Quantifying the cost of network computations to unpack structure-function relationships in the brain

Abstract

The brain supports computations through coordinated patterns of activity on an underlying network. These networks---from microscale navigational circuits in insects to macroscale brain areas in humans---are organized in structured ways that are thought to support their function. We seek a unifying quantitative framework to understand how network structure shapes the computations a network can readily support. To do so, we frame computation as a goal-directed transition of activity and quantify its cost on a given network using control theory. We then define the distribution of costs across all possible transitions as a $\textit{computational affordance landscape}$ that encodes which computations a network structure readily supports. We apply this framework to a circuit model for how insects maintain a sense of direction and show that updating orientation is the least costly computation, with predicted inputs consistent with known circuitry. In the human brain, we find that the affordance landscape varies systematically with the functional role of each network. Sensory networks display more heterogeneous landscapes (reflecting their role in specialized information processing), whereas association networks display more homogeneous landscapes (reflecting their role in generalized information processing). In recurrent neural networks trained on cognitive tasks, we show that learning progressively increases landscape heterogeneity, reshaping the distribution of affordable computations. Generally, we establish a quantitative framework for studying relationships between structure and computation in neural circuits, with future applications extending to other biological and physical networks.