From January 2023 to April 2023, 23 RD patients and 24 HCs were enrolled in this study. All participants were matched for age and sex; they all were examined in the same clinic and provided written informed consent to participate in the study. All experimental procedures were conducted in accordance with the Declaration of Helsinki, and the study protocol was approved by the Medical Ethics Committee of the First Affiliated Hospital of Nanchang University (Jiangxi Province, China).

The inclusion criteria for RD patients were (1) idiopathic RD involving one or two retinal tears, (2) RD affecting one or two quadrants, and (3) absence of any ocular illness (e.g., cataracts, glaucoma, optic neuritis, or maculopathy) in both eyes. The exclusion criteria for RD patients were (1) recurrent RD or recurrence after RD repair surgery, (2)RD caused by high myopia, (3) ocular trauma-related RD, (4) serious complications associated with RD (e.g., proliferative vitreoretinopathy, vitreous hemorrhage, or macular degeneration), (5) a history of laser treatment or surgery, (6) cardiovascular diseases (e.g., heart disease or hypertension), and (7) psychiatric disorders and cerebral infarction.

According to age, sex, and educational background, HCs were chosen at random from Nanchang City. The inclusion criteria for HCs were the absence of eye diseases and major illnesses (e.g., neurological illness or cerebral infarction); the presence of uncorrected vision or visual acuity better than 1.0; and the completion of MRI-related tests, optical coherence tomography, ultrasonography, and other ophthalmic examinations.

Rs-fMRI data were collected at the Department of Radiology in the First Affiliated Hospital, Nanchang University, China, using a 3 T MR scanner (Siemens, Erlangen, Germany) equipped with an 8-channel phased-array head coil. The following parameters were used to capture 240 resting-state volumes over 8-min: field of view, 240 mm × 240 mm; repetition time, 2,000 ms; echo time, 40 ms; flip angle, 90°; matrix, 64 × 64; slice thickness, 4 mm; and gap, 1 mm. Thirty axial slices were included in each brain volume. The following three-dimensional MRI parameters were used to acquire high-resolution T1-weighted images of each participant: repetition time, 1,900 ms; echo time, 2.26 ms; flip angle, 9°; field of view, 240 mm × 240 mm; matrix, 256 × 256; number of sagittal slices, 176; and slice thickness, 1 mm.

All data preprocessing was conducted using SPM12 and RESTplus (Jia et al., 2019) version 1.25 running in matlab2017b. The data preprocessing steps were as follows: (1) Data collation and classification. (2) Conversion of file format from DICOM to NIFTI. (3) Removal of the first 10 time points. (4) Slice timing correction. (5) Head movement correction. (6) Normalization (standardization of individual space to Montreal Neurological Institute [MNI] standard space). (7) Spatial smoothing. (8) Detrending. (9) Regression of nuisance covariates.

The Time Dynamic Analysis toolbox in RESTplus version 1.25 was used to calculate dynamic metrics. Appropriate window length is essential for dynamic analysis, and sliding windows have key roles in the assessment of dynamic spontaneous brain activity. Previous studies showed that an excessively short window length can increase dALFF signal instability, whereas an excessively long window length does not adequately reflect dynamic temporal changes in dALFF (Leonardi and Van De Ville, 2015; Li et al., 2019). To minimize subjective error caused by a single window length, we used a window length and step size of 1TR for 30TR (60 s), 50TR (100 s), and 80TR (160 s) to calculate the dALFF for each participant. For each participant’s window-based ALFF map, we calculated the mean and standard deviation of each voxel, then determined the appropriate coefficient of variation (CV = standard deviation/mean). Further statistical analyses were conducted using the CV maps.

One-sample t-tests were used for statistical analyses of the CVALFF maps of RD patients and HCs. Two-sample t-tests were used to assess differences in CVALFF maps between groups. The Gaussian random field (GRF) method was used to correct for multiple comparisons and regressed covariates of age and sex (two-tailed, voxel-level p < 0.05; GRF correction, cluster-level p < 0.05).

To determine the dALFF occurrence state, a k-means method was used to the dALFF values for each participant. The k-means algorithm combines together data that is related in “k” ways, ensuring that the total of squares within clusters is as small as possible (Zhang et al., 2018). The Manhattan (L1) distance function method was performed to assess the reoccurrence over time in patterns of ALFF. All of the dALFF windows were clustered using the clustering centroids for the departure points.

To determine whether changes in dynamic metrics can be used as diagnostic indicators of RD, we investigated possible diagnostic indices using Gaussian radial basis function kernel SVMs and the LIBSVM software package (Pereira et al., 2009). The steps were as follows: (1) region of interest signal values were extracted from all differential brain regions; (2) a NII file was created to mask differential brain regions; and (3) the radial basis function of the grid search optimization algorithm was used to calculate parameters.

This study included 23 RD patients (12 men and 11 women; mean age, 51.70 ± 19.37 years) and 24 HCs (11 men and 13 women; mean age, 50.46 ± 14.55 years). Demographic characteristics are shown in Table 1.

Figure 1 shows the spatial distribution of dALFF values between RD patients and HCs at a sliding window size of 30TR. In the bilateral middle frontal gyrus, left putamen, left superior occipital gyrus, and right calcarine, dALFF values were significantly higher in RD patients than in HCs (Figure 1; Table 2; two-tailed, voxel-level p < 0.05; GRF correction, cluster-level p < 0.05).

Figure 2 shows the spatial distribution of dALFF values between RD patients and HCs at a sliding window size of 50TR. In the right middle temporal gyrus, left middle frontal gyrus, right calcarine, left putamen, left middle occipital gyrus, and right inferior frontal gyrus, dALFF values were significantly higher in RD patients than in HCs. Conversely, in the right superior parietal gyrus, dALFF values were significantly lower in RD patients than in HCs (Figure 2; Table 3; two-tailed, voxel-level p < 0.05; GRF correction, cluster-level p < 0.05).

Figure 3 shows the spatial distribution of dALFF values between RD patients and HCs at a sliding window size of 80TR. In the left middle frontal gyrus, dALFF values were significantly higher in RD patients than in HCs. Conversely, in the right paracentral lobule, dALFF values were significantly lower in RD patients than in HCs (Figure 3; Table 4; two-tailed, voxel-level p < 0.05; GRF correction, cluster-level p < 0.05).

Figure 4 depicts the overall state transition mode of all participants at sliding window sizes of 30TR, 50TR, and 80TR. The frequency and mean dwell time are shown for different states, along with the probability of transition between states.

The mean altered dALFF values between RD patients and HCs at sliding window sizes of 30TR, 50TR, and 80TR are shown in Figure 5.

Figure 6A shows that the total accuracy and area under the curve score of SVM classification, based on dALFF with a sliding window size of 30TR, were 97.87% and 0.99, respectively. Figure 6B shows that the total accuracy and area under the curve score of SVM classification, based on dALFF with a sliding window size of 50TR, were 100% and 1.00, respectively. Figure 6C shows that the total accuracy and area under the curve score of SVM classification, based on dALFF with a sliding window size of 80TR, were 93.62% and 0.95, respectively. These results indicate that the dALFF may be useful in the clinical diagnosis of RD.

Pearson and Spearman correlation analyses revealed that region of interest values in positive brain regions identified in RD patients at sliding window sizes of 30TR, 50TR, and 80TR were not correlated with HAMA scores (Table 5).

The frontal lobe, which constitutes approximately one-third of the cerebral cortex in humans, is a region of the brain that develops more slowly than other regions. Its wide-ranging and complex functions encompass nearly all cognitive neuropsychological activities. In this study, we found that the RD group had significantly higher dALFF values in the bilateral middle frontal gyrus and right inferior frontal gyrus, which are important for high-level cognition (e.g., executive function and working memory; Zheng et al., 2015). The decreased central vision, visual distortion, and reduced field of vision in RD patients may cause some motor execution impairment and poor memory. Kawashima et al. (2021) found that functional activation of the bilateral dorsolateral prefrontal cortex and middle frontal gyrus was reduced in Parkinson’s disease patients, presumably in relation to the pathophysiology of working memory disorder in such patients. Through voxel-based morphometry analysis, Zhao et al. (2021) demonstrated that gray matter volume was decreased in the bilateral middle frontal gyrus of patients with major depressive disorder, which may influence executive function in those patients. Chen et al. (2017) also revealed that FC between the right dorsolateral prefrontal cortex and right hippocampus was significantly reduced in long-term breast cancer survivors who had been treated with tamoxifen, implying significant defects in working memory and overall executive function. The above studies indicated that dALFF values in the bilateral middle frontal gyrus and right inferior frontal gyrus are significantly higher in RD patients than in HCs. Accordingly, we speculate that RD patients display motor execution impairment and poor working memory. In such patients, motor function and working memory are maintained before visual decline through compensatory mechanisms involving the bilateral middle frontal gyrus and right inferior frontal gyrus.

The putamen, a key component of the basal ganglia, is important for motor regulation (Romero et al., 2008; Vicente et al., 2012). We observed increased dALFF values in the left putamen of RD patients. Huang et al. (2018) found that the gray matter volume in the left putamen was increased among high myopia (HM) patients, suggesting that HM causes structural alterations in the bilateral putamen; this finding is consistent with the compensatory motor function observed in HM patients. Tong et al. (2021) revealed an increase in regional homogeneity in the left putamen among patients with iridocyclitis; they speculated that iridocyclitis causes functional changes in the putamen, which may lead to compensatory motor function. Hu et al. (2022) also demonstrated that voxel-based morphometry values were decreased in the left putamen of female menopausal dry eye patients, indicating that these patients may exhibit cognitive or motor impairments. Because RD causes sudden vision loss, patients cannot rapidly adapt to monocular vision, and their motor regulation is partially decreased relative to the pre-injury state; this phenomenon may also explain a portion of the increase in dALFF in the left putamen of RD patients. Therefore, we suspect that the increased dALFF in the left putamen compensates for the decrease in motor regulation among RD patients.

The occipital lobe, located in the posterior cerebral cortex, is responsible for visual perception. In this study, we found that dALFF values were increased in the left superior occipital gyrus, left middle occipital gyrus, and right calcarine in RD patients. Shao et al. (2021) reported increased FC density values in the left inferior occipital gyrus of RD patients, which may influence the brain’s effectiveness and accuracy in terms of processing visual digital information. Huang et al. (2017) also demonstrated that RD patients had decreased regional homogeneity in the right occipital lobe; they speculated that the decreased regional homogeneity reflected diminished synchrony among local brain regions, consistent with altered function in the primary visual cortex of RD patients. Wu et al. (2021) revealed that voxel-mirrored homotopic connectivity (VMHC) values in the bilateral calcarine were lower in bronchial asthma patients than in HCs. They suggested that the reduced VMHC values represent aberrant visual network function in asthma patients, leading to changes in visual function. The calcarine divides the occipital lobe into the cuneus above and lingual gyrus below; the primary visual cortex is located on both sides of the calcarine. Because the detached portion of the retina in RD patients cannot perceive light stimuli, the occipital lobe receives weaker visual signals, which may explain the increased dALFF values in the left superior occipital gyrus, left middle occipital gyrus, and right calcarine in RD patients. We suspect that these elevated dALFF values represent a compensatory mechanism by which the brain attempts to cope with vision loss in RD patients.

The temporal lobe, located below the lateral fissure, is divided into the superior temporal, middle temporal, and inferior temporal gyri; the inferior temporal gyrus is mainly involved in language comprehension (Dronkers et al., 2004). We found that dALFF values in the right middle temporal gyrus were increased in RD patients. Yu et al. (2008) reported that FC between the left superior temporal gyrus and middle temporal gyrus was decreased in patients with early blindness, whereas Huang et al. (2019) showed that degree centrality (DC) in the left inferior temporal gyrus was increased in patients with advanced monocular blindness. They speculated that the increase in DC compensated for vision loss in patients with advanced monocular blindness. Qi et al. (2022) showed that VMHC values in the bilateral medial temporal gyrus were decreased in patients with thyroid-associated ophthalmopathy, which may reflect diminished visual processing and attention in such patients. To our knowledge, there have been no reports of language comprehension problems among RD patients. We suspect that RD patients undergo a long period of visual improvement from the initial detachment until postoperative recovery; they may experience some reductions in the ability to learn and perceive external things, which could affect language comprehension. Thus, the elevated dALFF value in the right temporal gyrus may represent a compensatory mechanism for the decrease in language comprehension.

Finally, our study showed that dALFF values were decreased in the right superior parietal gyrus and right paracentral lobule in RD patients. The parietal gyrus, located above the medial parietal sulci, is involved in the transmission of visual information and the integration of visual movement (Caminiti et al., 1996; Iacoboni and Zaidel, 2004). Tan et al. (2018) found that the DC of the right superior parietal gyrus was decreased in comitant exotropia strabismus patients; this decreased DC may reflect functional impairment of the right superior parietal gyrus, which would explain eye movement dysfunction in such patients. In a previous study, we found that FC between the left V1 and L-SPG was increased in HM patients; we speculated that this increase in FC was a compensatory response to prevent impaired top-down control of visual attention in HM patients (Ji et al., 2023). Considering the previous findings, the decreased dALFF values in the right superior parietal gyrus of RD patients may reflect functional impairment in this brain area, which would explain why RD patients experience visual impairment. Moreover, the paracentral lobule extends from the lateral surface of the anterior and posterior central dorsal gyrus to the medial surface, which is closely associated with cognitive impairment (Mascalchi et al., 2014). Kim et al. (2019) found that changes in subnetworks, such as the paracentral lobule, were associated with cognitive scores in patients with subjective cognitive decline. However, Liang et al. (2020) showed that gray matter volume in the paracentral lobule was increased in patients with subjective cognitive decline; they suggested that the increased gray matter volume in the paracentral lobule represents a compensatory mechanism, although it is unclear whether the mechanism is associated with cognitive function. This notion is consistent with our findings that the dALFF value of the right paracentral lobule was decreased in RD patients, although we found no correlation between this brain region and HAMA scores. Therefore, we speculate that the decreased dALFF value of the right paracentral lobule in RD patients reflects inhibition of this brain region. However, there is no clear evidence of diminished cognitive function in RD patients.

In our study, the overall accuracies of SVM classification were 97.87, 100, and 93.62% under three different time windows; area under the curve values were 0.99, 1.00, and 0.95, respectively. Thus, dALFF may offer sensitive biomarkers for distinguishing patients with RD from HCs.

Importantly, there were significant differences in the temporal characteristics of dALFF states between the two groups. Our results showed that the number of transitions in RD patients was higher than that in HC group at both 30TR and 50TR, while the number of transitions in RD patients and HC group was zero at 80TR. At the same time, compared with the HC group, RD patients at 30TR and 50TR showed 3 different time states, and RD patients at 80TR showed 4 different time states. In other words, during the entire resting state MRI scanning period, the brain’s working mode can be divided into three states at 30TR and 50TR, and the brain’s working mode can be divided into four states at 80TR. For patients with RD, state 1 accounted for a larger proportion of these states, suggesting that state 1 may represent a pattern of major brain activity in individuals with RD. In general, the mean dwell time and number of transitions are used as parameters in dynamic pattern analysis to describe state properties that represent brain functional activity and can be reconfigured during illness (Xu et al., 2023). Previous studies have found that patients with diabetic retinopathy exhibit three different temporal states, with state 1 occupying a larger proportion, while patients with diabetic retinopathy have a lower number of transitions than those in the HC group (Huang et al., 2021). Zhao et al. (2021) proposed that an increase in the number of transitions is associated with a decrease in the efficiency of information flow in brain networks. Therefore, we speculate that visual dysfunction leads to a decrease in the efficiency of information flow, which increases the number of conversions in patients with RD. This result also suggests that the whole brain integration of visual functions is abnormal.