As we move forward in the environment, we experience a radial expansion of the retinal image, wherein the center corresponds to the instantaneous direction of self-motion. Humans can precisely perceive their heading direction even when the retinal motion is distorted by gaze shifts due to eye/body rotations. Previous studies have suggested that both retinal and extra-retinal strategies can compensate for the retinal image distortion. However, the relative contributions of each strategy remain unclear. To address this issue, we devised a two-alternative-headings discrimination task, in which participants had either real or simulated pursuit eye movements. The two conditions had the same retinal input but either with or without extra-retinal eye movement signals. Thus, the behavioral difference between conditions served as a metric of extra-retinal contribution. We systematically and independently manipulated pursuit speed, heading
speed, and the reliability of retinal signals. We found that the levels of extra-retinal contributions increased with increasing pursuit speed (stronger extra-retinal signal), and with decreasing heading speed (weaker retinal signal). In addition, extra-retinal contributions also increased as we corrupted retinal signals with noise. Our results revealed that the relative magnitude of retinal and extra-retinal contributions was not fixed but rather flexibly adjusted to each specific task condition. This task-dependent, flexible integration appears to take the form of a reliability-based weighting scheme that maximizes heading performance.