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.

Influence of sensory modality and control dynamics on human path integration.

Path integration is a sensorimotor computation that can be used to infer latent dynamical states by integrating self-motion cues. We studied the influence of sensory observation (visual/vestibular) and latent control dynamics (velocity/acceleration) on human path integration using a novel motion-cueing algorithm. Sensory modality and control dynamics were both varied randomly across trials, as participants controlled a joystick to steer to a memorized target location in virtual reality. Visual and vestibular steering cues allowed comparable accuracies only when participants controlled their acceleration, suggesting that vestibular signals, on their own, fail to support accurate path integration in the absence of sustained acceleration. Nevertheless, performance in all conditions reflected a failure to fully adapt to changes in the underlying control dynamics, a result that was well explained by a bias in the dynamics estimation. This work demonstrates how an incorrect internal model of control dynamics affects navigation in volatile environments in spite of continuous sensory feedback.