Extracellular Potentials Modify the Transfer of Information at Photoreceptor Output Synapses in the Blowfly Compound Eye

Abstract

Signal processing in fly photoreceptors and visual interneurons takes place with graded potentials. Photoreceptors drive large monopolar cells (LMCs) with synapses that, like their counterparts in vertebrates, have a high gain and introduce strong spatiotemporal antagonism (Laughlin et al., 1987) that implements predictive coding (Srinivasan et al., 1982). The synapses are contained in compartments, lamina cartridges, whose extracellular potentials change with illumination (Shaw, 1984). We described these extracellular field potentials (FPs) using a novel permeabilization technique that converts neurons into extracellular recording probes. Having characterized extracellular FPs, we went on to study them using conventional microelectrodes. Extracellular space in a cartridge is electrically isolated from the body cavity and retina [input resistance (R(in)) = 6.0 MOmega in dark], and light adaptation increases this isolation (R(in) = 7.8 MOmega). In the dark, the extracellular space is 30 mV hyperpolarized compared with retina, and this promotes tonic synaptic activity by depolarizing the synaptic terminals. Illumination depolarizes the extracellular space, and voltage-clamp studies suggest that the postsynaptic chloride current in LMCs contributes to this light response. The presynaptic transmembrane potential in the photoreceptor axon was estimated by subtracting the FP from intracellular recordings. By backing off the presynaptic input, the FP can reset the synaptic operating range, produce response transients, and contribute to predictive coding by subtracting redundant low frequencies.