A Mammalian Retinal Ganglion Cell Implements a Neuronal Computation That Maximizes the SNR of Its Postsynaptic Currents.

Neurons perform computations by integrating excitatory and inhibitory synaptic inputs. Yet, it is rarely understood what computation is being performed, or how much excitation or inhibition this computation requires. Here we present evidence for a neuronal computation that maximizes the signal-to-noise power ratio (SNR). We recorded from OFF delta retinal ganglion cells in the guinea pig retina and monitored synaptic currents that were evoked by visual stimulation (flashing dark spots). These synaptic currents were mediated by a decrease in an outward current from inhibitory synapses (disinhibition) combined with an increase in an inward current from excitatory synapses. We found that the SNR of combined excitatory and disinhibitory currents was voltage sensitive, peaking at membrane potentials near resting potential. At the membrane potential for maximal SNR, the amplitude of each current, either excitatory or disinhibitory, was proportional to its SNR. Such proportionate scaling is the theoretically best strategy for combining excitatory and disinhibitory currents to maximize the SNR of their combined current. Moreover, as spot size or contrast changed, the amplitudes of excitatory and disinhibitory currents also changed but remained in proportion to their SNRs, indicating a dynamic rebalancing of excitatory and inhibitory currents to maximize SNR.SIGNIFICANCE STATEMENT We present evidence that the balance of excitatory and disinhibitory inputs to a type of retinal ganglion cell maximizes the signal-to-noise ratio power ratio (SNR) of its postsynaptic currents. This is significant because chemical synapses on a retinal ganglion cell require the probabilistic release of transmitter. Consequently, when the same visual stimulus is presented repeatedly, postsynaptic currents vary in amplitude. Thus, maximizing SNR may be a strategy for producing the most reliable signal possible given the inherent unreliability of synaptic transmission.