Cortical afferents modulate striatal gap junction permeability via nitric oxide

Nitric oxide is a ubiquitous cellular messenger that plays a role in a variety of biological mechanisms. Within the central nervous system, it is formed in glia and neuronal cells and can diffuse away from its site of origin to modulate membrane conductances, neurotransmitter release, behavior, or to control the blood flow within its region of action. Nitric oxide has been shown to modulate gap junction conductance in the retina and cortex, an action it shares with a number of neurotransmitters. In this study, we found that the activation of cortical afferents increased dye coupling between rat neostriatal neurons recorded in vitro. This effect was mimicked by a nitric oxide donor and prevented by a nitric oxide synthase inhibitor, suggesting that activation of corticostriatal fibers may open putative gap junctions in the striatum via release of nitric oxide. This is the first report showing that synaptic modulation of gap junctions can be mediated by nitric oxide, and may provide a mechanism to explain cortical modulation of subcortical pattern formation within this highly integrative structure.

[1]  D S Faber,et al.  Activity-dependent short-term enhancement of intercellular coupling , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[2]  H. Korn,et al.  Morphological correlates of electrical and other interactions through low-resistance pathways between neurons of the vertebrate central nervous system. , 1978, International review of cytology.

[3]  A. Grace,et al.  Synaptic interactions among excitatory afferents to nucleus accumbens neurons: hippocampal gating of prefrontal cortical input , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[4]  S. Snyder,et al.  Behavioural abnormalities in male mice lacking neuronal nitric oxide synthase , 1995, Nature.

[5]  Nitric oxide tonically depresses a voltage- and Ca-dependent outward current in hippocampal slices , 1995, Neuroscience Letters.

[6]  J. Borowitz,et al.  NMDA Receptor Activation Produces Concurrent Generation of Nitric Oxide and Reactive Oxygen Species: Implications for Cell Death , 1995, Journal of neurochemistry.

[7]  D. Madison,et al.  Nitric oxide and synaptic function. , 1994, Annual review of neuroscience.

[8]  E. A. Schwartz,et al.  Modulation of an electrical synapse between solitary pairs of catfish horizontal cells by dopamine and second messengers. , 1989, The Journal of physiology.

[9]  A. Grace,et al.  Intracellular and extracellular electrophysiology of nigral dopaminergic neurons—3. Evidence for electrotonic coupling , 1983, Neuroscience.

[10]  K. Johnson,et al.  Inhibitory Effects of Nitric Oxide on the Uptake of [3H]Dopamine and [3H]Glutamate by Striatal Synaptosomes , 1994, Journal of neurochemistry.

[11]  F. Dudek,et al.  Dye transfer through gap junctions between neuroendocrine cells of rat hypothalamus. , 1981, Science.

[12]  S. Hyodo,et al.  Cellular localization of gap junction mRNA in the neonatal rat brain , 1991, Neuroscience Letters.

[13]  Charles J. Wilson,et al.  The origins of two-state spontaneous membrane potential fluctuations of neostriatal spiny neurons , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[15]  G. Christ,et al.  Dynamic gap junctional communication: a delimiting model for tissue responses. , 1994, Biophysical journal.

[16]  R. Llinás,et al.  Morphological artifacts induced in intracellularly stained neurons by dehydration: Circumvention using rapid dimethyl sulfoxide clearing , 1985, Neuroscience.

[17]  S. Snyder,et al.  Nitric oxide synthase protein and mRNA are discretely localized in neuronal populations of the mammalian CNS together with NADPH diaphorase , 1991, Neuron.

[18]  P. O’Donnell,et al.  Dopaminergic modulation of dye coupling between neurons in the core and shell regions of the nucleus accumbens , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[19]  A. Grace,et al.  Dye coupling between rat striatal neurons recorded in vivo: compartmental organization and modulation by dopamine. , 1994, Journal of neurophysiology.

[20]  G. Arbuthnott,et al.  Some Consequences of Local Blockade of Nitric-Oxide Synthase in the Rat Neostriatum , 1994 .

[21]  G. I. Hatton,et al.  Activation of excitatory amino acid inputs to supraoptic neurons. I. Induced increases in dye-coupling in lactating, but not virgin or male rats , 1990, Brain Research.

[22]  H. Takagi,et al.  Localizations of α1 and β1 subunits of soluble guanylate cyclase in the rat brain , 1993 .

[23]  H. Kimura,et al.  Histochemical mapping of nitric oxide synthase in the rat brain , 1992, Neuroscience.

[24]  M. Kuhar,et al.  Nitric oxide inhibits [3H]dopamine uptake , 1994, Brain Research.

[25]  Satoru Kato,et al.  Dopamine modulates S-potential amplitude and dye-coupling between external horizontal cells in carp retina , 1983, Nature.

[26]  E. Miyachi,et al.  Blocking effect of L-arginine on retinal gap junctions by activating guanylate cyclase via generation of nitric oxide , 1994 .

[27]  W. W. Stewart.  Lucifer dyes—highly fluorescent dyes for biological tracing , 1981, Nature.

[28]  J. Walsh,et al.  Dye‐Coupling in the neostriatum of the rat: I. Modulation by dopamine‐depleting lesions , 1989, Synapse.

[29]  B. Rörig,et al.  Nitric oxide‐stimulated increase in intracellular cGMP modulates gap junction coupling in rat neocortex , 1996, Neuroreport.

[30]  J. Garthwaite,et al.  Endothelium-derived relaxing factor release on activation of NMDA receptors suggests role as intercellular messenger in the brain , 1988, Nature.

[31]  G. Hatton,et al.  Synaptically released histamine increases dye coupling among vasopressinergic neurons of the supraoptic nucleus: mediation by H1 receptors and cyclic nucleotides , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.