Oscillations and variability in neuronal systems: interplay of autonomous transient dynamics and fast deterministic fluctuations

Neuronal systems are subject to rapid fluctuations both intrinsically and externally. These fluctuations can be disruptive or constructive. We investigate the dynamic mechanisms underlying the interactions between rapidly fluctuating signals and the intrinsic properties of the target cells to produce variable and/or coherent responses. We use linearized and non-linear conductance-based models and piecewise constant (PWC) inputs with short duration pieces. The amplitude distributions of the constant pieces consist of arbitrary permutations of a baseline PWC function. In each trial within a given protocol we use one of these permutations and each protocol consists of a subset of all possible permutations, which is the only source of uncertainty in the protocol. We show that sustained oscillatory behavior can be generated in response to various forms of PWC inputs independently of whether the stable equilibria of the corresponding unperturbed systems are foci or nodes. The oscillatory voltage responses are amplified by the model nonlinearities and attenuated for conductance-based PWC inputs as compared to current-based PWC inputs, consistent with previous theoretical and experimental work. In addition, the voltage responses to PWC inputs exhibited variability across trials, which is reminiscent of the variability generated by stochastic noise (e.g., Gaussian white noise). Our analysis demonstrates that both oscillations and variability are the result of the interaction between the PWC input and the target cells autonomous transient dynamics with little to no contribution from the dynamics in vicinities of the steady-state, and do not require input stochasticity.