Precise timing in fly motion vision is mediated by fast components of combined graded and spike signals

Firing of an individual neuron is determined by the activity of its presynaptic input ensemble. In this study we analyzed how presynaptic signals with different dynamics interact to control postsynaptic activity. In the blowfly's visual system we simultaneously recorded in vivo from an identified motion-sensitive neuron and from elements of the presynaptic ensemble. The presynaptic cells themselves are mutually electrically coupled and convey both graded and spike signals to their common postsynaptic target. We elicited spikes in the postsynaptic neuron by voltage-clamping one of the presynaptic neurons to various holding potentials and then analyzed the time course of the holding current. Current transients in the clamped presynaptic cell were found to coincide with postsynaptic spikes. The current transients were highly variable in amplitude and occasionally absent during postsynaptic spiking. These characteristics indicate that the current transients in the voltage-clamped neuron result from spikes in electrically coupled co-members of the presynaptic ensemble. Our results suggest that electrical coupling among presynaptic neurons mediates synchronization of spikes within the cell ensemble. Moreover, our findings demonstrate that the graded response component of the presynaptic cells effectively controls the postsynaptic firing rate on a coarse scale while the precise timing of the postsynaptic spikes is a consequence of spikes superimposed on the graded signals of the presynaptic neurons.