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Geometric constraints on human brain function
Nature ( IF 64.8 ) Pub Date : 2023-05-31 , DOI: 10.1038/s41586-023-06098-1
James C Pang 1 , Kevin M Aquino 2, 3 , Marianne Oldehinkel 4 , Peter A Robinson 2 , Ben D Fulcher 2 , Michael Breakspear 5, 6 , Alex Fornito 1
Affiliation  

The anatomy of the brain necessarily constrains its function, but precisely how remains unclear. The classical and dominant paradigm in neuroscience is that neuronal dynamics are driven by interactions between discrete, functionally specialized cell populations connected by a complex array of axonal fibres1,2,3. However, predictions from neural field theory, an established mathematical framework for modelling large-scale brain activity4,5,6, suggest that the geometry of the brain may represent a more fundamental constraint on dynamics than complex interregional connectivity7,8. Here, we confirm these theoretical predictions by analysing human magnetic resonance imaging data acquired under spontaneous and diverse task-evoked conditions. Specifically, we show that cortical and subcortical activity can be parsimoniously understood as resulting from excitations of fundamental, resonant modes of the brain’s geometry (that is, its shape) rather than from modes of complex interregional connectivity, as classically assumed. We then use these geometric modes to show that task-evoked activations across over 10,000 brain maps are not confined to focal areas, as widely believed, but instead excite brain-wide modes with wavelengths spanning over 60 mm. Finally, we confirm predictions that the close link between geometry and function is explained by a dominant role for wave-like activity, showing that wave dynamics can reproduce numerous canonical spatiotemporal properties of spontaneous and evoked recordings. Our findings challenge prevailing views and identify a previously underappreciated role of geometry in shaping function, as predicted by a unifying and physically principled model of brain-wide dynamics.



中文翻译:

人脑功能的几何约束

大脑的解剖结构必然会限制其功能,但具体如何限制仍不清楚。神经科学中的经典和主导范式是,神经元动力学是由离散的、功能特化的细胞群之间的相互作用驱动的,这些细胞群由复杂的轴突纤维阵列连接1,2,3。然而,神经场理论(一种用于模拟大规模大脑活动的数学框架4,5,6 )的预测表明,大脑的几何形状可能代表比复杂的区域间连接更基本的动力学约束7,8。在这里,我们通过分析在自发和不同任务诱发条件下获取的人体磁共振成像数据来证实这些理论预测。具体来说,我们表明,皮层和皮层下活动可以简单地理解为由大脑几何形状(即其形状)的基本共振模式的激发引起的,而不是像经典假设的那样由复杂的区域间连接模式引起。然后,我们使用这些几何模式来表明,超过 10,000 个大脑图谱中的任务诱发激活并不像人们普遍认为的那样局限于焦点区域,而是激发波长跨度超过 60 毫米的全脑模式。最后,我们证实了这样的预测:几何学和功能之间的密切联系可以通过波状活动的主导作用来解释,表明波动力学可以再现自发和诱发记录的许多规范时空特性。我们的研究结果挑战了主流观点,并确定了几何学在塑造功能中先前被低估的作用,正如全脑动力学的统一且具有物理原理的模型所预测的那样。

更新日期:2023-06-01
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