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PLoS One. 2015 Sep 11;10(9):e0136846. doi: 10.1371/journal.pone.0136846. eCollection 2015.

Nitric Oxide-Mediated Modulation of Central Network Dynamics during Olfactory Perception.

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Department of Bioengineering and Robotics, Graduate School of Engineering, Tohoku University, Sendai, Japan; Graduate School of Pharmaceutical Sciences, University of Tokyo, Tokyo, Japan.
Graduate School of Pharmaceutical Sciences, University of Tokyo, Tokyo, Japan.
Department of Correlative Study in Physics and Chemistry, Graduate School of Integrated Basic Sciences, Nihon University, Tokyo, Japan.
Kagawa School of Pharmaceutical Sciences, Tokushima Bunri University, Sanuki, Japan.
College of Science and Engineering, Kanto Gakuin University, Yokohama, Japan.


Nitric oxide (NO) modulates the dynamics of central olfactory networks and has been implicated in olfactory processing including learning. Land mollusks have a specialized olfactory lobe in the brain called the procerebral (PC) lobe. The PC lobe produces ongoing local field potential (LFP) oscillation, which is modulated by olfactory stimulation. We hypothesized that NO should be released in the PC lobe in response to olfactory stimulation, and to prove this, we applied an NO electrode to the PC lobe of the land slug Limax in an isolated tentacle-brain preparation. Olfactory stimulation applied to the olfactory epithelium transiently increased the NO concentration in the PC lobe, and this was blocked by the NO synthase inhibitor L-NAME at 3.7 mM. L-NAME at this concentration did not block the ongoing LFP oscillation, but did block the frequency increase during olfactory stimulation. Olfactory stimulation also enhanced spatial synchronicity of activity, and this response was also blocked by L-NAME. Single electrical stimulation of the superior tentacle nerve (STN) mimicked the effects of olfactory stimulation on LFP frequency and synchronicity, and both of these effects were blocked by L-NAME. L-NAME did not block synaptic transmission from the STN to the nonbursting (NB)-type PC lobe neurons, which presumably produce NO in an activity-dependent manner. Previous behavioral experiments have revealed impairment of olfactory discrimination after L-NAME injection. The recording conditions in the present work likely reproduce the in vivo brain state in those behavioral experiments. We speculate that the dynamical effects of NO released during olfactory perception underlie precise odor representation and memory formation in the brain, presumably through regulation of NB neuron activity.

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