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The Journal of Neuroscience, July 7, 2004, 24(27):6070-6077; doi:10.1523/JNEUROSCI.0710-04.2004
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Cellular/Molecular
Odorant-Evoked Nitric Oxide Signals in the Antennal Lobe of Manduca sexta
Chad Collmann,1 Mikael A. Carlsson,2 Bill S. Hansson,2 andAlan Nighorn1 1Arizona Research Laboratories, Division of Neurobiology, University of Arizona, Tucson, Arizona 85721, and 2Division of Chemical Ecology, Department of Crop Science, Swedish University of Agricultural Sciences, S-230 53 Alnarp, Sweden
The gaseous signaling molecule nitric oxide (NO) can affect the activities of neurons and neural networks in many different systems. The strong expression of NO synthase (NOS) in the primary synaptic neuropil (the antennal lobe in insects and the olfactory bulb in vertebrates) of the olfactory system of most organisms, and the unique spheroidal geometry of olfactory glomeruli in those neuropils, have led to suggestions that NO signaling is important for processing olfactory information. No direct evidence exists, however, that NO signals are produced in olfactory glomeruli. We investigated the production of NO in the antennal lobe of the moth, Manduca sexta, by using immunocytochemistry and real-time optical imaging with a NO-sensitive fluorescent marker, diaminofluorescein diacetate. We confirmed that NOS was expressed in the axons of olfactory receptor neurons projecting to all glomeruli. Soluble guanylyl cyclase, the best characterized target of NO, was found in a subset of postsynaptic antennal lobe neurons that included projection neurons, a small number of GABA-immunoreactive neurons, and a serotonin-immunoreactive neuron. We found that odorant stimulation evoked NO signals that were reproducible and spatially focused. Different odorants evoked spatially distinct patterns of NO production. Increased concentrations of pheromone and plant odorants caused increases in peak signal intensity. Increased concentrations of plant odorants also evoked a dramatic increase in signal area. The results of these experiments show clearly that odorant stimulation can evoke NO production in the olfactory system. The NO signals produced are likely to play an important role in processing olfactory information.
Key words: diaminofluorescein; nitric oxide synthase; moth; olfactory; optical imaging; soluble guanylyl cyclase
Received Feb 27, 2004; revised May 5, 2004; accepted May 22, 2004.
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