Skip to main content
Journal of Anatomy logoLink to Journal of Anatomy
. 2001 Oct;199(Pt 4):375–383. doi: 10.1046/j.1469-7580.2001.19940375.x

The role of early neural activity in the maturation of turtle retinal function

EVELYNE SERNAGOR 1,, VANDANA MEHTA 1
PMCID: PMC1468348  PMID: 11693298

Abstract

In the developing vertebrate retina, ganglion cells fire spontaneous bursts of action potentials long before the eye becomes exposed to sensory experience at birth. These early bursts are synchronised between neighbouring retinal ganglion cells (RGCs), yielding unique spatiotemporal patterns: ‘waves’ of activity sweep across large retinal areas every few minutes. Both at retinal and extraretinal levels, these embryonic retinal waves are believed to guide the wiring of the visual system using hebbian mechanisms of synaptic strengthening.

In the first part of this review, we recapitulate the evidence for a role of these embryonic spontaneous bursts of activity in shaping developing complex receptive field properties of RGCs in the turtle embryonic retina. We also discuss the role of visual experience in establishing RGC visual functions, and how spontaneous activity and visual experience interact to bring developing receptive fields to maturation. We have hypothesised that the physiological changes associated with development reflect modifications in the dendritic arbours of RGCs, the anatomical substrate of their receptive fields. We demonstrate that there is a temporal correlation between the period of receptive field expansion and that of dendritic growth. Moreover, the immature spontaneous activity contributes to dendritic growth in developing RGCs. Intracellular staining of RGCs reveals, however, that immature receptive fields only rarely show direct correlation with the layout of the corresponding dendritic tree. To investigate the possibility that not only the presence of the spontaneous activity, but even the precise spatiotemporal patterns encoded in retinal waves might contribute to the refinement of retinal neural circuitry, first we must clarify the mechanisms mediating the generation and propagation of these waves across development. In the second part of this review, we present evidence that turtle retinal waves, visualised using calcium imaging, exhibit profound changes in their spatiotemporal patterns during development. From fast waves sweeping across large retinal areas and recruiting many cells on their trajectory at early stages, waves become slower and eventually stop propagating towards hatching, when they become stationary patches of neighbouring coactive RGCs. A developmental switch from excitatory to inhibitory GABAA responses appears to mediate the modification in spontaneous activity patterns while the retina develops. Future chronic studies using specific spatiotemporal alterations of the waves will shed a new light on how the wave dynamics help in sculpting retinal receptive fields.

Keywords: Retinal waves, ganglion cells, receptor fields, dark-rearing, dendritic growth, calcium imaging

Full Text

The Full Text of this article is available as a PDF (556.3 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Bansal A., Singer J. H., Hwang B. J., Xu W., Beaudet A., Feller M. B. 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 Oct 15;20(20):7672–7681. doi: 10.1523/JNEUROSCI.20-20-07672.2000. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. 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 Jul 8;364(6433):144–146. doi: 10.1038/364144a0. [DOI] [PubMed] [Google Scholar]
  3. 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 Nov;15(11):7037–7045. doi: 10.1523/JNEUROSCI.15-11-07037.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Burgi P. Y., Grzywacz N. M. Possible roles of spontaneous waves and dendritic growth for retinal receptive field development. Neural Comput. 1997 Apr 1;9(3):533–553. doi: 10.1162/neco.1997.9.3.533. [DOI] [PubMed] [Google Scholar]
  5. Campbell G., Ramoa A. S., Stryker M. P., Shatz C. J. Dendritic development of retinal ganglion cells after prenatal intracranial infusion of tetrodotoxin. Vis Neurosci. 1997 Jul-Aug;14(4):779–788. doi: 10.1017/s0952523800012724. [DOI] [PubMed] [Google Scholar]
  6. Catsicas M., Bonness V., Becker D., Mobbs P. Spontaneous Ca2+ transients and their transmission in the developing chick retina. Curr Biol. 1998 Feb 26;8(5):283–286. doi: 10.1016/s0960-9822(98)70110-1. [DOI] [PubMed] [Google Scholar]
  7. Crair M. C. Neuronal activity during development: permissive or instructive? Curr Opin Neurobiol. 1999 Feb;9(1):88–93. doi: 10.1016/s0959-4388(99)80011-7. [DOI] [PubMed] [Google Scholar]
  8. Dacheux R. F., Miller R. F. An intracellular electrophysiological study of the ontogeny of functional synapses in the rabbit retina. I. Receptors, horizontal, and bipolar cells. J Comp Neurol. 1981 May 10;198(2):307–326. doi: 10.1002/cne.901980209. [DOI] [PubMed] [Google Scholar]
  9. Dacheux R. F., Miller R. F. An intracellular electrophysiological study of the ontogeny of functional synapses in the rabbit retina. II. Amacrine cells. J Comp Neurol. 1981 May 10;198(2):327–334. doi: 10.1002/cne.901980210. [DOI] [PubMed] [Google Scholar]
  10. Feller M. B., Wellis D. P., Stellwagen D., Werblin F. S., Shatz C. J. Requirement for cholinergic synaptic transmission in the propagation of spontaneous retinal waves. Science. 1996 May 24;272(5265):1182–1187. doi: 10.1126/science.272.5265.1182. [DOI] [PubMed] [Google Scholar]
  11. Fischer K. F., Lukasiewicz P. D., Wong R. O. Age-dependent and cell class-specific modulation of retinal ganglion cell bursting activity by GABA. J Neurosci. 1998 May 15;18(10):3767–3778. doi: 10.1523/JNEUROSCI.18-10-03767.1998. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Goodman C. S., Shatz C. J. Developmental mechanisms that generate precise patterns of neuronal connectivity. Cell. 1993 Jan;72 (Suppl):77–98. doi: 10.1016/s0092-8674(05)80030-3. [DOI] [PubMed] [Google Scholar]
  13. Grzywacz N. M., Sernagor E. Spontaneous activity in developing turtle retinal ganglion cells: statistical analysis. Vis Neurosci. 2000 Mar-Apr;17(2):229–241. doi: 10.1017/s0952523800172050. [DOI] [PubMed] [Google Scholar]
  14. Lau K. C., So K. F., Tay D. APV prevents the elimination of transient dendritic spines on a population of retinal ganglion cells. Brain Res. 1992 Nov 6;595(1):171–174. doi: 10.1016/0006-8993(92)91471-p. [DOI] [PubMed] [Google Scholar]
  15. Leinekugel X., Khalilov I., McLean H., Caillard O., Gaiarsa J. L., Ben-Ari Y., Khazipov R. GABA is the principal fast-acting excitatory transmitter in the neonatal brain. Adv Neurol. 1999;79:189–201. [PubMed] [Google Scholar]
  16. Maffei L., Galli-Resta L. Correlation in the discharges of neighboring rat retinal ganglion cells during prenatal life. Proc Natl Acad Sci U S A. 1990 Apr;87(7):2861–2864. doi: 10.1073/pnas.87.7.2861. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Masland R. H. Maturation of function in the developing rabbit retina. J Comp Neurol. 1977 Oct 1;175(3):275–286. doi: 10.1002/cne.901750303. [DOI] [PubMed] [Google Scholar]
  18. Meister M., Wong R. O., Baylor D. A., Shatz C. J. Synchronous bursts of action potentials in ganglion cells of the developing mammalian retina. Science. 1991 May 17;252(5008):939–943. doi: 10.1126/science.2035024. [DOI] [PubMed] [Google Scholar]
  19. O'Donovan M. J. The origin of spontaneous activity in developing networks of the vertebrate nervous system. Curr Opin Neurobiol. 1999 Feb;9(1):94–104. doi: 10.1016/s0959-4388(99)80012-9. [DOI] [PubMed] [Google Scholar]
  20. Sernagor E., Eglen S. J., Wong R. O. Development of retinal ganglion cell structure and function. Prog Retin Eye Res. 2001 Mar;20(2):139–174. doi: 10.1016/s1350-9462(00)00024-0. [DOI] [PubMed] [Google Scholar]
  21. Sernagor E., Grzywacz N. M. Emergence of complex receptive field properties of ganglion cells in the developing turtle retina. J Neurophysiol. 1995 Apr;73(4):1355–1364. doi: 10.1152/jn.1995.73.4.1355. [DOI] [PubMed] [Google Scholar]
  22. Sernagor E., Grzywacz N. M. Influence of spontaneous activity and visual experience on developing retinal receptive fields. Curr Biol. 1996 Nov 1;6(11):1503–1508. doi: 10.1016/s0960-9822(96)00755-5. [DOI] [PubMed] [Google Scholar]
  23. Sernagor E., Grzywacz N. M. Spontaneous activity in developing turtle retinal ganglion cells: pharmacological studies. J Neurosci. 1999 May 15;19(10):3874–3887. doi: 10.1523/JNEUROSCI.19-10-03874.1999. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Tootle J. S. Early postnatal development of visual function in ganglion cells of the cat retina. J Neurophysiol. 1993 May;69(5):1645–1660. doi: 10.1152/jn.1993.69.5.1645. [DOI] [PubMed] [Google Scholar]
  25. Wong R. O., Chernjavsky A., Smith S. J., Shatz C. J. Early functional neural networks in the developing retina. Nature. 1995 Apr 20;374(6524):716–718. doi: 10.1038/374716a0. [DOI] [PubMed] [Google Scholar]
  26. Wong R. O., Herrmann K., Shatz C. J. Remodeling of retinal ganglion cell dendrites in the absence of action potential activity. J Neurobiol. 1991 Oct;22(7):685–697. doi: 10.1002/neu.480220704. [DOI] [PubMed] [Google Scholar]
  27. Wong R. O. Retinal waves and visual system development. Annu Rev Neurosci. 1999;22:29–47. doi: 10.1146/annurev.neuro.22.1.29. [DOI] [PubMed] [Google Scholar]
  28. Wong W. T., Myhr K. L., Miller E. D., Wong R. O. Developmental changes in the neurotransmitter regulation of correlated spontaneous retinal activity. J Neurosci. 2000 Jan 1;20(1):351–360. doi: 10.1523/JNEUROSCI.20-01-00351.2000. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Wong W. T., Sanes J. R., Wong R. O. Developmentally regulated spontaneous activity in the embryonic chick retina. J Neurosci. 1998 Nov 1;18(21):8839–8852. doi: 10.1523/JNEUROSCI.18-21-08839.1998. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Zhou Z. J. Direct participation of starburst amacrine cells in spontaneous rhythmic activities in the developing mammalian retina. J Neurosci. 1998 Jun 1;18(11):4155–4165. doi: 10.1523/JNEUROSCI.18-11-04155.1998. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Zhou Z. J., Zhao D. Coordinated transitions in neurotransmitter systems for the initiation and propagation of spontaneous retinal waves. J Neurosci. 2000 Sep 1;20(17):6570–6577. doi: 10.1523/JNEUROSCI.20-17-06570.2000. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Journal of Anatomy are provided here courtesy of Anatomical Society of Great Britain and Ireland

RESOURCES