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

Wilson, Caroline H.; Christensen, Thomas A.; Nighorn, Alan

doi:10.1007/s00359-007-0227-9

Cited by 25 publications

(23 citation statements)

References 40 publications

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“…It has been reported that the behavioral changes in losers are also suppressed when the nitric oxide (NO) signal in the brain is pharmacologically inhibited (Iwasaki et al, 2007). Some previous reports suggested that NO is required for proper chemical information processing in the antennal lobe (Collmann et al, 2004;Wilson et al, 2007). It has also been reported that antennal mechanosensory neurons contain the target of NO, soluble guanylyl cyclase (Elphick and Jones, 1998), suggesting that the NO signal may modulate the sensitivities of the mechanosensory neurons in the antennae.…”

Section: The Journal Of Experimental Biology 216 (12)mentioning

confidence: 99%

Aggressive behavior in the antennectomized male cricket Gryllus bimaculatus

Sakura

Aonuma

2013

Journal of Experimental Biology

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SUMMARYMale crickets (Gryllus bimaculatus) exhibit intensively defensive aggressive behavior towards attacking males most often culminating in fighting. After the fight, the loser no longer exhibits aggressiveness in a second, separate encounter with another male; rather, the defeated male exhibits avoidance behavior. Here, we investigated the role of sensory input from the antennae in male defensive aggressive behavior. When we removed antennae from males (antennectomized males), we found that they showed little aggressiveness towards each other whereas they continued to exhibit typical fighting behavior towards an intact male. In addition, in a second encounter, antennectomized losers showed significantly higher aggressiveness towards another male than did intact losers. We further found that antennectomized crickets do not utilize visual or palpal sensory input to elicit aggressive behavior. In contrast, intact males showed aspects of aggressive behavior to male cuticular substances before and after winning a fight, and if they lost a fight they showed avoidance behavior. It thus appears that antennal sensory information is crucial in the mediation of aggressive and avoidance behaviors. However, sensory inputs from the antennae are not necessary to elicit defensive aggressive behavior but are necessary to discriminate conspecific males and initiate attacks against them. Supplementary material available online at

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Section: The Journal Of Experimental Biology 216 (12)mentioning

confidence: 99%

Aggressive behavior in the antennectomized male cricket Gryllus bimaculatus

Sakura

Aonuma

2013

Journal of Experimental Biology

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“…NO is abundant in olfactory centers of both invertebrates and vertebrates, and in some animals, NO is involved in olfactory learning. For example, NO is released in the antennal lobe of insects, the first order olfactory center (Collmann et al 2004) and modulates neural activity (Wilson et al 2007). In the honeybee, NO is involved in habituation (Muller and Hildebrandt 2002) and long-term memory in associative olfactory learning (Muller 1996).…”

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confidence: 99%

Nitric oxide is involved in appetitive but not aversive olfactory learning in the land mollusk Limax valentianus

Yabumoto¹,

Takanashi²,

Kirino³

et al. 2008

Learn. Mem.

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The land slug Limax performs both aversive and appetitive olfactory learning, and we investigated neurotransmitters involved in each type of learning. Slugs were conditioned by presenting a vegetable juice (appetitive conditioning) or a mixture of vegetable juice and quinidine (aversive conditioning), and the latency to reach the juice became shorter (appetitive conditioning) or longer (aversive conditioning) after conditioning. L-NAME injected either before conditioning or testing blocked the reduction in latency in appetitive conditioning but had no significant effects in aversive conditioning. 5,7-dihydroxytryptamine had no significant effects in appetitive conditioning. These results suggest different mechanisms for appetitive and aversive learning.The land mollusk Limax has a highly developed olfactory system and performs olfactory learning. Both aversive (Gelperin 1975;Sahley et al. 1981) and appetitive (Sahley et al. 1990) olfactory learning have been reported, and therefore, it is possible to compare these two forms of learning in Limax. Aversive learning occurs when an odor is associated with an aversive chemical or electrical shock, and appetitive learning occurs when an odor is associated with food. So far, aversive learning has been more extensively studied than appetitive learning. Our previous study showed using the serotonergic neurotoxin 5,7-dihydroxytryptamine (DHT), which reduces the serotonin content in the CNS to less than half, that serotonin is essential for aversive learning (Shirahata et al. 2006). However, it is not known whether appetitive learning also depends on serotonin, or whether it requires other neurotransmitters.Nitric oxide (NO) synthase is abundant in the procerebrum (PC) (Fujie et al. 2002(Fujie et al. , 2005, which is a region of the cerebral ganglion essential for olfactory learning (Kasai et al. 2006). NO applied extrinsically modulates the rhythmic activity of the local field potential (LFP) of the PC (Gelperin 1994;Gelperin et al. 2000). These observations suggest significance of NO in olfactory processing in Limax. In Helix pomatia, a related land mollusk, appetitive learning is blocked by N -nitro-L-arginine methyl ester (L-NAME), a blocker of NO synthase. In the present work, we examine using L-NAME whether NO is involved in appetitive and aversive learning in Limax. We examine dependence of the acquisition and retrieval stages on NO separately. We also examine dependence of appetitive learning on serotonin using DHT.Limax valentianus 2-4 mo old from the laboratory colony were used. The slugs were freely fed with a mixture of rat chow (Oriental Yeast), wheat starch (Wako Pure Chemical), and mixed vitamins (Oriental Yeast), until 5 d before the experiment. The slugs were kept under the light/dark cycle of 10 h/14 h, and conditioning and testing were done within 4 h from the onset of the dark period. Five days before conditioning, the slugs were moved to individual boxes floored with moistened filter paper and starved. The training and testing were made on a glass plat...

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“…In the antennal lobe of M. sexta, NO production patterns are spatially focused and dependent on the identity and concentration of the odor stimulus (Collmann et al, 2004). In AL neurons, NO affects basal neuronal activity, suggesting a persistent presence of NO (Wilson et al, 2007), and affects whole-cell currents (Higgins et al, 2012). These studies indicate that NO has profound physiological effects in the olfactory system that are likely to influence olfactory processing and olfactory-guided behaviors.…”

Section: Introductionmentioning

confidence: 75%

“…Previous studies have shown that NO exists at tonic low levels (Wilson et al, 2007) that dramatically increase in response to odorants (Collmann et al, 2004;Lowe et al, 2008). We also know that NO modifies whole-cell current in AL neurons (Higgins et al, 2012).…”

Section: Discussionmentioning

confidence: 93%

“…This concentration was determined to be the minimal effective dose in extracellular recording in M. sexta (Wilson et al, 2007) and approximate to the concentrations used in molluscan preparations (Gelperin, 1994). Drug delivery into the ALs was performed according to the method described in Lei et al (Lei et al, 2009).…”

Section: Pharmacology and Microinjection Surgerymentioning

confidence: 99%

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Nitric oxide affects short-term olfactory memory in the antennal lobe ofManduca Sexta

Gage

Daly

Nighorn

2013

Journal of Experimental Biology

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SUMMARYNitric oxide (NO) is thought to play an important neuromodulatory role in olfaction. We are using the hawkmoth Manduca sexta to investigate the function of NO signaling in the antennal lobe (AL; the primary olfactory network in invertebrates). We have found previously that NO is present at baseline levels, dramatically increases in response to odor stimulation, and alters the electrophysiology of AL neurons. It is unclear, however, how these effects contribute to common features of olfactory systems such as olfactory learning and memory, odor detection and odor discrimination. In this study, we used chemical detection and a behavioral approach to further examine the function of NO in the AL. We found that basal levels of NO fluctuate with the daily light cycle, being higher during the nocturnal active period. NO also appears to be necessary for short-term olfactory memory. NO does not appear to affect odor detection, odor discrimination between dissimilar odorants, or learning acquisition. These findings suggest a modulatory role for NO in the timing of olfactory-guided behaviors. Supplementary material available online at

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

Cited by 25 publications

References 40 publications

Aggressive behavior in the antennectomized male cricket Gryllus bimaculatus

Aggressive behavior in the antennectomized male cricket Gryllus bimaculatus

Nitric oxide is involved in appetitive but not aversive olfactory learning in the land mollusk Limax valentianus

Nitric oxide affects short-term olfactory memory in the antennal lobe ofManduca Sexta

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