Spontaneous oscillatory activity of starburst amacrine cells in the mouse retina.
Using patch-clamp techniques, we investigated the characteristics of the spontaneous oscillatory activity displayed by starburst amacrine cells in the mouse retina. At a holding potential of -70 mV, oscillations appeared as spontaneous, rhythmic inward currents with a frequency of approximately 3.5 Hz and an average maximal amplitude of approximately 120 pA. Application of TEA, a potassium channel blocker, increased the amplitude of oscillatory currents by >70% but reduced their frequency by approximately 17%. The TEA effects did not appear to result from direct actions on starburst cells, but rather a modulation of their synaptic inputs. Oscillatory currents were inhibited by 6-cyano-7-nitroquinoxalene-2,3-dione (CNQX), an antagonist of AMPA/kainate receptors, indicating that they were dependent on a periodic glutamatergic input likely from presynaptic bipolar cells. The oscillations were also inhibited by the calcium channel blockers cadmium and nifedipine, suggesting that the glutamate release was calcium dependent. Application of AP4, an agonist of mGluR6 receptors on on-center bipolar cells, blocked the oscillatory currents in starburst cells. However, application of TEA overcame the AP4 blockade, suggesting that the periodic glutamate release from bipolar cells is intrinsic to the inner plexiform layer in that, under experimental conditions, it can occur independent of photoreceptor input. The GABA receptor antagonists picrotoxin and bicuculline enhanced the amplitude of oscillations in starburst cells prestimulated with TEA. Our results suggest that this enhancement was due to a reduction of a GABAergic feedback inhibition from amacrine cells to bipolar cells and the resultant increased glutamate release. Finally, we found that some ganglion cells and other types of amacrine cell also displayed rhythmic activity, suggesting that oscillatory behavior is expressed by a number of inner retinal neurons.
Petit-Jacques
Jerome
J
Department of Ophthalmology, New York University School of Medicine, 550 First Ave., New York, New York 10016, USA.
Völgyi
Béla
B
Rudy
Bernardo
B
Bloomfield
Stewart
S
D018750:6-Cyano-7-nitroquinoxaline-2,3-dione / Q000494:pharmacology; D025042:Amacrine Cells / Q000187:drug effects / Q000502:physiology* / Q000528:radiation effects; D000613:Aminobutyrates / Q000494:pharmacology; D000818:Animals; D001640:Bicuculline / Q000494:pharmacology; D001683:Biological Clocks / Q000187:drug effects / Q000502:physiology* / Q000528:radiation effects; D019256:Cadmium Chloride / Q000494:pharmacology; D004307:Dose-Response Relationship, Radiation; D004347:Drug Interactions; D004558:Electric Stimulation / Q000379:methods; D018690:Excitatory Amino Acid Agonists / Q000494:pharmacology; D018691:Excitatory Amino Acid Antagonists / Q000494:pharmacology; D018756:GABA Antagonists / Q000494:pharmacology; D066298:In Vitro Techniques; D008239:Lysine / Q000031:analogs & derivatives / Q000378:metabolism; D008564:Membrane Potentials / Q000187:drug effects / Q000502:physiology* / Q000528:radiation effects; D051379:Mice; D008813:Mice, Inbred ICR; D018345:Mice, Knockout; D018408:Patch-Clamp Techniques / Q000379:methods; D010852:Picrotoxin / Q000494:pharmacology; D026902:Potassium Channel Blockers / Q000494:pharmacology; D024642:Potassium Channels, Voltage-Gated / Q000172:deficiency; D012160:Retina / Q000166:cytology*; D012165:Retinal Ganglion Cells / Q000187:drug effects / Q000502:physiology / Q000528:radiation effects; D051670:Shaw Potassium Channels; D019789:Tetraethylammonium / Q000494:pharmacology; D013997:Time Factors
D018750:6-Cyano-7-nitroquinoxaline-2,3-dione; D000613:Aminobutyrates; D001640:Bicuculline; D019256:Cadmium Chloride; D018690:Excitatory Amino Acid Agonists; D018691:Excitatory Amino Acid Antagonists; D018756:GABA Antagonists; D008239:Lysine; D010852:Picrotoxin; D026902:Potassium Channel Blockers; D024642:Potassium Channels, Voltage-Gated; D051670:Shaw Potassium Channels; D019789:Tetraethylammonium; C490839:Kcnc1 protein, mouse; C013411:biocytin; C012729:2-amino-4-phosphonobutyric acid