Postnatal Development of Neurotransmitter Systems in the Mammalian Retina

  • Jon Robbins
  • Hisako Ikeda

Abstract

The mammalian retina is not fully developed at birth and many mammals eyes do not open for many days post partum. Much of the gross morphological development is complete before the eyes open. For example in the cat retina most of the morphological development is complete by postnatal day (PND) 40 (Fig. 1.), whilst spatial resolution of the cells in the lateral geniculate nucleus (Ikeda & Tremain, 1978), visual acuity measured by visual evoked potentials (Freeman & Marg, 1975) or behaviourally (Mitchell et al, 1976) have not reached adult levels until PND 100. Likewise in humans, the time to reach adult like visual acuity is 3–5 years (Teller & Movshon, 1986).

Keywords

Tyrosine Hydroxylase Retinal Ganglion Cell Amacrine Cell Postnatal Development Excitatory Amino Acid Receptor 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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References

  1. Barlow, H.B. and Pettigrew, J.D. (1971) Lack of specificity in neurones in the visual cortex of young kittens, J. Physiol. 218:739–744.Google Scholar
  2. Bodenant, C., Leroux, P., Gonzalez, B. J. and Vaudry, H. (1991) Transient expression of somatostatin receptors in the rat visual system during development, Neurosci. 41:595–606.CrossRefGoogle Scholar
  3. 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 364:144–146.PubMedCrossRefGoogle Scholar
  4. Bonds, A.B. and Freeman, R.D. (1978) Development of optical quality in the kitten eye, Vision Res. 18:391–398.PubMedCrossRefGoogle Scholar
  5. Casini, G. and Brecha, N.C. (1992) Postnatal development of tyrosine hydroxylase immunoreactive amacrine cells in the rabbit retina: I morphological characterisation, J. Comp. Neurol. 326:283–301.PubMedCrossRefGoogle Scholar
  6. Cohen, J. (1987) Postnatal development of phenylethanolamine-N-methyltransferase activity of rat retina, Neurosci. Lett. 83:138–142.PubMedCrossRefGoogle Scholar
  7. Cohen, J. and Neff, N.N. (1982) Retinal amacrine cell system tyrosine hydroxylase: the development of responsiveness to light and neuroleptic drugs, Develop. Brain Res. 3:160–163.CrossRefGoogle Scholar
  8. Cutcliffe, N. and Osborne, N.N. (1987) Serotonergic and cholinergic stimulation of inositol phosphate formation in the rabbit retina. Evidence for the presence of serotonin and muscarinic receptors, Brain Res. 421:95–104.PubMedCrossRefGoogle Scholar
  9. Dann, J.F. (1989) Cholinergic amacrine cells in the developing cat retina, J. Comp. Neurol. 289:143–155.PubMedCrossRefGoogle Scholar
  10. Dann, J.F., Buhl, E.H. and Peichl, L. (1988) Postnatal dendritic maturation of alpha and beta ganglion cells in cat retina, J. Neurosci. 8:1485–1499.PubMedGoogle Scholar
  11. Donovan, A. (1966) The postnatal development of the cat retina, Exp. Eye Res. 5:249–254.PubMedCrossRefGoogle Scholar
  12. Ferriero, D.M. (1992) Developmental expression of somatostatin receptors in the rat retina, Develop. Brain Res. 67:309–315.CrossRefGoogle Scholar
  13. Ferriero, D.M., Head, V.A., Edwards, R.H. and Sagar, S.M. (1990) Somatostatin mRNA and molecular forms during development of the rat retina, Develop. Brain Res. 57:15–19.CrossRefGoogle Scholar
  14. Ferriero, D.M. and Sagar, S.M. (1987) Development of somatostatin immunoreactive neurons in rat retina, Develop. Brain Res. 34:207–214.CrossRefGoogle Scholar
  15. Ferriero, D.M. and Sagar, S.M. (1989) Development of neuropeptide Y-immunoreactive neurons in the rat retina, Develop. Brain Res. 48:19–26CrossRefGoogle Scholar
  16. Ferriero, D.M., Sheldon, R.A. and Domingo, J. (1992) Somatostatin is altered in developing retina from ethanol-exposed rats, Neurosci. Lett. 147:29–32.PubMedCrossRefGoogle Scholar
  17. Freeman, D.N. and Marg, E. (1975) Visual acuity development coincides with the sensitive period in kittens, Nature 254:614–615.PubMedCrossRefGoogle Scholar
  18. Fry, K.R., Chen, N-X., Glazebrook, P. A. and Lam, D.M-K. (1991) Postnatal development of ganglion cells in the rabbit retina: characterisations with AB5 and GABA antibodies, Develop. Brain Res. 61:45–53.CrossRefGoogle Scholar
  19. Fung, S-K., Kong, Y-C. and Lam, D.M-K. (1982) Prenatal development of GABAergic, glycinergic and dopaminergic neurons in the rabbit retina, J. Neurosci. 2:1623–1632.PubMedGoogle Scholar
  20. Gentleman, S., Hemmings, B.A., Russell, P. and Chader, G.J. (1989) Developmental expression of the RI subunit of cyclic AMP-dependent protein kinase in retina, Exp. Eye Res. 48:717–731.PubMedCrossRefGoogle Scholar
  21. Guameri, P., Corda, M.G., Concas, A., Salis, M., Caldeini, G., Toffano, G. and Biggio, G. (1982) Age related changes of benzodiazepine and GABA binding sites in the rat retina, Neurobiol. Aging 3:227–231.CrossRefGoogle Scholar
  22. Hamasaki, D.I. and Flynn, J.T. (1977) Physiological properties of retinal ganglion cells of 3-week-old kittens, Vision Res. 17:275–284.PubMedCrossRefGoogle Scholar
  23. Hamasaki, D.I. and Sutija, V.G. (1979) Development of X-and Y-cells in kittens. Exp. Brain Res. 35:9–23.PubMedGoogle Scholar
  24. Hoover, F. and Goldman, D. (1992) Temporally correlated expression of nAChR genes during development of mammalian retina, Exp. Eye Res. 54:561–565.PubMedCrossRefGoogle Scholar
  25. Hubei, D.H., and Wiesel, T.H. (1963) Receptive fields of cells in the striate of very young, visually inexperienced kittens, J. Neurophysiol. 26:994–1002.Google Scholar
  26. Hubei, D.H. and Wiesel, T.N. (1970) The period of susceptibility to the physiological effects of unilateral eye closure in kittens, J. Physiol. 206:419–436.Google Scholar
  27. Huttenlocker, P.R. (1967) Development of cortical neuronal activity in the neonatal cat, Exp. Neurol. 17:347–415.Google Scholar
  28. Ikeda, H. (1979) Physiological basis of visual acuity and its development in kitten, Child Care Health Develop. 5:375–383.CrossRefGoogle Scholar
  29. Ikeda, H. (1985) Transmitter actions at the cat retinal ganglion cells, Prog. Retinal Res. 4:1–32.CrossRefGoogle Scholar
  30. Ikeda, H., Kay, C.D., and Robbins, J. (1989) Properties of excitatory amino acid receptors on sustained retinal ganglion cells in the cat retina, Neurosci. 32:27–38.CrossRefGoogle Scholar
  31. Ikeda, H., Priest, T.D., Robbins, J. and Wakakuwa K. (1986) Silent dopaminergic synapse at feline retinal ganglion cells, Clin. Vision Sci. 1:25–38.Google Scholar
  32. Ikeda, H. and Robbins, J. (1984) Development of inhibitory transmission at the retinal ganglion cells in cats. In Development of visual pathways in mammals, Eds Stone, J. Dreher, B. and Rapaport D.H., Alan R. Liss Inc. New York, pp 115-124.Google Scholar
  33. Ikeda, H. and Robbins, J. (1985a) Postnatal development of GABA-and glycine-mediated inhibition of feline retinal ganglion cells in the area centralis, Develop. Brain Res. 23:1–17.CrossRefGoogle Scholar
  34. Ikeda, H. and Robbins, J. (1985b) Postnatal development of GABA and glycine actions on the surround inhibition of cat retinal ganglion cells in the area centralis. In. Neurocircuitry of the retina: a Cajal memorial. Eds Gallego, A. & Gouras, P. Elsevier, New York, pp. 257–264.Google Scholar
  35. Ikeda, H. and Robbins, J. (1989) Development of neurochemical segregation of ON and OFF retinal channels which subserve contrast vision. In: Seeing contour and colour, Eds Kulikowski, J.J., Dickinson, C.M. and Murray, I.J. Pergamon Press, Oxford, pp 164–166.Google Scholar
  36. Ikeda, H., Robbins, J. and Kay, C. (1990) Excitatory amino acid receptors on sustained retinal ganglion cell in the kitten during the critical period of development, Develop. Brain Res. 51:85–91.CrossRefGoogle Scholar
  37. Ikeda. H., Robbins. J. and Wakakuwa, K. (1987) Evidence for dopaminergic innervation on kitten retinal ganglion cells. Develop. Brain Res. 35:83–89.CrossRefGoogle Scholar
  38. Ikeda, H. and Tremain, K.E. (1978) The development of spatial resolving power of lateral geniculate neurones in kittens. Exp. Brain Res. 31:193–206.PubMedGoogle Scholar
  39. Ikeda, H. and Tremain, K.E. (1979) Amblyopia occurs in retinal ganglion cells in cats reared with convergent squint without alternating fixation, Exp. Brain Res. 35:559–582.PubMedCrossRefGoogle Scholar
  40. Jacobson, S.G., Ikeda, H. and Ruddock, K. (1987) Cone mediated retinal function in cats during development, Docum. Ophthalmol. 65:7–14.CrossRefGoogle Scholar
  41. Kato, S., Nakamura, T. and Negishi, K. (1980) Postnatal development of dopaminergic cells in the rat retina, J. Comp. Neurol. 191:227–236.CrossRefGoogle Scholar
  42. Lam, D.M-K., Fung, S-C. and Kong, Y-C. (1980) Postnatal development of GABA-ergic neurons in the rabbit retina, J. Comp. Neurol. 193:89–102.PubMedCrossRefGoogle Scholar
  43. Lankford, K.L., DeMello, F.G. and Klein, W.L. (1988) Dl-type dopamine receptors inhibit growth cone motility in cultured retina neurons: evidence that neurotransmitters act as morphogenic growth regulators in the developing central nervous system, Proc. Natl Acad Sci. USA 85:4567–4571.PubMedCrossRefGoogle Scholar
  44. Madtes, Jr, P. and Redburn, D.A. (1982) [3H]GABA binding in developing rabbit retina, Neurochem. Res. 7:495–503.PubMedCrossRefGoogle Scholar
  45. Martin-Martinelli, E., Simon, A., Vigny, A. and Nguyen-Legros, J. (1989) Postnatal development of Tyrosine-Hydroxylase-Immunoreactive cells in the rat retina, Develop. Neurosci. 11:11–25.CrossRefGoogle Scholar
  46. Maslim, J. and Stone, J. (1988) Time course of stratification of the dendritic fields of ganglion cells in the retina of the cat, Develop. Brain Res. 44:87–93.CrossRefGoogle Scholar
  47. Messersmith. E.K. and Redburn, D.A. (1992) y-Aminobutyric acid immunoreactivity in multiple cell types of the developing rabbit retina, Visual Neurosci. 8:201–211.CrossRefGoogle Scholar
  48. Mitchell, D.E., Giffin, F., Wilkinson, F., Anderson, P. and Smith, M.L. (1976) Visual resolution in young kittens. Vision Res. 16:363–366.PubMedCrossRefGoogle Scholar
  49. Mitrofanis, J. and Finlay, B.L. (1990) Developmental changes in the distribution of retinal catecholaminergic neurones in hamsters and gerbils, J. Comp. Neurol. 292:480–494.PubMedCrossRefGoogle Scholar
  50. Mitrofanis, J., Maslim, J. and Stone, J. (1988) Catecholaminergic and cholinergic neurons in the developing retina of the rat, J. Comp. Neurol 276:343–359.PubMedCrossRefGoogle Scholar
  51. Mitrofanis, J., Maslim, J. and Stone, J. (1989) Ontogeny of catecholaminergic and cholinergic cell distributions in the cat’s retina, J. Comp. Neurol. 289:228–246.PubMedCrossRefGoogle Scholar
  52. Mitrofanis, J., Robinson, S.R. and Ashwell, K. (1992) Development of catecholaminergic, Indoleamine-accumulating and NADPH-diaphorase amacrine cells in rabbit retinae, J. Comp. Neurol. 319:560–585.PubMedCrossRefGoogle Scholar
  53. Mitrofanis, J., Robinson, S.R. and Provis, J.M. (1989) Somatostatinergic neurones of the developing human and cat retinae, Neurosci. Lett. 104:209–216.PubMedCrossRefGoogle Scholar
  54. Moore, C.L., Kalil, R. and Richards, W. (1976) Development of myelination in optic tract of the cat, J. Comp. Neurol. 165:125–136.PubMedCrossRefGoogle Scholar
  55. Morgan, W.W. and Kamp. C.W. (1982) Postnatal development of the light response of the dopaminergic neurons in the rat retina, J. Neurochem. 39:283–285.PubMedCrossRefGoogle Scholar
  56. Morrison, J.D. (1982) Postnatal development of the area centralis of the kitten retina: an electron microscopic study, J. Anat. 135:255–271.PubMedGoogle Scholar
  57. Osborne, N.N. (1985) Interplexiform, horizontal and bipolar-like cells of the rabbit retina take up exogenous serotonin during early developmental stages, Int. J. Develop. Neurosci. 3:643–646.CrossRefGoogle Scholar
  58. Osborne, N.N. (1988) Muscarinic stimulation of inositol phosphate formation in rat retina: developmental changes, Vision Res. 28:875–881.PubMedCrossRefGoogle Scholar
  59. Osborne, N.N., Patel, S. Beaton, D.W. and Neuhoff, V. (1986) GABA neurones in retinas of different species and their postnatal development in situ and in culture in the rabbit retina. Cell Tissue Res. 243:117–123.PubMedCrossRefGoogle Scholar
  60. Parkinson, D. and Rando, R.R. (1984) Ontogenesis of dopaminergic neurons in the post-natal rabbit retina: pre-and post-synaptic elements. Develop. Brain Res. 13:207–217.CrossRefGoogle Scholar
  61. Parkinson, D., Spira, A., Wyse, J.P and Patten, M. (1985) The ontogenesis of the dopaminergic cell in the pre-and postnatal guinea pig retina, Int. J. Develop. Neurosci. 3:157–167.CrossRefGoogle Scholar
  62. Pourcho, R.G. (1982) Dopaminergic amacrine cells in the cat retina. Vision Res. 252:101–109.Google Scholar
  63. Priest. T.D., Robbins, J. and Ikeda, H. (1985) The action of inhibitory neurotransmitters y-aminobutyric acid and glycine may distinguish between the area centralis and the peripheral retina in cats, Vision Res. 25:1761–1770.PubMedCrossRefGoogle Scholar
  64. Pritchett, D.B., Sontheimer, H., Shivers, B.D., Ymer, S., Kettenmann, H., Schofield, PR. and Seeburg, PH. (1989) Importance of a novel GABAA receptor subunit for benzodiazepine pharmacology, Nature 338:582–585.PubMedCrossRefGoogle Scholar
  65. Puro, D.G., Battelle, B-A. and Hansmann, K.E. (1982) Development of cholinergic neurons of the rat retina, Develop. Biol. 91:138–148.PubMedCrossRefGoogle Scholar
  66. Ramoa, A.S., Campbell, G. and Shatz C.J. (1988) Dendritic growth and remodelling of cat retinal ganglion cells during fetal and postnatal development, J. Neurosci. 8:4239–4261.PubMedGoogle Scholar
  67. Redbum, D.A. (1992) Development of GABAergic neurons in the mammalian retina, Prog. Brain Res. 90:133–147.CrossRefGoogle Scholar
  68. Redburn, D.A., Agarwal, S.H. Messersmith, E.K. and Mitchell, C.K. (1992) Development of the glutamate system in rabbit retina, Neurochem. Res. 17:61–66.PubMedCrossRefGoogle Scholar
  69. Redbum, D.A. and Madtes Jr, P. (1986) GABA-Its role and development in retina, Prog. Retinal Res. 6:69–84.Google Scholar
  70. Redburn, D.A. and Mitchell, C.K. (1981) 3H-muscimol binding in synaptosomal fractions from bovine and developing rabbit retinas, J. Neurosci. Res. 6:487–495.PubMedCrossRefGoogle Scholar
  71. Robbins, J. and Ikeda, H. (1989) Benzodiazepines and the mammalian retina: III postnatal development, Brain Res. 479:334–338.PubMedCrossRefGoogle Scholar
  72. Robbins, J., Wakakuwa, K. and Ikeda, H. (1988) Noradrenaline action on cat retinal ganglion cells is mediated by dopamine (D2) receptors, Brain Res. 438:52–60.PubMedCrossRefGoogle Scholar
  73. Rose, G.H. and Lindsley, D.B. (1968) Development of visually evoked potentials in kittens: specific and non-specific responses, J. Neurophysiol. 31:607–623.PubMedGoogle Scholar
  74. Rusoff, A.C. (1979) Development of ganglion cells in the retina of the cat. In Developmental neurobiology of vision, Ed. Freeman, R.D. Plenum Press, New York, pp 19–30.CrossRefGoogle Scholar
  75. Rusoff, A.C. and Dubin. M.W. (1977) Development of receptive-field properties of retinal ganglion cells in kittens. J. Neurophysiol. 40:188–1198.Google Scholar
  76. Schnitzer, J. and Rusoff, A.C. (1984) Horizontal cells of the mouse retina contain glutamic acid decarboxylase-like immunoreactivity during early developmental stages, J. Neurosci. 4:2948–2955.PubMedGoogle Scholar
  77. Schliebs, R., Rothe, T. and Bigl, V. (1986) Dark-rearing affects the development of benzodiazepine receptors in the central visual structures of rat brain, Develop. Brain Res. 24:179–185.CrossRefGoogle Scholar
  78. Spira, A. W. and Parkinson, D. (1991) Effects of dark-rearing on the retinal dopaminergic system in the neonatal and postnatal guinea pig, Develop. Brain Res. 62:142–145.CrossRefGoogle Scholar
  79. Teller, D.Y. and Movshon, J.A. (1986) Visual development, Vision Res. 26:1483–1506.PubMedCrossRefGoogle Scholar
  80. Thomas, S.A., Matsumoto, A.M. and Palmiter, R.D. (1995) Noradrenaline is essential for mouse fetal development, Nature 374:643–646.PubMedCrossRefGoogle Scholar
  81. Tootle, J.S. and Friedlander, M.J. (1989) Postnatal development of the spatial contrast sensitivity of X-and Y-cells in the kitten retinogeniculate pathway, J. Neurosci. 9:1325–1340.PubMedGoogle Scholar
  82. Tucker, G.S. (1978) Light microscopic analysis of the kitten retina: postnatal development in the area centralis, J. Comp. Neurol. 180:489–500.PubMedCrossRefGoogle Scholar
  83. Tucker, G.S., Hamasaki, D.I., Labbie, A. and Muroff, J. (1979) Anatomic and Physiologic development of the photoreceptor of the kitten, Exp Brain Res. 37:459–474.PubMedCrossRefGoogle Scholar
  84. Vogel, M. (1978) Postnatal development of the cat’s retina, Adv. Anat. Embiyol. Cell Biol. 54:1–66.Google Scholar
  85. Wang, H-H., Cuenca, N. and Kolb, H. (1990) Development of morphological types and distribution patterns of amacrine cells immunoreactive to tyrosine hydroxylase in the cat retina, Visual Neurosci. 4:159–175.CrossRefGoogle Scholar
  86. Wassle, H. (1988) Dendritic maturation of retinal ganglion cells, Trends Neurosci. 11:87–89.PubMedCrossRefGoogle Scholar
  87. White, C.A. and Chalupa, L.M. (1992) Ontogeny of somatostatin immunoreactivity in the cat retina, J. Comp. Neurol. 317:129–144.PubMedCrossRefGoogle Scholar
  88. Windle, W.F. (1930) Normal behavioural reactions of kittens correlated with the postnatal development of nerve-fibre density in spinal grey matter, J. Comp. Neurol. 50:479–503.CrossRefGoogle Scholar
  89. Wollner, D.A., Scheinman, R. and Catterall, W.A. (1988) Sodium channel expression and assembly during development of retinal ganglion cells, Neuron 1:727–737.PubMedCrossRefGoogle Scholar
  90. Wong, R.O.L. and Collin, S.P (1989) Dendritic maturation of displaced putative cholinergic amacrine cells in the rabbit retina, J. Comp. Biol. 287:164–178.Google Scholar
  91. Wulle, I. and Schnitzer, J. (1989) Distribution and morphology of tyrosine hydroxylase-immunoreactive neurons in the developing mouse retina, Develop. Brain Res. 48:59–72.CrossRefGoogle Scholar
  92. Yeh, H.H., Battelle, B-B. and Puro, D.G. (1983) Maturation of Neurotransmission at cholinergic synapses formed in culture by rat retinal neurones: regulation by cyclic AMP, Develop. Brain Res. 10:63–72.CrossRefGoogle Scholar
  93. Yew, D.T., Luo, C.B., Zheng, D.R. Guan, Y.L. Tsang, D. and Stadlin, A. (1991) Immunohistochemical localisation of substance P, enkephalin and serotonin in the developing human retina, J. Hirnforsh. 32:61–71.Google Scholar
  94. Zetterstrom, B. (1955) The effect of light on the appearance and development of the electroretinogram in newborn kittens, Acta Physiol. Scand. 35:272–279.CrossRefGoogle Scholar
  95. Zhang, D., Gallagher, M., Sladek, C.D. and Yeh, H.H. (1990) Postnatal development of corticotropin releasing factor-like immunoreactive amacrine cells in the rat retina, Develop. Brain Res. 51:185–194.CrossRefGoogle Scholar
  96. Zhang, D. and Yeh, H.H. (1990) Histogenesis of corticotrophin releasing factor-like immunoreactive amacrine cells in the rat retina, Develop. Brain Res. 53:194–199.CrossRefGoogle Scholar
  97. Zhang, D. and Yeh, H.H. (1991a) Corticotrophin releasing factor-like immunoreactivity (CRF-LI) in horizontal cells of the developing rat retina, Visual Neurosci. 6:383–391.CrossRefGoogle Scholar
  98. Zhang, D. and Yeh, H.H. (1991b) Protein kinase C-like immunoreactivity in rod bipolar cells of the rat retina: a developmental study. Visual Neurosci. 6:429–437.CrossRefGoogle Scholar
  99. Zhang, D. and Yeh, H.H. (1992) Substance-P-like immunoreactive amacrine cells in the adult and the developing rat retina, Develop. Brain Res. 68:55–65.CrossRefGoogle Scholar
  100. Zhou, Q-Y., Quaife, C.J. and Palmiter, R.D. (1995) Targeted disruption of the tyrosine hydroxylase gene reveals that catecholamines are required for mouse fetal development. Nature 374:640–643.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 1995

Authors and Affiliations

  • Jon Robbins
    • 1
  • Hisako Ikeda
    • 2
  1. 1.Biomedical Sciences Division, King’s CollegePharmacology GroupLondonUK
  2. 2.Vision Research Unit, UMDS, Rayne InstituteSt Thomas’s HospitalLondonUK

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