Geometric constraints on human brain function

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 fibres(1-3). However, predictions from neural field theory, an established mathematical framework for modelling large-scale brain activity(4-6), suggest that the geometry of the brain may represent a more fundamental constraint on dynamics than complex interregional connectivity(7,8). 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.

Automated summary

The anatomy of the brain imposes constraints on its function, but how exactly these constraints work is not well understood. The traditional view in neuroscience is that the interaction between different specialized cell populations connected by a complex network of axonal fibers drives neuronal dynamics. However, neural field theory suggests that the geometry of the brain may be a more fundamental constraint than interregional connectivity. In this study, we confirm these predictions by analyzing human MRI data and show that brain activity can be explained by excitations of the brain's geometric modes rather than complex interregional connectivity.