Analysis and simulation of gain control and precision in crayfish visual interneurons

Impulse trains in sustaining and dimming fibers of crayfish optic lobe (in situ) were elicited with sinusoidal extrinsic current and sine-wave illumination. Extrinsic currents and currents derived from postsynaptic potentials (PSPs) were used to compute the time course of the spike train with an adaptive integrate-and-fire model. The neurons exhibit variations in gain and spike timing precision related to the frequency of stimulation. These phenomena are influenced by spike-frequency adaptation and nonlinearities in the PSP. Dimming fibers exhibit relatively strong spike-frequency adaptation and an associated increase in gain with the frequency of sinusoidal extrinsic current and sine-wave illumination. The dimming fiber IPSP promotes spike train rectification, and rectification contributes to spike timing precision. Sustaining fibers exhibit weaker spike-frequency adaptation and the gain of the current-elicited response is less sensitive to stimulus frequency. The sustaining fiber excitatory PSP, however, exhibits a strong frequency-dependent nonlinearity that influences the frequency response. Spike timing precision is a function of stimulus frequency in all cells and it is enhanced by rectification of the discharge and/or resonance. In rectified responses the jitter in spike times is closely related to the variance in the times the membrane potential reaches spike threshold. These gain and spike timing results are well approximated by the simulated responses. Because the nonlinearity of the sustaining fiber PSP entails a high rate of depolarization, the PSP can increase the precision of spike timing by 10- to 100-fold compared with the response to pure sine-wave stimuli. This enhanced precision has implications for crayfish oculomotor reflexes that are driven by sustaining fibers and highly sensitive to impulse timing during transient excitation.