Temporal precision of the encoding of motion information by visual interneurons

Background: There is much controversy about the timescale on which neurons process and transmit information. On the one hand, a vast amount of information can be processed by the nervous system if the precise timing of individual spikes on a millisecond timescale is important. On the other hand, neuronal responses to identical stimuli often vary considerably and stochastic response fluctuations can exceed the mean response amplitude. Here, we examined the timescale on which neural responses could be locked to visual motion stimuli. Results: Spikes of motion-sensitive neurons in the visual system of the blowfly are time-locked to visual motion with a precision in the range of several tens of milliseconds. Nevertheless, different motion-sensitive neurons with largely overlapping receptive fields generate a large proportion of spikes almost synchronously. This precision is brought about by stochastic rather than by: motion-induced membrane-potential fluctuations elicited by the common peripheral input. The stochastic membrane-potential fluctuations contain more power at frequencies above 30-40 Hz than the motion-induced potential changes. A model of spike generation indicates that such fast membrane-potential changes are a major determinant of the precise timing of spikes. Conclusions: The timing of spikes in neurons of the motion pathway of the blowfly is controlled on a millisecond timescale by fast membrane-potential fluctuations. Despite this precision, spikes do not lock to motion stimuli on this timescale because visual motion does not induce sufficiently rapid changes in the membrane potential.