Nogo-A deletion increases the plasticity of the optokinetic response and changes retinal projection organization in the adult mouse visual system

详细信息    查看全文

• 作者：Anna Guzik-Kornacka ; Alexander van der Bourg ; Flora Vajda…
• 关键词：Optokinetic response ; Retinogeniculate projections ; Monocular deprivation ; Subcortical visual system ; Plasticity
• 刊名：Brain Structure and Function
• 出版年：2016
• 出版时间：January 2016
• 年：2016
• 卷：221
• 期：1
• 页码：317-329
• 全文大小：6,159 KB
• 参考文献：Akbik FV, Bhagat SM, Patel PR, Cafferty WB, Strittmatter SM (2013) Anatomical plasticity of adult brain is titrated by Nogo Receptor 1. Neuron 77(5):859–866. doi:10.​1016/​j.​neuron.​2012.​12.​027 PubMedCentral CrossRef PubMed
  Benassi C, Lui F, Biral G, Ferrari R, Corazza R (1991) Correlation between amount of retinal afferents to the pretectal nucleus of the optic tract and dorsal terminal accessory optic nucleus and performance of horizontal optokinetic reflex in rat. Behav Brain Res 45(1):87–95. doi:10.​1016/​S0166-4328(05)80184-6 CrossRef PubMed
  Chapman B (2000) Necessity for afferent activity to maintain eye-specific segregation in ferret lateral geniculate nucleus. Science 287(5462):2479–2482. doi:10.​1126/​science.​287.​5462.​2479 PubMedCentral CrossRef PubMed
  Daw NW, Fox K, Sato H, Czepita D (1992) Critical period for monocular deprivation in the cat visual cortex. J Neurophysiol 67(1):197–202PubMed
  Delekate A, Zagrebelsky M, Kramer S, Schwab ME, Korte M (2011) NogoA restricts synaptic plasticity in the adult hippocampus on a fast time scale. Proc Natl Acad Sci USA 108(6):2569–2574. doi:10.​1073/​pnas.​1013322108 PubMedCentral CrossRef PubMed
  Demas J, Sagdullaev BT, Green E, Jaubert-Miazza L, McCall MA, Gregg RG, Wong RO, Guido W (2006) Failure to maintain eye-specific segregation in nob, a mutant with abnormally patterned retinal activity. Neuron 50(2):247–259. doi:10.​1016/​j.​neuron.​2006.​03.​033 CrossRef PubMed
  Dickendesher TL, Baldwin KT, Mironova YA, Koriyama Y, Raiker SJ, Askew KL, Wood A, Geoffroy CG, Zheng B, Liepmann CD, Katagiri Y, Benowitz LI, Geller HM, Giger RJ (2012) NgR1 and NgR3 are receptors for chondroitin sulfate proteoglycans. Nat Neurosci 15(5):703–712. doi:10.​1038/​nn.​3070 PubMedCentral CrossRef PubMed
  Douglas RM, Alam NM, Silver BD, McGill T, Tschetter WW, Prusky GT (2005) Independent visual threshold measurements in the two eyes of freely moving rats and mice using a virtual-reality optokinetic system. Vis Neurosci 22(5):677–684. doi:10.​1017/​S095252380522516​6 CrossRef PubMed
  Eysel UT, Schweigart G, Mittmann T, Eyding D, Qu Y, Vandesande F, Orban G, Arckens L (1999) Reorganization in the visual cortex after retinal and cortical damage. Restor Neurol Neurosci 15(2–3):153–164PubMed
  Giolli RA, Blanks RH, Lui F (2006) The accessory optic system: basic organization with an update on connectivity, neurochemistry, and function. Prog Brain Res 151:407–440. doi:10.​1016/​S0079-6123(05)51013-6 CrossRef PubMed
  Godement P, Salaun J, Imbert M (1984) Prenatal and postnatal development of retinogeniculate and retinocollicular projections in the mouse. J Comp Neurol 230:552–575. doi:10.​1002/​cne.​902300406 CrossRef PubMed
  Gordon JA, Stryker MP (1996) Experience-dependent plasticity of binocular responses in the primary visual cortex of the mouse. J Neurosci 16(10):3274–3286PubMed
  Grasse KL, Cynader MS, Douglas RM (1984) Alterations in response properties in the lateral and dorsal terminal nuclei of the cat accessory optic system following visual cortex lesions. Exp Brain Res 55(1):69–80CrossRef PubMed
  Hayhow WR, Webb C, Jervie A (1960) The accessory optic fiber system in the rat. J Comp Neurol 115(2):187–215. doi:10.​1002/​cne.​901150207 CrossRef PubMed
  Hensch TK (2005) Critical period plasticity in local cortical circuits. Nat Rev Neurosci 6(11):877–888. doi:10.​1038/​nrn1787 CrossRef PubMed
  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(5393):1504–1508PubMedCentral CrossRef PubMed
  Hofer SB, Mrsic-Flogel TD, Bonhoeffer T, Hubener M (2006) Prior experience enhances plasticity in adult visual cortex. Nat Neurosci 9(1):127–132. doi:10.​1038/​nn1610 CrossRef PubMed
  Hooks BM, Chen C (2006) Distinct roles for spontaneous and visual activity in remodeling of the retinogeniculate synapse. Neuron 52(2):281–291. doi:10.​1016/​j.​neuron.​2006.​07.​007 CrossRef PubMed
  Hooks BM, Chen C (2008) Vision triggers an experience-dependent sensitive period at the retinogeniculate synapse. J Neurosci 28(18):4807–4817. doi:10.​1523/​JNEUROSCI.​4667-07.​2008 PubMedCentral CrossRef PubMed
  Hubel DH, Wiesel TN (1970) The period of susceptibility to the physiological effects of unilateral eye closure in kittens. J Physiol 206(2):419–436PubMedCentral CrossRef PubMed
  Huber AB, Weinmann O, Brosamle C, Oertle T, Schwab ME (2002) Patterns of Nogo mRNA and protein expression in the developing and adult rat and after CNS lesions. J Neurosci 22(9):3553–3567PubMed
  Jaubert-Miazza L, Green E, Lo FS, Bui K, Mills J, Guido W (2005) Structural and functional composition of the developing retinogeniculate pathway in the mouse. Vis Neurosci 22(5):661–676. doi:10.​1017/​S095252380522515​4 CrossRef PubMed
  Kiernan JA (1984) Chromoxane cyanine R. II. Staining of animal tissues by the dye and its iron complexes. J Microsc 134(Pt 1):25–39CrossRef PubMed
  Lehmann K, Lowel S (2008) Age-dependent ocular dominance plasticity in adult mice. PLoS ONE 3(9):e3120. doi:10.​1371/​journal.​pone.​0003120 PubMedCentral CrossRef PubMed
  Lehmann K, Schmidt KF, Lowel S (2012) Vision and visual plasticity in ageing mice. Restor Neurol Neurosci 30(2):161–178. doi:10.​3233/​RNN-2012-110192 PubMed
  Linden DC, Guillery RW, Cucchiaro J (1981) The dorsal lateral geniculate nucleus of the normal ferret and its postnatal development. J Comp Neurol 203:89–211 doi:10.​1002/​cne.​902030204
  McGee AW, Yang Y, Fischer QS, Daw NW, Strittmatter SM (2005) Experience-driven plasticity of visual cortex limited by myelin and Nogo receptor. Science 309(5744):2222–2226. doi:10.​1126/​science.​1114362 PubMedCentral CrossRef PubMed
  Muir-Robinson G, Hwang BJ, Feller MB (2002) Retinogeniculate axons undergo eye-specific segregation in the absence of eye-specific layers. J Neurosci 22(13):5259–5264PubMed
  Pak MW, Giolli RA, Pinto LH, Mangini NJ, Gregory KM, Vanable JW (1987) Retinopretectal and accessory optic projections of normal mice and the Okn-defective mutant mice beige, beige-J, and pearl. J Comp Neurol 258(3):435–446. doi:10.​1002/​cne.​902580311 CrossRef PubMed
  Paxinos G, Franklin KBJ (2001) The mouse brain in stereotaxic coordinates, 2nd edn. Academic Press, San Diego
  Penn AA, Riquelme PA, Feller MB, Shatz CJ (1998) Competition in retinogeniculate patterning driven by spontaneous activity. Science 279(5359):2108–2112CrossRef PubMed
  Pernet V, Schwab ME (2012) The role of Nogo-A in axonal plasticity, regrowth and repair. Cell Tissue Res 349(1):97–104. doi:10.​1007/​s00441-012-1432-6 CrossRef PubMed
  Pernet V, Joly S, Dalkara D, Schwarz O, Christ F, Schaffer D, Flannery JG, Schwab ME (2012) Neuronal Nogo-A upregulation does not contribute to ER stress-associated apoptosis but participates in the regenerative response in the axotomized adult retina. Cell Death Differ 19(7):1096–1108. doi:10.​1038/​cdd.​2011.​191 PubMedCentral CrossRef PubMed
  Pernet V, Joly S, Jordi N, Dalkara D, Guzik-Kornacka A, Flannery JG, Schwab ME (2013) Misguidance and modulation of axonal regeneration by Stat3 and Rho/ROCK signaling in the transparent optic nerve. Cell Death Dis 4:e734. doi:10.​1038/​cddis.​2013.​266 PubMedCentral CrossRef PubMed
  Pizzorusso T, Medini P, Berardi N, Chierzi S, Fawcett JW, Maffei L (2002) Reactivation of ocular dominance plasticity in the adult visual cortex. Science 298(5596):1248–1251. doi:10.​1126/​science.​1072699 CrossRef PubMed
  Prusky GT, Alam NM, Beekman S, Douglas RM (2004) Rapid quantification of adult and developing mouse spatial vision using a virtual optomotor system. Invest Ophthalmol Vis Sci 45(12):4611–4616. doi:10.​1167/​iovs.​04-0541 CrossRef PubMed
  Prusky GT, Alam NM, Douglas RM (2006) Enhancement of vision by monocular deprivation in adult mice. J Neurosci 26(45):11554–11561. doi:10.​1523/​JNEUROSCI.​3396-06.​2006 CrossRef PubMed
  Rabchevsky AG, Fugaccia I, Sullivan PG, Scheff SW (2001) Cyclosporin A treatment following spinal cord injury to the rat: behavioral effects and stereological assessment of tissue sparing. J Neurotrauma 18(5):513–522. doi:10.​1089/​0897715013002273​14 CrossRef PubMed
  Raiker SJ, Lee H, Baldwin KT, Duan YT, Shrager P, Giger RJ (2010) Oligodendrocyte-myelin glycoprotein and nogo negatively regulate activity-dependent synaptic plasticity. J Neurosci 30(37):12432–12445. doi:10.​1523/​Jneurosci.​0895-10.​2010 PubMedCentral CrossRef PubMed
  Sawtell NB, Frenkel MY, Philpot BD, Nakazawa K, Tonegawa S, Bear MF (2003) NMDA receptor-dependent ocular dominance plasticity in adult visual cortex. Neuron 38(6):977–985. doi:10.​1016/​s0896-6273(03)00323-4 CrossRef PubMed
  Schwab ME (2010) Functions of Nogo proteins and their receptors in the nervous system. Nat Rev Neurosci 11(12):799–811. doi:10.​1038/​nrn2936 CrossRef PubMed
  Shutoh F, Ohki M, Kitazawa H, Itohara S, Nagao S (2006) Memory trace of motor learning shifts transsynaptically from cerebellar cortex to nuclei for consolidation. Neuroscience 139(2):767–777. doi:10.​1016/​j.​neuroscience.​2005.​12.​035 CrossRef PubMed
  Simonen M, Pedersen V, Weinmann O, Schnell L, Buss A, Ledermann B, Christ F, Sansig G, van der Putten H, Schwab ME (2003) Systemic deletion of the myelin-associated outgrowth inhibitor Nogo-A improves regenerative and plastic responses after spinal cord injury. Neuron 38(2):201–211CrossRef PubMed
  Simpson JI, Soodak RE, Hess R (1979) The accessory optic system and its relation to the vestibulocerebellum. Prog Brain Res 50:715–724. doi:10.​1016/​S0079-6123(08)60868-7 CrossRef PubMed
  Soodak RE, Simpson JI (1988) The accessory optic system of rabbit. I. Basic visual response properties. J Neurophysiol 60(6):2037–2054PubMed
  Syken J, Grandpre T, Kanold PO, Shatz CJ (2006) PirB restricts ocular-dominance plasticity in visual cortex. Science 313(5794):1795–1800. doi:10.​1126/​science.​1128232 CrossRef PubMed
  Tews B, Schonig K, Arzt ME, Clementi S, Rioult-Pedotti MS, Zemmar A, Berger SM, Schneider M, Enkel T, Weinmann O, Kasper H, Schwab ME, Bartsch D (2013) Synthetic microRNA-mediated downregulation of Nogo-A in transgenic rats reveals its role as regulator of synaptic plasticity and cognitive function. Proc Natl Acad Sci USA 110(16):6583–6588. doi:10.​1073/​pnas.​1217665110 PubMedCentral CrossRef PubMed
  Wada N, Funabiki K, Nakanishi S (2014) Role of granule-cell transmission in memory trace of cerebellum-dependent optokinetic motor learning. Proc Natl Acad Sci USA 111(14):5373–5378. doi:10.​1073/​pnas.​1402546111 PubMedCentral CrossRef PubMed
  Wiesel TN, Hubel DH (1963) Single-cell responses in striate cortex of kittens deprived of vision in one eye. J Neurophysiol 26:1003–1017PubMed
  
• 作者单位：Anna Guzik-Kornacka (1) (2)
  Alexander van der Bourg (1)
  Flora Vajda (1) (2)
  Sandrine Joly (1) (2)
  Franziska Christ (1) (2)
  Martin E. Schwab (1) (2)
  Vincent Pernet (1) (2) (3)
  
  1. Brain Research Institute, University of Zurich/ETH, Winterthurerstrasse 190, Room 55J04, 8057, Zurich, Switzerland
  2. Department of Health Sciences and Technology, ETH Zurich, 8057, Zurich, Switzerland
  3. CUO-Recherche, Hôpital St-Sacrement, CRCHU of Québec/University Laval, Local # H2-06, 1050 Chemin Ste-Foy, Québec, QC, G1S 4L8, Canada
  
• 刊物主题：Neurosciences; Cell Biology; Neurology;
• 出版者：Springer Berlin Heidelberg
• ISSN：1863-2661

文摘

The inhibitory action of Nogo-A on axonal growth has been well described. However, much less is known about the effects that Nogo-A could exert on the plasticity of neuronal circuits under physiological conditions. We investigated the effects of Nogo-A knock-out (KO) on visual function of adult mice using the optokinetic response (OKR) and the monocular deprivation (MD)-induced OKR plasticity and analyzed the anatomical organization of the eye-specific retinal projections. The spatial frequency sensitivity was higher in intact Nogo-A KO than in wild-type (WT) mice. After MD, Nogo-A KO mice reached a significantly higher spatial frequency and contrast sensitivity. Bilateral ablation of the visual cortex did not affect the OKR sensitivity before MD but reduced the MD-induced enhancement of OKR by approximately 50 % in Nogo-A KO and WT mice. These results suggest that cortical and subcortical brain structures contribute to the OKR plasticity. The tracing of retinal projections to the dorsal lateral geniculate nucleus (dLGN) revealed that the segregation of eye-specific terminals was decreased in the adult Nogo-A KO dLGN compared with WT mice. Strikingly, MD of the right eye led to additional desegregation of retinal projections in the left dLGN of Nogo-A KO but not in WT mice. In particular, MD promoted ectopic varicosity formation in Nogo-A KO dLGN axons. The present data show that Nogo-A restricts visual experience-driven plasticity of the OKR and plays a role in the segregation and maintenance of retinal projections to the brain. Keywords Optokinetic response Retinogeniculate projections Monocular deprivation Subcortical visual system Plasticity