 |
 Previous Article | Next Article 
Journal of Neuroscience, Vol 14, 3805-3815, Copyright © 1994 by Society for Neuroscience
Neuronal coupling in the developing mammalian retina
AA Penn, RO Wong and CJ Shatz
Department of Molecular and Cell Biology, University of California, Berkeley 94720.
During the first 3 weeks of postnatal development in the ferret retina,
cells in the ganglion cell layer spontaneously generate waves of electrical
activity that travel across the retina in the absence of mature
photoreceptors (Meister et al., 1991; Wong et al., 1993). Since few
chemical synapses are present at the earliest stages when waves are
present, we have explored whether gap junctions could act to correlate the
activity of cells in the immature ganglion cell layer. Retinal ganglion
cells in a living in vitro preparation from postnatal day 1 (P1) to P45
were intracellularly injected with the tracer Neurobiotin and the
fluorescent dye Lucifer yellow, molecules that are known to pass through
gap junctions. Lucifer yellow consistently filled only the injected cell,
whereas Neurobiotin filled not only the injected cell but also passed to a
constellation of neighboring cells. Coupling revealed by Neurobiotin is
seen as early as P1, but, at this stage, it was not possible to identify
the various morphological types of cells that were coupled. Thereafter,
alpha ganglion cells showed homologous coupling to other alpha cells and to
both conventionally placed and displaced amacrine cells. Likewise, gamma
ganglion cells appeared coupled to other gamma cells and to amacrine cells.
However, beta ganglion cells never showed tracer coupling in the neonatal
or in adult retinas. The percentage of alpha and gamma cells that were
coupled to other cells increased progressively with age. By the end of the
third postnatal week, the pattern of Neurobiotin coupling in the ferret
retina was adult-like, with virtually every injected alpha cell showing
tracer coupling. Our observations suggest that intercellular junctions able
to pass Neurobiotin are present in the inner plexiform layer during the
period when the firing of retinal ganglion cells is highly correlated. Such
junctions could contribute to synchronization of the activity of subsets of
neighboring ganglion cells during development, but it cannot be the sole
mediator of this activity because beta cells, which also participate in the
correlated activity, showed no coupling at any stage. In addition, the
continued presence of coupling in the adult retina implies that other
changes in retinal circuitry are likely to contribute to the disappearance
of the waves.
This article has been cited by other articles:
|
|
|
|
 
L.-L. Zhang, H. R. Pathak, D. A. Coulter, M. A. Freed, and N. Vardi
Shift of Intracellular Chloride Concentration in Ganglion and Amacrine Cells of Developing Mouse Retina
J Neurophysiol,
April 1, 2006;
95(4):
2404 - 2416.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
A. Marin-Burgin, F. J. Eisenhart, S. M. Baca, W. B. Kristan Jr, and K. A. French
Sequential Development of Electrical and Chemical Synaptic Connections Generates a Specific Behavioral Circuit in the Leech
J. Neurosci.,
March 9, 2005;
25(10):
2478 - 2489.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
S. Hidaka, Y. Akahori, and Y. Kurosawa
Dendrodendritic Electrical Synapses between Mammalian Retinal Ganglion Cells
J. Neurosci.,
November 17, 2004;
24(46):
10553 - 10567.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
M. Md. Syed, S. Lee, S. He, and Z. J. Zhou
Spontaneous Waves in the Ventricular Zone of Developing Mammalian Retina
J Neurophysiol,
May 1, 2004;
91(5):
1999 - 2009.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
K. Cusato, A. Bosco, R. Rozental, C. A. Guimaraes, B. E. Reese, R. Linden, and D. C. Spray
Gap Junctions Mediate Bystander Cell Death in Developing Retina
J. Neurosci.,
July 23, 2003;
23(16):
6413 - 6422.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
K. D. Curtin, Z. Zhang, and R. J. Wyman
Gap Junction Proteins Expressed during Development Are Required for Adult Neural Function in the Drosophila Optic Lamina
J. Neurosci.,
August 15, 2002;
22(16):
7088 - 7096.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
R. E. Marc and B. W. Jones
Molecular Phenotyping of Retinal Ganglion Cells
J. Neurosci.,
January 15, 2002;
22(2):
413 - 427.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
J. H. Singer, R. R. Mirotznik, and M. B. Feller
Potentiation of L-Type Calcium Channels Reveals Nonsynaptic Mechanisms that Correlate Spontaneous Activity in the Developing Mammalian Retina
J. Neurosci.,
November 1, 2001;
21(21):
8514 - 8522.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
N. Tian, C. Petersen, S. Kash, S. Baekkeskov, D. Copenhagen, and R. Nicoll
The role of the synthetic enzyme GAD65 in the control of neuronal gamma -aminobutyric acid release
PNAS,
October 26, 1999;
96(22):
12911 - 12916.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
E. Sernagor and N. M. Grzywacz
Spontaneous Activity in Developing Turtle Retinal Ganglion Cells: Pharmacological Studies
J. Neurosci.,
May 15, 1999;
19(10):
3874 - 3887.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
D. A. Butts, M. B. Feller, C. J. Shatz, and D. S. Rokhsar
Retinal Waves Are Governed by Collective Network Properties
J. Neurosci.,
May 1, 1999;
19(9):
3580 - 3593.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
L. D. Milner and L. T. Landmesser
Cholinergic and GABAergic Inputs Drive Patterned Spontaneous Motoneuron Activity before Target Contact
J. Neurosci.,
April 15, 1999;
19(8):
3007 - 3022.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
B. Wiechers, G. Gestwa, A. Mack, P. Carroll, H.-P. Zenner, and M. Knipper
A Changing Pattern of Brain-Derived Neurotrophic Factor Expression Correlates with the Rearrangement of Fibers during Cochlear Development of Rats and Mice
J. Neurosci.,
April 15, 1999;
19(8):
3033 - 3042.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
S. H. DeVries
Correlated Firing in Rabbit Retinal Ganglion Cells
J Neurophysiol,
February 1, 1999;
81(2):
908 - 920.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
N. Tian, T. N. Hwang, and D. R. Copenhagen
Analysis of Excitatory and Inhibitory Spontaneous Synaptic Activity in Mouse Retinal Ganglion Cells
J Neurophysiol,
September 1, 1998;
80(3):
1327 - 1340.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
K. F. Fischer, P. D. Lukasiewicz, and R. O. L. Wong
Age-Dependent and Cell Class-Specific Modulation of Retinal Ganglion Cell Bursting Activity by GABA
J. Neurosci.,
May 15, 1998;
18(10):
3767 - 3778.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
K. Bittman, D. F. Owens, A. R. Kriegstein, and J. J. LoTurco
Cell Coupling and Uncoupling in the Ventricular Zone of Developing Neocortex
J. Neurosci.,
September 15, 1997;
17(18):
7037 - 7044.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
F. Strata, M. Atzori, M. Molnar, G. Ugolini, F. Tempia, and E. Cherubini
A Pacemaker Current in Dye-Coupled Hilar Interneurons Contributes to the Generation of Giant GABAergic Potentials in Developing Hippocampus
J. Neurosci.,
February 15, 1997;
17(4):
1435 - 1446.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
