Increased resting-state functional connectivity in suprasellar tumor patients with postoperative visual improvement

Abstract

Background and Objective: Large suprasellar tumors often compress the optic chiasm and give rise to visual impairment. Most patients have significantly improved visual function at 1 to 4 months after chiasmal decompression surgery, and only a few individuals regain normal vision at 1 week after surgery. How the recovery of visual function in these patients affects the visual cortex is not fully understood. In this study, we aimed to investigate alterations in brain functional connectivity (FC) in suprasellar tumor patients with visual improvement using resting-state functional magnetic resonance imaging (rs-fMRI). Methods: This longitudinal study was conducted on 13 suprasellar tumor patients who had ophthalmological examinations and rs-fMRI at the following time points: within 1-week preoperation (Pre-op), 1-week postoperation (Post-1w) and 1-month postoperation (Post-1m). The visual impairment score (VIS), local functional correlation (LCOR) and FC values were subjected to one-way ANOVA. Pearson correlation coefficients between changes in the LCOR and clinical factors were calculated. Results: The VIS was significantly decreased at both Post-1w and Post-1m compared to that at Pre-op. Whole-brain analysis of LCOR values showed that the left V1 (primary occipital cortex) was increased significantly at Post-1m compared to that at Pre-op (p < 0.05, FDR corrected). ROI analysis exhibited a significant negative correlation between the LCOR and VIS changes at Post-1m compared to those at Pre-op (p < 0.05, r =-0.60). FC analysis within the visual network showed that the FC strengths were significantly increased between the left V5 and the left V4, right V3a, left V3, left V2d, and right V5 at Post-1m compared to those at Pre-op (p < 0.05, FDR corrected). Additionally, the FC strengths were significantly increased between the left V5 and the left V1, right orbital-frontal gyrus and left posterior supramarginal gyrus at the whole-brain network level at Post-1m compared to those at Pre-op (p < 0.05, FDR corrected). Conclusions: Postoperative visual improvement can be reflected by the increased FC of the visual cortex at Post-1w and Post-1m, especially at Post-1m. The LCOR value of the left V1 was associated with improved visual outcomes and may be used to objectively assess early visual recovery after chiasmal decompression at Post-1m.

fMRI Retinotopic Mapping in Patients with Brain Tumors and Space-Occupying Brain Lesions in the Area of the Occipital Lobe

“…Changes in the functional connectivity in resting-state fMRI were also found in blind subjects, as well as patients with primary open-angle glaucoma, compared to healthy controls [ 41 , 42 ]. Furthermore, in patients with a suprasellar tumor involving compression of the optic chiasm (meningioma and pituitary adenoma), functional connectivity within visual areas during rest significantly improved as a result of surgical treatment of the patients, which was consistent with an additional improvement of the visual abilities postoperatively [ 43 ]. Additionally, such patients showed reduced cortical thickness in some areas of the occipital lobe compared to healthy control subjects [ 44 ].…”

“…We also analyzed the percent signal change within the brain areas involved in higher visual perception and processing, the cluster sizes of activated voxels in the calcarine fissure and lateralization indices in the occipital lobe. Based on the previous results [ 43 , 44 , 45 ], where effects of the suprasellar tumors also in the nonaffected occipital lobe where found, the higher brain areas not directly invaded by the tumor should also show significant effects. Although eccentricity mapping is not originally intended to activate higher visual areas, we assume that these areas should show lower activity due to reduced inputs from tumor-affected areas in the affected hemisphere.…”

Good Visual Outcomes After Pituitary Tumor Surgery Are Associated With Increased Visual Cortex Functional Connectivity

“…Interestingly, V5 is often referred to as the "movement area," responsible for visual motion perception and smooth pursuit movements (9). Activation of subcortical extrastriate pathways through V5 and the middle temporal area may therefore represent a compensatory adaptation that potentiates recovery in patients with pituitary tumors (6,9,27,28).…”

“…Kerrison identified an "early fast phase" of visual recovery that occurs within 1 week of surgery, an "early slow phase" that manifests within 1-4 months, and a "late phase" of visual recovery that occurs from 6 months to 3 years (2). Factors that contribute to visual recovery phases may include remyelination, neuroaxonal remodeling, and cortical plasticity (1)(2)(3)(5)(6)(7)(8)(9). Resting-state functional MRI (rsfMRI) is an advanced functional imaging technique that permits quantification of statistical relationships between the spontaneous time courses of the blood oxygen level dependent (BOLD) signal from discrete regions of the brain, known as functional connectivity (FC) (10).…”

“…Several rsfMRI reports have shown that FC changes coincide with visual impairment in patients with chiasmal compression from pituitary tumors (See Supplemental Digital Content 1, Table E1, http://links.lww. com/WNO/A450) (6)(7)(8)(9). Yet, interpreting findings from these observational reports has been challenging because of differences in patient populations, study design, characterization of visual outcomes, and imaging protocols (5)(6)(7)(8)(9).…”