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

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.Author summary: Animals generate a multitude of rhythmic movement behaviors that enable them to interact with their environment, such as ventilating, locomoting, eating, and active sensing. Though these movements are highly structured, animals must implement them flexibly and adaptively to meet the demands of the environment. How do networks of neurons that generate the oscillatory neuronal activity for these movements enable this important flexibility? Here we focus on rodents’ use of their vibrissae (whiskers) to explore their environment by rhythmically scanning the tactile landscape around their faces. Through quantitative analyses of behavioral data and computational modeling, we show that rodents can exploit the difference in frequency between two interacting neuronal oscillator networks to dynamically adjust the size of their vibrissae movements, much like tuning a radio toward or away from a station adjusts the signal strength. Beyond the neuronal control of movement, interactions between brain rhythms with different underlying frequencies seem to be a ubiquitous phenomenon observed in studies of diverse cognitive processes. Based on such observations, we suggest that frequency-based amplitude control like this may represent a more general computational strategy utilized by nervous systems.