Real time encoding of motion: Answerable questions and questionable answers from the fly's visual system

Abstract

In the past decade, a small corner of the fly's visual system has become an important testing ground for ideas about coding and computation in the nervous system. A number of results demonstrate that this system operates with a precision and efficiency near the limits imposed by physics, and more generally these results point to the reliability and efficiency of the strategies that nature has selected for representing and processing visual signals. A recent series of papers by Egelhaaf and coworkers, however, suggests that almost all these conclusions are incorrect. In this contribution we place these controversies in a larger context, emphasizing that the arguments are not just about flies, but rather about how we should quantify the neural response to complex, naturalistic inputs. As an example, Egelhaaf et al. (and many others) compute certain correlation functions and use the apparent correlation times as a measure of temporal precision in the neural response. This analysis neglects the structure of the correlation function at short times, and we show how to analyze this structure to reveal a temporal precision 30 times better than suggested by the correlation time; this precision is confirmed by a much more detailed information theoretic analysis. In reviewing other aspects of the controversy, we find that the analysis methods used by Egelhaaf et al. suffer from some mathematical inconsistencies, and that in some cases we are unable to reproduce their experimental results. Finally, we present results from new experiments that probe the neural response to inputs that approach more closely the natural context for freely flying flies. These new experiments demonstrate that the fly's visual system is even more precise and efficient under natural conditions than had been inferred from our earlier work.