Accumulating evidence suggests that the brain exhibits a remarkable capacity for functional compensation in response to neurological damage, a resilience potential that is deeply rooted in the malleable features of its underlying anatomo-functional architecture. This propensity is particularly exemplified by diffuse low-grade gliomas (DLGGs), a subtype of primary brain tumour. However, functional plasticity is not boundless, and surgical resections directed at structures with limited neuroplasticity may lead to incapacitating impairments. Yet, maximizing DLGG resections offers substantial oncological benefits, especially when the resection extends beyond the tumour margins (i.e., supra-tumour or supra-total resection). In this context, the primary objective of this study was to identify which cerebral structures were associated with less favourable cognitive outcomes after surgery, while accounting for intra-tumour and supra-tumour features of the surgical resections. To reach this objective, we leveraged a unique cohort of 400 DLGG patients who underwent surgery with awake cognitive mapping. Patients benefited from a neuropsychological assessment consisting of 18 subtests administered before and 3 months post-surgery. We analysed changes in performance and applied topography-focused and disconnection-focused multivariate lesion-symptom mapping (LSM) using support vector regressions with an attempt to capture resected cortico-subcortical structures less amenable to full cognitive compensations. The observed changes in performance were of a limited magnitude suggesting an overall recovery (13/18 tasks fully recovered despite a mean resection extent of 92.4%). Nevertheless, LSM analyses revealed that a lack of recovery in picture naming was linked to damage in the left inferior temporal gyrus and inferior longitudinal fasciculus. Similarly, for semantic fluency abilities, an association was established with damage to the left precuneus/posterior cingulate. For phonologic fluency abilities, the left dorso-medial frontal cortex and the frontal aslant tract were implicated. Moreover, difficulties in spatial exploration were associated with injury to the right dorsomedial prefrontal cortex and its underlying connectivity. An exploratory analysis suggested that supra-tumoral resections were associated with a less pronounced recovery following specific resection patterns, such as supra-tumour resections of the left uncinate fasciculus (picture naming), the left corticostriatal tract and the anterior corpus callosum (phonologic fluency), the hippocampus and para-hippocampus (episodic memory), and the right frontal-mesial areas (visuospatial exploration). Collectively, these patterns of results shed new light on both low-resilient neural systems and the prediction of cognitive recovery following glioma surgery. Furthermore, they indicate that supra-tumour resections were only occasionally less well-tolerated from a cognitive viewpoint. In doing so, they have deep implications for surgical planning and rehabilitation strategies.

中文翻译：

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低级别神经胶质瘤内部和周围低弹性神经认知系统的多变量绘图

越来越多的证据表明，大脑在应对神经损伤时表现出卓越的功能补偿能力，这种恢复潜力深深植根于其潜在的解剖功能结构的可塑性特征中。这种倾向尤其体现在弥漫性低级别神经胶质瘤（DLGG）（原发性脑肿瘤的一种亚型）中。然而，功能可塑性并不是无限的，针对神经可塑性有限的结构进行手术切除可能会导致失能性损伤。然而，最大化 DLGG 切除可带来显着的肿瘤学益处，特别是当切除范围超出肿瘤边缘时（即肿瘤上或超全切除）。在这种情况下，本研究的主要目的是确定哪些大脑结构与手术后较差的认知结果相关，同时考虑手术切除的肿瘤内和肿瘤上特征。为了实现这一目标，我们利用了 400 名 DLGG 患者组成的独特队列，这些患者接受了清醒认知映射手术。患者受益于神经心理学评估，该评估包括手术前和手术后 3 个月进行的 18 项分测试。我们分析了性能变化，并使用支持向量回归应用以地形为中心和以断开连接为中心的多变量病变症状映射（LSM），试图捕获不太适合完全认知补偿的切除的皮质-皮质下结构。观察到的性能变化幅度有限，表明总体恢复（尽管平均切除范围为 92.4%，但 13/18 任务完全恢复）。然而，LSM 分析显示，图片命名缺乏恢复与左颞下回和下纵束损伤有关。同样，对于语义流畅性能力，与左侧楔前叶/后扣带回的损伤建立了关联。对于语音流畅能力，涉及左背内侧额叶皮层和额叶倾斜束。此外，空间探索的困难与右侧背内侧前额叶皮层及其潜在连接性的损伤有关。一项探索性分析表明，肿瘤上切除与特定切除模式后不太明显的恢复相关，例如左钩束（图片命名）、左皮质纹状体束和前胼胝体的肿瘤上切除（语音流畅） 、海马体和海马旁体（情景记忆）以及右侧额叶内侧区域（视觉空间探索）。总的来说，这些结果模式为低弹性神经系统和神经胶质瘤手术后认知恢复的预测提供了新的线索。此外，他们表明，从认知角度来看，肿瘤上切除术只是偶尔耐受性较差。在这样做，它们对手术计划和康复策略具有深远的影响。