Biological profits of irrational computations in the orbitofrontal cortex

Making good decisions is essential for survival and success, yet humans and animals often exhibit perplexing irrational decision-making whose biological origin remains poorly understood. Recent theoretical work suggests that some forms of irrational decisions may arise from limited coding precision or metabolic budget in individual orbitofrontal neurons. Here, we consider the alternative possibility that systematic errors in decision-relevant computations are the inevitable consequence of the internal connectivity structure within orbitofrontal networks, which was molded under more distal biological constraints. We first trained cohorts of artificial neural networks to perform rational decision-relevant computations. Remarkably, they exhibited most electrophysiological coding properties of orbitofrontal neurons recorded in monkeys engaged in a preference-based decision task. We then distorted their internal connectivity to reproduce monkeys’ irrational choices. This induced systematic interferences in decision-relevant computations that generalize across individuals, at both the behavioral and neural level. Importantly, irrational networks also display enhanced behavioral resilience to neural loss when compared to their rational counterparts. This suggests that irrational behavior may be the incidental outcome of distal evolutionary pressure on the tolerance to orbitofrontal circuit’s damage.