Cooperative Phase Adaptation and Amplitude Amplification of Neuronal Activity in the Vagal Complex: An Interplay Between Microcircuits and Macrocircuits

Clusters of neurons can communicate with others through the cross-frequency coupling mechanism of oscillatory synchrony. We addressed the hypothesis that neuronal networks at various levels from micro- to macrocircuits implement this communication strategy. An abundance of local recurrent axons of vagal complex (VC) cells establish dense local microcircuits and seem to generate high-frequency noise-causing stochastic resonance (reverberation) and coherence resonance, even in in vitro slice preparations. These phenomena were observed in vitro as the generation of episodes of higher-frequency noise after an external stimulation and as stimulus-induced or spontaneous high-amplitude signals (postsynaptic activities). The in vitro microcircuit networks rarely sustained the stochastic resonance and coherence resonance cooperatively; however, in vivo networks involving additional intrabulbar mesocircuits and large-scale macrocircuits were able to sustain them cooperatively. This gave rise to large-scale oscillatory synchrony leading to robust power and coherence of signals with high amplitudes, reaching several millivolts in amplitude from a noise level of ~100 microV through cardiorespiratory frequency coupling. A regenerative mechanism of neuronal circuits might work for the generation of large-scale oscillatory synchrony. The amplitude and phase of neuronal activity in vivo may interact cooperatively to give rise to varying degrees of power and coherence of robust rhythmic activity for distinct physiological roles. The cooperative interaction between phase adaptation and amplitude amplification of neuronal activity may provide diverse nervous systems with both robustness and resilience.