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.

Synaptic transfer of dynamic motion information between identified neurons in the visual system of the blowfly

“…4A, B; see also Warzecha et al, 1998). Precise time locking of neuronal signals to motion stimuli occurs in fly TCs only after very rapid velocity changes (de Ruyter van Steveninck et al, 2001;Bialek, 1988, 1995;Warzecha and Egelhaaf, 2001). This To account for the rectification nonlinearity due to spike generation and the low spontaneous activity of V1, the presynaptic membrane potential traces and the velocity traces were rectified.…”

Variability of blowfly head optomotor responses

“…All variability at the level of those TCs that mediate optomotor head movements should affect the variability of the behavioural response. The variability of TCs has been thoroughly characterised in the last two decades (Borst and Theunissen, 1999;Egelhaaf, 2006;Egelhaaf and Warzecha, 1999;Egelhaaf et al, 2005;Grewe et al, 2003;Karmeier et al, 2005;Lewen et al, 2001;Nemenman et al, 2008;Ruyter van Steveninck et al, 2001;Warzecha and Egelhaaf, 2001). Karmeier and colleagues determined the response variability of a TC (VS1) with response properties very similar to VS2 and VS3.…”

“…Flies, despite their small brains, are capable of executing virtuosic flight manoeuvres, requiring that the sensory information is reliably processed and transformed into motor behaviour (Egelhaaf and Borst, 1993;Frye and Dickinson, 2001;Hengstenberg, 1993;Schilstra and van Hateren, 1998). The variability of visual information processing in the nervous system of flies was the subject of many studies in the last few years (Borst and Theunissen, 1999;Egelhaaf and Warzecha, 1999;Egelhaaf et al, 2005;Grewe et al, 2003;Grewe et al, 2007;Haag and Borst, 1997;Juusola et al, 1994;Ruyter van Steveninck and Laughlin, 1996;Ruyter van Steveninck et al, 2001;Warzecha and Egelhaaf, 1999;Warzecha and Egelhaaf, 2001;Warzecha et al, 1998;Warzecha et al, 2000). Compared with the detailed characterisation of the variability of the neuronal responses in the fly's visual motion pathway, relatively little is known about the consequences of this variability for behavioural performance.…”

Neural Coding of Natural Stimuli: Information at Sub-Millisecond Resolution

“…But the natural visual world of flies involves not only the enormous angular velocities associated with acrobatic flight; natural light intensities and the dynamic range of their variations are very large as well, and both of the fly's compound eyes are stimulated over more than 2p steradians. All of these features are difficult to replicate in the laboratory [21]. As an alternative, we have moved our experiments outside [9], so that flies experience the scenes from the region in which they were caught.…”