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Journal of Neuroscience, Vol 15, 7653-7664, Copyright © 1995 by Society for Neuroscience
Behavioral role for nitric oxide in chemosensory activation of feeding in a mollusc
MR Elphick, G Kemenes, K Staras and M O'Shea
Sussex Centre for Neuroscience, School of Biological Sciences, University of Sussex, Brighton, United Kingdom.
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.
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