Behavioral role for nitric oxide in chemosensory activation of feeding in a mollusc

Abstract

A role for the NO-cGMP pathway in mediating chemosensory activation of feeding is suggested by intense NADPH diaphorase staining observed in nerve fibers that project from sensory cells in the lips to the CNS and by the presence in the CNS of a NO-activated guanylyl cyclase. In preparations reduced to isolated lips and CNS, intracellular recordings were made from motoneurons driven by the interneurons of the central pattern generator (CPG) for feeding. Fictive feeding in such preparations can be recorded from these motoneurons following the application of sucrose to the lips. Sucrose activation of fictive feeding is inhibited by the NO scavenger hemoglobin, the NO synthase inhibitor N omega-Nitro-L-Arginine Methyl Ester (L-NAME) and by methylene blue, an inhibitor of guanylyl cyclase. Fictive feeding in isolated lip-CNS preparations can be activated without sucrose by superfusion of NO donor molecules such as SNAP and hydroxylamine and by the nonhydrolyzable analog of cGMP, 8-bromo-cGMP. The feeding CPG can also be activated centrally by depolarizing a modulatory interneuron, the slow oscillator (SO). When the CPG is activated in this way, fictive feeding is not susceptible to inhibition by hemoglobin, the most potent of the inhibitors of sucrose-activated fictive feeding. Behavioral experiments on intact snails confirm the findings from in vitro experiments and show that hemoglobin prevents feeding and methylene blue significantly delays the onset of feeding. These results indicate (1) that NO is a putative chemosensory transmitter in the snail L. stagnalis, (2) that the NO-cGMP pathway can mediate chemosensory activation of specific patterns of centrally generated behavior, (3) that NO is not involved in transmission within the central network of neurons responsible for the behavior, and more generally (4) that a freely diffusing and highly reactive gaseous signalling molecule can have restricted and specific behavioral functions.

Nitric Oxide Inhibits the Rate and Strength of Cardiac Contractions in the LobsterHomarus americanusby Acting on the Cardiac Ganglion

“…Despite the diffuse nature of its delivery, it is clear that NO activates and modulates particular neural network targets with stereotypical functional consequences (Moroz et al, 1993;Gelperin, 1994;Elphick et al, 1995;Scholz et al, 2001). This suggests that particular distributions of NO receptors (and/or other downstream targets) may enable a diffuse NO signal to sculpt the responses of specific cells within a population.…”

“…Because of its rapid membrane-permeating characteristics and short half-life in biological tissues, NO is typically used to transmit information between closely juxtaposed cells. For example, NO serves as a local modulator of blood pressure (Shesely et al, 1996;Hanafy et al, 2001), cardiac function (Balligand et al, 1993;Keaney et al, 1996;Zahradnikova et al, 1997;Gyurko et al, 2000), neuronal development (Cramer et al, 1998;Scholz et al, 1998;Champlin and Truman, 2000), synaptic transmission (Schuman and Madison, 1994;Huang, 1997), and oscillatory behavior in patterngenerating networks of neurons (Pape and Mager, 1992;Moroz et al, 1993;Gelperin, 1994;Elphick et al, 1995;Hedrick and Morales, 1999;Scholz et al, 2001;Newcomb and Watson, 2002;McLean and Sillar, 2000).…”

A review of soil NO transformation: Associated processes and possible physiological significance on organisms

“…Bakken et al (2012) showed that the ratio of N2O/(N2+N2O) is negatively 555 correlated with soil pH over the pH range 5-8, which is typical for 556 agricultural soils. The authors concluded that low pH interfers with the 557 synthesis of the N2O reductase enzyme, most likely by affecting the enzyme 558 assembly in the periplasm.…”

Identification of Nitric Oxide‐Sensitive and ‐Insensitive Forms of Cytoplasmic Guanylate Cyclase

“…It also suggests that electrophysiological identification of specific NO-sensitive neurons is likely to be quite straightforward. Although our understanding of the function of the NO/cyclic GMP pathway in invertebrate nervous systems is in its infancy, several potential roles have been established, including modulation of synaptic efficacy (Pivovarov et al, 1990(Pivovarov et al, , 1995Mothet et al, 1996), sensory integration (Gelperin, 1994;Muller and Hildebrandt, 1995;Elphick et al, 1996), central pattern generation (Moroz et al, 1993;Elphick et al, 1995), higher information processing (Muller, 1996), and control over neural development (Scholz et al, 1995;Kuzin et al, 1996;Truman et al, 1996). The large sizes and reproducible locations of the NO-sensitive cells in the lobster nervous system offer the prospect of further evaluating the properties of this important second messenger pathway in a relatively simple and well-studied set of neuronal networks.…”