Synaptic inputs onto spiking local interneurons in crayfish are depressed by nitric oxide.

We have analyzed the action of nitric oxide on the synaptic inputs of spiking local interneurons that form part of the local circuits in the terminal abdominal ganglion of the crayfish, Pacifastacus leniusculus. Increasing the availability of NO in the ganglion by bath applying the NO donor SNAP, or the substrate for its synthesis, L-arginine, caused a depression of synaptic inputs onto the interneurons evoked by electrically stimulating mechanosensory neurons in nerve 2 of the terminal ganglion. Conversely, reducing the availability of NO by bath application of an NO scavenger, PTIO, and an inhibitor of nitric oxide synthase, L-NAME, increased the amplitude of the evoked potentials. These results suggest that elevated NO concentration causes a depression of the synaptic inputs to spiking local interneurons. To determine whether these effects could be mediated through an NO/cGMP signaling pathway we bath applied a membrane permeable analogue of cGMP, 8-br-cGMP, which decreased the amplitude of the inputs to the interneurons. Bath application of an inhibitor of soluble guanlylyl cyclase, ODQ, produced an increase in the amplitude of the synaptic inputs. Our results suggest that NO causes a depression of synaptic inputs to spiking local interneurons probably by acting through an NO/cGMP signaling pathway. Moreover, application of NO scavengers modulates the inputs to these interneurons, suggesting that NO is continuously providing a powerful and dynamic means of modulating the outputs of local circuits.

[1]  D. Kennedy,et al.  Reflex Control of Abdominal Flexor Muscles in the Crayfish , 1965 .

[2]  M. Burrows,et al.  The morphology of two groups of spiking local interneurons in the metathoracic ganglion of the locust , 1984, The Journal of comparative neurology.

[3]  T. Nagayama,et al.  Morphological and physiological bases of crayfish local circuit neurones. , 1994, Histology and histopathology.

[4]  Physiology and morphology of spiking local interneurons in the terminal abdominal ganglion of the crayfish , 1993, The Journal of comparative neurology.

[5]  J. Garthwaite,et al.  The nitric oxide-cyclic GMP signalling pathway in rat brain , 1993, Neuropharmacology.

[6]  S. Snyder,et al.  Nitric oxide mediates glutamate-linked enhancement of cGMP levels in the cerebellum. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[7]  D. Madison,et al.  A requirement for the intercellular messenger nitric oxide in long-term potentiation. , 1991, Science.

[8]  M. Burrows,et al.  Nitric oxide synthase in the thoracic ganglia of the locust: Distribution in the neuropiles and morphology of neurones , 1998, The Journal of comparative neurology.

[9]  Solomon H. Snyder,et al.  Nitric oxide, a novel neuronal messenger , 1992, Neuron.

[10]  M. Burrows,et al.  Receptive fields of motor neurons underlying local tactile reflexes in the locust , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[11]  T. Nagayama,et al.  Cholinergic transmission at mechanosensory afferents in the crayfish terminal abdominal ganglion , 1996, Journal of Comparative Physiology A.

[12]  S. Moncada,et al.  Nitric oxide: physiology, pathophysiology, and pharmacology. , 1991, Pharmacological reviews.

[13]  T. Nagayama,et al.  Behavioral transition of crayfish avoidance reaction in response to uropod stimulation. , 1986, Experimental biology.

[14]  D. Stuehr.  Mammalian nitric oxide synthases. , 1999, Biochimica et biophysica acta.

[15]  M. Burrows.  The control of sets of motoneurones by local interneurones in the locust. , 1980, The Journal of physiology.

[16]  Williams,et al.  New features of the locust optic lobe: evidence of a role for nitric oxide in insect vision , 1996, The Journal of experimental biology.

[17]  J. Vente,et al.  The Nitric Oxide/Cyclic GMP Messenger System in Olfactory Pathways of the Locust Brain , 1996, The European journal of neuroscience.

[18]  M. Burrows,et al.  Spiking local interneurons mediate local reflexes. , 1982, Science.

[19]  J. Truman,et al.  The NO/cGMP pathway and the development of neural networks in postembryonic lobsters. , 1998, Journal of neurobiology.

[20]  H. Reichert,et al.  Local interneurons in the terminal abdominal ganglion of the crayfish , 1982, Journal of comparative physiology.

[21]  E. Kandel,et al.  Nitric Oxide Acts Directly in the Presynaptic Neuron to Produce Long-Term Potentiationin Cultured Hippocampal Neurons , 1996, Cell.

[22]  M. Burrows,et al.  The morphological diversity and receptive fields of spiking local interneurons in the locust metathoracic ganglion , 1984, The Journal of comparative neurology.

[23]  Morphology of a new population of spiking local interneurones in the locust metathoracic ganglion , 1989, The Journal of comparative neurology.

[24]  T. Bliss,et al.  Photolytically released nitric oxide produces a delayed but persistent suppression of LTP in area CA1 of the rat hippocampal slice , 1999, The Journal of physiology.

[25]  M. Burrows,et al.  NADPH diaphorase histochemistry in the thoracic ganglia of locusts, crickets, and cockroaches: Species differences and the impact of fixation , 1999, The Journal of comparative neurology.

[26]  Distribution of NADPH-diaphorase-positive ascending interneurones in the crayfish terminal abdominal ganglion , 2001, Cell and Tissue Research.

[27]  T. Nagayama,et al.  Modulatory effects of nitric oxide on synaptic depression in the crayfish neuromuscular system. , 2000, The Journal of experimental biology.

[28]  C. R. Fourtner,et al.  Nonspiking interneurons in walking system of the cockroach. , 1975, Journal of neurophysiology.

[29]  Crayfish Local Bilateral Spiking Interneurons : Role in Contralateral Uropod Motor Pattern Formation(Physiology) , 1985 .

[30]  A. Harreveld,et al.  A Physiological Solution for Freshwater Crustaceans , 1936 .

[31]  P. Newland,et al.  Opposing actions of nitric oxide on synaptic inputs of identified interneurones in the central nervous system of the crayfish. , 2001, The Journal of experimental biology.

[32]  B. Trimmer,et al.  The role of nitric oxide in motoneuron spike activity and muscarinic-evoked changes in cGMP in the CNS of larval Manduca sexta , 1999, Journal of Comparative Physiology A.

[33]  P. Newland,et al.  Physiology and Structure of Three New Uropod Proprioceptors in the Crayfish Procambarus Clarkii , 1990 .

[34]  M. Carlberg,et al.  NADPH-diaphorase histochemistry and nitric oxide synthase activity in deutocerebrum of the crayfish,Pacifastacus leniusculus (crustacea, decapoda) , 1994, Brain Research.

[35]  T. Nagayama,et al.  Parallel processing of proprioceptive information in the terminal abdominal ganglion of the crayfish , 1993, Journal of Comparative Physiology A.

[36]  M. León‐Olea,et al.  Histochemical distribution of NADPH-diaphorase in the cerebral ganglion of the crayfish Cambarellus montezumae , 1995, Neuroscience Letters.

[37]  Intersegmental ascending interneurones controlling uropod movements of the crayfish Procambarus clarkii , 1993 .

[38]  W. Grueber,et al.  Development and organization of a nitric‐ oxide‐sensitive peripheral neural plexus in larvae of the moth, Manduca sexta , 1999, The Journal of comparative neurology.