Central alterations of brain networks in patients with optic neuritis: a resting state fMRI study

Abstract

Aim: To assess the alterations in the resting-state function connections between the two cerebral hemispheres in patients with optic neuritis (ON) and healthy controls (HCs).

Methods: A total of 12 ON patients (six males and six females) and 12 HCs (six males and six females) who were highly matched for sex, age, and educational level were recruited. They underwent functional magnetic resonance imaging (fMRI), testing and brain activities were assessed using the degree centrality (DC) method. Correlation analysis between the mean DC values in specific brain areas and behavior performances was analyzed as well. Linear correlations between A anxiety scale (AS) and depression scale (DS) values and DC values in brain regions of patients with ON were also analyzed.

Results: The areas that showed a higher DC value in ON patients were the right angular gyrus and bilateral precuneus, while the left insula and left superior temporal gyrus (LSTG) were regions that presented a lower DC value in ON patients. A receiver operating characteristic (ROC) curve analysis confirmed the accuracy of the area under the curve (AUC) assessment. Linear analysis showed anxiety scale (AS) and depression scale (DS) values in the left insula were both negatively correlated with DC values, while best corrected visual acuity logMAR-R (BCVA logMAR-R) showed a negative correlation with DC in the LSTG.

Conclusion: The study explores altered brain activities of specific regions in patients with ON. The results provide clues for revealing the underlying mechanism of ON development.

Keywords: functional magnetic resonance imaging; optic neuritis; resting state.

Figure 1. Inclusion procedure

ON: Optic neuritis; HC: Healthy control.

Figure 2. Typical fundus photographs of optic neuritis patients.

Figure 3. The average DC values of the 4 specific brain regions in ON and HC groups

ON: Optic neuritis; HC: Healthy control; DC: Degree centrality; L: Left; R: Right; B: Bilateral.

Figure 4. Comparison of voxels between ON and HC groups

A: Changes of the mean value of horizontal DC in ON patients. In ON group, the DC values of the RAG and BP were significantly increased compared to HC group, while which of the LSTG and LI were decreased. Yellow areas indicated higher DC values (double tailed, voxel level: P<0.001, GRF correction, clustering level: P<0.05), and blue areas represented lower DC values. B: Three-dimensional shape of the brain. ON: Optic neuritis; HC: Healthy control; LSTG: Left superior temporal gyrus; LI: Left insula; BP: Bilateral precuneus; RAG: Right angular gyrus; DC: Degree centrality; GRF: Gaussian random field.

Figure 5. ROC curve analysis of the mean DC values for altered brain regions

A: AUC was 0.924 for RAG (P<0.001; 95%CI: 0.820-1.000), and 0.924 for BP (P<0.001; 95%CI: 0.808-1.000). B: AUC was 1 for LSTG (P<0.001; 95%CI: 1.000-1.000), and 0.979 for LI (P<0.001; 95%CI: 0.931-1.000). ROC: Receiver operating characteristic; DC: Degree centrality; CI: Confidence interval; AUC: Area under the curve; LSTG: Left superior temporal gyrus; LI: Left insula; BP: Bilateral precuneus; RAG: Right angular gyrus.

Figure 6. Correlation analysis between AS, DS, BCVA logMAR-R and DC values in specific brain areas

A: Negative correlation between BCVA logMAR-R and DC values in superior temporal gyrus-L; B: Negative correlation between AS and DC values in insula-L; C: Negative correlation between DS and DC values in insula-L. AS: Anxiety scale; DS: Depression scale; L: Left; BCVA: Best-corrected visual acuity.

Figure 7. DC results of ON patients' electroencephalogram activity

Compared to HCs, DC values of the following regions were significantly changed: 1) LSTG (BA 42, t-5.9006); 2) LI (t-6.7714); 3) BP (t-4.6888); 4) RAG (BA 40, t-5.326). The size of the spot indicated the degree of change in the DC results. ON: Optic neuritis; HC: Healthy control; LSTG: Left superior temporal gyrus; LI: Left insula; BP: Bilateral precuneus; RAG: Right angular gyrus; DC: Degree centrality; BA: Brodmann area.

Figure 8. The relationship between optic neuritis and fMRI

ON can lead to DC value changes in various brain areas, which can result in visual impairment and symptoms of depression and anxiety. At the same time, visual impairment and emotional disorders can interact with each other. ON: Optic neuritis; DC: Degree centrality; fMRI: Functional magnetic resonance imaging.