Book contents
- Frontmatter
- Contents
- List of contributors
- Foreword
- Preface
- Acknowledgements
- 1 Introduction – from eye field to eyesight
- 2 Formation of the eye field
- 3 Retinal neurogenesis
- 4 Cell migration
- 5 Cell determination
- 6 Neurotransmitters and neurotrophins
- 7 Comparison of development of the primate fovea centralis with peripheral retina
- 8 Optic nerve formation
- 9 Glial cells in the developing retina
- 10 Retinal mosaics
- 11 Programmed cell death
- 12 Dendritic growth
- 13 Synaptogenesis and early neural activity
- 14 Emergence of light responses
- New perspectives
- Index
- Plate section
- References
14 - Emergence of light responses
Published online by Cambridge University Press: 22 August 2009
Book contents
- Frontmatter
- Contents
- List of contributors
- Foreword
- Preface
- Acknowledgements
- 1 Introduction – from eye field to eyesight
- 2 Formation of the eye field
- 3 Retinal neurogenesis
- 4 Cell migration
- 5 Cell determination
- 6 Neurotransmitters and neurotrophins
- 7 Comparison of development of the primate fovea centralis with peripheral retina
- 8 Optic nerve formation
- 9 Glial cells in the developing retina
- 10 Retinal mosaics
- 11 Programmed cell death
- 12 Dendritic growth
- 13 Synaptogenesis and early neural activity
- 14 Emergence of light responses
- New perspectives
- Index
- Plate section
- References
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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- Information
- Retinal Development , pp. 288 - 304Publisher: Cambridge University PressPrint publication year: 2006
References
, , 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, 7672–81CrossRefGoogle ScholarPubMed
, , , and (2003). Melanopsin retinal ganglion cells receive bipolar and amacrine cell synapses. J. Comp. Neurol., 460, 380–93CrossRefGoogle ScholarPubMed
(2003). Strange vision: ganglion cells as circadian photoreceptors. Trends Neurosci., 26, 314–20CrossRefGoogle ScholarPubMed
, and (2002). Phototransduction by retinal ganglion cells that set the circadian clock. Science, 295, 1065–70CrossRefGoogle ScholarPubMed
, and (1998). Blockade of glutamate-mediated activity in the developing retina perturbs the functional segregation of ON and OFF pathways. J. Neurosci., 18, 5019–25CrossRefGoogle ScholarPubMed
, (1986). A functional organization of ON and OFF pathways in the rabbit retina. J. Neurosci., 6, 1–13CrossRefGoogle Scholar
and (1993). Stratification of ON and OFF ganglion cell dendrites depends on glutamate-mediated afferent activity in the developing retina. Nature, 364, 144–6CrossRefGoogle Scholar
, and (1995). Development and regulation of dendritic stratification in retinal ganglion cells by glutamate-mediated afferent activity. J. Neurosci., 15, 7037–45CrossRefGoogle ScholarPubMed
, and (1975). Developmental characteristics of receptive organization in the isolated retina eye-cup of the rabbit. Brain Res., 87, 61–5CrossRefGoogle Scholar
and (1961). Localization of origins of electroretinogram components by intra-retinal recording in the intact cat eye. J. Physiol., 158, 257–80CrossRefGoogle Scholar
and (1997). Possible roles of spontaneous waves and dendritic growth for retinal receptive field development. Neural Comput., 9, 533–53CrossRefGoogle ScholarPubMed
and (1998). A biophysical model for the developmental time course of retinal orientation selectivity. Vis. Res., 38, 2787–800CrossRefGoogle ScholarPubMed
and (2004). Development of On and Off retinal pathways and retinogeniculate projections. Prog. Retin. Eye Res., 23, 31–51CrossRefGoogle Scholar
, , et al. (2005). Melanopsin-expressing ganglion cells in primate retina signal color and irradiance and project to the LGN. Nature, 433, 749–54CrossRefGoogle ScholarPubMed
and (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, 307–26CrossRefGoogle Scholar
and (1981b). An intracellular electrophysiological study of the ontogeny of functional synapses in the rabbit retina. II. Amacrine cells. J. Comp. Neurol., 198, 327–34CrossRefGoogle Scholar
, and (1988). Postnatal dendritic maturation of alpha and beta ganglion cells in cat retina. J. Neurosci., 8, 1485–99CrossRefGoogle ScholarPubMed
and (1974). Raising rabbits in a moving visual environment: an attempt to modify directional sensitivity in the retina. J. Physiol., 240, 309–30CrossRefGoogle Scholar
, , et al. (2003). The pre-synaptic active zone protein Bassoon is essential for photoreceptor ribbon synapse formation in the retina. Neuron, 37, 775–86CrossRefGoogle Scholar
(1987). The Retina; an Approachable Part of the Brain. Cambridge, MA: Harvard University PressGoogle Scholar
, and (1986). A role for action-potential activity in the development of neuronal connections in the kitten retinogeniculate pathway. J. Neurosci., 6, 1021–36CrossRefGoogle ScholarPubMed
and (1995). Immunocytochemical identification of cone bipolar cells in the rat retina. J. Comp. Neurol., 361, 461–78CrossRefGoogle ScholarPubMed
, and (2004). Expression of melanopsin during development of the rat retina. NeuroReport, 15, 781–4CrossRefGoogle ScholarPubMed
(1983a). ‘Starburst’ amacrine cells and cholinergic neurons: mirror-symmetric on and off amacrine cells of rabbit retina. Brain Res., 261, 138–44CrossRefGoogle Scholar
(1983b). On and off pathways through amacrine cells in mammalian retina: the synaptic connections of ‘starburst’ amacrine cells. Vis. Res., 23, 1265–79CrossRefGoogle Scholar
and (1976). Structural basis for ON-and OFF-center responses in retinal ganglion cells. Science, 194, 193–5CrossRefGoogle ScholarPubMed
, and (1977). Neuronal architecture of on and off pathways to ganglion cells in carp retina. Science, 198, 1267–9CrossRefGoogle Scholar
, , and (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, 2265–73CrossRefGoogle Scholar
, and (2000). Segregation of on and off bipolar cell axonal arbors in the absence of retinal ganglion cells. J. Neurosci., 20, 306–14CrossRefGoogle Scholar
, and (1991). Disruption of retinogeniculate afferent segregation by antagonists to NMDA receptors. Nature, 351, 568–70CrossRefGoogle ScholarPubMed
and (2004). Melanopsin containing retinal ganglion cells are light responsive from birth. NeuroReport, 15, 2317–20CrossRefGoogle ScholarPubMed
, , , and (2002). Melanopsin- containing retinal ganglion cells: architecture, projections, and intrinsic photosensitivity. Science, 295, 1065–70CrossRefGoogle ScholarPubMed
, , et al. (2004). Transient requirement for ganglion cells during assembly of retinal synaptic layers. Development, 131, 1331–42CrossRefGoogle ScholarPubMed
(1997). Vesicular acetylcholine transporter (VAChT): a cellular marker in rat retinal development. NeuroReport, 8, 2845–8CrossRefGoogle ScholarPubMed
, and (1997). Cholinesterases precede “ON-OFF” channel dichotomy in the embryonic chick retina before onset of synaptogenesis. Cell Tissue Res., 288, 407–16CrossRefGoogle ScholarPubMed
, , and (1994). Ontogeny of photic-induced c-fos mRNA expression in rat suprachiasmatic nuclei. NeuroReport, 5, 2683–7CrossRefGoogle ScholarPubMed
, , , and (1999). Disruption of laminin β2 chain production causes alterations in morphology and function in the CNS. J. Neurosci., 19, 9399–411CrossRefGoogle ScholarPubMed
(1977). Maturation of function in the developing rabbit retina. J. Comp. Neurol., 175, 275–86CrossRefGoogle ScholarPubMed
, and (1984). Acetylcholine-synthesising amacrine cells: identification and selective staining by using radioautography and fluorescent markers. Proc. R. Soc. London B. Biol. Sci., 223, 79–100CrossRefGoogle Scholar
and (1988). Time course of stratification of the dendritic fields of ganglion cells in the retina of the cat. Brain Res. Dev. Brain Res., 44, 87–93CrossRefGoogle ScholarPubMed
and (2006a). Receptive–field structure function correlates in developing turtle retinal ganglion cells. Eur. J. Neurosci., In pressCrossRefGoogle Scholar
and (2006b). Early neural activity and dendritic growth in turtle retinal ganglion cells. Eur. J. Neurosci., In pressCrossRefGoogle Scholar
, and (1993). Recoverin immunoreactivity in mammalian cone bipolar cells. Vis. Neurosci., 10, 1–12CrossRefGoogle ScholarPubMed
, , , and (1999). Morphological differentiation of bipolar cells in the ferret retina. Vis. Neurosci., 16, 1133–44CrossRefGoogle ScholarPubMed
, , and (2000). Ontogeny of a photic response in the retina and suprachiasmatic nucleus in the mouse. Brain Res. Dev. Brain Res., 120, 1–6CrossRefGoogle Scholar
Nelson, R. and Kolb, B. (2004). ON and OFF pathways in the vertebrate retina and visual system. In The Visual Neurosciences, ed. and . Cambridge, MA: MIT Press, pp. 260–78Google Scholar
, and (1978). Intracellular staining reveals different levels of stratification for on- and off-center ganglion cells in cat retina. J. Neurophysiol., 41, 472–83CrossRefGoogle ScholarPubMed
and (1996). Extracellular matrix in early cortical development. Prog. Brain Res., 108, 117–34Google ScholarPubMed
, , , and (1998). Melanopsin: an opsin in melanophores, brain, and eye. Proc. Natl. Acad. Sci. U. S. A., 95, 340–5CrossRefGoogle Scholar
, and (1988). Dendritic growth and re-modeling of cat retinal ganglion cells during fetal and postnatal development. J. Neurosci., 8, 4239–61CrossRefGoogle Scholar
and (1983). Maternal coordination of the fetal biological clock in utero. Science, 220, 969–71CrossRefGoogle ScholarPubMed
(1976). The development of the electroretinogram in normal and light-deprived rabbits. Pflügers Arch., 363, 7–13CrossRefGoogle ScholarPubMed
, , et al. (2005). Melanopsin dependent photoreception provides earliest light detection in the mammalian retina. Curr. Biol, 15, 1099–107CrossRefGoogle ScholarPubMed
(2005). Retinal development: second sight comes first. Curr. Biol., 15, R556–9CrossRefGoogle ScholarPubMed
and (1995). Emergence of complex receptive field properties of ganglion cells in the developing turtle retina. J. Neurophysiol., 73, 1355–64CrossRefGoogle ScholarPubMed
and (1996). Influence of spontaneous activity and visual experience on developing retinal receptive-fields. Curr. Biol., 6, 1503–8CrossRefGoogle ScholarPubMed
and (2001). The role of early neural activity in the maturation of turtle retinal function. J. Anat., 199, 375–83CrossRefGoogle ScholarPubMed
, and (2001). Development of retinal ganglion cell structure and function. Prog. Retin. Eye Res., 20, 139–74CrossRefGoogle ScholarPubMed
, and (2003). Developmental modulation of retinal wave dynamics: shedding light on the GABA saga. J. Neurosci., 23, 7621–9CrossRefGoogle ScholarPubMed
, , et al. (2003). Expression of opsin genes early in ocular development of humans and mice. Exp. Eye Res., 76, 393–6CrossRefGoogle ScholarPubMed
and (1984). The shape and arrangement of the cholinergic neurons in the rabbit retina. Proc. R. Soc. London B. Biol. Sci., 223, 101–19CrossRefGoogle ScholarPubMed
(1997). First glances: the vision of infants. The Friedenwald lecture. Invest. Ophthalmol. Vis. Sci., 38, 2183–203Google ScholarPubMed
and (2001). Visual deprivation alters development of synaptic function in inner retina after eye-opening. Neuron, 32, 439–49CrossRefGoogle ScholarPubMed
and (2003). Visual stimulation is required for refinement of On and Off pathways in postnatal retina. Neuron, 39, 85–96CrossRefGoogle Scholar
(1993). Early postnatal development of visual function in ganglion cells of the cat retina. J. Neurophysiol., 69, 1645–60CrossRefGoogle ScholarPubMed
, and (2001). Unique functional properties of on and off pathways in the developing mammalian retina. J. Neurosci., 21, 4310–7CrossRefGoogle Scholar
and (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, 136–48CrossRefGoogle ScholarPubMed
(1984). Cell death during differentiation of the retina in the mouse. J. Comp. Neurol., 229, 362–73CrossRefGoogle ScholarPubMed
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