Theory and evidence of amplitude control by frequency detuning in a coupled neuronal oscillator system.

Abstract

Neuronal oscillator circuits that generate rhythmic movements must operate flexibly and reliably to produce the varied motor patterns that animals exhibit naturally. Rodents rhythmically "whisk" their vibrissae for haptic perception, and they dynamically adjust the whisking range to serve different perceptual goals. Whisking is controlled by a brainstem oscillator circuit that is coupled to breathing, yet how whisking amplitude is modulated remains unknown. Here we propose and evaluate an amplitude control mechanism based on principles of synchronization in coupled oscillators. Specifically, a re-analysis of rat behavioral data demonstrates that whisking exhibits kinematic signatures and phase dynamics of amplification via entrainment with "sniffing", a mode of high-frequency breathing. A neuronal network model of the whisking oscillator circuit suggests that whisking amplitude can be modulated by shifting the oscillator's intrinsic frequency relative to the sniffing frequency, analogous to the engineering technique of "detuning". Based on these results, we propose that detuning between coupled neuronal oscillators may represent a general computational strategy for gain control in nervous systems.