Inhibition of nitric oxide and soluble guanylyl cyclase signaling affects olfactory neuron activity in the moth, Manduca sexta

Journal of Comparative Physiology A: Neuroethology, Sensory, Neural, and Behavioral Physiology

Volumn 193, Issue 7, 2007, Pages 715-728

  Wilson, Caroline H ^a,b   Christensen, Thomas A ^a   Nighorn, Alan J ^a  

^a UNIVERSITY OF ARIZONA   (United States)

^b UNIVERSITY OF HAWAII   (United States)

Author keywords

Insect; Nitric oxide; Odor coding; Olfaction; Soluble guanylyl cyclase

Indexed keywords

CELL RECEPTOR; ENZYME INHIBITOR; GUANYLATE CYCLASE; NITRIC OXIDE; SOLUBLE GUANYLYL CYCLASE; UNCLASSIFIED DRUG;

ACTION POTENTIAL; ANIMAL; ARTICLE; DRUG EFFECT; DRUG INTERACTION; ELECTROSTIMULATION; IN VITRO STUDY; LEPIDOPTERA; MALE; METABOLISM; NERVE CELL INHIBITION; ODOR; OLFACTORY RECEPTOR; PHYSIOLOGY; RADIATION EXPOSURE;

ACTION POTENTIALS; ANIMALS; DRUG INTERACTIONS; ELECTRIC STIMULATION; ENZYME INHIBITORS; GUANYLATE CYCLASE; MALE; MANDUCA; NEURAL INHIBITION; NITRIC OXIDE; ODORS; OLFACTORY RECEPTOR NEURONS; RECEPTORS, CYTOPLASMIC AND NUCLEAR;

EID: 34447119484     PISSN: 03407594     EISSN: 14321351     Source Type: Journal    
DOI: 10.1007/s00359-007-0227-9     Document Type: Article

References (41)

1. Ahern G, Klyachko V, Jackson M (2002) cGMP and S-nitrosylation: two routes for modulation of neuronal excitability by NO. TINS 25:510-517 doi:10.1016/S0166-2236(02)02254-3
2. Alonso JR, Porteros A, Crespo C, Arevalo R, Brinon JG, Weruaga E, Aijon J (1998) Chemical anatomy of the macaque monkey olfactory bulb: NADPH-diaphorase/nitric oxide synthase activity. J Comp Neurol 402:419-434 doi:10.1002/(SICI)1096-9861(19981221)402:3<419::AID-CNE9>3.0.CO;2-C
3. Bicker G, Schmachtenberg O, De Vente J (1996) The nitric oxide/cyclic GMP messenger system in olfactory pathways of the locust brain. Eur J Neurosci 8:2635-2643 doi:10.1111/j.1460-9568.1996.tb01558.x
4. Bredt DS, Glatt CE, Hwang PM, Fotuhi M, Dawson TM, Snyder SH (1991) Nitric oxide synthase protein and mRNA are discretely localized in neuronal populations of the mammalian CNS together with NADPH diaphorase. Neuron 7:615-624 doi:10.1016/0896-6273(91)90374-9
5. Breer H, Shepherd GM (1993) Implications of the NO/cGMP system for olfaction. Trends Neurosci 16:5-9 doi:10.1016/0166-2236(93)90040-S
6. Castel H, Vaudry H (2001) Nitric oxide directly activates GABA(A) receptor function through a cGMP/protein kinase-independent pathway in frog pituitary melanotrophs. J Neuroendocrinol 13:695-705 doi:10.1046/j.1365-2826. 2001.00683.x
7. Chase R, Tolloczko B (1986) Synaptic glomeruli in the olfactory system of a snail, Achatina fulica. Cell Tissue Res 246:567-573 doi: 10.1007/BF00215198
8. Christensen T, Hildebrand J (1987) Male-specific, sex pheromone-selective projection neurons in the antennal lobes of the moth Manduca sexta. J Comp Physiol A 160:553-569 doi:10.1007/BF00611929
9. Christensen TA, Waldrop B, Harrow I, Hildebrand JG (1993) Local interneurons and information processing in the olfactory glomeruli of the moth Manduca sexta. J Comp Physiol 173:385-399 doi:10.1007/BF00193512
10. Christensen TA, Waldrop BR, Hildebrand J (1998a) GABAergic mechanisms that shape the temporal response to odors in moth olfactory projection neurons. In: Murphy C (ed) Olfaction and taste. Ann N Y Acad Sci, NY, pp 475-481
11. Christensen TA, Waldrop BR, Hildebrand JG (1998b) Multitasking in the olfactory system: context-dependent responses to odors reveal dual GABA-regulated coding mechanisms in single olfactory projection neurons. J Neurosci 18:5999-6008
12. Collmann C, Carlsson MA, Hansson BS, Nighorn A (2004) Odorant-evoked nitric oxide signals in the antennal lobe of Manduca sexta. J Neurosci 24:6070-6077 doi:10.1523/JNEUROSCI.0710-04.2004
13. Elphick MR, Jones IW (1998) Localization of soluble guanylyl cyclase alpha-subunit in identified insect neurons. Brain Res 800:174-179 doi:10.1016/S0006-8993(98)00522-8
14. Elphick M, Rayne R, Riveros-Moreno VV, Moncada S, Shea M (1995) Nitric oxide synthesis in locust olfactory interneurones. J Exp Biol 198:821-829
15. Fujie S, Aonuma H, Ito I, Gelperin A, Ito E (2002) The nitric oxide/cyclic GMP pathway in the olfactory processing system of the terrestrial slug Limax marginatus. Zool Sci 19:15-26 doi:10.2108/zsj.19.15
16. Fujie S, Yamamoto T, Murakami J, Hatakeyama D, Shiga H, Suzuki N, Ito E (2005) Nitric oxide synthase and soluble guanylyl cyclase underlying the modulation of electrical oscillations in a central olfactory organ. J Neurobiol 62:14-30 doi:10.1002/neu.20046
17. Garthwaite J, Boulton CL (1995) Nitric oxide signaling in the central nervous system. Annu Rev Physiol 57:683-706 doi: 10.1146/annurev.ph.57.030195. 003343
18. Garthwaite J, Southam E, Boulton CL, Nielsen EB, Schmidt K, Mayer B (1995) Potent and selective inhibition of nitric oxide-sensitive guanylyl cyclase by 1H-[1,2,4]oxadiazolo[4,3-a]quinoxalin-1-one. Mol Pharmacol 48:184-188
19. Gelperin A (1994) Nitric oxide mediates network oscillations of olfactory interneurons in a terrestrial mollusc. Nature 369:61-63 doi:10.1038/369061a0
20. Gelperin A, Flores J, Raccuia-Behling F, Cooke IR (2000) Nitric oxide and carbon monoxide modulate oscillations of olfactory interneurons in a terrestrial mollusk. J Neurophysiol 83:116-127
21. Hansson BS, Carlsson MA, Kalinova B (2003) Olfactory activation patterns in the antennal lobe of the sphinx moth, Manduca sexta. J Comp Physiol A 189:301-308
22. Homberg U, Montague RA, Hildebrand JG (1988) Anatomy of antenno-cerebral pathways in the brain of the sphinx moth Manduca sexta. Cell Tissue Res 254:255-281 doi:10.1007/BF00225800
23. Hopkins DA, Steinbusch HW, Markerink-van Ittersum M, De Vente J (1996) Nitric oxide synthase, cGMP, and NO-mediated cGMP production in the olfactory bulb of the rat. J Comp Neurol 375:641-658 doi:10.1002/(SICI)1096-9861(19961125) 375:4<641::AID-CNE6>3.0.CO;2-1
24. Hosler JS, Buxton KL, Smith BH (2000) Impairment of olfactory discrimination by blockade of GABA and nitric oxide activity in the honeybee antennal lobes. Behav Neurosci 114:514-525 doi:10.1037/0735-7044.114.3.514
25. Inoue T, Watanabe S, Kawahara S, Kirino Y (2000) Phase-dependent filtering of sensory information in the oscillatory olfactory center of a terrestrial mollusk. J Neurophysiol 84:1112-1115
26. Kendrick KM, Guevara-Guzman R, Zorrilla J, Hinton MR, Broad KD, Mimmack M, Ohkura S (1997) Formation of olfactory memories mediated by nitric oxide. Nature 388:670-674 doi:10.1038/41765
27. Lei H, Christensen TA, Hildebrand JG (2002) Local inhibition modulates odor-evoked synchronization of glomerulus-specific output neurons. Nat Neurosci 5:557-565 doi:10.1038/nn859
28. Li Z, Chapleau MW, Bates JN, Bielefeldt K, Lee HC, Abboud FM (1998) Nitric oxide as an autocrine regulator of sodium currents in baroreceptor neurons. Neuron 20:1039-1049 doi:10.1016/S0896-6273(00)80484-5
29. Matsumoto S, Hildebrand J (1981) Olfactory mechanisms in the moth Manduca sexta: response characteristics and morphology of central neurons in the antennal lobes. Proc R Soc Lond 213:249-277
30. Moore PK, Handy RL (1997) Selective inhibitors of neuronal nitric oxide synthase-is no NOS really good NOS for the nervous system? Trends Pharmacol Sci 18:204-211
31. Müller U (1996) Inhibition of nitric oxide synthase impairs a distinct form of long-term memory in the honeybee, Apis mellifera. Neuron 16:541-549 doi:10.1016/S0896-6273(00)80073-2
32. Müller U, Hildebrandt H (1995) The nitric oxide/cGMP system in the antennal lobe of Apis mellifera is implicated in integrative processing of chemosensory stimuli. Eur J Neurosci 7:2240-2248 doi:10.1111/j.1460-9568.1995. tb00645.x
33. Nighorn AJ, Gibson NJ, Rivers DM, Hildebrand JG, Morton DB (1998) The nitric oxide-cGMP pathway may mediate communication between sensory afferents and projection neurons in the antennal lobe of Manduca sexta. J Neurosci 18:7244-7255
34. Prast H, Philippu A (2001) Nitric oxide as modulator of neuronal function. Prog Neurobiol 64:51-68 doi:10.1016/S0301-0082(00)00044-7
35. Sakura M, Kabetani M, Watanabe S, Kirino Y (2004) Impairment of olfactory discrimination by blockade of nitric oxide activity in the terrestrial slug Limax valentianus. Neurosci Lett 370:257-261 doi:10.1016/j.neulet.2004.08.025
36. Samama B, Boehm N (1999) Inhibition of nitric oxide synthase impairs early olfactory associative learning in newborn rats. Neurobiol Learn Mem 71:219-231 doi:10.1006/nlme.1998.3869
37. Teyke T, Gelperin A (1999) Olfactory oscillations augment odor discrimination not odor identification by Limax CNS. Neuroreport 10:1061-1068
38. Waldrop B, Christensen TA, Hildebrand J (1987) GABA-mediated synaptic inhibition of projection neurons in the antennal lobes of the sphinx moth, Manduca sexta. J Comp Physiol 161:23-32 doi:10.1007/BF00609452
39. White RE (1999) Cyclic GMP and ion channel regulation. Adv Second Messenger Phosphoprotein Res 33:251-277
40. Wilson C (2005) An examination of the effects and possible targets of nitric oxide in olfactory neurons in the moth, Manduca sexta. Ph.D thesis. University of Arizona
41. Wilson C, Christensen T, Nighorn A (2003) The effects of nitric oxide on synaptic inhibition in the antennal lobe of Manduca sexta. Soc Neurosci Abstr 821.19