Environmental Enrichment Rescues Binocular Matching of Orientation Preference in Mice that Have a Precocious Critical Period

Neuron

Volumn 80, Issue 1, 2013, Pages 198-209

  Wang, Bor Shuen ^a   Feng, Liang ^b   Liu, Mingna ^a   Liu, Xiaorong ^a,b   Cang, Jianhua ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

^b NORTHWESTERN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; HISTONE H4; SOMATOMEDIN C;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BINOCULAR MATCHING; BINOCULAR VISION; CONTROLLED STUDY; ENVIRONMENTAL ENRICHMENT; EYE DOMINANCE; FEMALE; HISTONE ACETYLATION; MALE; MOUSE; NERVE CELL PLASTICITY; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; ORIENTATION PREFERENCE; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; STRIATE CORTEX; VISUAL ORIENTATION;

ANIMALS; CRITICAL PERIOD (PSYCHOLOGY); MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; NEURONAL PLASTICITY; ORIENTATION; SENSORY DEPRIVATION; VISION, BINOCULAR; VISUAL CORTEX;

EID: 84884821458     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2013.07.023     Document Type: Article

References (83)

1. Alonso J.M., Martinez L.M. Functional connectivity between simple cells and complex cells in cat striate cortex. Nat. Neurosci. 1998, 1:395-403.
2. Baroncelli L., Sale A., Viegi A., Maya Vetencourt J.F., De Pasquale R., Baldini S., Maffei L. Experience-dependent reactivation of ocular dominance plasticity in the adult visual cortex. Exp. Neurol. 2010, 226:100-109.
3. Baroncelli L., Braschi C., Spolidoro M., Begenisic T., Maffei L., Sale A. Brain plasticity and disease: a matter of inhibition. Neural Plast. 2011, 2011:286073.
4. Begenisic T., Spolidoro M., Braschi C., Baroncelli L., Milanese M., Pietra G., Fabbri M.E., Bonanno G., Cioni G., Maffei L., Sale A. Environmental enrichment decreases GABAergic inhibition and improves cognitive abilities, synaptic plasticity, and visual functions in a mouse model of Down syndrome. Front. Cell Neurosci. 2011, 5:29.
5. Brainard M.S., Knudsen E.I. Sensitive periods for visual calibration of the auditory space map in the barn owl optic tectum. J.Neurosci. 1998, 18:3929-3942.
6. Cancedda L., Putignano E., Impey S., Maffei L., Ratto G.M., Pizzorusso T. Patterned vision causes CRE-mediated gene expression in the visual cortex through PKA and ERK. J.Neurosci. 2003, 23:7012-7020.
7. Cancedda L., Putignano E., Sale A., Viegi A., Berardi N., Maffei L. Acceleration of visual system development by environmental enrichment. J.Neurosci. 2004, 24:4840-4848.
8. Cang J., Kalatsky V.A., Löwel S., Stryker M.P. Optical imaging of the intrinsic signal as a measure of cortical plasticity in the mouse. Vis. Neurosci. 2005, 22:685-691.
9. Cang J., Niell C.M., Liu X., Pfeiffenberger C., Feldheim D.A., Stryker M.P. Selective disruption of one Cartesian axis of cortical maps and receptive fields by deficiency in ephrin-As and structured activity. Neuron 2008, 57:511-523.
10. Carro E., Nuñez A., Busiguina S., Torres-Aleman I. Circulating insulin-like growth factor I mediates effects of exercise on the brain. J.Neurosci. 2000, 20:2926-2933.
11. Chen L., Yang C., Mower G.D. Developmental changes in the expression of GABA(A) receptor subunits (alpha(1), alpha(2), alpha(3)) in the cat visual cortex and the effects of dark rearing. Brain Res. Mol. Brain Res. 2001, 88:135-143.
12. Ciucci F., Putignano E., Baroncelli L., Landi S., Berardi N., Maffei L. Insulin-like growth factor 1 (IGF-1) mediates the effects of enriched environment (EE) on visual cortical development. PLoS ONE 2007, 2:e475.
13. Cynader M., Berman N., Hein A. Recovery of function in cat visual cortex following prolonged deprivation. Exp. Brain Res. 1976, 25:139-156.
14. Daw N.W. Critical periods and strabismus: what questions remain?. Optom. Vis. Sci. 1997, 74:690-694.
15. Daw N.W., Berman N.E., Ariel M. Interaction of critical periods in the visual cortex of kittens. Science 1978, 199:565-567.
16. Dölen G., Osterweil E., Rao B.S., Smith G.B., Auerbach B.D., Chattarji S., Bear M.F. Correction of fragile X syndrome in mice. Neuron 2007, 56:955-962.
17. Emerson V.F., Chalupa L.M., Thompson I.D., Talbot R.J. Behavioural, physiological, and anatomical consequences of monocular deprivation in the golden hamster (Mesocricetus auratus). Exp. Brain Res. 1982, 45:168-178.
18. Erwin E., Miller K.D. The subregion correspondence model of binocular simple cells. J.Neurosci. 1999, 19:7212-7229.
19. Fagiolini M., Hensch T.K. Inhibitory threshold for critical-period activation in primary visual cortex. Nature 2000, 404:183-186.
20. Fagiolini M., Pizzorusso T., Berardi N., Domenici L., Maffei L. Functional postnatal development of the rat primary visual cortex and the role of visual experience: dark rearing and monocular deprivation. Vision Res. 1994, 34:709-720.
21. Fagiolini M., Katagiri H., Miyamoto H., Mori H., Grant S.G., Mishina M., Hensch T.K. Separable features of visual cortical plasticity revealed by N-methyl-D-aspartate receptor 2A signaling. Proc. Natl. Acad. Sci. USA 2003, 100:2854-2859.
22. Fagiolini M., Fritschy J.M., Löw K., Möhler H., Rudolph U., Hensch T.K. Specific GABAA circuits for visual cortical plasticity. Science 2004, 303:1681-1683.
23. Fass D.M., Butler J.E., Goodman R.H. Deacetylase activity is required for cAMP activation of a subset of CREB target genes. J.Biol. Chem. 2003, 278:43014-43019.
24. Ferster D., Miller K.D. Neural mechanisms of orientation selectivity in the visual cortex. Annu. Rev. Neurosci. 2000, 23:441-471.
25. Fischer A., Sananbenesi F., Wang X., Dobbin M., Tsai L.H. Recovery of learning and memory is associated with chromatin remodelling. Nature 2007, 447:178-182.
26. Gilbert C.D., Kelly J.P. The projections of cells in different layers of the cat's visual cortex. J.Comp. Neurol. 1975, 163:81-105.
27. Gogolla N., Leblanc J.J., Quast K.B., Südhof T.C., Fagiolini M., Hensch T.K. Common circuit defect of excitatory-inhibitory balance in mouse models of autism. J.Neurodev. Disord. 2009, 1:172-181.
28. Gordon J.A., Stryker M.P. Experience-dependent plasticity of binocular responses in the primary visual cortex of the mouse. J.Neurosci. 1996, 16:3274-3286.
29. Hanover J.L., Huang Z.J., Tonegawa S., Stryker M.P. Brain-derived neurotrophic factor overexpression induces precocious critical period in mouse visual cortex. J.Neurosci. 1999, 19:RC40.
30. Harwerth R.S., Smith E.L., Duncan G.C., Crawford M.L., von Noorden G.K. Multiple sensitive periods in the development of the primate visual system. Science 1986, 232:235-238.
31. Harwerth R.S., Smith E.L., Crawford M.L., von Noorden G.K. Behavioral studies of the sensitive periods of development of visual functions in monkeys. Behav. Brain Res. 1990, 41:179-198.
32. Hensch T.K. Critical period plasticity in local cortical circuits. Nat. Rev. Neurosci. 2005, 6:877-888.
33. Hensch T.K., Fagiolini M., Mataga N., Stryker M.P., Baekkeskov S., Kash S.F. Local GABA circuit control of experience-dependent plasticity in developing visual cortex. Science 1998, 282:1504-1508.
34. Huang Z.J., Kirkwood A., Pizzorusso T., Porciatti V., Morales B., Bear M.F., Maffei L., Tonegawa S. BDNF regulates the maturation of inhibition and the critical period of plasticity in mouse visual cortex. Cell 1999, 98:739-755.
35. Hubel D.H., Freeman D.C. Projection into the visual field of ocular dominance columns in macaque monkey. Brain Res. 1977, 122:336-343.
36. Hubel D.H., Wiesel T.N. Receptive fields, binocular interaction and functional architecture in the cat's visual cortex. J.Physiol. 1962, 160:106-154.
37. Hubel D.H., Wiesel T.N. The period of susceptibility to the physiological effects of unilateral eye closure in kittens. J.Physiol. 1970, 206:419-436.
38. Hubel D.H., Wiesel T.N., LeVay S. Plasticity of ocular dominance columns in monkey striate cortex. Philos. Trans. R. Soc. Lond. B Biol. Sci. 1977, 278:377-409.
39. Issa N.P., Trachtenberg J.T., Chapman B., Zahs K.R., Stryker M.P. The critical period for ocular dominance plasticity in the Ferret's visual cortex. J.Neurosci. 1999, 19:6965-6978.
40. Iwai Y., Fagiolini M., Obata K., Hensch T.K. Rapid critical period induction by tonic inhibition in visual cortex. J.Neurosci. 2003, 23:6695-6702.
41. Jia H., Rochefort N.L., Chen X., Konnerth A. Dendritic organization of sensory input to cortical neurons invivo. Nature 2010, 464:1307-1312.
42. Johnson J., Sherry D.M., Liu X., Fremeau R.T., Seal R.P., Edwards R.H., Copenhagen D.R. Vesicular glutamate transporter 3 expression identifies glutamatergic amacrine cells in the rodent retina. J.Comp. Neurol. 2004, 477:386-398.
43. Jones K.R., Spear P.D., Tong L. Critical periods for effects of monocular deprivation: differences between striate and extrastriate cortex. J.Neurosci. 1984, 4:2543-2552.
44. Kanold P.O., Kim Y.A., GrandPre T., Shatz C.J. Co-regulation of ocular dominance plasticity and NMDA receptor subunit expression in glutamic acid decarboxylase-65 knock-out mice. J.Physiol. 2009, 587:2857-2867.
45. Knudsen E.I. Sensitive periods in the development of the brain and behavior. J.Cogn. Neurosci. 2004, 16:1412-1425.
46. Ko H., Hofer S.B., Pichler B., Buchanan K.A., Sjöström P.J., Mrsic-Flogel T.D. Functional specificity of local synaptic connections in neocortical networks. Nature 2011, 473:87-91.
47. Korzus E., Rosenfeld M.G., Mayford M. CBP histone acetyltransferase activity is a critical component of memory consolidation. Neuron 2004, 42:961-972.
48. Kuhlman S.J., Tring E., Trachtenberg J.T. Fast-spiking interneurons have an initial orientation bias that is lost with vision. Nat. Neurosci. 2011, 14:1121-1123.
49. Landi S., Cenni M.C., Maffei L., Berardi N. Environmental enrichment effects on development of retinal ganglion cell dendritic stratification require retinal BDNF. PLoS ONE 2007, 2:e346.
50. LeBlanc J.J., Fagiolini M. Autism: a "critical period" disorder?. Neural Plast. 2011, 2011:921680.
51. Levenson J.M., O'Riordan K.J., Brown K.D., Trinh M.A., Molfese D.L., Sweatt J.D. Regulation of histone acetylation during memory formation in the hippocampus. J.Biol. Chem. 2004, 279:40545-40559.
52. Lewis T.L., Maurer D. Multiple sensitive periods in human visual development: evidence from visually deprived children. Dev. Psychobiol. 2005, 46:163-183.
53. Lewis T.L., Maurer D. Effects of early pattern deprivation on visual development. Optom. Vis. Sci. 2009, 86:640-646.
54. Li Y.T., Ma W.P., Pan C.J., Zhang L.I., Tao H.W. Broadening of cortical inhibition mediates developmental sharpening of orientation selectivity. J.Neurosci. 2012, 32:3981-3991.
55. Liu X., Grishanin R.N., Tolwani R.J., Rentería R.C., Xu B., Reichardt L.F., Copenhagen D.R. Brain-derived neurotrophic factor and TrkB modulate visual experience-dependent refinement of neuronal pathways in retina. J.Neurosci. 2007, 27:7256-7267.
56. Majdan M., Shatz C.J. Effects of visual experience on activity-dependent gene regulation in cortex. Nat. Neurosci. 2006, 9:650-659.
57. Martinez L.M., Alonso J.M. Construction of complex receptive fields in cat primary visual cortex. Neuron 2001, 32:515-525.
58. Morales B., Choi S.Y., Kirkwood A. Dark rearing alters the development of GABAergic transmission in visual cortex. J.Neurosci. 2002, 22:8084-8090.
59. Mower G.D. The effect of dark rearing on the time course of the critical period in cat visual cortex. Brain Res. Dev. Brain Res. 1991, 58:151-158.
60. Mrsic-Flogel T.D., Hofer S.B., Ohki K., Reid R.C., Bonhoeffer T., Hübener M. Homeostatic regulation of eye-specific responses in visual cortex during ocular dominance plasticity. Neuron 2007, 54:961-972.
61. Nelson C.A., Zeanah C.H., Fox N.A., Marshall P.J., Smyke A.T., Guthrie D. Cognitive recovery in socially deprived young children: the Bucharest Early Intervention Project. Science 2007, 318:1937-1940.
62. Niell C.M., Stryker M.P. Highly selective receptive fields in mouse visual cortex. J.Neurosci. 2008, 28:7520-7536.
63. Peixoto L., Abel T. The role of histone acetylation in memory formation and cognitive impairments. Neuropsychopharmacology 2013, 38:62-76.
64. Popescu M.V., Polley D.B. Monaural deprivation disrupts development of binaural selectivity in auditory midbrain and cortex. Neuron 2010, 65:718-731.
65. Putignano E., Lonetti G., Cancedda L., Ratto G., Costa M., Maffei L., Pizzorusso T. Developmental downregulation of histone posttranslational modifications regulates visual cortical plasticity. Neuron 2007, 53:747-759.
66. Rochefort N.L., Narushima M., Grienberger C., Marandi N., Hill D.N., Konnerth A. Development of direction selectivity in mouse cortical neurons. Neuron 2011, 71:425-432.
67. Sale A., Maya Vetencourt J.F., Medini P., Cenni M.C., Baroncelli L., De Pasquale R., Maffei L. Environmental enrichment in adulthood promotes amblyopia recovery through a reduction of intracortical inhibition. Nat. Neurosci. 2007, 10:679-681.
68. Sarnaik R., Wang B.S., Cang J. Experience-Dependent and Independent Binocular Correspondence of Receptive Field Subregions in Mouse Visual Cortex. Cereb. Cortex 2013, Published online February 6, 2013. 10.1093/cercor/bht027.
69. Sato M., Stryker M.P. Genomic imprinting of experience-dependent cortical plasticity by the ubiquitin ligase gene Ube3a. Proc. Natl. Acad. Sci. USA 2010, 107:5611-5616.
70. Scali M., Baroncelli L., Cenni M.C., Sale A., Maffei L. A rich environmental experience reactivates visual cortex plasticity in aged rats. Exp. Gerontol. 2012, 47:337-341.
71. Shafaati M., O'Driscoll R., Björkhem I., Meaney S. Transcriptional regulation of cholesterol 24-hydroxylase by histone deacetylase inhibitors. Biochem. Biophys. Res. Commun. 2009, 378:689-694.
72. Sweatt J.D. Experience-dependent epigenetic modifications in the central nervous system. Biol. Psychiatry 2009, 65:191-197.
73. Tropea D., Kreiman G., Lyckman A., Mukherjee S., Yu H., Horng S., Sur M. Gene expression changes and molecular pathways mediating activity-dependent plasticity in visual cortex. Nat. Neurosci. 2006, 9:660-668.
74. Tropea D., Giacometti E., Wilson N.R., Beard C., McCurry C., Fu D.D., Flannery R., Jaenisch R., Sur M. Partial reversal of Rett Syndrome-like symptoms in MeCP2 mutant mice. Proc. Natl. Acad. Sci. USA 2009, 106:2029-2034.
75. Van Sluyters R.C., Stewart D.L. Binocular neurons of the rabbit's visual cortex: effects of monocular sensory deprivation. Exp. Brain Res. 1974, 19:196-204.
76. Vecsey C.G., Hawk J.D., Lattal K.M., Stein J.M., Fabian S.A., Attner M.A., Cabrera S.M., McDonough C.B., Brindle P.K., Abel T., Wood M.A. Histone deacetylase inhibitors enhance memory and synaptic plasticity via CREB:CBP-dependent transcriptional activation. J.Neurosci. 2007, 27:6128-6140.
77. Wang L., Rangarajan K.V., Lawhn-Heath C.A., Sarnaik R., Wang B.S., Liu X., Cang J. Direction-specific disruption of subcortical visual behavior and receptive fields in mice lacking the beta2 subunit of nicotinic acetylcholine receptor. J.Neurosci. 2009, 29:12909-12918.
78. Wang B.S., Sarnaik R., Cang J. Critical period plasticity matches binocular orientation preference in the visual cortex. Neuron 2010, 65:246-256.
79. Wang L., Sarnaik R., Rangarajan K., Liu X., Cang J. Visual receptive field properties of neurons in the superficial superior colliculus of the mouse. J.Neurosci. 2010, 30:16573-16584.
80. Weaver I.C., Meaney M.J., Szyf M. Maternal care effects on the hippocampal transcriptome and anxiety-mediated behaviors in the offspring that are reversible in adulthood. Proc. Natl. Acad. Sci. USA 2006, 103:3480-3485.
81. Wiesel T.N., Hubel D.H. Effects of visual deprivation on morphology and physiology of cells in the cat's lateral geniculate body. J.Neurophysiol. 1963, 26:978-993.
82. Wiesel T.N., Hubel D.H. Extent of recovery from the effects of visual deprivation in kittens. J.Neurophysiol. 1965, 28:1060-1072.
83. Yashiro K., Riday T.T., Condon K.H., Roberts A.C., Bernardo D.R., Prakash R., Weinberg R.J., Ehlers M.D., Philpot B.D. Ube3a is required for experience-dependent maturation of the neocortex. Nat. Neurosci. 2009, 12:777-783.