Structural underpinnings of functional plasticity in rodent visual cortex

Chiara Cerri, Marta Pietrasanta, Laura Restani

Abstract


Functional plasticity in rodent visual cortex has been intensively studied since the pioneering experiments of Hubel and Wiesel in the sixties. Nevertheless, the structural modifications underlying this phenomenon remain elusive. In this article, we will review recent data focused on the dynamic of excitatory and inhibitory synapses and their structural changes linked to functional modifications. We also review novel evidence on structural remodeling that promote functional plasticity and on the role of cytoskeleton modifications in experience-dependent plasticity of rodent visual cortex.


Keywords


visual cortex; dendritic spine; rodent; experience-dependent plasticity

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Antonini A, Fagiolini M, Stryker MP Anatomical correlates of functional plasticity in mouse visual cortex. J Neurosci, 19:4388-4406, (1999)

Antonini A, Stryker MP Rapid remodeling of axonal arbors in the visual cortex. Science, 260:1819-1821, (1993)

Bonhoeffer T, Yuste R Spine motility. Phenomenology, mechanisms, and function. Neuron, 35:1019-1027, (2002)

Buttery P, Beg AA, Chih B, Broder A, Mason CA, Scheiffele P The diacylglycerol-binding protein alpha1-chimaerin regulates dendritic morphology. Proc Natl Acad Sci U S A, 103:1924-1929, (2006)

Cerri C, Fabbri A, Vannini E, Spolidoro M, Costa M, Maffei L, Fiorentini C, Caleo M Activation of Rho GTPases triggers structural remodeling and functional plasticity in the adult rat visual cortex. The Journal of neuroscience : the official journal of the Society for Neuroscience, 31:15163-15172, (2011)

Chen JL, Flanders GH, Lee WC, Lin WC, Nedivi E Inhibitory dendrite dynamics as a general feature of the adult cortical microcircuit. J Neurosci, 31:12437-12443, (2011a)

Chen JL, Lin WC, Cha JW, So PT, Kubota Y, Nedivi E Structural basis for the role of inhibition in facilitating adult brain plasticity. Nat Neurosci, 14:587-594, (2011b)

Chen JL, Villa KL, Cha JW, So PT, Kubota Y, Nedivi E Clustered dynamics of inhibitory synapses and dendritic spines in the adult neocortex. Neuron, 74:361-373, (2012)

Dahlhaus M, Hermans JM, Van Woerden LH, Saiepour MH, Nakazawa K, Mansvelder HD, Heimel JA, Levelt CN Notch1 signaling in pyramidal neurons regulates synaptic connectivity and experience-dependent modifications of acuity in the visual cortex. J Neurosci, 28:10794-10802, (2008)

de Vivo L, Landi S, Panniello M, Baroncelli L, Chierzi S, Mariotti L, Spolidoro M, Pizzorusso T, Maffei L, Ratto GM Extracellular matrix inhibits structural and functional plasticity of dendritic spines in the adult visual cortex. Nat Commun, 4:1484, (2013)

Diamond MC, Lindner B, Johnson R, Bennett EL, Rosenzweig MR Differences in occipital cortical synapses from environmentally enriched, impoverished, and standard colony rats. J Neurosci Res, 1:109-119, (1975)

Diana G, Valentini G, Travaglione S, Falzano L, Pieri M, Zona C, Meschini S, Fabbri A, Fiorentini C Enhancement of learning and memory after activation of cerebral Rho GTPases. Proc Natl Acad Sci U S A, 104:636-641, (2007)

Djurisic M, Vidal GS, Mann M, Aharon A, Kim T, Ferrao Santos A, Zuo Y, Hubener M, Shatz CJ PirB regulates a structural substrate for cortical plasticity. Proc Natl Acad Sci U S A, 110:20771-20776, (2013)

Engert F, Bonhoeffer T Dendritic spine changes associated with hippocampal long-term synaptic plasticity. Nature, 399:66-70, (1999)

Fabbri A, Travaglione S, Fiorentini C Escherichia coli cytotoxic necrotizing factor 1 (CNF1): toxin biology, in vivo applications and therapeutic potential. Toxins (Basel), 2:283-296, (2010)

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, 34:709-720, (1994)

Fiorentini C, Fabbri A, Flatau G, Donelli G, Matarrese P, Lemichez E, Falzano L, Boquet P Escherichia coli cytotoxic necrotizing factor 1 (CNF1), a toxin that activates the Rho GTPase. J Biol Chem, 272:19532-19537, (1997)

Flatau G, Lemichez E, Gauthier M, Chardin P, Paris S, Fiorentini C, Boquet P Toxin-induced activation of the G protein p21 Rho by deamidation of glutamine. Nature, 387:729-733, (1997)

Frenkel MY, Bear MF How monocular deprivation shifts ocular dominance in visual cortex of young mice. Neuron, 44:917-923, (2004)

Gordon JA, Stryker MP Experience-dependent plasticity of binocular responses in the primary visual cortex of the mouse. J Neurosci, 16:3274-3286, (1996)

Govek EE, Newey SE, Akerman CJ, Cross JR, Van der Veken L, Van Aelst L The X-linked mental retardation protein oligophrenin-1 is required for dendritic spine morphogenesis. Nat Neurosci, 7:364-372, (2004)

Grutzendler J, Kasthuri N, Gan WB Long-term dendritic spine stability in the adult cortex. Nature, 420:812-816, (2002)

Guire ES, Lickey ME, Gordon B Critical period for the monocular deprivation effect in rats: assessment with sweep visually evoked potentials. J Neurophysiol, 81:121-128, (1999)

Hall A Rho GTPases and the actin cytoskeleton. Science, 279:509-514, (1998)

Hofer SB, Mrsic-Flogel TD, Bonhoeffer T, Hubener M Lifelong learning: ocular dominance plasticity in mouse visual cortex. Curr Opin Neurobiol, 16:451-459, (2006)

Hofer SB, Mrsic-Flogel TD, Bonhoeffer T, Hubener M Experience leaves a lasting structural trace in cortical circuits. Nature, 457:313-317, (2009)

Holtmaat A, Wilbrecht L, Knott GW, Welker E, Svoboda K Experience-dependent and cell-type-specific spine growth in the neocortex. Nature, 441:979-983, (2006)

Holtmaat AJ, Trachtenberg JT, Wilbrecht L, Shepherd GM, Zhang X, Knott GW, Svoboda K Transient and persistent dendritic spines in the neocortex in vivo. Neuron, 45:279-291, (2005)

Impey S, Davare M, Lesiak A, Fortin D, Ando H, Varlamova O, Obrietan K, Soderling TR, Goodman RH, Wayman GA An activity-induced microRNA controls dendritic spine formation by regulating Rac1-PAK signaling. Mol Cell Neurosci, 43:146-156, (2010)

Kang MG, Guo Y, Huganir RL AMPA receptor and GEF-H1/Lfc complex regulates dendritic spine development through RhoA signaling cascade. Proc Natl Acad Sci U S A, 106:3549-3554, (2009)

Kawaguchi Y, Karube F, Kubota Y Dendritic branch typing and spine expression patterns in cortical nonpyramidal cells. Cereb Cortex, 16:696-711, (2006)

Keck T, Mrsic-Flogel TD, Vaz Afonso M, Eysel UT, Bonhoeffer T, Hubener M Massive restructuring of neuronal circuits during functional reorganization of adult visual cortex. Nat Neurosci, 11:1162-1167, (2008)

Keck T, Scheuss V, Jacobsen RI, Wierenga CJ, Eysel UT, Bonhoeffer T, Hubener M Loss of sensory input causes rapid structural changes of inhibitory neurons in adult mouse visual cortex. Neuron, 71:869-882, (2011)

Knott GW, Quairiaux C, Genoud C, Welker E Formation of dendritic spines with GABAergic synapses induced by whisker stimulation in adult mice. Neuron, 34:265-273, (2002)

Lai KO, Ip NY Structural plasticity of dendritic spines: the underlying mechanisms and its dysregulation in brain disorders. Biochim Biophys Acta, 1832:2257-2263, (2013)

Lee WC, Chen JL, Huang H, Leslie JH, Amitai Y, So PT, Nedivi E A dynamic zone defines interneuron remodeling in the adult neocortex. Proc Natl Acad Sci U S A, 105:19968-19973, (2008)

Lee WC, Huang H, Feng G, Sanes JR, Brown EN, So PT, Nedivi E Dynamic remodeling of dendritic arbors in GABAergic interneurons of adult visual cortex. PLoS Biol, 4:e29, (2006)

Leggio MG, Mandolesi L, Federico F, Spirito F, Ricci B, Gelfo F, Petrosini L Environmental enrichment promotes improved spatial abilities and enhanced dendritic growth in the rat. Behav Brain Res, 163:78-90, (2005)

Lehmann K, Lowel S Age-dependent ocular dominance plasticity in adult mice. PLoS One, 3:e3120, (2008)

Lendvai B, Stern EA, Chen B, Svoboda K Experience-dependent plasticity of dendritic spines in the developing rat barrel cortex in vivo. Nature, 404:876-881, (2000)

Li Z, Van Aelst L, Cline HT Rho GTPases regulate distinct aspects of dendritic arbor growth in Xenopus central neurons in vivo. Nat Neurosci, 3:217-225, (2000)

Luo L, Hensch TK, Ackerman L, Barbel S, Jan LY, Jan YN Differential effects of the Rac GTPase on Purkinje cell axons and dendritic trunks and spines. Nature, 379:837-840, (1996)

Majewska A, Sur M Motility of dendritic spines in visual cortex in vivo: changes during the critical period and effects of visual deprivation. Proc Natl Acad Sci U S A, 100:16024-16029, (2003)

Majewska A, Tashiro A, Yuste R Regulation of spine calcium dynamics by rapid spine motility. J Neurosci, 20:8262-8268, (2000)

Majewska AK, Newton JR, Sur M Remodeling of synaptic structure in sensory cortical areas in vivo. J Neurosci, 26:3021-3029, (2006)

Marik SA, Yamahachi H, McManus JN, Szabo G, Gilbert CD Axonal dynamics of excitatory and inhibitory neurons in somatosensory cortex. PLoS Biol, 8:e1000395, (2010)

Markram H, Toledo-Rodriguez M, Wang Y, Gupta A, Silberberg G, Wu C Interneurons of the neocortical inhibitory system. Nat Rev Neurosci, 5:793-807, (2004)

Martino A, Ettorre M, Musilli M, Lorenzetto E, Buffelli M, Diana G Rho GTPase-dependent plasticity of dendritic spines in the adult brain. Front Cell Neurosci, 7:62, (2013)

Mataga N, Mizuguchi Y, Hensch TK Experience-dependent pruning of dendritic spines in visual cortex by tissue plasminogen activator. Neuron, 44:1031-1041, (2004)

Medini P, Pizzorusso T Visual experience and plasticity of the visual cortex: a role for epigenetic mechanisms. Front Biosci, 13:3000-3007, (2008)

Morishita H, Hensch TK Critical period revisited: impact on vision. Curr Opin Neurobiol, 18:101-107, (2008)

Nakayama AY, Luo L Intracellular signaling pathways that regulate dendritic spine morphogenesis. Hippocampus, 10:582-586, (2000)

Oray S, Majewska A, Sur M Dendritic spine dynamics are regulated by monocular deprivation and extracellular matrix degradation. Neuron, 44:1021-1030, (2004)

Penzes P, Beeser A, Chernoff J, Schiller MR, Eipper BA, Mains RE, Huganir RL Rapid induction of dendritic spine morphogenesis by trans-synaptic ephrinB-EphB receptor activation of the Rho-GEF kalirin. Neuron, 37:263-274, (2003)

Pizzorusso T, Medini P, Berardi N, Chierzi S, Fawcett JW, Maffei L Reactivation of ocular dominance plasticity in the adult visual cortex. Science, 298:1248-1251, (2002)

Pizzorusso T, Medini P, Landi S, Baldini S, Berardi N, Maffei L Structural and functional recovery from early monocular deprivation in adult rats. Proc Natl Acad Sci U S A, 103:8517-8522, (2006)

Sato M, Stryker MP Distinctive features of adult ocular dominance plasticity. J Neurosci, 28:10278-10286, (2008)

Sawtell NB, Frenkel MY, Philpot BD, Nakazawa K, Tonegawa S, Bear MF NMDA receptor-dependent ocular dominance plasticity in adult visual cortex. Neuron, 38:977-985, (2003)

Schmidt G, Sehr P, Wilm M, Selzer J, Mann M, Aktories K Gln 63 of Rho is deamidated by Escherichia coli cytotoxic necrotizing factor-1. Nature, 387:725-729, (1997)

Sin WC, Haas K, Ruthazer ES, Cline HT Dendrite growth increased by visual activity requires NMDA receptor and Rho GTPases. Nature, 419:475-480, (2002)

Skoff RP, Hamburger V Fine structure of dendritic and axonal growth cones in embryonic chick spinal cord. J Comp Neurol, 153:107-147, (1974)

Spolidoro M, Putignano E, Munafo C, Maffei L, Pizzorusso T Inhibition of matrix metalloproteinases prevents the potentiation of nondeprived-eye responses after monocular deprivation in juvenile rats. Cereb Cortex, 22:725-734, (2012)

Tashiro A, Minden A, Yuste R Regulation of dendritic spine morphology by the rho family of small GTPases: antagonistic roles of Rac and Rho. Cereb Cortex, 10:927-938, (2000)

Threadgill R, Bobb K, Ghosh A Regulation of dendritic growth and remodeling by Rho, Rac, and Cdc42. Neuron, 19:625-634, (1997)

Trachtenberg JT, Chen BE, Knott GW, Feng G, Sanes JR, Welker E, Svoboda K Long-term in vivo imaging of experience-dependent synaptic plasticity in adult cortex. Nature, 420:788-794, (2002)

Tropea D, Majewska AK, Garcia R, Sur M Structural dynamics of synapses in vivo correlate with functional changes during experience-dependent plasticity in visual cortex. J Neurosci, 30:11086-11095, (2010)

Van Aelst L, Cline HT Rho GTPases and activity-dependent dendrite development. Curr Opin Neurobiol, 14:297-304, (2004)

van Versendaal D, Rajendran R, Saiepour MH, Klooster J, Smit-Rigter L, Sommeijer JP, De Zeeuw CI, Hofer SB, Heimel JA, Levelt CN Elimination of inhibitory synapses is a major component of adult ocular dominance plasticity. Neuron, 74:374-383, (2012)

Wallace W, Bear MF A morphological correlate of synaptic scaling in visual cortex. J Neurosci, 24:6928-6938, (2004)

Wilbrecht L, Holtmaat A, Wright N, Fox K, Svoboda K Structural plasticity underlies experience-dependent functional plasticity of cortical circuits. J Neurosci, 30:4927-4932, (2010)

Yu H, Majewska AK, Sur M Rapid experience-dependent plasticity of synapse function and structure in ferret visual cortex in vivo. Proc Natl Acad Sci U S A, 108:21235-21240, (2011)

Zuo Y, Lin A, Chang P, Gan WB Development of long-term dendritic spine stability in diverse regions of cerebral cortex. Neuron, 46:181-189, (2005)




DOI: https://doi.org/10.4449/aib.v152i4.1588

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