Patton Andrew, Davidsen Jörn
Department of Physics and Astronomy, University of Calgary, Calgary, Alberta, Canada.
Hotchkiss Brain Institute, University of Calgary, Calgary, Alberta, Canada.
PLoS Comput Biol. 2025 Sep 2;21(9):e1013093. doi: 10.1371/journal.pcbi.1013093. eCollection 2025 Sep.
Although the brain's structural and functional alterations with age are individually well documented, how differences in cognitive abilities emerge from variations in the underlying spatio-temporal patterns of regional brain activity is largely unknown. Patterns of increased synchronization between brain regions are taken as enhanced cognitive integration, while decreased synchronization is indicative of cognitive segregation. The ability to dynamically switch between different levels of integration and segregation across different cognitive systems is believed to be crucial for overall cognitive performance. Building on a recently proposed cognitively informed, synchronization-based framework, we study here age-related variations in dynamical flexibility between segregation and integration, as captured by changes in the variable patterns of partial synchronization or chimera states. Leveraging personalized brain network models based on large-scale, multisite datasets of cross-sectional healthy cohorts, we systematically show how regional brain stimulation produces distinct patterns of synchronization. We find that chimera states play a crucial role in regulating the balance between cognitive integration and segregation as the brain ages, providing new insights into the mechanisms underlying cognitive decline and preservation in aging. Whereas the emergent synchronization behavior of brain regions belonging to the same cognitive system often show the same aging trends, different cognitive systems can demonstrate distinct trends. This supports the idea that aging affects cognitive systems differently and that understanding this variability is essential for a more comprehensive view of neuro-cognitive aging. At the same time, dynamical flexibility increases in the oldest age groups across most cognitive systems. This may reflect compensatory mechanisms to counteract age-related cognitive declines and points towards a phenomenon of dedifferentiation. Yet, the multiplicity of behaviors highlights that whereas dedifferentiation emerges in certain cognitive systems, differentiation can also occur in others. This illustrates that these processes, though seemingly oppositional, can coexist and unfold in parallel across different cognitive systems.
尽管大脑随年龄增长的结构和功能变化已有详细记录，但认知能力的差异如何从大脑区域活动的潜在时空模式变化中产生，在很大程度上仍不清楚。大脑区域间同步性增加的模式被视为认知整合增强，而同步性降低则表明认知分离。人们认为，在不同认知系统之间动态切换不同程度的整合和分离的能力对整体认知表现至关重要。基于最近提出的基于同步性的认知框架，我们在此研究分离与整合之间动态灵活性的年龄相关变化，这种变化通过部分同步或嵌合状态的可变模式变化来体现。利用基于大规模、多站点健康横断面队列数据集的个性化脑网络模型，我们系统地展示了区域脑刺激如何产生不同的同步模式。我们发现，随着大脑衰老，嵌合状态在调节认知整合与分离之间的平衡中起着关键作用，这为衰老过程中认知衰退和保持的潜在机制提供了新的见解。属于同一认知系统的大脑区域出现的同步行为通常呈现相同的衰老趋势，而不同的认知系统可能表现出不同的趋势。这支持了这样一种观点，即衰老对不同认知系统的影响不同，理解这种变异性对于更全面地了解神经认知衰老至关重要。同时，在大多数认知系统中，最年长者的动态灵活性有所增加。这可能反映了抵消与年龄相关的认知衰退的补偿机制，并指向一种去分化现象。然而，行为的多样性凸显出，虽然在某些认知系统中出现了去分化，但在其他认知系统中也可能发生分化。这表明，这些过程虽然看似相反，但可以在不同的认知系统中同时并存并并行展开。
