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Kolb H, Fernandez E, Nelson R, editors. Webvision: The Organization of the Retina and Visual System [Internet]. Salt Lake City (UT): University of Utah Health Sciences Center; 1995-.

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Webvision: The Organization of the Retina and Visual System [Internet].

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Development of Retinal Ganglion Cell Dendritic Structure and Synaptic Connections

, MD-PhDcorresponding author1.

Associate Professor of Ophthalmology and Neurobiology, Moran Eye Center, University of Utah School of Medicine.
corresponding authorCorresponding author.

Created: .

1. Introduction

The neuronal information of the visual scene that is processed by the retina is conducted to the brain by a set of separate spatio-temporal synaptic pathways. The morphological basis for the formation of these parallel synaptic pathways is the laminar-specific structure of the retina, in which specific subtypes of retinal neurons form synapses only with highly selective presynaptic and postsynaptic cells (1-3).

Retinal ganglion cells (RGCs) are the output neurons of the retina. In the retina, RGCs synapse with bipolar and amacrine cells in the inner plexiform layer (IPL) to receive excitatory and inhibitory synaptic inputs respectively. The axons of RGCs travel through the optic nerve to retinorecipient structures in the brain, where they transfer their specific aspects of visual information to the higher centers (3). Because different subtypes of bipolar cells (Fig 1) (4) and amacrine cells (Fig. 2) (5) have their axonal/dendritic terminals in the specific sublaminae of the IPL, it is crucial that dendrites of individual RGCs are also confined to specific strata in order to synapses with them.

Figure 1: The major subtypes of bipolar cells of primate retina (Adapted from Wässle, 2004 (10))


Figure 1: The major subtypes of bipolar cells of primate retina (Adapted from Wässle, 2004 (10)). Similar types have been observed in the rats (4), rabbit, cat (15, 74), monkey (75) and human (76).

Figure 2


Figure 2. Schematic drawings of some of the amacrine cells of rabbit retina show each type has a characteristic morphology and stratification of the dendrites to specific strata (1-5) of the inner plexiform layer. All other mammals have similar cells. (more...)

Thus, the synaptic circuitries processing distinct visual features, the so called “parallel pathways” (1, 2, 6-10), start in the retina. In most mammals, RGCs can be divided into about 20 morphological subtypes based on their distinctive dendritic structure and synaptic connections (11-19). The wholemount drawings of mouse RGCs (Fig. 3) illustrate the diversity of morphologies present in mammalian RGCs ((19). See also RGCs of human, cat and rabbit retinas in the ganglion cell chapter in Webvision).

Figure 3


Figure 3. About 22 subtypes of retinal ganglion cells (RGCs) are present in the mammalian retina (See chapter on ganglion cells, Webvision). Camera lucida drawings show the RGCs of mouse retina. Adapted from Volgyi et al., 2009 (19).

Most of these RGCs have specific dendritic distribution in the IPL in adult retina as exemplified by the schematic (Fig. 4) showing the branching patterns of mouse RGCs. In most mammals, these lamina-restricted distributions of RGC dendrites and synaptic connections are formed during pre- and post-natal development. The question is how this lamination arises.

Figure 4


Figure 4. Dendritic ramification depth of the 22 mouse RGC subtypes (From Volgi et al., 2009 (19)). Solid horizontal lines represent the inner and outer borders of the IPL, whereas dashed lines separate the 5 IPL strata. Numbers on the left represent (more...)

2. Neurogenesis and synaptogenesis of retina

The neurogenesis and synaptogenesis of mammalian retina is an orderly process. Figure 5 shows an overview drawing of the development of mouse retinal neurons. RGCs differentiate first followed by amacrine cells, cones and horizontal cells. Rod photoreceptors differentiate shortly afterward. Bipolar cells are the last neurons to differentiate. In mammals most retinal neurons differentiate before birth (20-22).

Figure 5


Figure 5. In mouse retina, neurogenesis begins before birth and is largely completed shortly after birth (A.). However neurogenesis of rods and bipolar cells starts before birth and continues for 1-2 weeks after birth (77). B: Synaptogenesis of mouse (more...)

The order of synaptogenesis of retinal neurons is somewhat different from the order of neurogenesis. The synapses of amacrine cells in the IPL appear first. These are followed by the synaptic formation between photoreceptors and horizontal cells in the OPL. The last synaptic element to link photoreceptors in the outer retina and RGCs in the inner retina is the synaptic connection between bipolar cells and RGCs (Fig. 5A) (23, 24). In mouse, the density of both ribbons and conventional synapses in the IPL continuously increases after eye opening and reaches the peak level by the age of P21 (Fig. 5B). Functionally, the strength of RGC synaptic inputs measured by the frequency of spontaneous synaptic activity is low before eye opening in mice. After eye opening, a surge of glutamate receptor-mediated spontaneous excitatory postsynaptic currents (sEPSCs) and GABA/glycine receptor-mediated spontaneous inhibitory postsynaptic currents emerges around P25 (Fig. 5B). Amplitudes of RGC light responses in cat and ferret retina are also found to increase after eye opening (25, 26). In rabbit and rat, the amplitudes of retinal light responses measured by electroretinography continuously increases in the first month after birth and reaches the adult level by the ages of P30 to P40 (27, 28).

During synaptogenesis, the dendrites of mouse RGCs undergo very active remodeling. More than 30% of dendritic filopodial branches in the mouse are replaced every hour by continuous dendritic growth and elimination (pruning) between P10-13 (see Fig 6 and movie 1). This developmental remodeling of RGC dendrites is thought to play an important role in synaptogenesis and the formation of lamina-restricted dendritic distributions of RGCs.

Figure 6: Dendrites of mouse RGCs undergo very active remodeling during synaptogenesis in postnatal development


Figure 6: Dendrites of mouse RGCs undergo very active remodeling during synaptogenesis in postnatal development. RGC dendritic motility was examined using time-lapse confocal imaging on retinas of YFP+ mice at P13-14. A: Representative image of an A1 (more...)

Movie 1. Changes in filopodial growth and shape in the course of one hour.

Movie 1

Changes in filopodial growth and shape in the course of one hour.

3. Formation of lamina-restricted dendritic distributions of RGCs

Many studies have shown that the dendritic morphology and synaptic connections of RGCs undergo profound refinement during postnatal development. Early in postnatal development, the dendrites of many RGCs ramify diffusely throughout the IPL of the retina in cats, rats and mice (Fig. 7, A1, A2). With subsequent maturation, RGC dendrites become much more narrowly stratified in the IPL (Fig. 7, A2, B2 and B3) (26, 29-34) at least partially due to a developmental restriction of RGC dendrites (31). Recent studies suggest that different subtypes of RGCs acquire their lamina-restricted dendritic ramification patterns in different ways.

Figure 7: Dendrites of RGCs can reach mature stratified pattern through selective pruning


Figure 7: Dendrites of RGCs can reach mature stratified pattern through selective pruning. A1 and A2: Light micrographs of DiI (1,10-dioctadecyl-3,3,30,30-tetramethyl indocarbocyanine perchlorate) labeled RGCs from transverse sections of the central region (more...)

Some RGCs seem to achieve their restricted lamina patterns by direct targeting without significant pruning. In Figure 8 A1-A3, a bistratified RGC has a bistratified dendritic distribution pattern early at P5 (A1) and retains this bistratified pattern into adulthood (A2 and A3) without an initial diffuse distribution pattern. Similarly in Zebrafish some RGCs directly elaborate their dendrites to the middle of the IPL and later became strictly monostratified, occupying a single stratum in the middle of the IPL (Fig. 8 B1, B2 and B3) (35).

Figure 8


Figure 8. Dendrites of RGCs can reach mature stratified pattern by direct targeting. A1, A2 and A3: Retinal sections from P5, P8, and P12-P13 BD mice, respectively. RGCs were labeled with anti-GFP (green) and starburst amacrines with anti-ChAT (red). (more...)

It is also clear that some RGCs form their lamina-restricted dendritic patterns through both direct targeting and selective dendritic pruning (Fig. 9). In Figure 9, A1-A3, the dendritic trees of a subtype of RGCs are diffusely ramified with many side branches originally and become bistratified to two strata above and below the cholinergic starburst type a cell with significant pruning of their dendritic branches (33). Similarly in Figure 9 B1-B3, a zebrafish RGC starts its dendrites in the inner strata of the IPL and then selectively prunes the dendrites in the inner strata and grows the dendrites in the outer strata of the IPL over time (35).

Figure 9


Figure 9. Dendrites of RGCs can reach mature stratified pattern by targeted growth and selective pruning. A1, A2 and A3: Retinal sections from P5, P8, and P12-P13 W7 mice, respectively. RGCs were labeled with anti-GFP (green) and starburst amacrines with (more...)

4. Regulation of the formation of lamina-restricted dendritic patterns of RGCs

The regulatory mechanisms for the formation of the lamina-restricted dendritic patterns of RGCs are not completely understood. It has been reported that many molecular cues play crucial roles in the formation of laminar-restricted dendritic pattern of some subtypes of RGCs. The immunoglobulin superfamily adhesion molecules, DSCAMs and sidekicks, have been reported to direct laminar-specific axonal and dendritic ramification of bipolar cells and RGCs in chick retina (36) and RGC neurite arborization and mosaic formation in mouse retina (37). The transmembrane semaphorin Sema6A and its receptor PlexinA4 (PlexA4) have also been reported to control the stratification of the dendrites of dopaminergic amacrine cells, melanopsin containing RGCs and calbindin-positive cells into ON and OFF sublaminae of the IPL in mouse retina (38). Fig 10A shows that transmembrane semaphorin Sema5A and Sema5B normally constrain dendritic targeting of melanopsin-expressing RGCs to the IPL. In Sema5A-/- and Sema5B-/- mice the RGCs exhibit aberrant dendritic branching in INL, OPL and ONL (Fig. 10B, 10C and 10G).

Figure 10


Figure 10. Sema5A and Sema5B constrain dendritic targeting of RGCs to the IPL. WT; Thy-1:GFP-M (A) and Sema5A-/-; Sema5B-/-; Thy-1:GFP-M (B and C) adult retina sections were immunostained with anti-GFP or WT (E) and Sema5A-/-; Sema5B-/- (F and G) adult (more...)

Several reports have also shown that both spontaneous synaptic activity mediated by glutamate receptor (GluR) before eye opening and light evoked retinal activity after eye opening regulate the normal development of the lamina-restricted dendritic patterns of RGCs. In an early developing vertebrate retina like mouse, RGCs fire periodic bursts of action potentials that are highly correlated and propagate across the RGC layer in a wave-like fashion (39). These spontaneous retinal waves are mainly mediated by cholinergic and glutamatergic synaptic transmission (40-45) (see chapter by Ford and Feller, Webvision). The retinal wave mediated by AChR seems to have little effect on the formation of laminar-restricted dendritic pattern of RGCs. In mice, genetic deletion of β2 subunits of nAChR or the sole synthetic enzyme for acetylcholine, choline acetyltransferase, eliminates the retinal waves mediated by nAChRs and causes an insignificant or non detectable change of the development of the lamina-restricted dendritic ramification of RGCs (40, 46).

On the other hand, intraocular injection of APB, an agonist for class III metabotropic GluRs (mGluR6), results in a blockade of glutamate release from ON and rod bipolar cells and causes an arrest of the developmental stratification and segregation of RGC dendrites into ON and OFF synaptic pathways in cats, ferrets and rats (29, 30, 47, 48) (Fig 11).

Figure 11


Figure 11. Glutamate released from bipolar cells regulates the dendritic development of RGCs. A, B and C: Light micrographs of DiI labeled RGCs from sections of a P2, a P10 and an APB-treated P10 cat retina, respectively. At P2 the RGC dendrites are distributed (more...)

Also, intraocular injection of antagonists for NMDA and AMPA receptors, AP5 and NBQX, increases the density of filopodia by more than 100% after 5 days of treatment in mice (see Fig 12, compare A and B). Xu et al. (44) showed that pharmacological blockade of GluR-mediated activity slows the kinetics of RGC dendritic growth and elimination by approximately 50% (Fig. 12D). The disrupted GluR-mediated activity in retina during early postnatal development is associated with profound and permanent defects of RGC dendritic morphology and synaptic function in adults (44). Similarly, Lau et al. (49) showed that blockade of NMDA receptors before eye opening increases the spine density of RGCs in hamsters.

Figure 12


Figure 12. GluR-mediated activity regulates the dendritic development of RGCs. A and B: Representative images and dendritic reconstructions of YFP-expressing RGCs of P12 retinas in control and with intraocular treatment of NBQX+AP5. Note that NBQX+AP5 (more...)

However, genetic blockade of glutamate release from ON bipolar cells eliminates spontaneous and light evoked synaptic inputs to ON RGCs without effect on the spontaneous and light evoked synaptic activity of OFF RGCs and causes no detectable effect on the lamina-restricted dendritic ramification of either ON or OFF RGCs (50). In addition, genetic deletion of the mGluR6 receptor, which blocks ON bipolar cell light evoked synaptic activity, failed to impair dendritic stratification of mouse RGCs (51). Therefore, the effect of GluR-mediated synaptic activity on the development of the lamina-restricted dendritic ramification and synaptic connections of RGCs is somewhat controversial and needs to be further investigated. The effect of light evoked synaptic activity on the development of RGC dendritic restriction and synaptic connection seems to vary among subtypes of RGCs and selective to some synaptic features. Morphologically, dark rearing blocks an age-dependent remodeling of dendritic complexity of a class of “aberrant” RGCs in hamster retina (52). In mice, light deprivation increases the density of conventional synapses in the IPL (53). The developmental ramification of RGC dendrites into OFF lamina of the IPL is selectively impaired by light deprivation in RGCs of mouse retina (54). Functionally, light deprivation blocks the surge of spontaneous synaptic inputs to RGCs, the age-dependent increase of inner retinal light responses measured by ERG oscillatory potentials (55, 56), the segregation of RGC synaptic inputs from ON and OFF synaptic pathways (54), and the maturation of the size of inhibitory receptive field of RGCs (57).

However, light deprivation seems preferentially to affect the maturation of dendrites of OFF RGCs, but not ON RGCs. Xu and Tian (54) quantitatively analyzed the developmental refinement of the dendrites of a random group of RGCs in mouse retina and determined the ramification depth and width of RGC dendrites in the IPL at different postnatal ages (Fig. 13). They showed that a large proportion of RGCs have a single layer of narrowly stratified dendritic plexus ramifying near the centre of the IPL before eye opening (P12), where they could synapse with both ON and OFF bipolar cells. After eye opening, a significant portion of RGCs redistribute their dendrites from the centre of the IPL toward the inner and outer borders of the IPL (Fig. 14A). This laminar-specific redistribution of RGC dendrites is associated with an age-dependent decrease of the number of RGCs receiving synaptic inputs from both ON and OFF bipolar cells (Fig. 14C). In dark reared mice, the RGC dendritic redistribution from the centre of the IPL to sublamina a of the IPL is blocked, which results in a significant increase of the number of RGCs ramifying at the center of the IPL, and a decrease of the number of RGCs ramifying only in sublamina a, in comparison with age-matched controls (Fig. 14A). Physiologically, the number of RGCs responding to both the onset and the offset of light stimulation of mice raised in constant darkness from birth to the ages of P27-30 was 4-fold higher than that of age-matched controls raised in cyclic light, but comparable to the percentage of ON-OFF responsive RGCs of P10-12 mice (58) (Fig. 14C). Similarly, long-term treatment of cat eyes with intraocular injection of APB significantly reduced the number of αRGCs ramifying in the sublamina a and increased the number of multistratified α cells (48).

Figure 13


Figure 13. RGC dendritic distribution in the IPL can be quantified. The dendritic distribution of YFP-expressing RGCs in the IPL was quantified from confocal images Thy1-YFP mice. A: A stacked image (A1), the 90° rotation view (A2) and the quantitative (more...)

Figure 14


Figure 14. Light deprivation alters the dendritic ramification and synaptic inputs of mouse RGCs. A: Peak dendritic location of all mono-stratified RGCs of P12, P33 and P33 dark-reared mice. Note that the number of RGC with peak located near 30% of the (more...)

5. The possible mechanisms of developmental regulation of RGC dendrites

During developmental refinement, the dendritic arborizations of RGCs undergo dynamic elaboration, maintenance or elimination to attain their lamina-restricted ramification pattern. Although neuronal activity influences this remodeling in many subtypes, the underlying molecular mechanisms have not yet been identified. Several studies suggest that calcium is important to link the neuronal activity with dendritic growth and patterning (59). Thus, it has been reported that synaptic stimulation induces calcium influx through voltage-dependent calcium channels and is sufficient to activate a transcriptional program that regulates dendritic growth (60).

BDNF/TrkB has also been shown to play an essential role in the activity-dependent development of RGC dendrites (61). Activation of BDNF promotes the anatomical segregation of the dendrites of ON- and OFF-center RGCs in different sublaminae of the IPL (61, 62), while deletion of TrkB strongly inhibits visual experience-dependent refinement of RGC dendrites (62). In addition, the expression of BDNF in the retina is up-regulated by visual stimulation (61, 63-65). This suggests that light deprivation retards RGC dendritic maturation by reduction of the expression of BDNF. Conversely, over-expression of BDNF precludes the retardation of laminar refinement in dark reared mice (62).

Recent studies demonstrated that genes typically associated with the immune system, such as those in the major histocompatibility complex (MHC), are expressed by neurons in various regions of the CNS, including retina, and play important roles in synapse formation and activity-dependent synaptic plasticity (66-72). Genetic deletion or mutation of a number of MHC class I genes result in the failure of eye-specific segregation of RGC axon projections to the dosal lateral geniculat nucleus (dLGN) (68, 72). Also, long-term potentiation, long-term depression, learning, memory, and neurogenesis in hippocampus are impaired (68, 73).

Xu et al. (44) reported that the key component of MHCI receptor, CD3ζ is specifically expressed by RGCs in mouse retina. Similar to the pharmacological blockade of GluR-mediated activity, genetic mutation of CD3ζ profoundly reduces the kinetics of RGC dendritic growth and pruning, and impairs the lamina-specific segregation of RGC dendrites in the IPL. In addition, CD3ζ-/- mice show a selective reduction of GluR-mediated synaptic transmission in RGCs suggesting that CD3ζ-mediated signaling participates in activity-dependent synaptic maturation of RGCs. However, some of the important questions, such as what are the exact molecule mechanisms with which activation of MHC/CD3ζ on neurons affects the maturation of RGC dendrites, and how MHC/CD3ζ-mediated signaling interacts with neurotransmitter-mediated synaptic activity in dendritic maturation, need to be further addressed.

About the Author

Image NingTian.jpg

Dr. Ning Tian was initially trained as a physician in China (Yichang Medical School) and then received his Master Degree in clinical visual physiology from Zhong-sen Ophthalmic Center, Sun Yat-sen University of Medical Sciences, China. He practiced clinical ophthalmology for a while before doing a PhD in Biophysics and Physiology at the State University of New York at Buffalo with Dr. Malcolm Slaughter. Ning then did a postdoc with Dr. David Copenhagen at University of California, San Francisco. After being an Assistant Research Ophthalmologist at the University of California, San Francisco from 1998-2000, he headed a laboratory at Yale University (2000-2009). Ning is presently an Associate Professor of Ophthalmology and Neurobiology in the Moran Eye Center, University of Utah. His research is focused on understanding the cellular and molecular mechanisms that regulate the maturation of retinal ganglion cell synaptic function and dendritic structure.


Famiglietti E.V. Jr, Kolb H. Structural basis for ON-and OFF-center responses in retinal ganglion cells. Science. 1976;194(4261):193–5. [PubMed: 959847]
Nelson R., Famiglietti E.V. Jr, Kolb H. Intracellular staining reveals different levels of stratification for on- and off-center ganglion cells in the cat retina. J. Neurophysiol. 1978;41(2):472–483. [PubMed: 650277]
Schiller P.H. Parallel information processing channels created in the retina. Proc Natl Acad Sci U S A. 2010;107(40):17087–94. [PMC free article: PMC2951406] [PubMed: 20876118]
Euler T., Wassle H. Immunocytochemical identification of cone bipolar cells in the rat retina. J Comp Neurol. 1995;361(3):461–78. [PubMed: 8550893]
MacNeil M.A., Masland R.H. Extreme diversity among amacrine cells: implications for function. Neuron. 1998;20(5):971–82. [PubMed: 9620701]
Ghosh K.K. et al. Types of bipolar cells in the mouse retina. J Comp Neurol. 2004;469(1):70–82. [PubMed: 14689473]
. J., C. and L.M. Chalupa, Morphological, functional, and developmental properties of mouse retinal ganglion cells., in Eye, retina, and visual system of the mouse, L.M. Chalupa and R.W. Williams, Editors. 2008, MIT Press: Cambridge, Mass. p. 189-199.
Kuffler S.W. Discharge patterns and functional organization of mammalian retina. J Neurophysiol. 1953;16(1):37–68. [PubMed: 13035466]
Masland R.H. The fundamental plan of the retina. Nat Neurosci. 2001;4(9):877–86. [PubMed: 11528418]
Wässle H. Parallel processing in the mammalian retina. Nat Rev Neurosci. 2004;5(10):747–57. [PubMed: 15378035]
Badea T.C., Nathans J. Quantitative analysis of neuronal morphologies in the mouse retina visualized by using a genetically directed reporter. J Comp Neurol. 2004;480(4):331–51. [PubMed: 15558785]
Berson, D.M., Retinal ganglion cell types and their central projections., Volume 1, in The senses : a comprehensive reference, A.I. Basbaum, et al., Editors. 2008, Elsevier: Amsterdam; Boston. p. 491–520.
Coombs J. et al. Morphological properties of mouse retinal ganglion cells. Neuroscience. 2006;140(1):123–36. [PubMed: 16626866]
Dacey D.M., Packer O.S. Colour coding in the primate retina: diverse cell types and cone-specific circuitry. Curr Opin Neurobiol. 2003;13(4):421–7. [PubMed: 12965288]
Kolb H., Nelson R., Mariani A. Amacrine cells, bipolar cells and ganglion cells of the cat retina: a Golgi study. Vision Res. 1981;21(7):1081–1114. [PubMed: 7314489]
Kong J.H. et al. Diversity of ganglion cells in the mouse retina: unsupervised morphological classification and its limits. J Comp Neurol. 2005;489(3):293–310. [PubMed: 16025455]
Rockhill R.L. et al. The diversity of ganglion cells in a mammalian retina. J Neurosci. 2002;22(9):3831–43. [PubMed: 11978858]
Sun W., Li N., He S. Large-scale morphological survey of mouse retinal ganglion cells. J Comp Neurol. 2002;451(2):115–26. [PubMed: 12209831]
Volgyi B., Chheda S., Bloomfield S.A. Tracer coupling patterns of the ganglion cell subtypes in the mouse retina. J Comp Neurol. 2009;512(5):664–87. [PMC free article: PMC3373319] [PubMed: 19051243]
Cepko C.L. et al. Cell fate determination in the vertebrate retina. Proc Natl Acad Sci U S A. 1996;93(2):589–95. [PMC free article: PMC40096] [PubMed: 8570600]
. D, A., T. D, and C.L. Cepko, Specification of cell types in the vertebrate retina. in Proceedings of the Retina Research Foundation symposia, Volume 3, in Development of the Visual System, D.M.-K. Lam and C.J. Shatz, Editors. 1991, MIT Press: Cambridge, Mass. p. 37-58.
Marquardt T., Gruss P. Generating neuronal diversity in the retina: one for nearly all. Trends Neurosci. 2002;25(1):32–8. [PubMed: 11801336]
Nishimura Y., Rakic P. Development of the rhesus monkey retina: II. A three-dimensional analysis of the sequences of synaptic combinations in the inner plexiform layer. J Comp Neurol. 1987;262(2):290–313. [PubMed: 3624556]
Stone, J. and D.H. Rapaport, The development of the topographical organization of the cat’s retina., in Development of visual pathways in mammals : proceedings of a satellite symposium of the XXIX International Congress of the Union of Physiological Sciences, held in Sydney, Australia, August 24-27, 1983, J. Stone, B. Dreher, and D.H. Rapaport, Editors. 1984, A.R. Liss: New York. p. 1-21.
Tootle J.S. Early postnatal development of visual function in ganglion cells of the cat retina. J Neurophysiol. 1993;69(5):1645–60. [PubMed: 8509831]
Wang G.Y., Liets L.C., Chalupa L.M. Unique functional properties of on and off pathways in the developing mammalian retina. J Neurosci. 2001;21(12):4310–7. [PubMed: 11404416]
Gorfinkel J., Lachapelle P., Molotchnikoff S. Maturation of the electroretinogram of the neonatal rabbit. Doc Ophthalmol. 1988;69(3):237–45. [PubMed: 3168725]
Wachtmeister L. Oscillatory potentials in the retina: what do they reveal. Prog Retin Eye Res. 1998;17(4):485–521. [PubMed: 9777648]
Bodnarenko S.R., Chalupa L.M. Stratification of ON and OFF ganglion cell dendrites depends on glutamate-mediated afferent activity in the developing retina. Nature. 1993;364(6433):144–6. [PubMed: 8100613]
Bodnarenko S.R., Jeyarasasingam G., Chalupa L.M. Development and regulation of dendritic stratification in retinal ganglion cells by glutamate-mediated afferent activity. J Neurosci. 1995;15(11):7037–45. [PubMed: 7472459]
Coombs J.L., Van Der List D., Chalupa L.M. Morphological properties of mouse retinal ganglion cells during postnatal development. J Comp Neurol. 2007;503(6):803–14. [PubMed: 17570502]
Diao L. et al. Development of the mouse retina: emerging morphological diversity of the ganglion cells. J Neurobiol. 2004;61(2):236–49. [PubMed: 15389605]
Kim I.J. et al. Laminar restriction of retinal ganglion cell dendrites and axons: subtype-specific developmental patterns revealed with transgenic markers. J Neurosci. 2010;30(4):1452–62. [PMC free article: PMC2822471] [PubMed: 20107072]
Maslim J., Stone J. Time course of stratification of the dendritic fields of ganglion cells in the retina of the cat. Brain Res Dev Brain Res. 1988;44(1):87–93. [PubMed: 3233733]
Mumm J.S. et al. In Vivo Imaging Reveals Dendritic Targeting of Laminated Afferents by Zebrafish Retinal Ganglion Cells. Neuron. 2006;52(4):609–621. [PMC free article: PMC1716713] [PubMed: 17114046]
Yamagata M., Sanes J.R. Dscam and Sidekick proteins direct lamina-specific synaptic connections in vertebrate retina. Nature. 2008;451(7177):465–9. [PubMed: 18216854]
Fuerst P.G. et al. Neurite arborization and mosaic spacing in the mouse retina require DSCAM. Nature. 2008;451(7177):470–4. [PMC free article: PMC2259282] [PubMed: 18216855]
Matsuoka R.L. et al. Transmembrane semaphorin signalling controls laminar stratification in the mammalian retina. Nature. 2011;470(7333):259–63. [PMC free article: PMC3063100] [PubMed: 21270798]
Wong R.O. Retinal waves and visual system development. Annu Rev Neurosci. 1999;22:29–47. [PubMed: 10202531]
Bansal A. et al. Mice lacking specific nicotinic acetylcholine receptor subunits exhibit dramatically altered spontaneous activity patterns and reveal a limited role for retinal waves in forming ON and OFF circuits in the inner retina. J Neurosci. 2000;20(20):7672–81. [PubMed: 11027228]
Demas J., Eglen S.J., Wong R.O. Developmental loss of synchronous spontaneous activity in the mouse retina is independent of visual experience. J Neurosci. 2003;23(7):2851–60. [PubMed: 12684472]
Feller, M. and A. Blankenship, The function of the retina prior to vision: The phenomenon of retinal waves and retinotopic refinement., in Eye, retina, and visual system of the mouse, L.M. Chalupa and R.W. Williams, Editors. 2008, MIT Press: Cambridge, Mass. p. 343-351.
Feller M.B. et al. Requirement for cholinergic synaptic transmission in the propagation of spontaneous retinal waves. Science. 1996;272(5265):1182–7. [PubMed: 8638165]
Xu H.P. et al. The immune protein CD3ζ is required for normal development of neural circuits in the retina. Neuron. 2010;65(4):503–15. [PMC free article: PMC3037728] [PubMed: 20188655]
Zhou Z.J. The function of the cholinergic system in the developing mammalian retina. Prog Brain Res. 2001;131:599–613. [PubMed: 11420974]
Stacy R.C. et al. Disruption and recovery of patterned retinal activity in the absence of acetylcholine. J Neurosci. 2005;25(41):9347–57. [PubMed: 16221843]
Bodnarenko S.R. et al. The development of retinal ganglion cell dendritic stratification in ferrets. Neuroreport. 1999;10(14):2955–9. [PubMed: 10549804]
Deplano S. et al. Long-term treatment of the developing retina with the metabotropic glutamate agonist APB induces long-term changes in the stratification of retinal ganglion cell dendrites. Dev Neurosci. 2004;26(5-6):396–405. [PubMed: 15855769]
Lau K.C., So K.F., Tay D. Postnatal development of type I retinal ganglion cells in hamsters: a lucifer yellow study. J Comp Neurol. 1992;315(4):375–81. [PubMed: 1560113]
Kerschensteiner D. et al. Neurotransmission selectively regulates synapse formation in parallel circuits in vivo. Nature. 2009;460(7258):1016–20. [PMC free article: PMC2746695] [PubMed: 19693082]
Tagawa Y. et al. Immunohistological studies of metabotropic glutamate receptor subtype 6-deficient mice show no abnormality of retinal cell organization and ganglion cell maturation. J Neurosci. 1999;19(7):2568–79. [PubMed: 10087070]
Wingate R.J., Thompson I.D. Targeting and activity-related dendritic modification in mammalian retinal ganglion cells. J Neurosci. 1994;14(11 Pt 1):6621–37. [PubMed: 7965065]
Fisher L.J. Development of retinal synaptic arrays in the inner plexiform layer of dark-reared mice. J Embryol Exp Morphol. 1979;54:219–27. [PubMed: 528867]
Xu H.P., Tian N. Retinal ganglion cell dendrites undergo a visual activity-dependent redistribution after eye opening. J Comp Neurol. 2007;503(2):244–59. [PubMed: 17492624]
Tian N., Copenhagen D.R. Visual deprivation alters development of synaptic function in inner retina after eye opening. Neuron. 2001;32(3):439–49. [PubMed: 11709155]
Vistamehr S., Tian N. Light deprivation suppresses the light response of inner retina in both young and adult mouse. Vis Neurosci. 2004;21(1):23–37. [PubMed: 15137579]
Di Marco S. et al. Permanent functional reorganization of retinal circuits induced by early long-term visual deprivation. J Neurosci. 2009;29(43):13691–701. [PubMed: 19864581]
Tian N., Copenhagen D.R. Visual stimulation is required for refinement of ON and OFF pathways in postnatal retina. Neuron. 2003;39(1):85–96. [PubMed: 12848934]
Wong R.O., Ghosh A. Activity-dependent regulation of dendritic growth and patterning. Nat Rev Neurosci. 2002;3(10):803–12. [PubMed: 12360324]
Redmond L., Kashani A.H., Ghosh A. Calcium regulation of dendritic growth via CaM kinase IV and CREB-mediated transcription. Neuron. 2002;34(6):999–1010. [PubMed: 12086646]
Landi S. et al. Environmental enrichment effects on development of retinal ganglion cell dendritic stratification require retinal BDNF. PLoS One. 2007;2(4):e346. [PMC free article: PMC1829175] [PubMed: 17406670]
Liu X. et al. Brain-derived neurotrophic factor and TrkB modulate visual experience-dependent refinement of neuronal pathways in retina. J Neurosci. 2007;27(27):7256–67. [PMC free article: PMC2579893] [PubMed: 17611278]
Mandolesi G. et al. A role for retinal brain-derived neurotrophic factor in ocular dominance plasticity. Curr Biol. 2005;15(23):2119–24. [PubMed: 16332537]
Pollock G.S. et al. Effects of early visual experience and diurnal rhythms on BDNF mRNA and protein levels in the visual system, hippocampus, and cerebellum. J Neurosci. 2001;21(11):3923–31. [PubMed: 11356880]
Seki M. et al. BDNF is upregulated by postnatal development and visual experience: quantitative and immunohistochemical analyses of BDNF in the rat retina. Invest Ophthalmol Vis Sci. 2003;44(7):3211–8. [PubMed: 12824273]
Baudouin S.J. et al. The signaling adaptor protein CD3zeta is a negative regulator of dendrite development in young neurons. Mol Biol Cell. 2008;19(6):2444–56. [PMC free article: PMC2397320] [PubMed: 18367546]
Corriveau R.A., Huh G.S., Shatz C.J. Regulation of class I MHC gene expression in the developing and mature CNS by neural activity. Neuron. 1998;21(3):505–20. [PubMed: 9768838]
Huh G.S. et al. Functional requirement for class I MHC in CNS development and plasticity. Science. 2000;290(5499):2155–9. [PMC free article: PMC2175035] [PubMed: 11118151]
Ishii T., Hirota J., Mombaerts P. Combinatorial coexpression of neural and immune multigene families in mouse vomeronasal sensory neurons. Curr Biol. 2003;13(5):394–400. [PubMed: 12620187]
Syken J. et al. PirB restricts ocular-dominance plasticity in visual cortex. Science. 2006;313(5794):1795–800. [PubMed: 16917027]
Syken J., Shatz C.J. Expression of T cell receptor beta locus in central nervous system neurons. Proc Natl Acad Sci U S A. 2003;100(22):13048–53. [PMC free article: PMC240742] [PubMed: 14569018]
Xu, Y. and N. Vardi, Modulation of the Light-Activated Cation Channel in Retinal ON Bipolar Cells by G-Protein Subunits. ARVO Meeting Abstracts, 201051(5): p. 4797.
Ziv Y. et al. Immune cells contribute to the maintenance of neurogenesis and spatial learning abilities in adulthood. Nat Neurosci. 2006;9(2):268–75. [PubMed: 16415867]
Sterling, P., Retina, in The Synaptic Organization of the Brain, G.M. Shepard, Editor. 1990, Oxford University Press: New York. p. 170-213.
Boycott B.B., Wässle H. Morphological Classification of Bipolar Cells of the Primate Retina. Eur J Neurosci. 1991;3(11):1069–1088. [PubMed: 12106238]
Kolb H., Linberg K.A., Fisher S.K. Neurons of the human retina: a Golgi study. J Comp Neurol. 1992;318(2):147–87. [PubMed: 1374766]
Young R.W. Cell differentiation in the retina of the mouse. Anat Rec. 1985;212(2):199–205. [PubMed: 3842042]
Fisher L.J. Development of synaptic arrays in the inner plexiform layer of neonatal mouse retina. J Comp Neurol. 1979;187(2):359–72. [PubMed: 489784]
Xu H., Tian N. Pathway-specific maturation, visual deprivation, and development of retinal pathway. Neuroscientist. 2004;10(4):337–46. [PubMed: 15271261]
Matsuoka R.L. et al. Class 5 transmembrane semaphorins control selective Mammalian retinal lamination and function. Neuron. 2011;71(3):460–73. [PMC free article: PMC3164552] [PubMed: 21835343]


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