Noisy inputs and the induction of on-off switching behavior in a neuronal pacemaker

Neuronal oscillators can function as bistable toggle switches, flipping between quiescence and rhythmic firing in response to an input stimulus. In theory, such switching should be sensitive to small noisy inputs if the bistable states are in close proximity, which we test here using a perfused squid axon preparation. We find that small noisy stimulus currents induce a multitude of paths between two nearby stable states: repetitive firing and quiescence. The pattern of on-off switching of the pacemaker depends on the intensity, spectral properties, and phase angle of stimulus current fluctuations. Analysis by spike-triggered averaging of the stimulus currents near the transitions reveals that sinusoidal stimuli timed antiphase or in phase with repetitive firing correlates with switching of the pacemaker off or on, respectively. Our results reveal a distinct form of bistability in which noise can either silence pacemaker activity, trigger repetitive firing, or induce sporadic burst patterns similar to those recorded in a variety of normal and pathological neurons.