Emergence of light responses

doi:10.1017/CBO9780511541629.016

14 - Emergence of light responses

Published online by Cambridge University Press: 22 August 2009

Evelyne Sernagor and

Edited by

Bill Harris and

Evelyne Sernagor: Affiliation:
School of Neurology, Neurobiology and Psychiatry, Medical Sciences, University of Newcastle upon Tyne, Framlington Place, Newcastle upon Tyne NE2 4HH, UK
Leo M. Chalupa: Affiliation:
Distinguished Professor of Ophthalmology and Neurobiology, Chair, Section of Neurobiology, Physiology and Behavior Division of Biological Sciences, UC Davis, One Shields Avenue, Davis, CA 95616, USA
Evelyne Sernagor: Affiliation:
University of Newcastle upon Tyne
Stephen Eglen: Affiliation:
University of Cambridge
Bill Harris: Affiliation:
University of Cambridge
Rachel Wong: Affiliation:
Washington University, St Louis

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Summary

Introduction

Although the newborn retina is highly active, with spontaneous waves propagating across the amacrine and the ganglion cell layers every few minutes (see Chapter 13), at that time it is not yet possible to elicit light responses in retinal ganglion cells (RGCs). This lack of responsiveness to light is due to the immaturity of the vertical synaptic pathway between photoreceptors and RGCs provided by bipolar cells (BCs), despite the fact that lateral connections in the inner retina are already well established (see Chapter 13). Moreover, rod and cone opsins are not yet functional at birth. In mouse for example, ultraviolet cone opsin does not appear until postnatal day (P)1, rod opsin until P5 and green cone opsin until P7 (Tarttelin et al., 2003). Hence, RGCs become visually responsive only shortly before eye opening (around P10 in rabbit; Masland, 1977; Dacheux and Miller, 1981a, b; P7 to P10 in cat; Tootle, 1993; P12 in mouse; Sekaran et al., 2005). Humans and other primates, on the other hand, are born with their eyes open and although primate vision is poor at birth a newborn human infant is capable of tracking visual stimuli (Teller, 1997).

This chapter reviews the earliest light responses that can be detected in the developing retina. New studies show that the newborn retina is actually not insensitive to light and this will be considered in the first part of the chapter.

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Type: Chapter
Information: Retinal Development , pp. 288 - 304

DOI: https://doi.org/10.1017/CBO9780511541629.016 [Opens in a new window]

Publisher: Cambridge University Press

Print publication year: 2006

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References

Bansal, A., Singer, J. H., Hwang, B. J.et al. (2000). 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., 20, 7672–81CrossRef Google Scholar PubMed

Belenky, M. A., Smeraski, C. A., Provencio, I., Sollars, P. J. and Pickard, G. E. (2003). Melanopsin retinal ganglion cells receive bipolar and amacrine cell synapses. J. Comp. Neurol., 460, 380–93CrossRef Google Scholar PubMed

Berson, D. M. (2003). Strange vision: ganglion cells as circadian photoreceptors. Trends Neurosci., 26, 314–20CrossRef Google Scholar PubMed

Berson, D. M., Dunn, F. A. and Takao, M. (2002). Phototransduction by retinal ganglion cells that set the circadian clock. Science, 295, 1065–70CrossRef Google Scholar PubMed

Bisti, S., Gargini, C. and Chalupa, L. M. (1998). Blockade of glutamate-mediated activity in the developing retina perturbs the functional segregation of ON and OFF pathways. J. Neurosci., 18, 5019–25CrossRef Google Scholar PubMed

Bloomfield, S. A., Miller, R. F. (1986). A functional organization of ON and OFF pathways in the rabbit retina. J. Neurosci., 6, 1–13CrossRef Google Scholar

Bodnarenko, S. R. and Chalupa, L. M. (1993). Stratification of ON and OFF ganglion cell dendrites depends on glutamate-mediated afferent activity in the developing retina. Nature, 364, 144–6CrossRef Google Scholar

Bodnarenko, S. R., Jeyarasasingam, G. and Chalupa, L. M. (1995). Development and regulation of dendritic stratification in retinal ganglion cells by glutamate-mediated afferent activity. J. Neurosci., 15, 7037–45CrossRef Google Scholar PubMed

Bowe-Anders, C., Miller, R. F. and Dacheux, R. F. (1975). Developmental characteristics of receptive organization in the isolated retina eye-cup of the rabbit. Brain Res., 87, 61–5CrossRef Google Scholar

Brown, K. T. and Wiesel, T. N. (1961). Localization of origins of electroretinogram components by intra-retinal recording in the intact cat eye. J. Physiol., 158, 257–80CrossRef Google Scholar

Burgi, P. Y. and Grzywacz, N. M. (1997). Possible roles of spontaneous waves and dendritic growth for retinal receptive field development. Neural Comput., 9, 533–53CrossRef Google Scholar PubMed

Burgi, P. Y. and Grzywacz, N. M. (1998). A biophysical model for the developmental time course of retinal orientation selectivity. Vis. Res., 38, 2787–800CrossRef Google Scholar PubMed

Chalupa, L. M. and Gunhan, E. (2004). Development of On and Off retinal pathways and retinogeniculate projections. Prog. Retin. Eye Res., 23, 31–51CrossRef Google Scholar

Dacey, D. M., Liao, H.-S., Peterson, B.et al. (2005). Melanopsin-expressing ganglion cells in primate retina signal color and irradiance and project to the LGN. Nature, 433, 749–54CrossRef Google Scholar PubMed

Dacheux, R. F. and Miller, R. F. (1981a). An intracellular electrophysiological study of the ontogeny of functional synapses in the rabbit retina. I. Receptors, horizontal, and bipolar cells. J. Comp. Neurol., 198, 307–26CrossRef Google Scholar

Dacheux, R. F. and Miller, R. F. (1981b). An intracellular electrophysiological study of the ontogeny of functional synapses in the rabbit retina. II. Amacrine cells. J. Comp. Neurol., 198, 327–34CrossRef Google Scholar

Dann, J. F., Buhl, E. H. and Peichl, L. (1988). Postnatal dendritic maturation of alpha and beta ganglion cells in cat retina. J. Neurosci., 8, 1485–99CrossRef Google Scholar PubMed

Daw, N. W. (1995). Visual Development. New York: Plenum PressCrossRef Google Scholar

Daw, N. W. and Wyatt, H. J. (1974). Raising rabbits in a moving visual environment: an attempt to modify directional sensitivity in the retina. J. Physiol., 240, 309–30CrossRef Google Scholar

Dick, O., Dieck, S. T., Altrock, W. D.et al. (2003). The pre-synaptic active zone protein Bassoon is essential for photoreceptor ribbon synapse formation in the retina. Neuron, 37, 775–86CrossRef Google Scholar

Dowling, J. E. (1987). The Retina; an Approachable Part of the Brain. Cambridge, MA: Harvard University PressGoogle Scholar

Dubin, M. W., Stark, L. A. and Archer, S. M. (1986). A role for action-potential activity in the development of neuronal connections in the kitten retinogeniculate pathway. J. Neurosci., 6, 1021–36CrossRef Google Scholar PubMed

Euler, T. and Wässle, H. (1995). Immunocytochemical identification of cone bipolar cells in the rat retina. J. Comp. Neurol., 361, 461–78CrossRef Google Scholar PubMed

Fahrenkrug, J., Nielsen, H. S. and Hannibal, J. (2004). Expression of melanopsin during development of the rat retina. NeuroReport, 15, 781–4CrossRef Google Scholar PubMed

Famiglietti, E. V. Jr. (1983a). ‘Starburst’ amacrine cells and cholinergic neurons: mirror-symmetric on and off amacrine cells of rabbit retina. Brain Res., 261, 138–44CrossRef Google Scholar

Famiglietti, E. V. Jr. (1983b). On and off pathways through amacrine cells in mammalian retina: the synaptic connections of ‘starburst’ amacrine cells. Vis. Res., 23, 1265–79CrossRef Google Scholar

Famiglietti, E. V. Jr. and Kolb, H. (1976). Structural basis for ON-and OFF-center responses in retinal ganglion cells. Science, 194, 193–5CrossRef Google Scholar PubMed

Famiglietti, E. V. Jr, Kaneko, A. and Tachibana, M. (1977). Neuronal architecture of on and off pathways to ganglion cells in carp retina. Science, 198, 1267–9CrossRef Google Scholar

Gunhan, E., Choudary, P. V., Landerholm, T. E. and Chalupa, L. M. (2002). Depletion of cholinergic amacrine cells by a novel immunotoxin does not perturb the formation of segregated on and off cone bipolar cell projections. J. Neurosci., 22, 2265–73CrossRef Google Scholar

Gunhan-Agar, E., Kahn, D. and Chalupa, L. M. (2000). Segregation of on and off bipolar cell axonal arbors in the absence of retinal ganglion cells. J. Neurosci., 20, 306–14CrossRef Google Scholar

Hahm, J. O., Langdon, R. B. and Sur, M. (1991). Disruption of retinogeniculate afferent segregation by antagonists to NMDA receptors. Nature, 351, 568–70CrossRef Google Scholar PubMed

Hannibal, J. and Fahrenkrug, J. (2004). Melanopsin containing retinal ganglion cells are light responsive from birth. NeuroReport, 15, 2317–20CrossRef Google Scholar PubMed

Hattar, S., Liao, H. W., Takao, M., Berson, D. M. and Yau, K. W. (2002). Melanopsin- containing retinal ganglion cells: architecture, projections, and intrinsic photosensitivity. Science, 295, 1065–70CrossRef Google Scholar PubMed

Kay, J. N., Roeser, T., Mumm, J. S.et al. (2004). Transient requirement for ganglion cells during assembly of retinal synaptic layers. Development, 131, 1331–42CrossRef Google Scholar PubMed

Koulen, P. (1997). Vesicular acetylcholine transporter (VAChT): a cellular marker in rat retinal development. NeuroReport, 8, 2845–8CrossRef Google Scholar PubMed

Layer, P. G., Berger, J. and Kinkl, N. (1997). Cholinesterases precede “ON-OFF” channel dichotomy in the embryonic chick retina before onset of synaptogenesis. Cell Tissue Res., 288, 407–16CrossRef Google Scholar PubMed

Leard, L. E., Macdonald, E. S., Heller, H. C. and Kilduff, T. S. (1994). Ontogeny of photic-induced c-fos mRNA expression in rat suprachiasmatic nuclei. NeuroReport, 5, 2683–7CrossRef Google Scholar PubMed

Libby, R. T., Lavallee, C. R., Balkema, G. W., Brunken, W. J. and Hunter, D. D. (1999). Disruption of laminin β2 chain production causes alterations in morphology and function in the CNS. J. Neurosci., 19, 9399–411CrossRef Google Scholar PubMed

Masland, R. H. (1977). Maturation of function in the developing rabbit retina. J. Comp. Neurol., 175, 275–86CrossRef Google Scholar PubMed

Masland, R. H. and Tauchi, M. (1986). The cholinergic amacrine cells. Trends Neurosci., 9, 218–23CrossRef Google Scholar

Masland, R. H., Mills, J. W. and Hayden, S. A. (1984). Acetylcholine-synthesising amacrine cells: identification and selective staining by using radioautography and fluorescent markers. Proc. R. Soc. London B. Biol. Sci., 223, 79–100CrossRef Google Scholar

Maslim, J. and Stone, J. (1988). Time course of stratification of the dendritic fields of ganglion cells in the retina of the cat. Brain Res. Dev. Brain Res., 44, 87–93CrossRef Google Scholar PubMed

Mehta, V. and Sernagor, E. (2006a). Receptive–field structure function correlates in developing turtle retinal ganglion cells. Eur. J. Neurosci., In pressCrossRef Google Scholar

Mehta, V. and Sernagor, E. (2006b). Early neural activity and dendritic growth in turtle retinal ganglion cells. Eur. J. Neurosci., In pressCrossRef Google Scholar

Milam, A. H., Dacey, D. M. and Dizhoor, A. M. (1993). Recoverin immunoreactivity in mammalian cone bipolar cells. Vis. Neurosci., 10, 1–12CrossRef Google Scholar PubMed

Miller, E. D., Tran, M. I., Wong, G. K., Oakley, D. M. and Wong, R. O. (1999). Morphological differentiation of bipolar cells in the ferret retina. Vis. Neurosci., 16, 1133–44CrossRef Google Scholar PubMed

Llamosas, Munoz M., Huerta, J. J., Cernuda-Cernuda, R. and Garcia-Fernandez, J. M. (2000). Ontogeny of a photic response in the retina and suprachiasmatic nucleus in the mouse. Brain Res. Dev. Brain Res., 120, 1–6CrossRef Google Scholar

Nelson, R. and Kolb, B. (2004). ON and OFF pathways in the vertebrate retina and visual system. In The Visual Neurosciences, ed. Chalupa, L. M. and Werner, J. S.. Cambridge, MA: MIT Press, pp. 260–78Google Scholar

Nelson, R., Famiglietti, E. V. Jr and Kolb, H. (1978). Intracellular staining reveals different levels of stratification for on- and off-center ganglion cells in cat retina. J. Neurophysiol., 41, 472–83CrossRef Google Scholar PubMed

Pearlman, A. L. and Sheppard, A. M. (1996). Extracellular matrix in early cortical development. Prog. Brain Res., 108, 117–34Google Scholar PubMed

Provencio, I., Jiang, G., Grip, W. J., Hayes, W. P. and Rollag, M. D. (1998). Melanopsin: an opsin in melanophores, brain, and eye. Proc. Natl. Acad. Sci. U. S. A., 95, 340–5CrossRef Google Scholar

Ramoa, A. S., Campbell, G. and Shatz, C. J. (1988). Dendritic growth and re-modeling of cat retinal ganglion cells during fetal and postnatal development. J. Neurosci., 8, 4239–61CrossRef Google Scholar

Reppert, S. M. and Schwartz, W. J. (1983). Maternal coordination of the fetal biological clock in utero. Science, 220, 969–71CrossRef Google Scholar PubMed

Reuter, J. H. (1976). The development of the electroretinogram in normal and light-deprived rabbits. Pflügers Arch., 363, 7–13CrossRef Google Scholar PubMed

Sekaran, S., Lupi, D., Jones, S. L.et al. (2005). Melanopsin dependent photoreception provides earliest light detection in the mammalian retina. Curr. Biol, 15, 1099–107CrossRef Google Scholar PubMed

Sernagor, E. (2005). Retinal development: second sight comes first. Curr. Biol., 15, R556–9CrossRef Google Scholar PubMed

Sernagor, E. and Grzywacz, N. M. (1995). Emergence of complex receptive field properties of ganglion cells in the developing turtle retina. J. Neurophysiol., 73, 1355–64CrossRef Google Scholar PubMed

Sernagor, E. and Grzywacz, N. M. (1996). Influence of spontaneous activity and visual experience on developing retinal receptive-fields. Curr. Biol., 6, 1503–8CrossRef Google Scholar PubMed

Sernagor, E. and Mehta, V. (2001). The role of early neural activity in the maturation of turtle retinal function. J. Anat., 199, 375–83CrossRef Google Scholar PubMed

Sernagor, E., Eglen, S. J. and Wong, R. O. L. (2001). Development of retinal ganglion cell structure and function. Prog. Retin. Eye Res., 20, 139–74CrossRef Google Scholar PubMed

Sernagor, E., Young, C. and Eglen, S. J. (2003). Developmental modulation of retinal wave dynamics: shedding light on the GABA saga. J. Neurosci., 23, 7621–9CrossRef Google Scholar PubMed

Tarttelin, E. E., Bellingham, J., Bibb, L. C.et al. (2003). Expression of opsin genes early in ocular development of humans and mice. Exp. Eye Res., 76, 393–6CrossRef Google Scholar PubMed

Tauchi, M. and Masland, R. H. (1984). The shape and arrangement of the cholinergic neurons in the rabbit retina. Proc. R. Soc. London B. Biol. Sci., 223, 101–19CrossRef Google Scholar PubMed

Teller, D. Y. (1997). First glances: the vision of infants. The Friedenwald lecture. Invest. Ophthalmol. Vis. Sci., 38, 2183–203Google Scholar PubMed

Thorn, F., Gollender, M. and Erikson, P. (1976). The development of the kitten's visual optics. Vis. Res., 16, 1145–9Google Scholar

Tian, N. and Copenhagen, D. R. (2001). Visual deprivation alters development of synaptic function in inner retina after eye-opening. Neuron, 32, 439–49CrossRef Google Scholar PubMed

Tian, N. and Copenhagen, D. R. (2003). Visual stimulation is required for refinement of On and Off pathways in postnatal retina. Neuron, 39, 85–96CrossRef Google Scholar

Tootle, J. S. (1993). Early postnatal development of visual function in ganglion cells of the cat retina. J. Neurophysiol., 69, 1645–60CrossRef Google Scholar PubMed

Wang, G. Y., Liets, L. C. and Chalupa, L. M. (2001). Unique functional properties of on and off pathways in the developing mammalian retina. J. Neurosci., 21, 4310–7CrossRef Google Scholar

Weaver, D. R. and Reppert, S. M. (1995). Definition of the developmental transition from dopaminergic to photic regulation of c-fos gene expression in the rat suprachiasmatic nucleus. Brain Res. Mol. Brain Res., 33, 136–48CrossRef Google Scholar PubMed

Young, R. W. (1984). Cell death during differentiation of the retina in the mouse. J. Comp. Neurol., 229, 362–73CrossRef Google Scholar PubMed