Montreal Neurological Institute, Department of Neurology and Neurosurgery, McGill University, Montreal, Canada; Ludmer Centre for Neuroinformatics and Mental Health, McGill University, Montreal, Canada.
Centre de recherche de l'Institut universitaire de cardiologie et de pneumologie de Québec, Université Laval, Québec, Canada.
Neuroimage. 2021 Nov 1;241:118419. doi: 10.1016/j.neuroimage.2021.118419. Epub 2021 Jul 21.
Metabolic disorders associated with obesity could lead to alterations in brain structure and function. Whether these changes can be reversed after weight loss is unclear. Bariatric surgery provides a unique opportunity to address these questions because it induces marked weight loss and metabolic improvements which in turn may impact the brain in a longitudinal fashion. Previous studies found widespread changes in grey matter (GM) and white matter (WM) after bariatric surgery. However, findings regarding changes in spontaneous neural activity following surgery, as assessed with the fractional amplitude of low frequency fluctuations (fALFF) and regional homogeneity of neural activity (ReHo), are scarce and heterogenous. In this study, we used a longitudinal design to examine the changes in spontaneous neural activity after bariatric surgery (comparing pre- to post-surgery), and to determine whether these changes are related to cardiometabolic variables.
The study included 57 participants with severe obesity (mean BMI=43.1 ± 4.3 kg/m) who underwent sleeve gastrectomy (SG), biliopancreatic diversion with duodenal switch (BPD), or Roux-en-Y gastric bypass (RYGB), scanned prior to bariatric surgery and at follow-up visits of 4 months (N = 36), 12 months (N = 29), and 24 months (N = 14) after surgery. We examined fALFF and ReHo measures across 1022 cortical and subcortical regions (based on combined Schaeffer-Xiao parcellations) using a linear mixed effect model. Voxel-based morphometry (VBM) based on T1-weighted images was also used to measure GM density in the same regions. We also used an independent sample from the Human Connectome Project (HCP) to assess regional differences between individuals who had normal-weight (N = 46) or severe obesity (N = 46).
We found a global increase in the fALFF signal with greater increase within dorsolateral prefrontal cortex, precuneus, inferior temporal gyrus, and visual cortex. This effect was more significant 4 months after surgery. The increase within dorsolateral prefrontal cortex, temporal gyrus, and visual cortex was more limited after 12 months and only present in the visual cortex after 24 months. These increases in neural activity measured by fALFF were also significantly associated with the increase in GM density following surgery. Furthermore, the increase in neural activity was significantly related to post-surgery weight loss and improvement in cardiometabolic variables, such as blood pressure. In the independent HCP sample, normal-weight participants had higher global and regional fALFF signals, mainly in dorsolateral/medial frontal cortex, precuneus and middle/inferior temporal gyrus compared to the obese participants. These BMI-related differences in fALFF were associated with the increase in fALFF 4 months post-surgery especially in regions involved in control, default mode and dorsal attention networks.
Bariatric surgery-induced weight loss and improvement in metabolic factors are associated with widespread global and regional increases in neural activity, as measured by fALFF signal. These findings alongside the higher fALFF signal in normal-weight participants compared to participants with severe obesity in an independent dataset suggest an early recovery in the neural activity signal level after the surgery.
与肥胖相关的代谢紊乱可导致大脑结构和功能发生改变。减肥后这些变化是否可以逆转尚不清楚。减重手术为解决这些问题提供了一个独特的机会,因为它可以显著减轻体重和改善代谢,从而可能以纵向的方式影响大脑。先前的研究发现减重手术后灰质(GM)和白质(WM)广泛变化。然而,关于手术后自发神经活动变化的研究结果(通过分数低频波动幅度(fALFF)和神经活动局部一致性(ReHo)评估)很少且存在异质性。在这项研究中,我们使用纵向设计来研究减重手术后自发神经活动的变化(比较手术前和手术后),并确定这些变化是否与心脏代谢变量有关。
该研究纳入了 57 名患有严重肥胖症(平均 BMI=43.1±4.3kg/m²)的患者,他们接受了袖状胃切除术(SG)、胆胰分流十二指肠转位术(BPD)或 Roux-en-Y 胃旁路术(RYGB),在减重手术前和手术后 4 个月(N=36)、12 个月(N=29)和 24 个月(N=14)进行了扫描。我们使用线性混合效应模型,对基于联合 Schaeffer-Xiao 分区的 1022 个皮质和皮质下区域(1022 个皮质和皮质下区域)的 fALFF 和 ReHo 指标进行了检查。还使用 T1 加权图像的基于体素的形态计量学(VBM)测量了相同区域的 GM 密度。我们还使用了来自人类连接组计划(HCP)的独立样本,以评估正常体重(N=46)或严重肥胖(N=46)个体之间的区域差异。
我们发现 fALFF 信号整体增加,背外侧前额叶皮层、楔前叶、下颞叶和视觉皮层的增加更为明显。这种效应在手术后 4 个月更为显著。手术后 12 个月,背外侧前额叶皮层、颞叶和视觉皮层的增加更为有限,24 个月后仅在视觉皮层中存在。fALFF 测量的神经活动增加也与手术后 GM 密度的增加显著相关。此外,神经活动的增加与术后体重减轻和心脏代谢变量的改善(如血压)显著相关。在独立的 HCP 样本中,与肥胖参与者相比,正常体重参与者的全局和区域 fALFF 信号更高,主要在背外侧/内侧前额叶皮层、楔前叶和中/下颞叶。这些与 BMI 相关的 fALFF 差异与术后 4 个月的 fALFF 增加有关,尤其是在控制、默认模式和背侧注意网络的区域。
减重手术引起的体重减轻和代谢因素的改善与 fALFF 信号所示的广泛的全局和区域神经活动增加有关。这些发现以及独立数据集中正常体重参与者的 fALFF 信号高于严重肥胖参与者的发现表明,手术后神经活动信号水平的早期恢复。