Oscillatory neural activities have been implicated in various types of information processing in the CNS. The procerebral (PC) lobe of the land mollusk Limax valentianus shows an ongoing oscillatory local field potential (LFP). Olfactory input increases both the frequency and spatial synchrony of the LFP oscillation by a nitric oxide (NO)-mediated mechanism, but how NO modulates the activity in a specific manner has been unclear. In the present study, we used electrical stimulation and NO uncaging to systematically analyze the response of the LFP oscillation, and found phase-dependent effects on phase shifting and synchrony. The neurons that presumably release NO in the PC lobe preferentially fired at phases in which NO has a synchronizing effect, suggesting that the timing of NO release is regulated to induce a stereotyped response to natural sensory stimuli. The phase-response curve (PRC) describes the timing dependence of responses of an oscillatory system to external input. PRCs are usually constructed by recording the temporal shifts of the neural activity in response to brief electrical pulses. However, NO evokes a long-lasting depolarization persisting for several cycles of oscillation. The phase-response relationship obtained by NO stimulation was approximately the integral of the PRC. A similar relationship was also shown for regular firing of mouse cerebellar Purkinje cells receiving step depolarization, suggesting the generality of the results to oscillatory neural systems with highly distinct properties. These results indicate novel dynamic effects of long-lasting inputs on network oscillation and synchrony, which are based on simple and ubiquitous mechanisms.
Significance Statement: Oscillatory neural activities are modulated by sensory stimuli in a stereotyped manner, while isolated networks display a variety of responses to stimuli. We investigated how nitric oxide-mediated input to a molluscan olfactory center modulates the oscillatory network activity, and found that its effect on network synchrony was variable depending on the stimulus phase. This suggests that the input timing should be regulated for stereotyped response to sensory stimuli, and we found that feedback inhibition of the NO-producing neurons by the rhythm-generating neurons serves to restrict the spike phase. These results suggest a novel mechanism essential for sensory processing in oscillatory networks.
Authors report no conflict of interest.
Japan Society for the Promotion of Science (JSPS).