Synaptic noise is an information bottleneck in the inner retina during dynamic visual stimulation

Key points At chemical synapses, vesicles fuse with the presynaptic membrane at random, generating noise in postsynaptic currents. To determine how much noise synapses generate, we recorded excitatory postsynaptic currents from ganglion cells in an in vitro preparation of the mammalian retina during flickering visual stimulation. Postsynaptic currents received noise from three sources: substantial noise from bipolar cell synapses, somewhat more from the presynaptic retinal circuitry, but little from sources intrinsic to the ganglion cell. Presynaptic circuit elements but not bipolar cell synapses were significant sources of noise shared by pairs of ganglion cells. Signal-to-noise ratio was substantially reduced from the presynaptic bipolar cell array to the postsynaptic ganglion cell, indicating that synaptic noise can reduce the amount of information transmitted to a neuron. In daylight, noise generated by cones determines the fidelity with which visual signals are initially encoded. Subsequent stages of visual processing require synapses from bipolar cells to ganglion cells, but whether these synapses generate a significant amount of noise was unknown. To characterize noise generated by these synapses, we recorded excitatory postsynaptic currents from mammalian retinal ganglion cells and subjected them to a computational noise analysis. The release of transmitter quanta at bipolar cell synapses contributed substantially to the noise variance found in the ganglion cell, causing a significant loss of fidelity from bipolar cell array to postsynaptic ganglion cell. Virtually all the remaining noise variance originated in the presynaptic circuit. Circuit noise had a frequency content similar to noise shared by ganglion cells but a very different frequency content from noise from bipolar cell synapses, indicating that these synapses constitute a source of independent noise not shared by ganglion cells. These findings contribute a picture of daylight retinal circuits where noise from cones and noise generated by synaptic transmission of cone signals significantly limit visual fidelity.