Our preceding paper presented a relaxation oscillator model generally applicable to the description of the spike generation zone of an afferent nerve fiber. This model was shown to reproduce the measured stimulus-response characteristics of the elasmobranch ampullary electroreceptor. In this paper, our optimized model is shown to resolve input stimulus currents or current shifts as small as 50 fA. The fractional spike generator frequency shift produced by injection of this minimum resolvable current is A f/f ~ 2 x 10-3. Arguments based upon known properties of both glutamatergic postsynaptic membrane channels and the electroreceptor organ suggest that this resolvability substantially exceeds that required to account for the known sensitivity of elasmobranch fish to marine electric fields. Our estimates of synaptic input current noise indicate that it will limit the minimum resolvable fractional change of synaptic input current to the range 10-1 _ 10-z and will thereby limit the minimum resolvable in vivo spike generator fractional frequency shift to the same range. For our optimized model, increase of the minimum resolvable fractional shift of spike generator frequency into this range can be accomplished by injection of 'white' stimulus current noise of ~ 1 pA rms, over a bandwidth of 4-200 Hz. These results lead to the conclusion that synaptic input current noise, rather than inherent spike generator stability, limits electroreceptive sensitivity in vivo. This noise limit is also consistent with the Weber-Fechner criterion derived from psychophysical studies, which places the minimum resolvable fractional change of input stimulus in this same range. We suggest that synaptic current noise provides the physiological basis for the Weber-Fechner criterion. The model studies of this and the preceding paper indicate that the remarkable electroreceptive sensitivity exhibited by marine elasmobranches can be accounted for within the framework of well-known physical principles, with no requirement of ad hoc assumptions relating to the structure or function of the electroreceptor organ.