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The Journal of Neuroscience, April 1, 1999, 19(7):2489-2499
A Critical Role of the Nitric Oxide/cGMP Pathway in Corticostriatal Long-Term Depression
Paolo Calabresi1, Paolo Gubellini2, Diego Centonze1, Giuseppe Sancesario1, Maria Morello1, Mauro Giorgi3, Antonio Pisani1, and Giorgio Bernardi1, 4 1 Clinica Neurologica, Dipartimento di Neuroscienze, Universitá di Roma Tor Vergata, 00133 Rome, Italy, 2 Istituto di Medicina Sperimentale, Consiglio Nazionale delle Ricerche, 00133 Rome, Italy, 3 Dipartimento di Biologia di Base e Applicata, Università dell'Aquila, 67010 L'Aquila, Italy, and 4 IRCCS Ospedale S. Lucia, 00179 Rome, Italy
High-frequency stimulation (HFS) of corticostriatal glutamatergic fibers induces long-term depression (LTD) of excitatory synaptic potentials recorded from striatal spiny neurons. This form of LTD can be mimicked by zaprinast, a selective inhibitor of cGMP phosphodiesterases (PDEs). Biochemical analysis shows that most of the striatal cGMP PDE activity is calmodulin-dependent and inhibited by zaprinast. The zaprinast-induced LTD occludes further depression by tetanic stimulation and vice versa. Both forms of synaptic plasticity are blocked by intracellular 1H-[1,2,4]oxadiazolo[4,3-a]quinoxalin-1-one (ODQ), a selective inhibitor of soluble guanylyl cyclase, indicating that an increased cGMP production in the spiny neuron is a key step. Accordingly, intracellular cGMP, activating protein kinase G (PKG), also induces LTD. Nitric oxide synthase (NOS) inhibitors N(G)-nitro-L-arginine methyl ester hydrochloride (L-NAME) and 7-nitroindazole monosodium salt (7-NINA) block LTD induced by either HFS or zaprinast, but not that induced by cGMP. LTD is also induced by the NO donors S-nitroso-N-acetylpenicillamine (SNAP) and hydroxylamine. SNAP-induced LTD occludes further depression by HFS or zaprinast, and it is blocked by intracellular ODQ but not by L-NAME. Intracellular application of PKG inhibitors blocks LTD induced by HFS, zaprinast, and SNAP. Electron microscopy immunocytochemistry shows the presence of NOS-positive terminals of striatal interneurons forming synaptic contacts with dendrites of spiny neurons. These findings represent the first demonstration that the NO/cGMP pathway exerts a feed-forward control on the corticostriatal synaptic plasticity.
Key words: intracellular recordings; electron microscopy; nitric oxide synthase; calmodulin-dependent phosphodiesterases; striatum; zaprinast
Copyright © 1999 Society for Neuroscience 0270-6474/99/1972489-11$05.00/0
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