Aberrant neurovascular coupling in Leber’s hereditary optic neuropathy: Evidence from a multi-model MRI analysis
The study aimed to investigate the neurovascular coupling abnormalities in Leber’s hereditary optic neuropathy (LHON) and their associations with clinical manifestations. Twenty qualified acute Leber’s hereditary optic neuropathy (A-LHON, disease duration ≤ 1 year), 29 chronic Leber’s hereditary opt...
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| Format: | Article |
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Frontiers Media S.A.
2023-01-01
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| Series: | Frontiers in Neuroscience |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fnins.2022.1050772/full |
| _version_ | 1797956444671180800 |
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| author | Yi Ji Ling Wang Hao Ding Hao Ding Qin Tian Ke Fan Dapeng Shi Chunshui Yu Wen Qin |
| author_facet | Yi Ji Ling Wang Hao Ding Hao Ding Qin Tian Ke Fan Dapeng Shi Chunshui Yu Wen Qin |
| author_sort | Yi Ji |
| collection | DOAJ |
| description | The study aimed to investigate the neurovascular coupling abnormalities in Leber’s hereditary optic neuropathy (LHON) and their associations with clinical manifestations. Twenty qualified acute Leber’s hereditary optic neuropathy (A-LHON, disease duration ≤ 1 year), 29 chronic Leber’s hereditary optic neuropathy (C-LHON, disease duration > 1 year), as well as 37 healthy controls (HCs) were recruited. The neurovascular coupling strength was quantified as the ratio between regional homogeneity (ReHo), which represents intrinsic neuronal activity and relative cerebral blood flow (CBF), representing microcirculatory blood supply. A one-way analysis of variance was used to compare intergroup differences in ReHo/CBF ratio with gender and age as co-variables. Pearson’s Correlation was used to clarify the association between ReHo, CBF, and neurovascular coupling strength. Furthermore, we applied linear and exponential non-linear regression models to explore the associations among ReHo/CBF, disease duration, and neuro-ophthalmological metrics. Compared with HCs, A_LHON, and C_LHON patients demonstrated a higher ReHo/CBF ratio than the HCs in the bilateral primary visual cortex (B_CAL), which was accompanied by reduced CBF while preserved ReHo. Besides, only C_LHON had a higher ReHo/CBF ratio and reduced CBF in the left middle temporal gyrus (L_MTG) and left sensorimotor cortex (L_SMC) than the HCs, which was accompanied by increased ReHo in L_MTG (p < 1.85e–3, Bonferroni correction). A-LHON and C-LHON showed a negative Pearson correlation between ReHo/CBF ratio and CBF in B_CAL, L_SMC, and L_MTG. Only C_LHON showed a weak positive correlation between ReHo/CBF ratio and ReHo in L_SMC and L_MTG (p < 0.05, uncorrected). Finally, disease duration was positively correlated with ReHo/CBF ratio of L_SMC (Exponential: Radj2 = 0.23, p = 8.66e–4, Bonferroni correction). No statistical correlation was found between ReHo/CBF ratio and neuro-ophthalmological metrics (p > 0.05, Bonferroni correction). Brain neurovascular “dyscoupling” within and outside the visual system might be an important neurological mechanism of LHON. |
| first_indexed | 2024-04-10T23:49:20Z |
| format | Article |
| id | doaj.art-90dbff46f75247e0bb009d8542093ee1 |
| institution | Directory Open Access Journal |
| issn | 1662-453X |
| language | English |
| last_indexed | 2024-04-10T23:49:20Z |
| publishDate | 2023-01-01 |
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| series | Frontiers in Neuroscience |
| spelling | doaj.art-90dbff46f75247e0bb009d8542093ee12023-01-10T21:03:33ZengFrontiers Media S.A.Frontiers in Neuroscience1662-453X2023-01-011610.3389/fnins.2022.10507721050772Aberrant neurovascular coupling in Leber’s hereditary optic neuropathy: Evidence from a multi-model MRI analysisYi Ji0Ling Wang1Hao Ding2Hao Ding3Qin Tian4Ke Fan5Dapeng Shi6Chunshui Yu7Wen Qin8Tianjin Key Lab of Functional Imaging, Department of Radiology, Tianjin Medical University General Hospital, Tianjin, ChinaDepartment of Medical Imaging, Henan Provincial People’s Hospital, Zhengzhou, ChinaTianjin Key Lab of Functional Imaging, Department of Radiology, Tianjin Medical University General Hospital, Tianjin, ChinaSchool of Medical Imaging, Tianjin Medical University, Tianjin, ChinaDepartment of Medical Imaging, Henan Provincial People’s Hospital, Zhengzhou, ChinaHenan Eye Institute, Henan Eye Hospital, Henan Provincial People’s Hospital, Zhengzhou University People’s Hospital, Zhengzhou, ChinaDepartment of Medical Imaging, Henan Provincial People’s Hospital, Zhengzhou, ChinaTianjin Key Lab of Functional Imaging, Department of Radiology, Tianjin Medical University General Hospital, Tianjin, ChinaTianjin Key Lab of Functional Imaging, Department of Radiology, Tianjin Medical University General Hospital, Tianjin, ChinaThe study aimed to investigate the neurovascular coupling abnormalities in Leber’s hereditary optic neuropathy (LHON) and their associations with clinical manifestations. Twenty qualified acute Leber’s hereditary optic neuropathy (A-LHON, disease duration ≤ 1 year), 29 chronic Leber’s hereditary optic neuropathy (C-LHON, disease duration > 1 year), as well as 37 healthy controls (HCs) were recruited. The neurovascular coupling strength was quantified as the ratio between regional homogeneity (ReHo), which represents intrinsic neuronal activity and relative cerebral blood flow (CBF), representing microcirculatory blood supply. A one-way analysis of variance was used to compare intergroup differences in ReHo/CBF ratio with gender and age as co-variables. Pearson’s Correlation was used to clarify the association between ReHo, CBF, and neurovascular coupling strength. Furthermore, we applied linear and exponential non-linear regression models to explore the associations among ReHo/CBF, disease duration, and neuro-ophthalmological metrics. Compared with HCs, A_LHON, and C_LHON patients demonstrated a higher ReHo/CBF ratio than the HCs in the bilateral primary visual cortex (B_CAL), which was accompanied by reduced CBF while preserved ReHo. Besides, only C_LHON had a higher ReHo/CBF ratio and reduced CBF in the left middle temporal gyrus (L_MTG) and left sensorimotor cortex (L_SMC) than the HCs, which was accompanied by increased ReHo in L_MTG (p < 1.85e–3, Bonferroni correction). A-LHON and C-LHON showed a negative Pearson correlation between ReHo/CBF ratio and CBF in B_CAL, L_SMC, and L_MTG. Only C_LHON showed a weak positive correlation between ReHo/CBF ratio and ReHo in L_SMC and L_MTG (p < 0.05, uncorrected). Finally, disease duration was positively correlated with ReHo/CBF ratio of L_SMC (Exponential: Radj2 = 0.23, p = 8.66e–4, Bonferroni correction). No statistical correlation was found between ReHo/CBF ratio and neuro-ophthalmological metrics (p > 0.05, Bonferroni correction). Brain neurovascular “dyscoupling” within and outside the visual system might be an important neurological mechanism of LHON.https://www.frontiersin.org/articles/10.3389/fnins.2022.1050772/fullLeber’s hereditary optic neuropathymitochondrial diseasearterial spin labelingregional homogeneityneurovascular couplingcerebral blood flow |
| spellingShingle | Yi Ji Ling Wang Hao Ding Hao Ding Qin Tian Ke Fan Dapeng Shi Chunshui Yu Wen Qin Aberrant neurovascular coupling in Leber’s hereditary optic neuropathy: Evidence from a multi-model MRI analysis Frontiers in Neuroscience Leber’s hereditary optic neuropathy mitochondrial disease arterial spin labeling regional homogeneity neurovascular coupling cerebral blood flow |
| title | Aberrant neurovascular coupling in Leber’s hereditary optic neuropathy: Evidence from a multi-model MRI analysis |
| title_full | Aberrant neurovascular coupling in Leber’s hereditary optic neuropathy: Evidence from a multi-model MRI analysis |
| title_fullStr | Aberrant neurovascular coupling in Leber’s hereditary optic neuropathy: Evidence from a multi-model MRI analysis |
| title_full_unstemmed | Aberrant neurovascular coupling in Leber’s hereditary optic neuropathy: Evidence from a multi-model MRI analysis |
| title_short | Aberrant neurovascular coupling in Leber’s hereditary optic neuropathy: Evidence from a multi-model MRI analysis |
| title_sort | aberrant neurovascular coupling in leber s hereditary optic neuropathy evidence from a multi model mri analysis |
| topic | Leber’s hereditary optic neuropathy mitochondrial disease arterial spin labeling regional homogeneity neurovascular coupling cerebral blood flow |
| url | https://www.frontiersin.org/articles/10.3389/fnins.2022.1050772/full |
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