Brain Gray Matter Atrophy and Functional Connectivity Remodeling in Patients With Chronic LHON

Qin Tian; Ling Wang; Yu Zhang; Ke Fan; Meng Liang; Dapeng Shi; Wen Qin; Hao Ding

doi:10.3389/fnins.2022.885770

Brain Gray Matter Atrophy and Functional Connectivity Remodeling in Patients With Chronic LHON

Front Neurosci. 2022 May 12:16:885770. doi: 10.3389/fnins.2022.885770. eCollection 2022.

Authors

Qin Tian¹, Ling Wang¹, Yu Zhang^{2

3}, Ke Fan⁴, Meng Liang^{2

3

5}, Dapeng Shi¹, Wen Qin^{2

3}, Hao Ding^{2

3

5}

Affiliations

¹ Department of Medical Imaging, People's Hospital of Zhengzhou University, Henan Provincial People's Hospital, Zhengzhou, China.
² Department of Radiology, Tianjin Medical University, Tianjin, China.
³ Tianjin Key Laboratory of Functional Imaging, Tianjin Medical University General Hospital, Tianjin, China.
⁴ Henan Eye Institute, Henan Eye Hospital, Henan Provincial People's Hospital, Zhengzhou University People's Hospital, Zhengzhou, China.
⁵ School of Medical Imaging, Tianjin Medical University, Tianjin, China.

Abstract

Purpose: The aim of this study was to investigate the brain gray matter volume (GMV) and spontaneous functional connectivity (FC) changes in patients with chronic Leber's hereditary optic neuropathy (LHON), and their relations with clinical measures.

Methods: A total of 32 patients with chronic LHON and matched sighted healthy controls (HC) underwent neuro-ophthalmologic examinations and multimodel magnetic resonance imaging (MRI) scans. Voxel-based morphometry (VBM) was used to detect the GMV differences between the LHON and HC. Furthermore, resting-state FC analysis using the VBM-identified clusters as seeds was carried out to detect potential functional reorganization in the LHON. Finally, the associations between the neuroimaging and clinical measures were performed.

Results: The average peripapillary retinal nerve fiber layer (RNFL) thickness of the chronic LHON was significantly thinner (T = -16.421, p < 0.001), and the mean defect of the visual field was significantly higher (T = 11.28, p < 0.001) than the HC. VBM analysis demonstrated a significantly lower GMV of bilateral calcarine gyri (CGs) in the LHON than in the HC (p < 0.05). Moreover, in comparison with the HC, the LHON had significantly lower FC between the centroid of the identified left CG and ipsilateral superior occipital gyrus (SOG) and higher FC between this cluster and the ipsilateral posterior cingulate gyrus (p < 0.05, corrected). Finally, the GMV of the left CG was negatively correlated with the LHON duration (r = -0.535, p = 0.002), and the FC between the left CG and the ipsilateral posterior cingulate gyrus of the LHON was negatively correlated with the average peripapillary RNFL thickness (r = -0.522, p = 0.003).

Conclusion: The atrophied primary visual cortex of the chronic LHON may be caused by transneuronal degeneration following the retinal damage. Moreover, our findings suggest that the functional organization of the atrophied primary visual cortex has been reshaped in the chronic LHON.

Keywords: LHON; functional connectivity (FC); gray matter volume (GMV); reorganization; visual cortex (V1).