Abstract
Nitric oxide is emerging as an important modulator of many physiological processes including olfaction, yet the function of this gas in the processing of olfactory information remains poorly understood. In the antennal lobe of the moth, Manduca sexta, nitric oxide is produced in response to odor stimulation, and many interneurons express soluble guanylyl cyclase, a well-characterized nitric oxide target. We used intracellular recording and staining coupled with pharmacological manipulation of nitric oxide and soluble guanylyl cyclase to test the hypothesis that nitric oxide modulates odor responsiveness in olfactory interneurons through soluble guanylyl cyclase-dependent pathways. Nitric oxide synthase inhibition resulted in pronounced effects on the resting level of firing and the responses to odor stimulation in most interneurons. Effects ranged from bursting to strong attenuation of activity and were often accompanied by membrane depolarization coupled with a change in input resistance. Blocking nitric oxide activation of soluble guanylyl cyclase signaling mimicked the effects of nitric oxide synthase inhibitors in a subset of olfactory neurons, while other cells were differentially affected by this treatment. Together, these results suggest that nitric oxide is required for proper olfactory function, and likely acts through soluble guanylyl cyclase-dependent and -independent mechanisms in different subsets of neurons.
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Abbreviations
- 7NI:
-
7-Nitroindazole
- AC:
-
Anterior cell body cluster
- AL:
-
Antennal lobe
- cGMP:
-
Cyclic guanosine monophosphate
- LC:
-
Lateral cell body cluster
- L-NAME:
-
N-Nitro-l-arginine methyl ester
- LNs:
-
Local interneurons
- LY:
-
Lucifer yellow
- MC:
-
Medial cell body cluster
- MGC:
-
Macroglomerular complex
- NO:
-
Nitric oxide
- NOS:
-
Nitric oxide synthase
- ODQ:
-
1H-[1,2,4]Oxadiazolo[4,3-a]quinoxalin-1-one
- ORN:
-
Olfactory receptor neuron
- PNs:
-
Projection interneurons
- PIa:
-
Projections via the inner cerebral tract
- POa :
-
Projections via the outer cerebral tract
- RMP:
-
Resting membrane potential
- sGC:
-
Soluble guanylyl cyclase
- sGCir:
-
sGC-immunoreactive
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Acknowledgments
This work was supported by the National Institutes of Health-National Institute on Deafness and Other Communication Disorders Grants DC04292 to A.N. and DC005652 to T.C., and through a Ruth L. Kirschstein Individual Predoctoral Fellowship DC006368 to C.W. The authors also wish to thank Dr. Hong Lei, Dr. Carolina Reisenman, Dr. Andrew Dacks, and Jinhui Zhang for help with data and statistical analyses, as well as members of the Hildebrand laboratory for helpful discussions. We also appreciate help from Patricia Jansma for assistance with confocal microscopy, and Suzanne Mackzum for rearing M. sexta at the Arizona Research Laboratories, Division of Neurobiology. The experiments comply with the “Principles of animal care”, publication No. 86–23, revised 1985 of the National Institute of Health, and also with the current laws of the United States of America.
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Wilson, C.H., Christensen, T.A. & Nighorn, A.J. Inhibition of nitric oxide and soluble guanylyl cyclase signaling affects olfactory neuron activity in the moth, Manduca sexta . J Comp Physiol A 193, 715–728 (2007). https://doi.org/10.1007/s00359-007-0227-9
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DOI: https://doi.org/10.1007/s00359-007-0227-9