Hostname: page-component-cd9895bd7-hc48f Total loading time: 0 Render date: 2024-12-27T06:30:42.759Z Has data issue: false hasContentIssue false
  • English
  • Français

Early visual experience prevents but cannot reverse deprivation-induced loss of refinement in adult superior colliculus

Published online by Cambridge University Press:  30 January 2007

MARÍA MAGDALENA CARRASCO  and
SARAH L. PALLAS
MARÍA MAGDALENA CARRASCO
Affiliation:
Graduate Program in Neurobiology and Behavior, Department of Biology, Georgia State University, Atlanta, Georgia
SARAH L. PALLAS
Affiliation:
Graduate Program in Neurobiology and Behavior, Department of Biology, Georgia State University, Atlanta, Georgia
Get access Rights & Permissions [Opens in a new window]

Abstract

The role of sensory experience in the development and plasticity of the visual system has been widely studied. It has generally been reported that once animals reach adulthood, experience-dependent visual plasticity is reduced. We have found that visual experience is not needed for the refinement of receptive fields (RFs) in the superior colliculus (SC) but instead is necessary to maintain them in adulthood (Carrasco et al., 2005). Without light exposure, RFs in SC of hamsters refine by postnatal day 60 as usual but then enlarge, presumably reducing visual acuity. In this study we examine whether a brief period of light exposure during early postnatal development would be sufficient to prevent RF enlargement in adulthood, and whether prolonged light exposure in adulthood could reverse the deprivation-induced increase in RF size. We found that an early postnatal period of at least 30 days of visual experience was sufficient to maintain refined RFs in the adult SC. Prolonged visual experience in adulthood could not reverse the RF enlargement resulting from long-term dark rearing, reflecting a loss of plasticity at this age. Our results suggest that, unlike in visual cortex, dark rearing does not indefinitely extend the critical period of plasticity in SC. Rather, there is a limited time window when early experience can protect RFs from the detrimental effects of visual deprivation in adulthood. These results contribute to understanding adult brain plasticity and argue for the importance of early visual experience in protecting the adult visual system.

Keywords

RetinotectalVisual deprivationRodentAdult plasticityLow vision
Type
Research Article
Information
Visual Neuroscience , Volume 23 , Issue 6 , November 2006 , pp. 845 - 852
Copyright
© 2006 Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Akerman, C.J., Smyth, D., & Thompson, I.D. (2002). Visual experience before eye opening and the development of the retinogeniculate pathway. Neuron 36, 869–879.Google Scholar
Benevento, L.A., Bakkum, B.W., & Cohen, R.S. (1995). Gamma-amynobutiric acid and somatostin immunoreactivity in the visual cortex of normal and dark-reared rats. Brain Research 689, 172–182.Google Scholar
Binns, K.E. & Salt, T.E. (1998). Developmental changes in NMDA receptor mediated visual activity in the rat superior colliculus, and the effect of dark-rearing. Experimental Brain Research 120, 335–344.Google Scholar
Buisseret, P. & Imbert, M. (1975). Respones of neurons in the striate cortex in normal and dark-reared kittens during post-natal life. The Journal of Physiology 246, 98P–99P.Google Scholar
Carrasco, M.M., Razak, K.A., & Pallas, S.L. (2005). Visual experience is necessary for maintenance but not development of receptive fields in the superior colliculus. Journal of Neurophysiology 94, 1962–1970.Google Scholar
Carmignoto, G. & Vicini, S. (1992). Activity-dependent decrease in NMDA receptor responses during development of the visual cortex. Science 258, 1007–1011.Google Scholar
Chalupa, L.M. & Rhoades, R.W. (1978). Directional selectivity in hamster superior colliculus is modified by strobe-rearing but not by dark rearing. Science 199, 998–1001.Google Scholar
Chapman, B. (2000). Necessity for afferent activity to maintain eye-specific segregation in ferret lateral geniculate nucleus. Science 287, 2479–2482.Google Scholar
Crair, M.C., Horton, J.C., Antonini, A., & Stryker, M.P. (2001). Emergence of ocular dominance columns in cat visual cortex by 2 weeks of age. The Journal of Comparative Neurology 430, 235–249.Google Scholar
Crowley, J.C. & Katz, L.C. (1999). Development of ocular dominance columns in the absence of retinal input. Nature Neuroscience 2, 1125–1130.Google Scholar
Crowley, J.C. & Katz, L.C. (2000). Early development of ocular dominance columns. Science 290, 1321–1324.Google Scholar
Cynader, M. & Mitchell, D.E. (1980). Prolonged sensitivity to monocular deprivation in dark-reared cats. Journal of Neurophysiology 43, 1026–1040.Google Scholar
Cynader, M. (1983). Prolonged sensitivity to monocular deprivation in dark-reared cats: Effects of age and visual exposure. Developmental Brain Research 8, 155–164.Google Scholar
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 Research 34, 709–720.Google Scholar
Fortin, S., Chabli, A., Dumont, I., Shumikhina, S., Itaya, S.K., & Molotchnikoff, S. (1999). Maturation of visual receptive field properties in the rat superior colliculus. Developmental Brain Research 112, 55–64.Google Scholar
Fosse, V.M., Heggelund, P., & Fonnum, F. (1989). Postnatal development of glutamatergic, GABAergic and cholinergic neurotransmitter phenotypes in the visual cortex, lateral geniculate nucleus, pulvinar, and superior colliculus in cats. Journal of Neuroscience 9, 426–435.Google Scholar
Fregnac, Y. & Imbert, M. (1978). Early development of visual cortical cells in normal and dark-reared kittens: Relationship between orientation selectivity and ocular dominance. The Journal of Physiology 278, 27–44.Google Scholar
Frost, D.O., So, K.-F., & Schneider G.E. (1979). Postnatal development of retinal projections in Syrian hamsters: A study using autoradiographic and anterograde degeneration techniques. Neuroscience 4, 1649–1677.Google Scholar
Gordon, B., Kinch, G., Kato, N., Keele, C., Lissman, T., & Fu, L.N. (1997). Development of MK-801, kainate, AMPA, and muscimol binding sites and the effect of dark rearing in rat visual cortex. The Journal of Comparative Neurology 383, 73–81.Google Scholar
He, H.Y., Hodos, W., & Quinlan, E.M. (2006). Visual deprivation reactivates rapid ocular dominance plasticity in adult visual cortex. The Journal of Neuroscience 26, 2951–2955.Google Scholar
Hensch, T.K. (2004). Critical period regulation. Annual Review of Neuroscience 27, 549–579.Google Scholar
Hensch, T.K. (2005). Critical period plasticity in local cortical circuits. Nature Reviews Neuroscience 6, 877–888.Google Scholar
Hofer, S.B., Mrsic-Flogel, T.D., Bonhoeffer, T., & Hubener, M. (2006). Prior experience enhances plasticity in adult visual cortex. Nature Neuroscience 9, 127–132.Google Scholar
Huang, L. & Pallas, S.L. (2001). NMDA receptor blockade in the superior colliculus prevents developmental plasticity without blocking visual transmission or map compression. Journal of Neurophysiology 86, 1179–1194.Google Scholar
Huberman, A.D., Wang, G.Y., Liets, L.C., Collins, O.A., Chapman, B., & Chalupa, L.M. (2003). Eye-specific retinogeniculate segregation independent of normal neuronal activity. Science 300, 994–998.Google Scholar
Huhman, K.L. & Albers, H.E. (1994). Neuropeptide Y microinjected into the suprachiasmatic region phase shifts circadian rhythms in constant darkness. Peptides 15, 1475–1478.Google Scholar
Kirkwood, A., Rioult, M.C., & Bear, M.F. (1996). Experience-dependent modification of synaptic plasticity in visual cortex. Nature 381, 526–528.Google Scholar
Lee, W.C. & Nedivi, E. (2002). Extended plasticity of visual cortex in dark-reared animals may result from prolonged expression of cpg15-like genes. Journal of Neuroscience 22, 1807–1815.Google Scholar
Leventhal, A.G. (2003). GABA and its agonists improved visual cortical function in senescent monkeys. Science 300, 812–815.Google Scholar
Liao, D.S., Krahe, T.E., Prusky, G.T., Medina, A.E., & Ramoa, A.S. (2004). Recovery of cortical binocularity and orientation selectivity after the critical period for ocular dominance plasticity. Journal of Neurophysiology 92, 2113–2121.Google Scholar
Maggi, C.A. & Meli, A. (1986). Suitability of urethane anesthesia for physiopharmacological investigations in various systems. Part 1: General considerations. Experientia 42, 109–114.Google Scholar
Meister, M., Wong, R.O., Baylor, D.A., & Schatz, C.A. (1991). Synchronous bursts of action potential in ganglion cells of the developing mammalian retina. Science 252, 939–943.Google Scholar
Mitchell, D.E., Kind, P.C., Sengpiel, F., & Murphy, K. (2003). Brief daily periods of binocular vision prevent deprivation-induced acuity loss. Current Biology 13, 1704–1708.Google Scholar
Mitchell, D.E., Kind, P.C., Sengpiel, F., & Murphy, K. (2006). Short periods of concordant binocular vision prevent the development of deprivation amblyopia. European Journal of Neuroscience 23, 2458–2466.Google Scholar
Mower, G.D., Christen, W.G., & Caplan, C.J. (1983). Very brief visual experience eliminates plasticity in the cat visual cortex. Science 221, 178–180.Google Scholar
Mower, G.D., Caplan, C.J., Christen, W.G., & Duffy, F.H. (1985). Dark rearing prolongs physiological but not anatomical plasticity of the cat visual cortex. The Journal of Comparative Neurology 235, 448–466.Google Scholar
Mower, G.D. & Christen, W.G. (1985). Role of visual experience in activating critical period in cat visual cortex. Journal of Neurophysiology 53, 572–589.Google Scholar
Mower, G.D. (1991). The effect of dark rearing on the time course of the critical period in cat visual cortex. Developmental Brain Research 58, 151–158.Google Scholar
O'Leary, D.D., Crespo, D., Fawcett, J.W., & Cowan, W.M. (1986). The effect of intraocular tetrodotoxin on the postnatal reduction in the number of optic nerve axons in the rat. Brain Research 395, 96–103.Google Scholar
Pallas, S.L. & Finlay, B.L. (1989). Conservation of receptive field properties of superior colliculus cells after developmental rearrangements of retinal input. Visual Neuroscience 2, 121–135.Google Scholar
Pallas, S.L. & Finlay, B.L. (1991). Compensation for population size mismatches in the hamster retinotectal system: Alterations in the organization of retinal projections. Visual Neuroscience 6, 271–281.Google Scholar
Philpot, B.D., Sekhar, A.K., Shouval, H.Z., & Bear, M.F. (2001). Visual experience and deprivation bidirectionally modify the composition and function of NMDA receptor in visual cortex. Neuron 29, 157–169.Google Scholar
Quinlan, E.M., Olstein, D.H., & Bear, M.F. (1999). Bidirectional, experience-dependent regulation of N-methyl-D-aspartate receptor subunit composition in the rat visual cortex during postnatal development. Proceedings of the National Academy of Science 96, 12876–12880.Google Scholar
Razak, K.A., Huang, L., & Pallas, S.L. (2003). NMDA receptor blockade in the superior colliculus increases receptive field size without altering velocity and size tuning. Journal of Neurophysiology 90, 110–119.Google Scholar
Rhoades, R.W. & Chalupa, L.M. (1978). Functional and anatomical consequences of neonatal visual cortical damage in superior colliculus of the golden hamster. Journal of Neurophysiology 41, 1466–1494.Google Scholar
Schliebs, R., Hawken, M., & Bigl, V. (1986). Dark-rearing affects the development of benzodiazepine receptors in the central visual structures of rat brain. Brain Research 389, 179–185.Google Scholar
Stellwagen, D. & Shatz, C.J. (2002). An instructive role for retinal waves in the development of retinogeniculate connectivity. Neuron 33, 357–367.Google Scholar
Xiong, M., Pallas, S.L., Lim, S., & Finlay, B.L. (1994). Regulation of retinal ganglion cell axon arbor size by target availability: Mechanisms of compression and expansion of the retinotectal projection. Journal of Comparative Neurology 344, 581–597.Google Scholar