Abstract
Previous studies have shown that nitric oxide (NO) transforms the responses of various neurons to glutamate, though it remained unclear whether this mechanism is involved in the formation of behavior. We therefore studied the buccal generator of the feeding rhythm of the mollusk Lymnaea stagnalis (pond snail). In this organism, glutamate and NO are synthesized by defined neurons; glutamate is the neurotransmitter for the second phase of the standard triphasic feeding rhythm. Motoneuron B4 was used for monitoring. Studies using isolated CNS preparations showed that in some cases glutamate evoked hyperpolarization of B4 and terminated rhythmic network activity (n = 17; group 1), while in other cases glutamate evoked depolarization of B4 and activation of a non-standard biphasic rhythm (n = 12; group 2). In group 1, the NO donor nitroprusside lifted the inhibitory effect of glutamate (n = 13), with transformation into an excitatory effect in nine cases. In group 2, the NO acceptor PTIO transformed the excitatory effect of glutamate into an inhibitory effect (n = 7). These results provide evidence that: 1) the responses of the central generator of the buccal motor rhythm to glutamate depend on the NO level, and 2) this regulatory mechanism can modify feeding behavior.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
T. L. D’yakonova, “Neurochemical mechanisms of regulation of train activity in isolated endogenous cochlear oscillators: the role of monoamines and opioid peptides,” Neirofiziologiya, 23, No. 4, 472–480 (1991).
T. L. D’yakonova, “NO-producing compounds transform the responses of neurons to glutamate,” Ros. Fiziol. Zh. im. I. M. Sechenova, 84, No. 10, 1152–1160 (1998).
T. L. D’yakonova, “NO-dependent regulation of the activity of the serotoninergic system of the common snail by glutamate,” Zh. Évolyuts. Biokhim. Fiziol., 38, No. 2, 156–162 (2002).
D. A. Sakharov, “The multiplicity of neurotransmitters: functional significance,” Zh. Évolyuts. Biokhim. Fiziol., 26, No. 5, 733–741 (1990).
M. J. Brierley, M. S. Yeoman, and P. R. Benjamin, “Glutamate is the transmitter for N2v retraction phase interneurons of the Lymnaea feeding system,” J. Neurophysiol., 78, 3408–3414 (1997).
T. L. Dyakonova, A. S. Vehovszky, and K. Rozsa, “Helix neurons involved in rhythmic movement of the pneumostome,” Neurophysiology (Kiev), 20, No. 4, 509–517 (1988).
C. J. Elliott and A. J. Susswein, “Comparative neuroethology of feeding control in molluscs,” J. Exptl. Biol., 205, 877–896 (2002).
M. R. Elphick, G. Kemenes, K. Staras, and M. O’Shea, “Behavioral role for nitric oxide in chemosensory activation of feeding in a mollusc,” J. Neurosci., 15, No. 11, 7653–7664 (1995).
R. E. Flamm and R. M. Harris-Warrick, “Aminergic modulation in lobster stomatogastric ganglion. II. Target neurons of dopamine, octopamine, and serotonin within the pyloric circuit,” J. Neurophysiol., 55, No. 5, 866–881 (1996).
Ji-Ho Park, V. A. Straub, and M. O’Shea, “Anterograde signaling by nitric oxide: characterization and in vitro reconstitution of an identified nitrergic synapse,” J. Neurosci., 18, No. 14, 5463–5476 (1998).
B. R. Johnson and R. M. Harris-Warrick, “Amine modulation of glutamate responses from pyloric motor neurons in lobster stomatogastric ganglion,” J. Neurophysiol., 78, No. 6, 3210–3221 (1997).
M. S. Hedrick and R. D. Morales, “Nitric oxide as a modulator of central respiratory rhythm in the isolated brainstem of the bullfrog (Rana catesbeiana),” Comp. Biochem. Physiol., A124, No. 3, 243–251 (1999).
S. Kobayashi, H. Ogawa, Y. Fujito, and E. Ito, “Nitric oxide suppresses fictive feeding response in Lymnaea stagnalis,” Neurosci. Lett., 285, No. 3, 209–212 (2000).
S. A. Korneev, J. H. Park, and M. O’Shea, “Neuronal expression of neural nitric oxide synthase (nNOS) protein is suppressed by an antisense RNA transcribed from an NOS pseudogene,” J. Neurosci., 19, No. 18, 7711–7720 (1999).
S. A. Korneev, M. R. Piper, J. Picot, R. Phillips, E. I. Korneeva, and M. O’Shea, “Molecular characterization of NOS in a mollusc: expression in a giant modulatory neuron,” J. Neurobiol., 35, 65–71 (1998).
A. Mahadevan, J. Lappe, R. T. Rhyne, N. D. Cruz-Bermudez, E. Marder, and M. F. Goy, “Nitric oxide inhibits the rate and strength of cardiac contractions in the lobster Homarus americanus by acting on the cardiac ganglion,” J. Neurosci., 17, No. 11, 2813–2824 (2004).
L. L. Moroz, Ji-Ho Park, and W. Winlow, “Nitric oxide activates buccal motor patterns in Lymnaea stagnalis,” Neuroreport, 4, No. 6, 643–646 (1993).
L. L. Moroz, T. P. Norekian, T. J. Pirtle, K. J. Robertson, and R. A. Satterlie, “Distribution of NADPH-diaphorase reactivity and effects of nitric oxide on feeding and locomotory circuitry in the pteropod mollusc Clione limacina,” J. Comp. Neurol., 427, No. 2, 274–284 (2000).
O. Pierrefiche, F. Maniak, and N. Larnicol, “Rhythmic activity from transverse brainstem slice of neonatal rat is modulated by nitric oxide,” Neuropharmacology, 43, No. 1, 85–94 (2002).
H. Sadamoto, D. Hatakeyama, S. Kojima, S. Fujito, and E. Ito, “Histochemical study on the relation between NO-generative neurons and central circuitry for feeding in the pond snail, Lymnaea stagnalis,” Neurosci. Res., 32, 57–63 (1998).
N. L. Scholz, J. de Vente, J. W. Truman, and K. Graubard, “Neural network partitioning by NO and cGMP,” J. Neurosci., 21, No. 5, 1610–1618 (2001).
K. Staras, G. Kemenes, and P. R. Benjamin, “Pattern-generating role for motoneurons in a rhythmically active neuronal network,” J. Neurosci., 18, No. 10, 3669–3688 (1998).
W. Stein, C. C. Eberle, and U. B. Hedrich, “Motor pattern selection by nitric oxide in the stomatogastric nervous system of the crab,” Eur. J. Neurosci., 21, No. 10, 2767–2781 (2005).
V. A. Straub and P. R. Benjamin, “Extrinsic modulation and motor pattern generation in a feeding network: a cellular study,” J. Neurosci., 21, No. 5, 1767–1778 (2001).
T. Stühmer, A. Muriel, R. J. Harvey, I. Bermudez, I. van Minnen, and M. G. Darlison, “Structure and pharmacological properties of a molluscan glutamate-gated cation channel and its likely role in feeding behavior,” J. Neurosci., 16, No. 9, 2869–2880 (1996).
Author information
Authors and Affiliations
Additional information
__________
Translated from Rossiiskii Fiziologicheskii Zhurnal imeni I. M. Sechenova, Vol. 93, No. 3, pp. 236–247, March, 2007.
Rights and permissions
About this article
Cite this article
D’yakonova, T.L., D’yakonova, V.E. Modification of the effects of glutamate by nitric oxide (NO) in a pattern-generating network. Neurosci Behav Physi 38, 407–413 (2008). https://doi.org/10.1007/s11055-008-0058-3
Received:
Revised:
Issue Date:
DOI: https://doi.org/10.1007/s11055-008-0058-3