In sensory systems information is encoded by the activity of populations of neurons. To analyze the coding properties of neuronal populations sensory stimuli have usually been employed that were much simpler than those encountered in real life. It has been possible only recently to stimulate visual interneurons of the blowfly with naturalistic visual stimuli reconstructed from eye movements measured during free flight. Therefore, we now investigate with naturalistic optic flow the coding properties of a small neuronal population of identified visual interneurons in the blowfly, the so-called VS and HS neurons. These neurons are motion sensitive and directionally selective and are assumed to extract information about the animal’s self-motion from optic flow. We could show that neuronal responses of VS and HS neurons are mainly shaped by the characteristic dynamical properties of the fly’s saccadic flight and gaze strategy. Individual neurons encode information about both, the rotational and the translational components of the animal’s self-motion. Hence, the information carried by individual neurons is ambiguous. The ambiguities can be reduced by considering neuronal population activity. The joint responses of different sub-populations of VS and HS neurons can provide unambiguous information about the three rotational and the three translational components of the animal’s self-motion and also, indirectly, about the 3D layout of the environment.