Belief embodiment through eye movements facilitates memory-guided navigation

Neural network models optimized for task performance often excel at predicting neural activity but do not explain other properties such as the distributed representation across functionally distinct areas. Distributed representations may arise from animals’ strategies for resource utilization, however, fixation-based paradigms deprive animals of a vital resource: eye movements. During a naturalistic task in which humans use a joystick to steer and catch flashing fireflies in a virtual environment lacking position cues, subjects physically track the latent task variable with their gaze. We show this strategy to be true also during an inertial version of the task in the absence of optic flow and demonstrate that these task-relevant eye movements reflect an embodiment of the subjects’ dynamically evolving internal beliefs about the goal. A neural network model with tuned recurrent connectivity between oculomotor and evidence-integrating frontoparietal circuits accounted for this behavioral strategy. Critically, this model better explained neural data from monkeys’ posterior parietal cortex compared to task-optimized models unconstrained by such an oculomotor-based cognitive strategy. These results highlight the importance of unconstrained movement in working memory computations and establish a functional significance of oculomotor signals for evidence-integration and navigation computations via embodied cognition.