Ectopic retinal ON bipolar cell synapses in the OFF inner plexiform layer: contacts with dopaminergic amacrine cells and melanopsin ganglion cells.
A key principle of retinal organization is that distinct ON and OFF channels are relayed by separate populations of bipolar cells to different sublaminae of the inner plexiform layer (IPL). ON bipolar cell axons have been thought to synapse exclusively in the inner IPL (the ON sublamina) onto dendrites of ON-type amacrine and ganglion cells. However, M1 melanopsin-expressing ganglion cells and dopaminergic amacrine (DA) cells apparently violate this dogma. Both are driven by ON bipolar cells, but their dendrites stratify in the outermost IPL, within the OFF sublamina. Here, in the mouse retina, we show that some ON cone bipolar cells make ribbon synapses in the outermost OFF sublayer, where they costratify with and contact the dendrites of M1 and DA cells. Whole-cell recording and dye filling in retinal slices indicate that type 6 ON cone bipolars provide some of this ectopic ON channel input. Imaging studies in dissociated bipolar cells show that these ectopic ribbon synapses are capable of vesicular release. There is thus an accessory ON sublayer in the outer IPL.
Dumitrescu
Olivia N
ON
Department of Neuroscience, Brown University, Providence, Rhode Island 02912.
Pucci
Francesco G
FG
Wong
Kwoon Y
KY
Berson
David M
DM
D025042:Amacrine Cells / Q000502:physiology*; D000818:Animals; D004298:Dopamine / Q000378:metabolism*; D004558:Electric Stimulation / Q000379:methods; D049452:Green Fluorescent Proteins / Q000235:genetics; D066298:In Vitro Techniques; D055537:Light Signal Transduction / Q000235:genetics; D051379:Mice; D008810:Mice, Inbred C57BL; D008822:Mice, Transgenic; D018408:Patch-Clamp Techniques; D010775:Photic Stimulation / Q000379:methods; D011726:Pyridinium Compounds / Q000378:metabolism; D000644:Quaternary Ammonium Compounds / Q000378:metabolism; D018094:Receptors, Metabotropic Glutamate / Q000235:genetics; D012160:Retina / Q000166:cytology*; D051245:Retinal Bipolar Cells / Q000502:physiology*; D012165:Retinal Ganglion Cells / Q000502:physiology*; D017299:Rod Opsins / Q000235:genetics / Q000378:metabolism*; D013569:Synapses / Q000145:classification / Q000502:physiology*; D055366:Synaptic Potentials / Q000235:genetics; D014446:Tyrosine 3-Monooxygenase / Q000235:genetics; D014795:Visual Pathways / Q000502:physiology; D001616:beta-Galactosidase / Q000235:genetics; D000099210:Melanopsin
D004298:Dopamine; D049452:Green Fluorescent Proteins; D011726:Pyridinium Compounds; D000644:Quaternary Ammonium Compounds; D018094:Receptors, Metabotropic Glutamate; D017299:Rod Opsins; D014446:Tyrosine 3-Monooxygenase; D001616:beta-Galactosidase; D000099210:Melanopsin; C092350:FM 4-64; C485184:enhanced green fluorescent protein; C113897:metabotropic glutamate receptor 6