Vo Quan, Simon Zachary D, Park Gwoncheol, Nacionales Dina C, Gorski Carmelina, Barrios Evan L, Casadesus Gemma, Efron Philip A, Moldawer Lyle L, Nagpal Ravinder, Chakrabarty Paramita, Febo Marcelo
Department of Neuroscience, University of Florida, Gainesville, FL 32610, USA.
Department of Neuroscience, University of Florida, Gainesville, FL 32610, USA; Department of Psychiatry, University of Florida, Gainesville, FL 32610, USA.
Neuroimage. 2025 Jan;305:120995. doi: 10.1016/j.neuroimage.2024.120995. Epub 2025 Jan 1.
Sepsis is a state of systemic immune dysregulation and organ failure that is frequently associated with severe brain disability. Epidemiological studies have indicated that younger females have better prognosis and clinical outcomes relative to males, though the sex-dependent response of the brain to sepsis during post-sepsis recovery remains largely uncharacterized. Using a modified polymicrobial intra-abdominal murine model of surgical sepsis, we characterized the acute effects of intra-abdominal sepsis on peripheral inflammation, brain inflammation and brain functional connectivity in young adult mice of both sexes. Following sepsis, both male and female mice survived the procedure, regained body weight within 7 days post-sepsis and showed reduced diversity in their gut microbiome. Interestingly, compared to the sepsis-induced changes observed in female mice, the post-septic male mice exhibited a comparatively robust profile of splenic cell expansion and intracerebral glial proliferation relative to their healthy counterparts. Analysis of resting-state functional Magnetic Resonance Imaging (fMRI) data collected from the post-septic mice revealed that while connectivity to the somatosensory cortex were affected equally in both sexes, intra-network connectivity strength in the striatum preferentially increased in post-septic males but remained near baseline in post-septic female mice. Additionally, the female mice showed reduced network connectivity alterations in the projections from periaqueductal gray to the superior colliculus as also between the anterior cingulate cortex and the striatum. Coupled with the sustained intracerebral gliosis response, the intra-striatal fMRI response patterns in males could signify a delayed recovery from sepsis. Together, our study provides evidence that peripheral sepsis influences peripheral immunity, brain immunity and brain connectivity in a sex-dependent manner, with the fMRI response strongly indicating cognitive benefits in young females recovering from sepsis relative to their male counterparts.
脓毒症是一种全身免疫失调和器官衰竭的状态,常与严重脑功能障碍相关。流行病学研究表明,相对于男性,年轻女性的预后和临床结果更好,尽管在脓毒症恢复过程中大脑对脓毒症的性别依赖性反应在很大程度上仍未得到充分描述。我们使用改良的多微生物腹腔内小鼠手术脓毒症模型,对腹腔内脓毒症对年轻成年雌雄小鼠外周炎症、脑炎症和脑功能连接的急性影响进行了表征。脓毒症后,雌雄小鼠均在手术后存活,在脓毒症后7天内恢复体重,且肠道微生物群的多样性降低。有趣的是,与在雌性小鼠中观察到的脓毒症诱导的变化相比,脓毒症后的雄性小鼠相对于其健康对照表现出脾脏细胞扩张和脑内神经胶质细胞增殖的相对较强的特征。对脓毒症后小鼠收集的静息态功能磁共振成像(fMRI)数据的分析表明,虽然与体感皮层的连接在两性中受到同等影响,但纹状体内网络连接强度在脓毒症后的雄性小鼠中优先增加,而在脓毒症后的雌性小鼠中仍接近基线。此外,雌性小鼠在导水管周围灰质到上丘的投射以及前扣带回皮层和纹状体之间的网络连接变化也减少。与持续的脑内胶质增生反应相结合,雄性小鼠纹状体内的fMRI反应模式可能表明脓毒症恢复延迟。总之,我们的研究提供了证据,表明外周脓毒症以性别依赖的方式影响外周免疫、脑免疫和脑连接,fMRI反应强烈表明年轻女性相对于男性在从脓毒症中恢复时具有认知优势。