Synaptic transmission between pairs of retinal amacrine cells in culture

We have examined synaptic transmission between isolated pairs of chick GABAergic amacrine cells, maintained in sparse culture and identified by their binding of an amacrine cell-selective antibody. Using the perforated-patch method to whole-cell clamp both cells of a pair, postsynaptic currents were examined for step depolarizations of the “presynaptic” cell. Synaptic transmission, frequently reciprocal, was calcium dependent and reversibly blocked by bicuculline. Post-synaptic currents, excluding those due to ohmic electrical coupling, were elicited only for presynaptic voltage steps positive to about -40 mV and were always very noisy, suggesting that they were summed from relatively small numbers of quanta. Postsynaptic currents continued well after the termination of the 100 msec presynaptic voltage step when the step was to -10 mV, or positive to this value. This result is interpreted to imply that presynaptic calcium concentration remains elevated after the membrane is returned to its holding potential. When presynaptic voltages were kept low or else presynaptic voltage was uncontrolled, spontaneous quantal events mediated by GABAA receptors could often be seen. Quanta rose quickly (less than 4 msec) and decayed with a mean time constant of 19.3 msec. The amplitude distributions of quantal currents were positively skewed, sometimes showing rare quanta of exceptionally large amplitude. Peak conductance per quantum was about 300 pS, corresponding to the simultaneous opening of only 17 GABAA channels and corresponding to a net flux of only 32 x 10(3) Cl- ions per millivolt of driving force. Estimates of the maximum sustained release rate at individual release sites suggest an upper bound of between 19 and 42 quanta per second.

[1]  H. Wassle,et al.  Voltage- and transmitter-gated currents of all-amacrine cells in a slice preparation of the rat retina , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[2]  Antonio Malgaroli,et al.  Glutamate-induced long-term potentiation of the frequency of miniature synaptic currents in cultured hippocampal neurons , 1992, Nature.

[3]  D. O'Malley,et al.  Co-release of acetylcholine and GABA by the starburst amacrine cells , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[4]  P. Mobbs,et al.  Development of functional calcium channels in cultured avian photoreceptors , 1992, Visual Neuroscience.

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

[6]  H. Hofmann,et al.  Transmitter-gated currents of GABAergic amacrine-like cells in chick retinal cultures , 1991, Visual Neuroscience.

[7]  H. Hofmann,et al.  Identification of GABAergic amacrine cell-like neurons developing in chick retinal monolayer cultures , 1990, Neuroscience Letters.

[8]  N. Ropert,et al.  Characteristics of miniature inhibitory postsynaptic currents in CA1 pyramidal neurones of rat hippocampus. , 1990, The Journal of physiology.

[9]  W. R. Taylor,et al.  Concomitant activation of two types of glutamate receptor mediates excitation of salamander retinal ganglion cells. , 1990, The Journal of physiology.

[10]  C. Stevens,et al.  Presynaptic mechanism for long-term potentiation in the hippocampus , 1990, Nature.

[11]  R. Zucker,et al.  Calcium released by photolysis of DM‐nitrophen stimulates transmitter release at squid giant synapse. , 1990, The Journal of physiology.

[12]  C. Stevens,et al.  Origin of variability in quantal size in cultured hippocampal neurons and hippocampal slices. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[13]  K. Akagawa,et al.  Calcium- and voltage-dependent potassium channel in the rat retinal amacrine cells identified in vitro using a cell type-specific monoclonal antibody , 1990, Brain Research.

[14]  B. Sakmann,et al.  Functional properties of recombinant rat GABAA receptors depend upon subunit composition , 1990, Neuron.

[15]  Martin Wilson,et al.  Development of synapses between chick retinal neurons in dispersed culture , 1989, The Journal of comparative neurology.

[16]  Stephen J. Smith,et al.  Calcium ions, active zones and synaptic transmitter release , 1988, Trends in Neurosciences.

[17]  P. MacLeish,et al.  Growth and synapse formation among major classes of adult salamander retinal neurons in vitro , 1988, Neuron.

[18]  R. Masland Amacrine cells , 1988, Trends in Neurosciences.

[19]  R. Horn,et al.  Muscarinic activation of ionic currents measured by a new whole-cell recording method , 1988, The Journal of general physiology.

[20]  H. Kolb,et al.  Organization of the inner plexiform layer of the turtle retina: An electron microscopic study , 1988, The Journal of comparative neurology.

[21]  C. Watt,et al.  Quantitative studies of enkephalin's coexistence with γ-aminobutyric acid, glycine and neurotensin in amacrine cells of the chicken retina , 1988, Brain Research.

[22]  F. Werblin,et al.  The interaction of ionic currents mediating single spike activity in retinal amacrine cells of the tiger salamander , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[23]  E. A. Schwartz,et al.  Depolarization without calcium can release gamma-aminobutyric acid from a retinal neuron. , 1987, Science.

[24]  B. Sakmann,et al.  Mechanism of anion permeation through channels gated by glycine and gamma‐aminobutyric acid in mouse cultured spinal neurones. , 1987, The Journal of physiology.

[25]  R. O’Brien,et al.  Excitatory synaptic transmission between interneurons and motoneurons in chick spinal cord cell cultures , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[26]  J. Nicholls,et al.  Voltage dependence of 5‐hydroxytryptamine release at a synapse between identified leech neurones in culture. , 1986, The Journal of physiology.

[27]  F. Werblin,et al.  Gated currents generate single spike activity in amacrine cells of the tiger salamander retina. , 1986, Proceedings of the National Academy of Sciences of the United States of America.

[28]  C. Watt,et al.  The coexistence of two neuroactive peptides in a subpopulation of retinal amacrine cells , 1985, Brain Research.

[29]  C. Barnstable,et al.  A marker of early amacrine cell development in rat retina. , 1985, Brain research.

[30]  K. Negishi,et al.  Dye coupling between amacrine cells in carp retina , 1984, Neuroscience Letters.

[31]  H. Karten,et al.  Localization of neuroactive substances in the vertebrate retina: Evidence for lamination in the inner plexiform layer , 1983, Vision Research.

[32]  M. Gold,et al.  Characteristics of inhibitory post‐synaptic currents in brain‐stem neurones of the lamprey. , 1983, The Journal of physiology.

[33]  J. Kleinschmidt,et al.  Carrier-mediated release of GABA from retinal horizontal cells , 1983, Brain Research.

[34]  E. Raviola,et al.  Structure of the synaptic membranes in the inner plexiform layer of the retina: A freeze‐fracture study in monkeys and rabbits , 1982, The Journal of comparative neurology.

[35]  Ralph J. Jensen,et al.  Ganglion cells and (dye-coupled) amacrine cells in the turtle retina that have possible synaptic connection , 1982, Brain Research.

[36]  E. A. Schwartz,et al.  Calcium‐independent release of GABA from isolated horizontal cells of the toad retina. , 1982, The Journal of physiology.

[37]  K I Naka,et al.  Direct electrical connections between transient amacrine cells in the catfish retina. , 1981, Science.

[38]  Y. Dudai,et al.  Benzodiazepine receptors in chick retina: development and cellular localization , 1981, Brain Research.

[39]  W. F. Hughes,et al.  On the synaptogenic sequence in the chick retina , 1974, The Anatomical record.

[40]  M. Wong-Riley Synaptic organization of the inner plexiform layer in the retina of the tiger salamander , 1974, Journal of neurocytology.

[41]  M. Dubin The inner plexiform layer of the vertebrate retina: A quantitative and comparative electron microscopic analysis , 1970, The Journal of comparative neurology.

[42]  B. Katz,et al.  Membrane Noise produced by Acetylcholine , 1970, Nature.

[43]  J. Dowling,et al.  Organization of the retina of the mudpuppy, Necturus maculosus. II. Intracellular recording. , 1969, Journal of neurophysiology.

[44]  P Sterling,et al.  Computational model of the on-alpha ganglion cell receptive field based on bipolar cell circuitry. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[45]  J. Connor,et al.  Perforated Patch Recording , 1991 .

[46]  P. Michael Conn,et al.  Electrophysiology and microinjection , 1991 .

[47]  H Korn,et al.  Transmission at a central inhibitory synapse. IV. Quantal structure of synaptic noise. , 1990, Journal of neurophysiology.