Transfer of visual motion information via graded synapses operates linearly in the natural activity range

Synaptic transmission between a graded potential neuron and a spiking neuron was investigated in vivo using sensory stimulation instead of artificial excitation of the presynaptic neuron. During visual motion stimulation, individual presynaptic and postsynaptic neurons in the brain of the fly were electrophysiologically recorded together with concentration changes of presynaptic calcium (Delta [Ca2+](pre)). Preferred-direction motion leads to depolarization of the presynaptic neuron. It also produces pronounced increases in [Ca2+](pre) and the postsynaptic spike rate. Motion in the opposite direction was associated with hyperpolarization of the presynaptic cell but only a weak reduction in [Ca2+](pre) and the postsynaptic spike rate. Apart from this rectification, the relationships between presynaptic depolarizations, Delta [Ca2+](pre), and postsynaptic spike rates are, on average, linear over the entire range of activity levels that can be elicited by sensory stimulation. Thus, the inevitably limited range in which the gain of overall synaptic signal transfer is constant appears to be adjusted to sensory input strengths.