Distinct weak asymmetric interactions shape human brain functions as probability fluxes

Abstract

The functional computation of the human brain arises from the collective behaviour of the underlying neural network. The emerging technology enables the recording of population activity in neurons, and the theory of neural networks is expected to explain and extract functional computations from the data. Thermodynamically, a large proportion of the whole-body energy is consumed by the brain, and functional computation of the human brain seems to involve high energy consumption. The human brain, however, does not increase its energy consumption with its function, and most of its energy consumption is not involved in specific brain function: how can the human brain perform its wide repertoire of functional computations without drastically changing its energy consumption? Here, we present a mechanism to perform functional computation by subtle modification of the interaction network among the brain regions. We first show that, by analyzing the data of spontaneous and task-induced whole-cerebral-cortex activity, the probability fluxes, which are the microscopic irreversible measure of state transitions, exhibit unique patterns depending on the task being performed, indicating that the human brain function is a distinct sequence of the brain state transitions. We then fit the parameters of Ising spin systems with asymmetric interactions, where we reveal that the symmetric interactions among the brain regions are strong and task-independent, but the antisymmetric interactions are subtle and task-dependent, and the inferred model reproduces most of the observed probability flux patterns. Our results indicate that the human brain performs its functional computation by subtly modifying the antisymmetric interaction among the brain regions, which might be possible with a small amount of energy.