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

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.

[1]  T Inoue,et al.  Phase-dependent filtering of sensory information in the oscillatory olfactory center of a terrestrial mollusk. , 2000, Journal of neurophysiology.

[2]  J. G. Briñón,et al.  Chemical anatomy of the Macaque monkey olfactory bulb: NADPH‐diaphorase/nitric oxide synthase activity , 1998, The Journal of comparative neurology.

[3]  J Garthwaite,et al.  Nitric oxide signaling in the central nervous system. , 1995, Annual review of physiology.

[4]  A. Gelperin,et al.  Nitric oxide and carbon monoxide modulate oscillations of olfactory interneurons in a terrestrial mollusk. , 2000, Journal of neurophysiology.

[5]  S. Snyder,et al.  Nitric oxide synthase protein and mRNA are discretely localized in neuronal populations of the mammalian CNS together with NADPH diaphorase , 1991, Neuron.

[6]  J. Hildebrand,et al.  GABA-mediated synaptic inhibition of projection neurons in the antennal lobes of the sphinx moth,Manduca sexta , 2004, Journal of Comparative Physiology A.

[7]  I Rovira,et al.  Nitric oxide , 2021, Reactions Weekly.

[8]  B. Smith,et al.  Impairment of olfactory discrimination by blockade of GABA and nitric oxide activity in the honey bee antennal lobes. , 2000 .

[9]  J. Hildebrand,et al.  GABAergic Mechanisms That Shape the Temporal Response to Odors in Moth Olfactory Projection Neurons a , 1998, Annals of the New York Academy of Sciences.

[10]  N. Boehm,et al.  Inhibition of Nitric Oxide Synthase Impairs Early Olfactory Associative Learning in Newborn Rats , 1999, Neurobiology of Learning and Memory.

[11]  F. Abboud,et al.  Nitric Oxide as an Autocrine Regulator of Sodium Currents in Baroreceptor Neurons , 1998, Neuron.

[12]  Takehiro Yamamoto,et al.  Nitric oxide synthase and soluble guanylyl cyclase underlying the modulation of electrical oscillations in a central olfactory organ. , 2005, Journal of neurobiology.

[13]  White Re.  Cyclic GMP and ion channel regulation. , 1999 .

[14]  M. Elphick,et al.  Nitric oxide synthesis in locust olfactory interneurones , 1995, The Journal of experimental biology.

[15]  M. Carlsson,et al.  Odorant-Evoked Nitric Oxide Signals in the Antennal Lobe of Manduca sexta , 2004, The Journal of Neuroscience.

[16]  John G. Hildebrand,et al.  Male-specific, sex pheromone-selective projection neurons in the antennal lobes of the mothManduca sexta , 1987, Journal of Comparative Physiology A.

[17]  Gordon M. Shepherd,et al.  Implications of the NO/cGMP system for olfaction , 1993, Trends in Neurosciences.

[18]  T Teyke,et al.  Olfactory oscillations augment odor discrimination not odor identification by Limax CNS. , 1999, Neuroreport.

[19]  J. Hildebrand,et al.  Multitasking in the Olfactory System: Context-Dependent Responses to Odors Reveal Dual GABA-Regulated Coding Mechanisms in Single Olfactory Projection Neurons , 1998, The Journal of Neuroscience.

[20]  J. Hildebrand,et al.  Olfactory interneurons in the moth Manduca sexta: response characteristics and morphology of central neurons in the antennal lobes , 1981, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[21]  Alan Gelperin,et al.  Nitric oxide mediates network oscillations of olfactory interneurons in a terrestrial mollusc , 1994, Nature.

[22]  Hitoshi Aonuma,et al.  The Nitric Oxide/Cyclic GMP Pathway in the Olfactory Processing System of the Terrestrial Slug Limax marginatus , 2002, Zoological science.

[23]  B. H. Smith,et al.  Impairment of olfactory discrimination by blockade of GABA and nitric oxide activity in the honey bee antennal lobes. , 2000, Behavioral Neuroscience.

[24]  P. Moore,et al.  Selective inhibitors of neuronal nitric oxide synthase--is no NOS really good NOS for the nervous system? , 1997, Trends in pharmacological sciences.

[25]  D B Morton,et al.  The Nitric Oxide–cGMP Pathway May Mediate Communication between Sensory Afferents and Projection Neurons in the Antennal Lobe ofManduca Sexta , 1998, The Journal of Neuroscience.

[26]  Wenner-Grenska samfundet,et al.  Olfaction and taste , 1963 .

[27]  K. Kendrick,et al.  Formation of olfactory memories mediated by nitric oxide , 1997, Nature.

[28]  U. Müller,et al.  The Nitric Oxide/cGMP System in the Antennal Lobe of Apis mellifera is Implicated in Integrative Processing of Chemosensory Stimuli , 1995, The European journal of neuroscience.

[29]  H. Prast,et al.  Nitric oxide as modulator of neuronal function , 2001, Progress in Neurobiology.

[30]  H. Vaudry,et al.  Nitric Oxide Directly Activates GABAA Receptor Function Through a cGMP/Protein Kinase‐Independent Pathway in Frog Pituitary Melanotrophs , 2001, Journal of neuroendocrinology.

[31]  M. Carlsson,et al.  Olfactory activation patterns in the antennal lobe of the sphinx moth, Manduca sexta , 2003, Journal of Comparative Physiology A.

[32]  R. Chase,et al.  Synaptic glomeruli in the olfactory system of a snail, Achatina fulica , 1986, Cell and Tissue Research.

[33]  R. Weinberg,et al.  Localization of soluble guanylyl cyclase in the superficial dorsal horn , 2006, The Journal of comparative neurology.

[34]  Meyer B. Jackson,et al.  cGMP and S-nitrosylation: two routes for modulation of neuronal excitability by NO , 2002, Trends in Neurosciences.

[35]  J. Garthwaite,et al.  Potent and selective inhibition of nitric oxide-sensitive guanylyl cyclase by 1H-[1,2,4]oxadiazolo[4,3-a]quinoxalin-1-one. , 1995, Molecular pharmacology.

[36]  J. Vente,et al.  The Nitric Oxide/Cyclic GMP Messenger System in Olfactory Pathways of the Locust Brain , 1996, The European journal of neuroscience.

[37]  Hong Lei,et al.  Local inhibition modulates odor-evoked synchronization of glomerulus-specific output neurons , 2002, Nature Neuroscience.

[38]  J. Hildebrand,et al.  Local interneurons and information processing in the olfactory glomeruli of the moth Manduca sexta , 1993, Journal of Comparative Physiology A.

[39]  M. Elphick,et al.  Localization of soluble guanylyl cyclase α-subunit in identified insect neurons , 1998, Brain Research.

[40]  Caroline H. Wilson.  An Examination of the Effects and Possible Targets of Nitric Oxide on Olfactory Neurons in the Moth, Manduca Sexta , 2005 .

[41]  J. Hildebrand,et al.  Anatomy of antenno-cerebral pathways in the brain of the sphinx moth Manduca sexta , 1988, Cell and Tissue Research.

[42]  H. Steinbusch,et al.  Nitric oxide synthase, cGMP, and NO‐mediated cGMP production in the olfactory bulb of the rat , 1996, The Journal of comparative neurology.

[43]  U. Müller,et al.  Inhibition of Nitric Oxide Synthase Impairs a Distinct Form of Long-Term Memory in the Honeybee, Apis mellifera , 1996, Neuron.

[44]  Yutaka Kirino,et al.  Impairment of olfactory discrimination by blockade of nitric oxide activity in the terrestrial slug Limax valentianus , 2004, Neuroscience Letters.