Nitric oxide modulates local reflexes of the tailfan of the crayfish

Abstract

Electrical stimulation of sensory neurons that innervate receptors on the tailfan of crayfish evokes a reflex response of motor neurons that produce movements of the blades of the tailfan, the uropods. We analyzed the modulatory effects of nitric oxide (NO) on the spike frequency of the reflex response. Bath application of L-arginine and SNAP, which elevate endogenous and exogenous NO levels, increased the frequency of the evoked response, whereas the application of L-NAME and PTIO, which reduce NO levels, decreased the frequency of the response. To determine through what pathway and target NO exerted these effects we bath applied ODQ, an inhibitor of soluble guanylyl cyclase (sGC), which decreased the frequency of response, and 8-br-cGMP, which increased the spike frequency of response. To provide further evidence that NO acts via sGC, we elevated NO levels with L-arginine while simultaneously inhibiting sGC with ODQ. This application reduced the response to control levels, indicating that NO in the terminal ganglion of crayfish acts via sGC to modulate cGMP levels, which in turn regulate the responses of the uropod motor neurons.

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

“…In the vertebrate brain, NO is involved in synaptogenesis and in the synaptic plasticity that occurs during brain development, learning, memory, and disease (Boehning and Snyder, 2003;Keynes and Garthwaite, 2004). In invertebrates, NO is involved in rhythm generation in the stomatogastric system of mollusks (Park et al, 1998;Straub et al, 2007), crayfish (Stein et al, 2005), and locusts (Rand et al, 2008), and a role for NO has been shown in invertebrate sensory-motor processing, e.g., in the crayfish (Araki et al, 2004). In mollusk odor processing, NO is involved in controlling the periodic oscillations necessary for olfactory discrimination and learning (Gelperin, 1994;Watanabe et al, 2008).…”

Changes in the nitric oxide system in the shore crab Hemigrapsus sanguineus (Crustacea, decapoda) CNS induced by a nociceptive stimulus

“…In our study, these appeared to be the neurons that display maximum NADPH-d activity shortly after injury, and iNOS immunoreactivity thereafter. Using NOS donors and inhibitors, Araki and colleagues showed that NO enhances the activity of the motoneurons modulating the local tailfan reflexes in the crayfish (Araki et al, 2004). This suggests that NOsignaling, which is enhanced in the thoracic ganglion of shore crabs in response to nociceptive chemical stimulation, could be involved not only in sensory processing but also in motor program modulation.…”

Nitric oxide modulates a swimmeret beating rhythm in the crayfish

“…Some axons projecting from nerve 1 of the abdominal ganglia are immunopositive (H. Aonuma, personal communication). An NO-cGMP pathway has been widely reported in many sensory and motor systems in both vertebrates and invertebrates (Bawin et al, 1994;Bicker and Schmachtenberg, 1997;Araki et al, 2004;Moroz et al, 2004;Newland and Yates, 2007). Newland and Yates (Newland and Yates, 2007) show that bath application of the generic protein kinase inhibitor H-7 and a selective cGMP-dependent protein kinase (PKG) inhibitor KT-5823 reduced the frequency of the oviposition digging rhythm of the locust.…”

“…These drugs were prepared prior to application and used within 5 min. The concentration of drugs used in this study was based on Araki et al (Araki et al, 2004;Araki et al, 2005).…”

“…For example, the synaptic responses of intersegmental ascending interneurones or spiking local interneurones in the terminal abdominal ganglion of the crayfish to mechanosensory stimulation of the tail fan are enhanced or depressed by NO (Aonuma and Newland, 2001;Aonuma and Newland, 2002). Local reflexes of the tail fan motor neurones of the crayfish are also enhanced by NO (Araki et al, 2004). Furthermore, NO affects rhythmic motor activity induced by central pattern generators (CPGs).…”