The origins of aperiodicities in sensory neuron entrainment

Aperiodic entrainment to rhythmic sensory input was obtained with either a single neuron or an excitatory network model, without addition of a stochastic or "noisy" element. The entrainment properties of primary sensory neurons were well captured by the dynamics of the Hodgkin-Huxley ordinary differential equations with a quiescent resting state or threshold for spike output. The frequency-amplitude parameter space was compressed and aperiodic regimes were small in comparison to those of periodically activated pacemaker-like neurons. Transitions between phase-locked and aperiodic entrainment patterns were predictable and determined by the equation dynamics, supporting the contention that some aperiodicities observed in situ arise from the inherent membrane properties of neurons. When the rhythmically activated neuron was embedded in an excitatory network of Hodgkin-Huxley neurons with heterogeneous synaptic delays, aperiodic entrainment patterns were more frequently encountered and these were associated with asynchronous output from the network. Embedding the rhythmically activated neuron in a network with synaptic delays greatly reduced the range of entrained spike frequencies and increased the variability in the neuronal firing. The temporal coding of sensory stimuli may be dependent on these findings. Sensory stimuli are signaled in the periphery by a mixture of periodic and irregular interspike intervals. Most models of such temporal codes assume intrinsic rhythmicity arising from the ionic currents, with variations attributed to membrane or synaptic noise. In contrast, we demonstrate irregular neural codes that arise completely in the absence of noise. In the proposed model, the sources of these irregular sensory patterns are the extensive cross-connections and resultant interactions between neurons. The balance between the regular and irregular entrainment of a neuron in situ could uniquely identify a stimulus. Other biological mechanisms of modifying the entrainment properties and promoting aperiodic entrainment are discussed.