode network, such as the precentral gyrus and the ventromedial prefrontal cortex, respectively. The alternations in SC-FC coupling exhibited a correlation with the amelioration of clinical symptom. The results of our study illuminate the intricate relationship between white matter structures and neuronal activity in patients who are receiving low-frequency rTMS. This advances our understanding of the foundational mechanisms underlying rTMS treatment for AVH.

Keywords: auditory verbal hallucinations; network analysis; repetitive transcranial magnetic stimulation; schizophrenia; structural-functional coupling.

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Conflict of interest statement

The authors declare no conflicts of interest.

Figures

FIGURE 1
FIGURE 1
Illustrates the clinical symptom assessments of scores in patients prior to at baseline and following treatment. AHRS, auditory hallucination rating scale; G, general symptoms of PANSS; N, negative symptoms of PANSS; P, positive symptoms of positive and negative syndrome scale (PANSS). *p < .05, *** p < .001. Standard errors are represented by error bars.
FIGURE 2
FIGURE 2
An overview of whole‐brain the coupling between whole‐brain structural connectivity ‐functional connectivity (SC‐FC) coupling across the various the groups. (a) A comparison between groups of the average SC‐FC coupling across all network nodes between groups. Spatial representation of macroscale SC‐FC coupling spatial representations for in controls (b), patients at baseline (c), and patients at posttreatment (d). Consistently, SC‐FC coupling varied consistently throughout the cortex, with values highest exhibited variation across the cortex—higher in the visual cortices and lowest in the frontoparietal and sensorimotor cortices. The color bar in panels (b) through (D) feature color bars that represent reflects SC‐FC coupling values of for Spearman rank correlation. **p < .05.
FIGURE 3
FIGURE 3
Modular‐level comparisons of structural connectivity‐functional connectivity coupling (SC‐FC) coupling at the modular level. The bar chart depicts the mean modular SC‐FC coupling values across the groups: visual (VIS); somatomotor (SOM); dorsal attention (DAN); ventral attention (VEN); limbic (LIM); frontoparietal control (FPC); default mode network.(DMN). *p < .05.
FIGURE 4
FIGURE 4
Node‐level assessments of structural connectivity‐functional connectivity (SC‐FC) coupling. Comparisons of nodal SC‐FC coupling comparisons spanned all brain regions between patients at baseline and healthy controls (upper panel), as well as between patients post‐treatment and baseline (lower panel). The brain surface template displays nodes that have successfully undergone the false discovery rate (FDR) correction (q < 0.05). For group comparisons, the t‐statistic values are represented by a color scale. CAL, calcarine cortex; IFGtriang, triangular part of the inferior frontal gyrus; IPG, inferior parietal gyrus; MCC, middle cingulate cortex; MOG, middle occipital gyrus; MTG, middle temporal gyrus; PCC, posterior cingulate cortex; PFCventmed, ventromedial prefrontal cortex; PreCG, precentral gyrus; REC, rectus gyrus; ROL, Rolandic operculum; SFG, superior frontal gyrus; STG, superior temporal gyrus.
FIGURE 5
FIGURE 5
The correlations between changes in structural connectivity‐functional connectivity (SC‐FC) coupling changes and ameliorated improved clinical symptoms in patients. PFCventmed, ventromedial prefrontal cortex; PreCG, precentral gyrus. The presented p‐values have not been adjusted for multiple comparisons.
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