Skip to main content
Log in

Properties of mouse retinal ganglion cell dendritic growth during postnatal development

  • Research Papers
  • Published:
Science China Life Sciences Aims and scope Submit manuscript

Abstract

The property of dendritic growth dynamics during development is a subject of intense interest. Here, we investigated the dendritic motility of retinal ganglion cells (RGCs) during different developmental stages, using ex vivo mouse retina explant culture, Semliki Forest Virus transfection and time-lapse observations. The results illustrated that during development, the dendritic motility underwent a change from rapid growth to a relatively stable state, i.e., at P0 (day of birth), RGC dendrites were in a highly active state, whereas at postnatal 13 (P13) they were more stable, and at P3 and P8, the RGCs were in an intermediate state. At any given developmental stage, RGCs of different types displayed the same dendritic growth rate and extent. Since the mouse is the most popular mammalian model for genetic manipulation, this study provided a methodological foundation for further exploring the regulatory mechanisms of dendritic development.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. Pu M, Berson D M, Pan T. Structure and function of retinal ganglion cells innervating the cat’s geniculate wing: An in vitro study. J Neurosci, 1994, 14: 4338–4358 8027783, 1:STN:280:DyaK2czgtVemsw%3D%3D

    PubMed  CAS  Google Scholar 

  2. Rockhill R L, Daly F J, MacNeil M A, et al. The diversity of ganglion cells in a mammalian retina. J Neurosci, 2002, 22: 3831–3843 11978858, 1:CAS:528:DC%2BD38Xjs1Sls7k%3D

    PubMed  CAS  Google Scholar 

  3. Sun W, Li N, He S. Large-scale morophological survey of rat retinal ganglion cells. Vis Neurosci, 2002, 19: 483–493 12511081

    PubMed  Google Scholar 

  4. Sun W, Li N, He S. Large-scale morphological survey of mouse retinal ganglion cells. J Comp Neurol, 2002, 451: 115–126 10.1002/cne.10323, 12209831

    Article  PubMed  Google Scholar 

  5. Kong J H, Fish D R, Rockhill R L, et al. Diversity of ganglion cells in the mouse retina: unsupervised morphological classification and its limits. J Comp Neurol, 2005, 489: 293–310 10.1002/cne.20631, 16025455

    Article  PubMed  Google Scholar 

  6. Chen Y, Naito J. Morphological properties of chick retinal ganglion cells in relation to their central projections. J Comp Neurol, 2009, 514: 117–130 10.1002/cne.21995, 19263477

    Article  PubMed  Google Scholar 

  7. Masland R H. The fundamental plan of the retina. Nat Neurosci, 2001, 4: 877–886 10.1038/nn0901-877, 11528418, 1:CAS:528:DC%2BD3MXmtlaqu70%3D

    Article  PubMed  CAS  Google Scholar 

  8. 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: 7037–7045 7472459, 1:CAS:528:DyaK2MXptlOnur8%3D

    PubMed  CAS  Google Scholar 

  9. Chen M, Weng S, Deng Q, et al. Physiological properties of direction-selective ganglion cells in early postnatal and adult mouse retina. J Physiol, 2009, 587: 819–828 10.1113/jphysiol.2008.161240, 19103682, 1:CAS:528:DC%2BD1MXjtFGqt7s%3D

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  10. Chen Y, Hu M, Shibata H, et al. Changes in somal growth and dendritic patterns of the retinal ganglion cells in the chicks and chick embryos. J Vet Med Sci, 2003, 65: 1135–1137 10.1292/jvms.65.1135, 14600356

    Article  PubMed  Google Scholar 

  11. Diao L, Sun W, Deng Q, et al. Development of the mouse retina: Emerging morphological diversity of the ganglion cells. J Neurobiol, 2004, 61: 236–249 10.1002/neu.20041, 15389605

    Article  PubMed  Google Scholar 

  12. Leventhal A G, Schall J D, Ault S J. Extrinsic determinants of retinal ganglion cell structure in the cat. J Neurosci, 1988, 8: 2028–2038 3385487, 1:STN:280:DyaL1c3lvVKjsA%3D%3D

    PubMed  CAS  Google Scholar 

  13. Liets L C, Olshausen B A, Wang G Y, et al. Spontaneous activity of morphologically identified ganglion cells in the developing ferret retina. J Neurosci, 2003, 23: 7343–7350 12917368, 1:CAS:528:DC%2BD3sXms1Wntrw%3D

    PubMed  CAS  Google Scholar 

  14. Lin B, Wang S W, Masland R H. Retinal ganglion cell type, size, and spacing can be specified independent of homotypic dendritic contacts. Neuron, 2004, 43: 475–485 10.1016/j.neuron.2004.08.002, 15312647, 1:CAS:528:DC%2BD2cXnsVeitbw%3D

    Article  PubMed  CAS  Google Scholar 

  15. Maslim J, Webster M, Stone J. Stages in the structural differentiation of retinal ganglion cells. J Comp Neurol, 1986, 254: 382–402 10.1002/cne.902540310, 3794013, 1:STN:280:DyaL2s%2FosVWltg%3D%3D

    Article  PubMed  CAS  Google Scholar 

  16. Mumm J S, Godinho L, Morgan J L, et al. Laminar circuit formation in the vertebrate retina. Prog Brain Res, 2005, 147: 155–169 10.1016/S0079-6123(04)47012-5, 15581704

    Article  PubMed  Google Scholar 

  17. Mumm J S, Williams P R, Godinho L, et al. In vivo imaging reveals dendritic targeting of laminated afferents by zebrafish retinal ganglion cells. Neuron, 2006, 52: 609–621 10.1016/j.neuron.2006.10.004, 17114046, 1:CAS:528:DC%2BD28XhtlSmtLnO

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  18. Perry V H, Linden R. Evidence for dendritic competition in the developing retina. Nature, 1982, 297: 683–685 10.1038/297683a0, 7088156, 1:STN:280:DyaL383itVSnsg%3D%3D

    Article  PubMed  CAS  Google Scholar 

  19. Ramoa A S, Campbell G, Shatz C J. Dendritic growth and remodeling of cat retinal ganglion cells during fetal and postnatal development. J Neurosci, 1988, 8: 4239–4261 3183722, 1:STN:280:DyaL1M%2Fjs1enuw%3D%3D

    PubMed  CAS  Google Scholar 

  20. Ramoa A S, Yamasaki E N. Transient retinal ganglion cells in the developing rat are characterized by specific morphological properties. J Comp Neurol, 1996, 368: 582–596 10.1002/(SICI)1096-9861(19960513)368:4<582::AID-CNE9>3.0.CO;2-0, 8744445, 1:STN:280:DyaK28zgvV2jtQ%3D%3D

    Article  PubMed  CAS  Google Scholar 

  21. Tian N. Synaptic activity, visual experience and the maturation of retinal synaptic circuitry. J Physiol, 2008, 586: 4347–4355 10.1113/jphysiol.2008.159202, 18669531, 1:CAS:528:DC%2BD1cXht1SnsLzE

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  22. Weber A J, Kalil R E, Stanford L R. Dendritic field development of retinal ganglion cells in the cat following neonatal damage to visual cortex: Evidence for cell class specific interactions. J Comp Neurol, 1998, 390: 470–480 10.1002/(SICI)1096-9861(19980126)390:4<470::AID-CNE2>3.0.CO;2-Y, 9450530, 1:STN:280:DyaK1c7htV2qsw%3D%3D

    Article  PubMed  CAS  Google Scholar 

  23. Wong W T, Faulkner-Jones B E, Sanes J R, et al. Rapid dendritic remodeling in the developing retina: dependence on neurotransmission and reciprocal regulation by Rac and Rho. J Neurosci, 2000, 20: 5024–5036 10864960, 1:CAS:528:DC%2BD3cXksF2jt70%3D

    PubMed  CAS  Google Scholar 

  24. Wong W T, Wong R O. Changing specificity of neurotransmitter regulation of rapid dendritic remodeling during synaptogenesis. Nat Neurosci, 2001, 4: 351–352 10.1038/85987, 11276221, 1:CAS:528:DC%2BD3MXitlCmsLo%3D

    Article  PubMed  CAS  Google Scholar 

  25. Xu H P, Tian N. Retinal ganglion cell dendrites undergo a visual activity-dependent redistribution after eye opening. J Comp Neurol, 2007, 503: 244–259 10.1002/cne.21379, 17492624

    Article  PubMed  Google Scholar 

  26. Yamagata M, Sanes J R. Dscam and Sidekick proteins direct lamina-specific synaptic connections in vertebrate retina. Nature, 2008, 451: 465–469 10.1038/nature06469, 18216854, 1:CAS:528:DC%2BD1cXhtVGnsrw%3D

    Article  PubMed  CAS  Google Scholar 

  27. Yamagata M, Weiner J A, Sanes J R. Sidekicks: Synaptic adhesion molecules that promote lamina-specific connectivity in the retina. Cell, 2002, 110: 649–660 10.1016/S0092-8674(02)00910-8, 12230981, 1:CAS:528:DC%2BD38XntlOhsbc%3D

    Article  PubMed  CAS  Google Scholar 

  28. Yamasaki E N, Ramoa A S. Dendritic remodelling of retinal ganglion cells during development of the rat. J Comp Neurol, 1993, 329: 277–289 10.1002/cne.903290209, 8454733, 1:STN:280:DyaK3s3gtlCnsA%3D%3D

    Article  PubMed  CAS  Google Scholar 

  29. Ren L, Liang H, Diao L, et al. Changing dendritic field size of mouse retinal ganglion cells in early postnatal development. Dev Neurobiol, 2010, 70: 397–407 10.1002/dneu.20777, 19998271

    Article  PubMed  Google Scholar 

  30. Stacy R C, Wong R O. Developmental relationship between cholinergic amacrine cell processes and ganglion cell dendrites of the mouse retina. J Comp Neurol, 2003, 456: 154–166 10.1002/cne.10509, 12509872

    Article  PubMed  Google Scholar 

  31. Sherry D M, Wang M M, Bates J, et al. Expression of vesicular glutamate transporter 1 in the mouse retina reveals temporal ordering in development of rod vs. cone and ON vs. OFF circuits. J Comp Neurol, 2003, 465: 480–498 10.1002/cne.10838, 12975811, 1:CAS:528:DC%2BD3sXoslWqsbo%3D

    Article  PubMed  CAS  Google Scholar 

  32. Flores-Herr N, Protti D A, Wassle H. Synaptic currents generating the inhibitory surround of ganglion cells in the mammalian retina. J Neurosci, 2001, 21: 4852–4863 11425912, 1:CAS:528:DC%2BD3MXks1aktrk%3D

    PubMed  CAS  Google Scholar 

  33. Ehrengruber M U, Lundstrom K, Schweitzer C, et al. Recombinant Semliki Forest virus and Sindbis virus efficiently infect neurons in hippocampal slice cultures. Proc Natl Acad Sci USA, 1999, 96: 7041–7046 10.1073/pnas.96.12.7041, 10359835, 1:CAS:528:DyaK1MXks1Wktbw%3D

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  34. Bansal A, Singer J H, Hwang B J, 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: 7672–7681 11027228, 1:CAS:528:DC%2BD3cXns1eisbw%3D

    PubMed  CAS  Google Scholar 

  35. Blankenship A G, Feller M B. Mechanisms underlying spontaneous patterned activity in developing neural circuits. Nat Rev Neurosci, 2010, 11: 18–29 10.1038/nrn2759, 19953103, 1:CAS:528:DC%2BD1MXhsV2ktrjJ

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  36. Cepko C L, Austin C P, Yang X, et al. Cell fate determination in the vertebrate retina. Proc Natl Acad Sci USA, 1996, 93: 589–595 10.1073/pnas.93.2.589, 8570600, 1:CAS:528:DyaK28XnslOnsA%3D%3D

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  37. Young R W. Cell differentiation in the retina of the mouse. Anat Rec, 1985, 212: 199–205 10.1002/ar.1092120215, 3842042, 1:STN:280:DyaL2s%2FitlymsA%3D%3D

    Article  PubMed  CAS  Google Scholar 

  38. Hering H, Kroger S. Formation of synaptic specializations in the inner plexiform layer of the developing chick retina. J Comp Neurol, 1996, 375: 393–405 10.1002/(SICI)1096-9861(19961118)375:3<393::AID-CNE4>3.0.CO;2-Y, 8915838, 1:STN:280:DyaK2s%2FntlSqsg%3D%3D

    Article  PubMed  CAS  Google Scholar 

  39. Fisher L J. Development of synaptic arrays in the inner plexiform layer of neonatal mouse retina. J Comp Neurol, 1979, 187: 359–372 10.1002/cne.901870207, 489784, 1:STN:280:DyaL3c%2FislOmsw%3D%3D

    Article  PubMed  CAS  Google Scholar 

  40. McArdle C B, Dowling J E, Masland R H. Development of outer segments and synapses in the rabbit retina. J Comp Neurol, 1977, 175: 253–274 10.1002/cne.901750302, 903423, 1:STN:280:DyaE1c%2FgsFylug%3D%3D

    Article  PubMed  CAS  Google Scholar 

  41. Olney J W. An electron microscopic study of synapse formation, receptor outer segment development, and other aspects of developing mouse retina. Invest Ophthalmol, 1968, 7: 250–268 5655873, 1:STN:280:DyaF1c3ot1CmtQ%3D%3D

    PubMed  CAS  Google Scholar 

  42. Morgan J L, Dhingra A, Vardi N, et al. Axons and dendrites originate from neuroepithelial-like processes of retinal bipolar cells. Nat Neurosci, 2006, 9: 85–92 10.1038/nn1615, 16341211, 1:CAS:528:DC%2BD2MXhtlCms7vE

    Article  PubMed  CAS  Google Scholar 

  43. Naito J, Chen Y. Morphological features of chick retinal ganglion cells. Anat Sci Int, 2004, 79: 213–225 10.1111/j.1447-073x.2004.00084.x, 15633460

    Article  PubMed  Google Scholar 

  44. Naito J, Chen Y. Morphologic analysis and classification of ganglion cells of the chick retina by intracellular injection of Lucifer Yellow and retrograde labeling with DiI. J Comp Neurol, 2004, 469: 360–376 10.1002/cne.11010, 14730588

    Article  PubMed  Google Scholar 

  45. Urbanska M, Blazejczyk M, Jaworski J. Molecular basis of dendritic arborization. Acta Neurobiol Exp (Wars), 2008, 68: 264–288

    Google Scholar 

  46. Chan Y C, Chiao C C. Effect of visual experience on the maturation of ON-OFF direction selective ganglion cells in the rabbit retina. Vision Res, 2008, 48: 2466–2475 10.1016/j.visres.2008.08.010, 18782584

    Article  PubMed  Google Scholar 

  47. Lau K C, So K F, Tay D. Effects of visual or light deprivation on the morphology, and the elimination of the transient features during development, of type I retinal ganglion cells in hamsters. J Comp Neurol, 1990, 300: 583–592 10.1002/cne.903000411, 2273094, 1:STN:280:DyaK3M7gslygtQ%3D%3D

    Article  PubMed  CAS  Google Scholar 

  48. Niell C M, Smith S J. Functional imaging reveals rapid development of visual response properties in the zebrafish tectum. Neuron, 2005, 45: 941–951 10.1016/j.neuron.2005.01.047, 15797554, 1:CAS:528:DC%2BD2MXjt1Oitbk%3D

    Article  PubMed  CAS  Google Scholar 

  49. Tian N. Visual experience and maturation of retinal synaptic pathways. Vision Res, 2004, 44: 3307–3316 10.1016/j.visres.2004.07.041, 15535998

    Article  PubMed  Google Scholar 

  50. Tian N, Copenhagen D R. Visual stimulation is required for refinement of ON and OFF pathways in postnatal retina. Neuron, 2003, 39: 85–96 10.1016/S0896-6273(03)00389-1, 12848934, 1:CAS:528:DC%2BD3sXlsV2ku7Y%3D

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to ShiGang He.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Yang, X., Shi, X. & He, S. Properties of mouse retinal ganglion cell dendritic growth during postnatal development. Sci. China Life Sci. 53, 669–676 (2010). https://doi.org/10.1007/s11427-010-4004-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11427-010-4004-6

Keywords

Navigation