Frontal but not parietal cortex is required for decisions under risk

Neurons in frontal and parietal cortex encode task variables during decision-making, but causal manipulations of the two regions produce strikingly different results. For example, silencing the posterior parietal cortex (PPC) in rats and monkeys produces minimal effects in perceptual decisions requiring integration of sensory evidence, but silencing frontal cortex profoundly impairs the same decisions. Here, we tested the causal roles of the rat frontal orienting field (FOF) and PPC in economic choice under risk. On each trial, rats chose between a lottery and a small but guaranteed surebet. The magnitude of the lottery was independently varied across trials and was indicated to the rat by the pitch of an auditory cue. As in perceptual decisions, both unilateral and bilateral PPC muscimol inactivations produced minimal effects. FOF inactivations produced substantial changes in behavior even though our task had no working memory component. We quantified control and bilateral inactivation behavior with a multi-agent model consisting of a mixture of a rational utility-maximizing agent (U = V{rho}) with two habitual agents that either choose surebet or lottery. Effects of FOF silencing were best accounted for by a decrease in{rho} , the exponent of the utility function. The decrease in{rho} could be parsimoniously explained by a dynamical model where the FOF is part of a network that represents the value of the lottery to compare against a remembered boundary representing the value of the surebet. This dynamical model predicted that neurons in the FOF should increase their activity with increasing lottery values. In line with our predictions, single neurons recorded in the FOF encoded the value of the lottery even when controlling for choice. These results together demonstrate that FOF is a critical node in the neural circuit for decision under risk.