Amplitude and Frequency Dependence of Spike Timing: Implications for Dynamic Regulation

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Abstract
The spike-time reliability of motoneurons in the Aplysia buccal motor ganglion was studied as a function of the frequency content and the relative amplitude of the fluctuations in the neuronal input, calculated as the coefficient of variation (CV). Measurements of spike-time reliability to sinusoidal and aperiodic inputs, as well as simulations of a noisy leaky integrate-and-fire neuron stimulated by spike trains drawn from a periodically modulated process, demonstrate that there are three qualitatively different CV-dependent mechanisms that determine reliability: noise-dominated (CV < 0.05 for Aplysia motoneurons) where spike timing is unreliable regardless of frequency content; resonance-dominated (CV ≈ 0.05–0.25) where reliability is reduced by removal of input frequencies equal to motoneuron firing rate; and amplitude-dominated (CV >0.35) where reliability depends on input frequencies greater than motoneuron firing rate. In the resonance-dominated regime, changes in the activity of the presynaptic inhibitory interneuron B4/5 alter motoneuron spike-time reliability. The increases or decreases in reliability occur coincident with small changes in motoneuron spiking rate due to changes in interneuron activity. Injection of a hyperpolarizing current into the motoneuron reproduces the interneuron-induced changes in reliability. The rate-dependent changes in reliability can be understood from the phase-locking properties of regularly spiking motoneurons to periodic inputs. Our observations demonstrate that the ability of a neuron to support a spike-time code can be actively controlled by varying the properties of the neuron and its input.