Exposure to low (10 cGy) doses of simulated space radiation impairs reward-guided decision making in both male and female rats

Abstract

Decision-making under uncertainty depends on coordinated frontostriatal circuitry that integrates reward valuation, outcome monitoring, and cognitive control. Perturbations within this network can bias strategy selection, favoring immediate or uncertain rewards, without overtly impairing learning or motivation. Such subtle changes in decision bias may have significant operational consequences for astronauts, whose performance during long-duration missions will depend on maintaining cognitive flexibility and risk evaluation. During deep space travel, astronauts will be exposed to Space Radiation (SR), a complex field of highly energetic charged particles. Estimated cumulative doses during Mars-class missions may reach 1–1.2 Sv (∼200 cGy), raising concerns about its effects on brain function. Preclinical studies demonstrate that such SR doses disrupts dopamine-dependent cognition, alters striatal dopamine turnover and receptor expression, and perturbs oscillatory signaling that coordinates frontostriatal activity. Low-dose SR exposure in rodents produces decision-making alterations across multiple frontostriatal-dependent tasks, including the Associative Recognition Memory Interference Touchscreen (ARMIT) and the rat Risk Taking Predisposition task (rRTP), manifesting as changes in flexibility and decision bias rather than overt deficits. Moreover, SR effects are sex dependent: males exhibit slower response times (increased switch cost), whereas females maintain speed at the expense of accuracy, suggesting distinct compensatory mechanisms. Here, we show that exposure to 10 cGy of the Simplified Galactic Cosmic Radiation Simulator (SGS) alters cost–benefit decision-making in the rRTP in both sexes. SGS-exposed males displayed a global degradation of reward sensitivity, consistent with striatal dopaminergic dysfunction, whereas females exhibited a selective shift toward high-risk, low-probability choices, implicating orbitofrontal disruption of fine-grained value discrimination. These outcomes reflect distinct but converging failures of dopaminergic precision and cortical–striatal coordination. We propose a threshold-based model of cognitive reserve in which males rely primarily on striatal integrity and females on orbitofrontal precision. Once these sex-specific compensatory networks are exceeded, executive control deteriorates along divergent trajectories, revealing complementary mechanisms of radiation-induced cognitive vulnerability.