Permanent functional reorganization of retinal circuits induced by early long-term visual deprivation

Journal of Neuroscience

Volumn 29, Issue 43, 2009, Pages 13691-13701

  Di Marco, Stefano ^a,b   Nguyen, Vincent A ^b   Bisti, Silvia ^a   Protti, Dario A ^b  

^a UNIVERSITY OF L'AQUILA   (Italy)

^b UNIVERSITY OF SYDNEY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; NONHUMAN; PRIORITY JOURNAL; RAT; RETINA GANGLION CELL; RETINA RECEPTIVE FIELD; STIMULUS RESPONSE; VISUAL DEPRIVATION; VISUAL STIMULATION;

ACTION POTENTIALS; ANIMALS; ANIMALS, NEWBORN; DARKNESS; ELECTRIC CONDUCTIVITY; LIGHT; NEURAL INHIBITION; NEURONAL PLASTICITY; PATCH-CLAMP TECHNIQUES; PHOTIC STIMULATION; RATS; RATS, LONG-EVANS; RETINA; RETINAL GANGLION CELLS; SENSORY DEPRIVATION; SYNAPTIC POTENTIALS; TIME FACTORS; VISION, OCULAR; VISUAL PATHWAYS;

EID: 70350560667     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3854-09.2009     Document Type: Article

References (68)

1. Akerman CJ, Smyth D, Thompson ID (2002) Visual experience before eye-opening and the development of the retinogeniculate pathway. Neuron 36:869-879. (Pubitemid 35447858)
2. Balkema GW Jr, Pinto LH (1982) Electrophysiology of retinal ganglion cells in the mouse: a study of a normally pigmented mouse and a congenic hypopigmentation mutant, pearl. J Neurophysiol 48:968-980.
3. Barlow HB, Hill RM, Levick WR (1964) Retinal ganglion cells responding selectively to direction and speed of image motion in the rabbit. J Physiol 173:377-407.
4. Baro JA, Lehmkuhle S, Kratz KE (1990) Electroretinograms and visual evoked potentials in long-term monocularly deprived cats. Invest Ophthalmol Vis Sci 31:1405-1409. (Pubitemid 20212375)
5. Bisti S, Gargini C, Chalupa LM (1998) Blockade of glutamate-mediated activity in the developing retina perturbs the functional segregation of ON and OFF pathways. J Neurosci 18:5019-5025. (Pubitemid 28285410)
6. Bodnarenko SR, Chalupa LM (1993) Stratification of ON and OFF ganglion cell dendrites depends on glutamate-mediated afferent activity in the developing retina. Nature 364:144-146. (Pubitemid 23238195)
7. Bodnarenko SR, Jeyarasasingam G, Chalupa LM (1995) Development and regulation of dendritic stratification in retinal ganglion cells by glutamate-mediated afferent activity. J Neurosci 15:7037-7045.
8. Bodnarenko SR, Yeung G, Thomas L, McCarthy M (1999) The development of retinal ganglion cell dendritic stratification in ferrets. Neuroreport 10:2955-2959. (Pubitemid 29507760)
9. Borg-Graham LJ (2001) The computation of directional selectivity in the retina occurs presynaptic to the ganglion cell. Nat Neurosci 4:176-183.
10. Carrasco MM, Razak KA, Pallas SL (2005) Visual experience is necessary for maintenance but not development of receptive fields in superior colliculus. J Neurophysiol 94:1962-1970.
11. Chan YC, Chiao CC (2008) Effect of visual experience on the maturation of ON-OFF direction selective ganglion cells in the rabbit retina. Vision Res 48:2466-2475.
12. Coombs J, Van Der List D, Chalupa LM (2007) Morphological properties of mouse retinal ganglion cells during postnatal development. J Comp Neurol 503:803-814. (Pubitemid 47290564)
13. Croner LJ, Kaplan E (1995) Receptive fields of P and M ganglion cells across the primate retina. Vision Res 35:7-24.
14. Cynader M, Berman N, Hein A (1976) Recovery of function in cat visual cortex following prolonged deprivation. Exp Brain Res 25:139-156.
15. Daniels JD, Pettigrew JD, Norman JL (1978) Development of single-neuron responses in kitten's lateral geniculate nucleus. J Neurophysiol 41:1373-1393. (Pubitemid 9061311)
16. DeAngelis GC, Ghose GM, Ohzawa I, Freeman RD (1999) Functional micro-organization of primary visual cortex: receptive field analysis of nearby neurons. J Neurosci 19:4046-4064. (Pubitemid 29222277)
17. Demb JB, Haarsma L, Freed MA, Sterling P (1999) Functional circuitry of the retinal ganglion cell's nonlinear receptive field. J Neurosci 19:9756-9767. (Pubitemid 30226649)
18. Deplano S, Gargini C, Maccarone R, Chalupa LM, Bisti S (2004) Long-term treatment of the developing retina with the metabotropic glutamate agonist APB induces long-term changes in the stratification of retinal ganglion cell dendrites. Dev Neurosci 26:396-405. (Pubitemid 40663248)
19. Diao L, Sun W, Deng Q, He S (2004) Development of the mouse retina: emerging morphological diversity of the ganglion cells. J Neurobiol 61:236-249. (Pubitemid 39426149)
20. Elstrott J, Anishchenko A, Greschner M, Sher A, Litke AM, Chichilnisky EJ, Feller MB (2008) Direction selectivity in the retina is established independent of visual experience and cholinergic retinal waves. Neuron 58:499-506. (Pubitemid 351672354)
21. Enroth-Cugell C, Robson JG (1966) The contrast sensitivity of retinal ganglion cells of the cat. J Physiol 187:517-552.
22. Enroth-Cugell C, Robson JG (1984) Functional characteristics and diversity of cat retinal ganglion cells. Basic characteristics and quantitative description. Invest Ophthalmol Vis Sci 25:250-267.
23. Fagiolini M, Pizzorusso T, Berardi N, Domenici L, Maffei L (1994) Functional postnatal development of the rat primary visual cortex and the role of visual experience: dark rearing and monocular deprivation. Vision Res 34:709-720. (Pubitemid 24061922)
24. Fischer KF, Lukasiewicz PD, Wong RO (1998) Age-dependent and cell class-specific modulation of retinal ganglion cell bursting activity by GABA. J Neurosci 18:3767-3778.
25. Giovannelli A, Di Marco S, Maccarone R, Bisti S (2008) Long-term dark rearing induces permanent reorganization in retinal circuitry. Biochem Biophys Res Commun 365:349-354. (Pubitemid 350137296)
26. Grubb MS, Thompson ID (2004) The influence of early experience on the development of sensory systems. Curr Opin Neurobiol 14:503-512. (Pubitemid 39078499)
27. Hensch TK, Fagiolini M (2005) Excitatory-inhibitory balance and critical period plasticity in developing visual cortex. Prog Brain Res 147:115-124.
28. Hensch TK, Fagiolini M, Mataga N, Stryker MP, Baekkeskov S, Kash SF (1998) Local GABA circuit control of experience-dependent plasticity in developing visual cortex. Science 282:1504-1508. (Pubitemid 28538615)
29. Hochstein S, Shapley RM (1976) Quantitative analysis of retinal ganglion cell classifications. J Physiol 262:237-264.
30. Huberman AD, Feller MB, Chapman B (2008) Mechanisms underlying development of visual maps and receptive fields. Annu Rev Neurosci 31:479-509.
31. Katagiri H, Fagiolini M, Hensch TK (2007) Optimization of somatic inhibition at critical period onset in mouse visual cortex. Neuron 53:805-812. (Pubitemid 46367559)
32. Kuffler SW (1953) Discharge patterns and functional organization of mammalian retina. J Neurophysiol 16:37-68.
33. Landi S, Cenni MC, Maffei L, Berardi N (2007) Environmental enrichment effects on development of retinal ganglion cell dendritic stratification require retinal BDNF. PLoS One 2:e346.
34. Lee EJ, Gibo TL, Grzywacz NM (2006) Dark-rearing-induced reduction of GABA and GAD and prevention of the effect by BDNF in the mouse retina. Eur J Neurosci 24:2118-2134.
35. Leitch E, Coaker J, Young C, Mehta V, Sernagor E (2005) GABA type-A activity controls its own developmental polarity switch in the maturing retina. J Neurosci 25:4801-4805. (Pubitemid 40664128)
36. Liao DS, Krahe TE, Prusky GT, Medina AE, Ramoa AS (2004) Recovery of cortical binocularity and orientation selectivity after the critical period for ocular dominance plasticity. J Neurophysiol 92:2113-2121.
37. Linsenmeier RA, Frishman LJ, Jakiela HG, Enroth-Cugell C (1982) Receptive field properties of X and Y cells in the cat retina derived from contrast sensitivity measurements. Vision Res 22:1173-1183.
38. Liu X, Grishanin RN, Tolwani RJ, Rentería RC, Xu B, Reichardt LF, Copenhagen DR (2007a) Brain-derived neurotrophic factor and TrkB modulate visual experience-dependent refinement of neuronal pathways in retina. J Neurosci 27:7256-7267. (Pubitemid 47037559)
39. Liu Y, Zhang LI, Tao HW (2007b) Heterosynaptic scaling of developing GABAergic synapses: dependence on glutamatergic input and developmental stage. J Neurosci 27:5301-5312. (Pubitemid 46790163)
40. Masland RH (1977) Maturation of function in the developing rabbit retina. J Comp Neurol 175:275-286.
41. Maslim J, Stone J (1988) Time course of stratification of the dendritic fields of ganglion cells in the retina of the cat. Dev Brain Res 44:87-93. (Pubitemid 18275314)
42. Mehta V, Sernagor E (2006a) Early neural activity and dendritic growth in turtle retinal ganglion cells. Eur J Neurosci 24:773-786. (Pubitemid 44232523)
43. Mehta V, Sernagor E (2006b) Receptive field structure-function correlates in developing turtle retinal ganglion cells. Eur J Neurosci 24:787-794. (Pubitemid 44232524)
44. Merwine DK, Grzywacz NM, Amthor FR (1998) Persistent effects of dark rearing on the development of turtle retinal ganglion cells. Soc Neurosci Abstr 24:600.10.
45. Mitchell DE (1988) The extent of visual recovery from early monocular or binocular visual deprivation in kittens. J Physiol 395:639-660.
46. Morales B, Choi SY, Kirkwood A (2002) Dark rearing alters the development of GABAergic transmission in visual cortex. J Neurosci 22:8084-8090. (Pubitemid 35379114)
47. Mumm JS, Godinho L, Morgan JL, Oakley DM, Schroeter EH, Wong RO (2005) Laminar circuit formation in the vertebrate retina. Prog Brain Res 147:155-169. (Pubitemid 39577617)
48. Osswald IK, Galan A, Bowie D (2007) Light triggers expression of philanthotoxin-insensitive Ca2+-permeable AMPA receptors in the developing rat retina. J Physiol 582:95-111. (Pubitemid 46993564)
49. Prusky GT, Douglas RM (2003) Developmental plasticity of mouse visual acuity. Eur J Neurosci 17:167-173.
50. Prusky GT, West PW, Douglas RM (2000) Experience-dependent plasticity of visual acuity in rats. Eur J Neurosci 12:3781-3786. (Pubitemid 30796080)
51. Rodieck RW (1965) Quantitative analysis of cat retinal ganglion cell response to visual stimuli. Vision Res 5:583-601.
52. Rodieck RW, Stone J (1965) Analysis of receptive fields of cat retinal ganglion cells. J Neurophysiol 28:832-849.
53. Sernagor E, Grzywacz NM (1995) Emergence of complex receptive field properties of ganglion cells in the developing turtle retina. J Neurophysiol 73:1355-1364.
54. Sernagor E, Grzywacz NM (1996) Influence of spontaneous activity and visual experience on developing retinal receptive fields. Curr Biol 6:1503-1508. (Pubitemid 27012249)
55. Sernagor E, Young C, Eglen SJ (2003) Developmental modulation of retinal wave dynamics: shedding light on the GABA saga. J Neurosci 23:7621-7629. (Pubitemid 37034079)
56. Stone C, Pinto LH (1993) Response properties of ganglion cells in the isolated mouse retina. Vis Neurosci 10:31-39.
57. Sun W, Li N, He S (2002) Large-scale morophological survey of rat retinal ganglion cells. Vis Neurosci 19:483-493. (Pubitemid 36019870)
58. Tao HW, Poo MM (2005) Activity-dependent matching of excitatory and inhibitory inputs during refinement of visual receptive fields. Neuron 45:829-836.
59. Taylor WR, Vaney DI (2002) Diverse synaptic mechanisms generate direction selectivity in the rabbit retina. J Neurosci 22:7712-7720.
60. Tian N, Copenhagen DR (2001) Visual deprivation alters development of synaptic function in inner retina after eye opening. Neuron 32:439-449. (Pubitemid 33082045)
61. Tian N, Copenhagen DR (2003) Visual stimulation is required for refinement of ON and OFF pathways in postnatal retina. Neuron 39:85-96. (Pubitemid 36830950)
62. Timney B, Mitchell DE, Giffin F (1978) The development of vision in cats after extended periods of dark-rearing. Exp Brain Res 31:547-560. (Pubitemid 8308503)
63. Tootle JS (1993) Early postnatal development of visual function in ganglion cells of the cat retina. J Neurophysiol 69:1645-1660.
64. Wang CT, Blankenship AG, Anishchenko A, Elstrott J, Fikhman M, Nakanishi S, Feller MB (2007) GABAA receptor-mediated signaling alters the structure of spontaneous activity in the developing retina. J Neurosci 27:9130-9140. (Pubitemid 47312057)
65. Wang GY, Liets LC, Chalupa LM (2001) Unique functional properties of on and off pathways in the developing mammalian retina. J Neurosci 21:4310-4317.
66. Wiesel TN, Hubel DH (1963) Effects of visual deprivation on morphology and physiology of cells in the cats lateral geniculate body. J Neurophysiol 26:978-993.
67. Zhang J, Yang Z, Wu SM (2005) Development of cholinergic amacrine cells is visual activity-dependent in the postnatal mouse retina. J Comp Neurol 484:331-343. (Pubitemid 40316260)
68. Zhang LL, Pathak HR, Coulter DA, Freed MA, Vardi N (2006) Shift of intracellular chloride concentration in ganglion and amacrine cells of developing mouse retina. J Neurophysiol 95:2404-2416.