Abstract
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.
Highlights
Olfactory signals are transmitted from olfactory sensory neurons in the olfactory epithelium to olfactory centers via fast excitatory synapses, but besides these specific transmissions, olfactory processing is modulated both centrally and peripherally by slow diffusive neuromodulatory systems
When the air was switched to an odorant (0.001% hexanol or garlic), the nitric oxide (NO) concentration in the PC lobe increased by about 2 nM, and after termination of the stimulation, it returned to the pre-stimulus level
For the L-NAME group, Cohen’s d value was 1.68. These results suggest that the signal recorded by the NO electrode arises from NO released in response to olfactory stimulation
Summary
Olfactory signals are transmitted from olfactory sensory neurons in the olfactory epithelium to olfactory centers via fast excitatory synapses, but besides these specific transmissions, olfactory processing is modulated both centrally and peripherally by slow diffusive neuromodulatory systems. Widespread neuromodulatory systems including cholinergic and monoaminergic neurons may mediate context-dependent olfactory processing in the network, such as modification of sensitivity and discriminability by arousal state [1], satiety [2] and olfactory learning [3], and may be related to pathological conditions [4,5]. Gaseous neurotransmitters are another category of neuromodulators, and in olfactory systems, this category includes nitric oxide (NO) and carbon monoxide (CO) [6]. The functions of NO has been well documented in relation to learning, both in vertebrates [12,13,14] and invertebrates [15,16,17,18,19,20,21,22]
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