Synapses in the fly motion-vision pathway: evidence for a broad range of signal amplitudes and dynamics

Synapses are generally considered to operate efficiently only when their signaling range matches the spectrum of prevailing presynaptic signals in terms of both amplitudes and dynamics. However, the prerequisites for optimally matching the signaling ranges may differ between spike-mediated and graded synaptic transmission. This poses a problem for synapses that convey both graded and spike signals at the same time. We addressed this issue by tracing transmission systematically in vivo in the blowfly's visual-motion pathway by recording from single neurons that receive mixed potential signals consisting of rather slow graded fluctuations superimposed with highly variable spikes from a small number of presynaptic elements. Both pre- and postsynaptic neurons were previously shown to represent preferred-direction motion velocity reliably and linearly at low fluctuation frequencies. To selectively assess the performance of individual synapses and to precisely control presynaptic signals, we voltage clamped one of the presynaptic neurons. Results showed that synapses can effectively convey signals over a much larger amplitude and frequency range than is normally used during graded transmission of visual signals. An explanation for this unexpected finding might lie in the transmission of the spike component that reaches larger amplitudes and contains higher frequencies than graded signals.