Nitric oxide/cyclic guanosine monophosphate signaling in the central complex of the grasshopper brain inhibits singing behavior

Abstract

Grasshopper sound production, in the context of mate finding, courtship, and rivalry, is controlled by the central body complex in the protocerebrum. Stimulation of muscarinic acetylcholine receptors in the central complex has been demonstrated to stimulate specific singing in various grasshoppers including the species Chorthippus biguttulus. Sound production elicited by stimulation of muscarinic acetylcholine receptors in the central complex is inhibited by co-applications of various drugs activating the nitric oxide/cyclic guanosine monophosphate (cGMP) signaling pathway. The nitric oxide-donor sodium nitroprusside caused a reversible suppression of muscarine-stimulated sound production that could be blocked by 1H-[1,2,4]oxadiazolo-[4,3-a]quinoxaline-1-one (ODQ), which prevents the formation of cGMP by specifically inhibiting soluble guanylyl cyclase. Furthermore, injections of both the membrane-permeable cGMP analog 8-Br-cGMP and the specific inhibitor of the cGMP-degrading phosphodiesterase Zaprinast reversibly inhibited singing. To identify putative sources of nitric oxide, brains of Ch. biguttulus were subjected to both nitric oxide synthase immunocytochemistry and NADPH-diaphorase staining. Among other areas known to express nitric oxide synthase, both procedures consistently labeled peripheral layers in the upper division of the central body complex, suggesting that neurons supplying this neuropil contain nitric oxide synthase and may generate nitric oxide upon activation. Exposure of dissected brains to nitric oxide and 3-(5'hydroxymethyl-2'-furyl)-1-benzyl indazole (YC-1) induced cGMP-associated immunoreactivity in both the upper and lower division. Therefore, both the morphological and pharmacological data presented in this study strongly suggest a contribution of the nitric oxide/cGMP signaling pathway to the central control of grasshopper sound production.

Neuroarchitecture of the central complex of the desert locust: Intrinsic and columnar neurons

“…Lesions of the central complex in crickets (Huber, 1960a,b) led to inhibition of walking and acoustic behavior, whereas lesions in cockroaches caused deficits in turning behavior (Ridgel et al, 2007). Electrical and pharmacological stimulation in grasshoppers affected sound production (Wenzel et al, 2005;Hoffmann et al, 2007). Structural central-complex mutants in Drosophila showed defects in walking speed, leg coordination, and directional control of walking and flight, including abnormal optomotor responses (Bausenwein et al, 1986;Strauss and Heisenberg, 1993;Ilius et al, 1994;Strauss, 2002).…”

Development of nitrergic neurons in the nervous system of the locust embryo

“…Further involvement in visual information processing, e.g., for habituation and dishabituation of movement detectors, has been suggested by Elphick et al (1996) on the basis of anatomical observations. In the acoustic communication of grasshoppers, NO release in the central complex of the brain plays a vital role in suppressing stridulation behavior under unfavorable conditions (Wenzel et al, 2005;Weinrich et al, 2008). In the honeybee, the NO/cGMP system is involved in sensory integration (Müller and Hildebrandt, 1995) and habituation of the proboscis extension reflex via a protein kinase A pathway (Müller and Hildebrandt, 2002).…”

Distribution and characterization of nitric oxide synthase in the nervous system of Triatoma infestans (Insecta: Heteroptera)

“…Recent studies in the grasshopper Chorthippus biguttulus have shown NADPH-diaphorase staining in neurons, which supply the peripheral layer of the upper division of the central body. Furthermore, activation of the NO/cGMP pathway has been able to inhibit sound production provoked by stimulation of muscarinic receptors in the central complex (Wenzel et al 2005). T. infestans possesses a well-developed stridulatory organ (Di Luciano 1981), and sound production has been related to mating behavior (Manrique and Lazzari 1994).…”