SYNAPTIC MODULATION OF NEURONAL COUPLING

Electrotonic coupling among neurons in the vertebrate, and more specifically the mammalian, brain has now been demonstrated to exist in all major brain subdivisions and in the spinal cord. For many of these brain areas, recent studies have investigated the possibilities of modulation of that coupling by synaptically released transmitters and/or neuromodulators. Reviewed here is the evidence for coupling, the synaptically related factors that play roles in up‐ or downregulation of this type of intercellular interaction and, to the extent that they have been investigated, the intracellular mechanisms operative in changing the extent of coupled networks in the brain. The functional significance of coupling and its modulation is discussed for some of these areas.

[1]  B. Rörig,et al.  Intracellular acidification reduced gap junction coupling between immature rat neocortical pyramidal neurones. , 1996, The Journal of physiology.

[2]  M. V. Bennett,et al.  Gap junctions as electrical synapses. , 1997, Journal of neurocytology.

[3]  J. Gallagher,et al.  Morphological and electrophysiological evidence for electrotonic coupling of rat dorsolateral septal nucleus neurons in vitro , 1993, Synapse.

[4]  W. Armstrong,et al.  Evidence for excitatory actions of histamine on supraoptic neurons in vitro: Mediation by an H1-type receptor , 1985, Neuroscience.

[5]  G. Hatton,et al.  NMDA and non-NMDA receptors on rat supraoptic nucleus neurons activated monosynaptically by olfactory afferents , 1995, Brain Research.

[6]  M. Gutnick,et al.  Dye coupling and possible electrotonic coupling in the guinea pig neocortical slice. , 1981, Science.

[7]  B. Rose,et al.  Clustering of Cx43 cell-to-cell channels into gap junction plaques: regulation by cAMP and microfilaments. , 1995, Journal of cell science.

[8]  A. Grace,et al.  Cortical afferents modulate striatal gap junction permeability via nitric oxide , 1996, Neuroscience.

[9]  J. Halliwell,et al.  Evidence for enhancement of gap junctional coupling between rat island of Calleja granule cells in vitro by the activation of dopamine D3 receptors , 1998, The Journal of physiology.

[10]  G. Hatton,et al.  Histamine mediates fast synaptic inhibition of rat supraoptic oxytocin neurons via chloride conductance activation , 1994, Neuroscience.

[11]  M. Murakami,et al.  Synaptic inputs to turtle horizontal cells analyzed after blocking of gap junctions by intracellular injection of cyclic nucleotides , 1991, Vision Research.

[12]  T. Reese,et al.  Differences in membrane structure between excitatory and inhibitory components of the reciprocal synapse in the olfactory bulb , 1974, The Journal of comparative neurology.

[13]  A. Grace,et al.  Repeated treatment with haloperidol and clozapine exerts differential effects on dye coupling between neurons in subregions of striatum and nucleus accumbens , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[14]  P. Micevych,et al.  Connexin 32 mRNA levels in the rat supraoptic nucleus: up-regulation prior to parturition and during lactation. , 1996, Neuroendocrinology.

[15]  F. Dudek,et al.  Electrotonic coupling between pyramidal cells: a direct demonstration in rat hippocampal slices. , 1981, Science.

[16]  J. Parnavelas,et al.  Gap junctions in the adult cerebral cortex: Regional differences in their distribution and cellular expression of connexins , 1996, The Journal of comparative neurology.

[17]  R. Tsien,et al.  A new generation of Ca2+ indicators with greatly improved fluorescence properties. , 1985, The Journal of biological chemistry.

[18]  R. Llinás,et al.  GABAergic modulation of complex spike activity by the cerebellar nucleoolivary pathway in rat. , 1996, Journal of neurophysiology.

[19]  D. McMahon,et al.  Modulation of gap-junction channel gating at zebrafish retinal electrical synapses. , 1994, Journal of neurophysiology.

[20]  E. Mugnaini,et al.  The dendritic lamellar body: a new neuronal organelle putatively associated with dendrodendritic gap junctions , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[21]  B. Rörig,et al.  Beta‐adrenoreceptor activation reduces dye‐ coupling between immature rat neocortical neurones , 1995, Neuroreport.

[22]  R. Llinás,et al.  Electrotonic coupling between neurons in cat inferior olive. , 1974, Journal of neurophysiology.

[23]  J. McReynolds,et al.  The relationship between light, dopamine release and horizontal cell coupling in the mudpuppy retina. , 1991, The Journal of physiology.

[24]  J. Williams,et al.  Opioid inhibition in locus coeruleus. , 1995, Journal of neurophysiology.

[25]  D. Spray,et al.  Gap junctions in the brain: where, what type, how many and why? , 1993, Trends in Neurosciences.

[26]  R. Dyball,et al.  Intercommunication in the rat supraoptic nucleus. , 1983, Quarterly journal of experimental physiology.

[27]  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.

[28]  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.

[29]  B. Rörig,et al.  Serotonin Regulates Gap Junction Coupling in the Developing Rat Somatosensory Cortex , 1996, The European journal of neuroscience.

[30]  Whalen,et al.  Mixed synapses discovered and mapped throughout mammalian spinal cord. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[31]  Y. Nakajima Fine structure of the synaptic endings on the Mauthner cell of the goldfish , 1974, The Journal of comparative neurology.

[32]  R. Weiler,et al.  pH-gated dopaminergic modulation of horizontal cell gap junctions in mammalian retina , 1994, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[33]  Henri Korn,et al.  Long-term potentiation of electrotonic coupling at mixed synapses , 1990, Nature.

[34]  Robert E. Foster,et al.  Oscillatory behavior in inferior olive neurons: Mechanism, modulation, cell aggregates , 1986, Brain Research Bulletin.

[35]  G. Hatton,et al.  Supraoptic nucleus afferents from the main olfactory bulb—II. Intracellularly recorded responses to lateral olfactory tract stimulation in rat brain slices , 1989, Neuroscience.

[36]  P. Cobbett,et al.  Dye coupling in hypothalamic slices: dependence on in vivo hydration state and osmolality of incubation medium , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[38]  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.

[39]  J. Lubke,et al.  Olfactory bulb granule cell aggregates: morphological evidence for interperikaryal electrotonic coupling via gap junctions , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[40]  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.

[41]  M. Weiss,et al.  Supraoptic nucleus afferents from the main olfactory bulb—I. Anatomical evidence from anterograde and retrograde tracers in rat , 1989, Neuroscience.

[42]  M. Murakami,et al.  Decoupling of horizontal cells in carp and turtle retinae by intracellular injection of cyclic AMP. , 1989, The Journal of physiology.

[43]  P. Laming,et al.  Glial cells : their role in behaviour , 1998 .

[44]  R. Llinás,et al.  Electrotonic coupling between neurones in the rat mesencephalic nucleus , 1971, The Journal of physiology.

[45]  J. Rinzel,et al.  Rhythmogenic effects of weak electrotonic coupling in neuronal models. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[46]  B. Sutor,et al.  Dye coupling between pyramidal neurons in developing rat prefrontal and frontal cortex is reduced by protein kinase A activation and dopamine , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[47]  Andrew C. Charles,et al.  Intercellular Calcium Waves in Neurons , 1996, Molecular and Cellular Neuroscience.

[48]  E. Hertzberg,et al.  Gap junctions: New tools, new answers, new questions , 1991, Neuron.

[49]  R. Llinás,et al.  Structural study of inferior olivary nucleus of the cat: morphological correlates of electrotonic coupling. , 1974, Journal of neurophysiology.

[50]  J. N. Hayward,et al.  Increased hypothalamic glutamate receptors induced by water deprivation. , 1994, Neuroendocrinology.

[51]  P. Cobbett,et al.  Dye coupling among immunocytochemically identified neurons in the supraoptic nucleus: Increased incidence in lactating rats , 1987, Neuroscience.

[52]  G. I. Hatton Emerging concepts of structure-function dynamics in adult brain: The hypothalamo-neurohypophysial system , 1990, Progress in Neurobiology.

[53]  R. Weiler,et al.  Dopaminergic modulation of gap junction permeability between amacrine cells in mammalian retina , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[54]  M. Bennett Gap junctions as electrical synapses , 1997 .

[55]  W. Armstrong,et al.  Histamine enhances the depolarizing afterpotential of immunohistochemically identified vasopressin neurons in the rat supraoptic nucleus via H1-receptor activation , 1993, Neuroscience.

[56]  A. Charles,et al.  Intercellular calcium waves in glia , 1998, Glia.

[57]  F. Dudek,et al.  Electrotonic coupling between granule cells of rat dentate gyrus: physiological and anatomical evidence. , 1982, Journal of neurophysiology.

[58]  C. Sotelo,et al.  Gap junctions in ventral cochlear nucleus of the rat. A possible new example of electrotonic junctions in the mammalian C.N.S. , 1976, Neuroscience.

[59]  M. Meng,et al.  Compact and scattered gap junctions in diffusion mediated cell--cell communication. , 1995, Journal of theoretical biology.

[60]  C I De Zeeuw,et al.  Association between dendritic lamellar bodies and complex spike synchrony in the olivocerebellar system. , 1997, Journal of neurophysiology.

[61]  L. Koran,et al.  Effects of ovariectomy and estrogen replacement on dye coupling among rat supraoptic nucleus neurons , 1992, Brain Research.

[62]  D. Faber,et al.  Dopamine enhances both electrotonic coupling and chemical excitatory postsynaptic potentials at mixed synapses. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[63]  G. I. Hatton,et al.  Supraoptic nucleus afferents from the accessory olfactory bulb: Evidence from anterograde and retrograde tract tracing in the rat , 1992, Brain Research Bulletin.

[64]  J. Parnavelas,et al.  Differential Expression of Connexins during Neocortical Development and Neuronal Circuit Formation , 1997, The Journal of Neuroscience.

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

[66]  S. Snyder,et al.  Localization of nitric oxide synthase indicating a neural role for nitric oxide , 1990, Nature.

[67]  T. Nakaki,et al.  Arachidonic acid blocks gap junctions between retinal horizontal cells. , 1994, Neuroreport.

[68]  M. Weiss,et al.  Magnocellular tuberomammillary nucleus input to the supraoptic nucleus in the rat: Anatomical and in vitro electrophysiological investigations , 1989, Neuroscience.

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

[70]  P. Greengard,et al.  Phosphorylation of connexin 32, a hepatocyte gap-junction protein, by cAMP-dependent protein kinase, protein kinase C and Ca2+/calmodulin-dependent protein kinase II. , 1990, European journal of biochemistry.

[71]  J. Voogd,et al.  Ultrastructural study of the GABAergic, cerebellar, and mesodiencephalic innervation of the cat medial accessory olive: Anterograde tracing combined with immunocytochemistry , 1989, The Journal of comparative neurology.

[72]  S. Massey,et al.  Differential properties of two gap junctional pathways made by AII amacrine cells , 1995, Nature.

[73]  R. Llinás,et al.  Electrophysiology of mammalian inferior olivary neurones in vitro. Different types of voltage‐dependent ionic conductances. , 1981, The Journal of physiology.

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

[75]  A. Kriegstein,et al.  Clusters of coupled neuroblasts in embryonic neocortex. , 1991, Science.

[76]  W. Ovtscharoff,et al.  Structure of the synaptic junctions in the rat sensorimotor cortex: freeze-etching study of neuronal gap junctions , 1995, Neuroscience Letters.

[77]  N. Inagaki,et al.  Is the histaminergic neuron system a regulatory center for whole-brain activity? , 1991, Trends in Neurosciences.

[78]  K K Osen,et al.  Stellate neurons in rat dorsal cochlear nucleus studied with combined Golgi impregnation and electron microscopy: synaptic connections and mutual coupling by gap junctions , 1984, Journal of neurocytology.

[79]  R. Llinás,et al.  SPECIALIZED MEMBRANE JUNCTIONS BETWEEN NEURONS IN THE VERTEBRATE CEREBELLAR CORTEX , 1972, The Journal of cell biology.

[80]  G. I. Hatton Function-related plasticity in hypothalamus. , 1997, Annual review of neuroscience.

[81]  J. Fallon,et al.  The island of Calleja complex of rat basal forebrain. I. Light and electron microscopic observations , 1982, The Journal of comparative neurology.

[82]  R. Yuste,et al.  Extensive dye coupling between rat neocortical neurons during the period of circuit formation , 1993, Neuron.

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

[84]  P. Cobbett,et al.  Incidence of dye coupling among magnocellular paraventricular nucleus neurons in male rats is testosterone dependent , 1987, Brain Research Bulletin.

[85]  J. Trosko,et al.  Scrape-loading and dye transfer. A rapid and simple technique to study gap junctional intercellular communication. , 1987, Experimental cell research.

[86]  G. Zampighi,et al.  Androgenic regulation of gap junctions between motoneurons in the rat spinal cord , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[87]  G. I. Hatton,et al.  Histamine-induced prolonged depolarization in rat supraoptic neurons: G-protein-mediated, Ca2+-independent suppression of K+ leakage conductance , 1996, Neuroscience.

[88]  G. Hatton,et al.  Dye coupling among supraoptic nucleus neurons without dendritic damage: Differential incidence in nursing mother and virgin rats , 1987, Brain Research Bulletin.

[89]  J. Sloper,et al.  Gap junctions between dendrites in the primate neocortex. , 1972, Brain research.

[90]  D. I. Vaney,et al.  Patterns of neuronal coupling in the retina , 1994, Progress in Retinal and Eye Research.

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

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

[93]  D. I. Vaney,et al.  Many diverse types of retinal neurons show tracer coupling when injected with biocytin or Neurobiotin , 1991, Neuroscience Letters.