Synaptic input of ON-bipolar cells onto the dopaminergic neurons of the mouse retina.
In the retina, dopamine fulfills a crucial role in neural adaptation to photopic illumination, but the pathway that carries cone signals to the dopaminergic amacrine (DA) cells was controversial. We identified the site of ON-cone bipolar input onto DA cells in transgenic mice in which both types of catecholaminergic amacrine (CA) cells were labeled with green fluorescent protein or human placental alkaline phosphatase (PLAP). In confocal Z series of retinal whole mounts stained with antibodies to tyrosine hydroxylase (TH), DA cells gave rise to varicose processes that descended obliquely through the scleral half of the inner plexiform layer (IPL) and formed a loose, tangential plexus in the middle of this layer. Comparison with the distribution of the dendrites of type 2 CA cells and examination of neurobiotin-injected DA cells proved that their vitreal processes were situated in stratum S3 of the IPL. Electron microscope demonstration of PLAP activity showed that bipolar cell endings in S3 established ribbon synapses onto a postsynaptic dyad in which one or both processes were labeled by a precipitate of lead phosphate and therefore belonged to DA cells. In places, the postsynaptic DA cell processes returned a reciprocal synapse onto the bipolar endings. Confocal images of sections stained with antibodies to TH, kinesin Kif3a, which labels synaptic ribbons, and glutamate or GABA(A) receptors, confirmed that ribbon-containing endings made glutamatergic synapses onto DA cells processes in S3 and received from them GABAergic synapses. The presynaptic ON-bipolar cells most likely belonged to the CB3 (type 5) variety.
Contini
Massimo
M
Department of Neurobiology, Harvard Medical School, Boston, Massachusetts 02115, USA.
Lin
Bin
B
Kobayashi
Kazuto
K
Okano
Hideyuki
H
Masland
Richard H
RH
Raviola
Elio
E
D000469:Alkaline Phosphatase / Q000235:genetics / Q000378:metabolism; D000818:Animals; D004298:Dopamine / Q000378:metabolism*; D058851:GPI-Linked Proteins; D049452:Green Fluorescent Proteins / Q000235:genetics / Q000378:metabolism; D006801:Humans; D007527:Isoenzymes / Q000235:genetics / Q000378:metabolism; D051379:Mice; D008810:Mice, Inbred C57BL; D008822:Mice, Transgenic; D009474:Neurons / Q000166:cytology / Q000378:metabolism*; D012160:Retina / Q000166:cytology* / Q000378:metabolism; D051245:Retinal Bipolar Cells / Q000166:cytology / Q000378:metabolism*; D013569:Synapses / Q000378:metabolism* / Q000648:ultrastructure; D014446:Tyrosine 3-Monooxygenase / Q000235:genetics / Q000378:metabolism
D058851:GPI-Linked Proteins; D007527:Isoenzymes; D049452:Green Fluorescent Proteins; D014446:Tyrosine 3-Monooxygenase; D000469:Alkaline Phosphatase; C019839:alkaline phosphatase, placental; D004298:Dopamine
Neuron. 1997 May;18(5):723-36
9182798
Science. 1976 Oct 8;194(4261):193-5
959847
Vis Neurosci. 2001 Sep-Oct;18(5):675-85
11925003
J Neurosci. 2003 Aug 20;23(20):7670-6
12930806
J Neurophysiol. 1978 Mar;41(2):472-83
650277
Invest Ophthalmol Vis Sci. 1984 Jan;25(1):66-70
6142028
Proc Natl Acad Sci U S A. 2003 Feb 4;100(3):1358-63
12547914
J Comp Neurol. 1990 Mar 8;293(2):178-89
19189710
Brain Res. 1982 Dec 2;252(1):101-9
7172014
J Neurosci. 1987 Dec;7(12):4115-28
2891802
J Comp Neurol. 2002 Jul 22;449(2):195-205
12115689
J Comp Neurol. 1978 Jul 15;180(2):203-20
207745
Brain Res Dev Brain Res. 1989 Jul 1;48(1):59-72
2568894
Brain Res Bull. 1982 Jul-Dec;9(1-6):379-81
6129041
J Neurosci. 1999 Feb 1;19(3):1027-37
9920666
Neuroscience. 1997 Oct;80(4):987-1000
9284055
Brain Res. 1991 Nov 1;563(1-2):325-8
1664775
Vis Neurosci. 2007 Jul-Aug;24(4):573-80
17705893
Invest Ophthalmol. 1971 Jun;10(6):438-52
4325307
Neurochem Int. 1992 Feb;20(2):139-91
1304857
J Chem Neuroanat. 1996 Nov;12(1):37-50
9001947
J Neurosci. 2009 Jan 7;29(1):106-17
19129389
J Comp Neurol. 2004 Aug 23;476(3):254-66
15269969
J Comp Neurol. 1990 Nov 15;301(3):461-89
1979792
Neuron. 2001 Apr;30(1):211-25
11343656
Science. 1975 Apr 18;188(4185):270-3
804181
Eur J Neurosci. 1995 Apr 1;7(4):630-46
7620614
J Comp Neurol. 1982 Sep 1;210(1):65-79
6127354
J Neurosci. 1987 Sep;7(9):2785-93
2887643
J Neurosci. 1999 Sep 15;19(18):7812-22
10479684
Science. 1988 May 27;240(4856):1196-8
3375811
J Comp Neurol. 1992 Dec 8;326(2):283-301
1479076
Vis Neurosci. 1990 Feb;4(2):159-75
1980203
J Comp Neurol. 1980 Aug 15;192(4):665-85
6252252
J Neurophysiol. 2009 Jul;102(1):146-58
19403749
J Comp Neurol. 2008 Sep 10;510(2):221-36
18623177
FEBS Lett. 1991 Jun 17;284(1):15-8
1647972
Brain Res. 1989 Mar 13;482(1):164-8
2706474
J Neurocytol. 1990 Jun;19(3):343-66
2391538
Doc Ophthalmol. 2004 Jan;108(1):17-40
15104164
J Comp Neurol. 1988 Oct 1;276(1):81-91
2903868
Brain Res. 1979 Jun 22;169(2):261-73
445157
J Comp Neurol. 2004 Apr 19;472(1):73-86
15024753
Proc Natl Acad Sci U S A. 1993 Jun 15;90(12):5667-71
8516316
J Comp Neurol. 2004 Jan 26;469(1):70-82
14689473
J Comp Neurol. 2005 Jan 24;481(4):352-62
15593337
J Neurosci. 2009 Jul 15;29(28):8875-83
19605625
Neurosci Lett. 1981 Dec 23;27(3):255-9
6120490
J Neurosci. 1996 May 1;16(9):2934-44
8622124
Brain Res. 1988 Sep 27;461(1):17-26
2906268
Histochemie. 1967;11(1):88-96
5589645
J Neurosci. 2007 Jan 17;27(3):692-9
17234601
Neurosci Lett. 1991 Jun 10;127(1):125-8
1715535
J Neurochem. 2002 Jul;82(2):295-304
12124430
Proc Natl Acad Sci U S A. 2008 Sep 16;105(37):14181-6
18779590