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Prolonged Period of Cortical Plasticity upon Redox Dysregulation in Fast-Spiking Interneurons

  • Hirofumi Morishita
    Affiliations
    FM Kirby Neurobiology Center, Department of Neurology, Boston Children’s Hospital, Harvard Medical School, Boston, Massachusetts
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  • Jan-Harry Cabungcal
    Affiliations
    Department of Psychiatry, Center for Psychiatric Neuroscience, Centre Hospitalier Universitaire Vaudois and University of Lausanne, Lausanne, Switzerland
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  • Ying Chen
    Affiliations
    School of Pharmacy, University of Colorado at Denver, Boulder, Colorado
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  • Kim Q. Do
    Affiliations
    Department of Psychiatry, Center for Psychiatric Neuroscience, Centre Hospitalier Universitaire Vaudois and University of Lausanne, Lausanne, Switzerland
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  • Takao K. Hensch
    Correspondence
    Address correspondence to Takao K. Hensch, Harvard University, FM Kirby Neurobiology Center, Department of Neurology, Boston Children’s Hospital, Harvard Medical School, 300 Longwood Ave, Boston, MA 02115
    Affiliations
    FM Kirby Neurobiology Center, Department of Neurology, Boston Children’s Hospital, Harvard Medical School, Boston, Massachusetts

    Center for Brain Science, Department of Molecular Cellular Biology, Harvard University, Cambridge, Massachusetts.
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      Abstract

      Background

      Oxidative stress and the specific impairment of perisomatic gamma-aminobutyric acid circuits are hallmarks of the schizophrenic brain and its animal models. Proper maturation of these fast-spiking inhibitory interneurons normally defines critical periods of experience-dependent cortical plasticity.

      Methods

      Here, we linked these processes by genetically inducing a redox dysregulation restricted to such parvalbumin-positive cells and examined the impact on critical period plasticity using the visual system as a model (3–6 mice/group).

      Results

      Oxidative stress was accompanied by a significant loss of perineuronal nets, which normally enwrap mature fast-spiking cells to limit adult plasticity. Accordingly, the neocortex remained plastic even beyond the peak of its natural critical period. These effects were not seen when redox dysregulation was targeted in excitatory principal cells.

      Conclusions

      A cell-specific regulation of redox state thus balances plasticity and stability of cortical networks. Mistimed developmental trajectories of brain plasticity may underlie, in part, the pathophysiology of mental illness. Such prolonged developmental plasticity may, in turn, offer a therapeutic opportunity for cognitive interventions targeting brain plasticity in schizophrenia.

      Keywords

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      References

        • Lewis D.A.
        • Hashimoto T.
        • Volk D.W.
        Cortical inhibitory neurons and schizophrenia.
        Nat Rev Neurosci. 2005; 6: 312-324
        • Insel T.R.
        Rethinking schizophrenia.
        Nature. 2010; 468: 187-193
        • Do K.Q.
        • Cabungcal J.H.
        • Frank A.
        • Steullet P.
        • Cuenod M.
        Redox dysregulation, neurodevelopment, and schizophrenia.
        Curr Opin Neurobiol. 2009; 19: 220-230
        • Do K.Q.
        • Trabesinger A.H.
        • Kirsten-Kruger M.
        • Lauer C.J.
        • Dydak U.
        • Hell D.
        • et al.
        Schizophrenia: Glutathione deficit in cerebrospinal fluid and prefrontal cortex in vivo.
        Eur J Neurosci. 2000; 12: 3721-3728
        • Andreazza A.C.
        • Kauer-Sant’anna M.
        • Frey B.N.
        • Bond D.J.
        • Kapczinski F.
        • Young L.T.
        • Yatham L.N.
        Oxidative stress markers in bipolar disorder: A meta-analysis.
        J Affect Disord. 2008; 111: 135-144
        • Yao J.K.
        • Keshavan M.S.
        Antioxidants, redox signaling, and pathophysiology in schizophrenia: An integrative view.
        Antioxid Redox Signal. 2011; 15: 2011-2035
        • Wang J.F.
        • Shao L.
        • Sun X.
        • Young L.T.
        Increased oxidative stress in the anterior cingulate cortex of subjects with bipolar disorder and schizophrenia.
        Bipolar Disord. 2009; 11: 523-529
        • Gawryluk J.W.
        • Wang J.F.
        • Andreazza A.C.
        • Shao L.
        • Young L.T.
        Decreased levels of glutathione, the major brain antioxidant, in post-mortem prefrontal cortex from patients with psychiatric disorders.
        Int J Neuropsychopharmacol. 2011; 14: 123-130
        • Gysin R.
        • Kraftsik R.
        • Sandell J.
        • Bovet P.
        • Chappuis C.
        • Conus P.
        • et al.
        Impaired glutathione synthesis in schizophrenia: Convergent genetic and functional evidence.
        Proc Natl Acad Sci U S A. 2007; 104: 16621-16626
        • Tosic M.
        • Ott J.
        • Barral S.
        • Bovet P.
        • Deppen P.
        • Gheorghita F.
        • et al.
        Schizophrenia and oxidative stress: Glutamate cysteine ligase modifier as a susceptibility gene.
        Am J Hum Genet. 2006; 79: 586-592
        • Park Y.U.
        • Jeong J.
        • Lee H.
        • Mun J.Y.
        • Kim J.H.
        • Lee J.S.
        • et al.
        Disrupted-in-schizophrenia 1 (DISC1) plays essential roles in mitochondria in collaboration with Mitofilin.
        Proc Natl Acad Sci U S A. 2010; 107: 17785-17790
        • Gokhale A.
        • Larimore J.
        • Werner E.
        • So L.
        • Moreno-De-Luca A.
        • Lese-Martin C.
        • et al.
        Quantitative proteomic and genetic analyses of the schizophrenia susceptibility factor dysbindin identify novel roles of the biogenesis of lysosome-related organelles complex 1.
        J Neurosci. 2012; 32: 3697-3711
        • Goldshmit Y.
        • Erlich S.
        • Pinkas-Kramarski R.
        Neuregulin rescues PC12-ErbB4 cells from cell death induced by H(2)O(2). Regulation of reactive oxygen species levels by phosphatidylinositol 3-kinase.
        J Biol Chem. 2001; 276: 46379-46385
        • Otte D.M.
        • Sommersberg B.
        • Kudin A.
        • Guerrero C.
        • Albayram O.
        • Filiou M.D.
        • et al.
        N-acetyl cysteine treatment rescues cognitive deficits induced by mitochondrial dysfunction in G72/G30 transgenic mice.
        Neuropsychopharmacology. 2011; 36: 2233-2243
        • Krishnan N.
        • Dickman M.B.
        • Becker D.F.
        Proline modulates the intracellular redox environment and protects mammalian cells against oxidative stress.
        Free Radic Biol Med. 2008; 44: 671-681
        • Steullet P.
        • Cabungcal J.H.
        • Kulak A.
        • Kraftsik R.
        • Chen Y.
        • Dalton T.P.
        • et al.
        Redox dysregulation affects the ventral but not dorsal hippocampus: Impairment of parvalbumin neurons, gamma oscillations, and related behaviors.
        J Neurosci. 2010; 30: 2547-2558
        • Kulak A.
        • Steullet P.
        • Cabungcal J.H.
        • Werge T.
        • Ingason A.
        • Cuenod M.
        • Do K.Q.
        Redox dysregulation in the pathophysiology of schizophrenia and bipolar disorder: Insights from animal models.
        Antioxid Redox Signal. 2013; 18: 1428-1443
        • Cabungcal J.H.
        • Counotte D.S.
        • Lewis E.M.
        • Tejeda H.A.
        • Piantadosi P.
        • Pollock C.
        • et al.
        Juvenile antioxidant treatment prevents adult deficits in a developmental model of schizophrenia.
        Neuron. 2014; 83: 1073-1084
        • Hu W.
        • Zhang M.
        • Czeh B.
        • Flugge G.
        • Zhang W.
        Stress impairs GABAergic network function in the hippocampus by activating nongenomic glucocorticoid receptors and affecting the integrity of the parvalbumin-expressing neuronal network.
        Neuropsychopharmacology. 2010; 35: 1693-1707
        • Grillo C.A.
        • Piroli G.G.
        • Rosell D.R.
        • Hoskin E.K.
        • McEwen B.S.
        • Reagan L.P.
        Region specific increases in oxidative stress and superoxide dismutase in the hippocampus of diabetic rats subjected to stress.
        Neuroscience. 2003; 121: 133-140
        • Jiang Z.
        • Rompala G.R.
        • Zhang S.
        • Cowell R.M.
        • Nakazawa K.
        Social isolation exacerbates schizophrenia-like phenotypes via oxidative stress in cortical interneurons.
        Biol Psychiatry. 2013; 73: 1024-1034
        • Powell S.B.
        • Sejnowski T.J.
        • Behrens M.M.
        Behavioral and neurochemical consequences of cortical oxidative stress on parvalbumin-interneuron maturation in rodent models of schizophrenia.
        Neuropharmacology. 2012; 62: 1322-1331
        • Behrens M.M.
        • Ali S.S.
        • Dao D.N.
        • Lucero J.
        • Shekhtman G.
        • Quick K.L.
        • Dugan L.L.
        Ketamine-induced loss of phenotype of fast-spiking interneurons is mediated by NADPH-oxidase.
        Science. 2007; 318: 1645-1647
        • Schiavone S.
        • Sorce S.
        • Dubois-Dauphin M.
        • Jaquet V.
        • Colaianna M.
        • Zotti M.
        • et al.
        Involvement of NOX2 in the development of behavioral and pathologic alterations in isolated rats.
        Biol Psychiatry. 2009; 66: 384-392
        • Cabungcal J.H.
        • Steullet P.
        • Kraftsik R.
        • Cuenod M.
        • Do K.Q.
        Early-life insults impair parvalbumin interneurons via oxidative stress: Reversal by N-acetylcysteine.
        Biol Psychiatry. 2013; 73: 574-582
        • Hensch T.K.
        Critical period plasticity in local cortical circuits.
        Nat Rev Neurosci. 2005; 6: 877-888
        • Sugiyama S.
        • Di Nardo A.A.
        • Aizawa S.
        • Matsuo I.
        • Volovitch M.
        • Prochiantz A.
        • Hensch T.K.
        Experience-dependent transfer of Otx2 homeoprotein into the visual cortex activates postnatal plasticity.
        Cell. 2008; 134: 508-520
        • Fagiolini M.
        • Hensch T.K.
        Inhibitory threshold for critical-period activation in primary visual cortex.
        Nature. 2000; 404: 183-186
        • Morishita H.
        • Miwa J.M.
        • Heintz N.
        • Hensch T.K.
        Lynx1, a cholinergic brake, limits plasticity in adult visual cortex.
        Science. 2010; 330: 1238-1240
        • Minichiello L.
        • Korte M.
        • Wolfer D.
        • Kuhn R.
        • Unsicker K.
        • Cestari V.
        • et al.
        Essential role for TrkB receptors in hippocampus-mediated learning.
        Neuron. 1999; 24: 401-414
        • Hippenmeyer S.
        • Vrieseling E.
        • Sigrist M.
        • Portmann T.
        • Laengle C.
        • Ladle D.R.
        • Arber S.
        A developmental switch in the response of DRG neurons to ETS transcription factor signaling.
        PLoS Biol. 2005; 3: e159
        • Chen Y.
        • Yang Y.
        • Miller M.L.
        • Shen D.
        • Shertzer H.G.
        • Stringer K.F.
        • et al.
        Hepatocyte-specific Gclc deletion leads to rapid onset of steatosis with mitochondrial injury and liver failure.
        Hepatology. 2007; 45: 1118-1128
        • Kobayashi Y.
        • Hensch T.K.
        Germline recombination by conditional gene targeting with Parvalbumin-Cre lines.
        Front Neural Circuits. 2013; 7: 168
        • Harno E.
        • Cottrell E.C.
        • White A.
        Metabolic pitfalls of CNS Cre-based technology.
        Cell Metab. 2013; 18: 21-28
        • Schmued L.C.
        • Stowers C.C.
        • Scallet A.C.
        • Xu L.
        Fluoro-Jade C results in ultra high resolution and contrast labeling of degenerating neurons.
        Brain Res. 2005; 1035: 24-31
        • Dalton T.P.
        • Dieter M.Z.
        • Yang Y.
        • Shertzer H.G.
        • Nebert D.W.
        Knockout of the mouse glutamate cysteine ligase catalytic subunit (Gclc) gene: Embryonic lethal when homozygous, and proposed model for moderate glutathione deficiency when heterozygous.
        Biochem Biophys Res Commun. 2000; 279: 324-329
        • Do K.Q.
        • Monin A.
        • Klaey M.
        • Butticaz C.
        • Cabungcal J.H.
        • Steullet P.
        • et al.
        Redox dysregulation affects proliferation, differentiation of oligodendrocyte progenitors and myelination: Relevance to dysconnectivity in schizophrenia.
        Biol Psychiatry. 2012; 71: 4S
        • Pizzorusso T.
        • Medini P.
        • Berardi N.
        • Chierzi S.
        • Fawcett J.W.
        • Maffei L.
        Reactivation of ocular dominance plasticity in the adult visual cortex.
        Science. 2002; 298: 1248-1251
        • Gogolla N.
        • Caroni P.
        • Luthi A.
        • Herry C.
        Perineuronal nets protect fear memories from erasure.
        Science. 2009; 325: 1258-1261
        • Miyata S.
        • Komatsu Y.
        • Yoshimura Y.
        • Taya C.
        • Kitagawa H.
        Persistent cortical plasticity by upregulation of chondroitin 6-sulfation.
        Nat Neurosci. 2012; 15 (S1–S2): 414-422
        • Beurdeley M.
        • Spatazza J.
        • Lee H.H.
        • Sugiyama S.
        • Bernard C.
        • Di Nardo A.A.
        • et al.
        Otx2 binding to perineuronal nets persistently regulates plasticity in the mature visual cortex.
        J Neurosci. 2012; 32: 9429-9437
        • Tremblay M.E.
        • Lowery R.L.
        • Majewska A.K.
        Microglial interactions with synapses are modulated by visual experience.
        PLoS Biol. 2010; 8: e1000527
        • Paolicelli R.C.
        • Bolasco G.
        • Pagani F.
        • Maggi L.
        • Scianni M.
        • Panzanelli P.
        • et al.
        Synaptic pruning by microglia is necessary for normal brain development.
        Science. 2011; 333: 1456-1458
        • Schafer D.P.
        • Lehrman E.K.
        • Kautzman A.G.
        • Koyama R.
        • Mardinly A.R.
        • Yamasaki R.
        • et al.
        Microglia sculpt postnatal neural circuits in an activity and complement-dependent manner.
        Neuron. 2012; 74: 691-705
        • Tremblay M.E.
        • Majewska A.K.
        A role for microglia in synaptic plasticity?.
        Commun Integr Biol. 2011; 4: 220-222
        • Hensch T.K.
        • Fagiolini M.
        Excitatory-inhibitory balance and critical period plasticity in developing visual cortex.
        Prog Brain Res. 2005; 147: 115-124
        • Morishita H.
        • Hensch T.K.
        Critical period revisited: Impact on vision.
        Curr Opin Neurobiol. 2008; 18: 101-107
        • Yazaki-Sugiyama Y.
        • Kang S.
        • Cateau H.
        • Fukai T.
        • Hensch T.K.
        Bidirectional plasticity in fast-spiking GABA circuits by visual experience.
        Nature. 2009; 462: 218-221
        • Kuhlman S.J.
        • Olivas N.D.
        • Tring E.
        • Ikrar T.
        • Xu X.
        • Trachtenberg J.T.
        A disinhibitory microcircuit initiates critical-period plasticity in the visual cortex.
        Nature. 2013; 501: 543-546
        • Aton S.J.
        • Broussard C.
        • Dumoulin M.
        • Seibt J.
        • Watson A.
        • Coleman T.
        • Frank M.G.
        Visual experience and subsequent sleep induce sequential plastic changes in putative inhibitory and excitatory cortical neurons.
        Proc Natl Acad Sci U S A. 2013; 110: 3101-3106
        • Spatazza J.
        • Lee H.H.
        • Di Nardo A.A.
        • Tibaldi L.
        • Joliot A.
        • Hensch T.K.
        • Prochiantz A.
        Choroid-plexus-derived otx2 homeoprotein constrains adult cortical plasticity.
        Cell Rep. 2013; 3: 1815-1823
        • Rees M.D.
        • Hawkins C.L.
        • Davies M.J.
        Hypochlorite and superoxide radicals can act synergistically to induce fragmentation of hyaluronan and chondroitin sulphates.
        Biochem J. 2004; 381: 175-184
        • Cabungcal J.H.
        • Steullet P.
        • Morishita H.
        • Kraftsik R.
        • Cuenod M.
        • Hensch T.K.
        • Do K.Q.
        Perineuronal nets protect fast-spiking interneurons against oxidative stress.
        Proc Natl Acad Sci U S A. 2013; 110: 9130-9135
        • Beste C.
        • Wascher E.
        • Dinse H.R.
        • Saft C.
        Faster perceptual learning through excitotoxic neurodegeneration.
        Curr Biol. 2012; 22: 1914-1917
        • Daskalakis Z.J.
        • Christensen B.K.
        • Fitzgerald P.B.
        • Chen R.
        Dysfunctional neural plasticity in patients with schizophrenia.
        Arch Gen Psychiatry. 2008; 65: 378-385
        • McClintock S.M.
        • Freitas C.
        • Oberman L.
        • Lisanby S.H.
        • Pascual-Leone A.
        Transcranial magnetic stimulation: A neuroscientific probe of cortical function in schizophrenia.
        Biol Psychiatry. 2011; 70: 19-27
        • Mears R.P.
        • Spencer K.M.
        Electrophysiological assessment of auditory stimulus-specific plasticity in schizophrenia.
        Biol Psychiatry. 2012; 71: 503-511
        • Cavus I.
        • Reinhart R.M.
        • Roach B.J.
        • Gueorguieva R.
        • Teyler T.J.
        • Clapp W.C.
        • et al.
        Impaired visual cortical plasticity in schizophrenia.
        Biol Psychiatry. 2012; 71: 512-520
        • Hasan A.
        • Nitsche M.A.
        • Rein B.
        • Schneider-Axmann T.
        • Guse B.
        • Gruber O.
        • et al.
        Dysfunctional long-term potentiation-like plasticity in schizophrenia revealed by transcranial direct current stimulation.
        Behav Brain Res. 2011; 224: 15-22
        • Rauchensteiner S.
        • Kawohl W.
        • Ozgurdal S.
        • Littmann E.
        • Gudlowski Y.
        • Witthaus H.
        • et al.
        Test-performance after cognitive training in persons at risk mental state of schizophrenia and patients with schizophrenia.
        Psychiatry Res. 2011; 185: 334-339
        • Ehlers M.D.
        Hijacking hebb: Noninvasive methods to probe plasticity in psychiatric disease.
        Biol Psychiatry. 2012; 71: 484-486
        • Vinogradov S.
        • Fisher M.
        • de Villers-Sidani E.
        de Villers-Sidani E.
        Cognitive training for impaired neural systems in neuropsychiatric illness. Neuropsychopharmacology. 2012; 37: 43-76
        • Kaneko Y.
        • Keshavan M.
        Cognitive remediation in schizophrenia.
        Clin Psychopharmacol Neurosci. 2012; 10: 125-135
        • Fisher M.
        • Loewy R.
        • Hardy K.
        • Schlosser D.
        • Vinogradov S.
        Cognitive interventions targeting brain plasticity in the prodromal and early phases of schizophrenia.
        Annu Rev Clin Psychol. 2013; 9: 435-463
        • Berretta S.
        Extracellular matrix abnormalities in schizophrenia.
        Neuropharmacology. 2012; 62: 1584-1597
        • Pantazopoulos H.
        • Woo T.U.
        • Lim M.P.
        • Lange N.
        • Berretta S.
        Extracellular matrix-glial abnormalities in the amygdala and entorhinal cortex of subjects diagnosed with schizophrenia.
        Arch Gen Psychiatry. 2010; 67: 155-166
        • Mauney S.A.
        • Athanas K.M.
        • Pantazopoulos H.
        • Shaskan N.
        • Passeri E.
        • Berretta S.
        • Woo T.U.
        Developmental pattern of perineuronal nets in the human prefrontal cortex and their deficit in schizophrenia.
        Biol Psychiatry. 2013; 74: 427-435
        • Rokem A.
        • Yoon J.H.
        • Ooms R.E.
        • Maddock R.J.
        • Minzenberg M.J.
        • Silver M.A.
        Broader visual orientation tuning in patients with schizophrenia.
        Front Hum Neurosci. 2011; 5: 127
        • Yoon J.H.
        • Maddock R.J.
        • Rokem A.
        • Silver M.A.
        • Minzenberg M.J.
        • Ragland J.D.
        • Carter C.S.
        GABA concentration is reduced in visual cortex in schizophrenia and correlates with orientation-specific surround suppression.
        J Neurosci. 2010; 30: 3777-3781
        • Hashimoto T.
        • Bazmi H.H.
        • Mirnics K.
        • Wu Q.
        • Sampson A.R.
        • Lewis D.A.
        Conserved regional patterns of GABA-related transcript expression in the neocortex of subjects with schizophrenia.
        Am J Psychiatry. 2008; 165: 479-489
        • Kim D.
        • Zemon V.
        • Saperstein A.
        • Butler P.D.
        • Javitt D.C.
        Dysfunction of early-stage visual processing in schizophrenia: Harmonic analysis.
        Schizophr Res. 2005; 76: 55-65
        • Bavelier D.
        • Levi D.M.
        • Li R.W.
        • Dan Y.
        • Hensch T.K.
        Removing brakes on adult brain plasticity: From molecular to behavioral interventions.
        J Neurosci. 2010; 30: 14964-14971
        • Hagihara H.
        • Ohira K.
        • Takao K.
        • Miyakawa T.
        Transcriptomic evidence for immaturity of the prefrontal cortex in patients with schizophrenia.
        Mol Brain. 2014; 7: 41
        • McGee A.W.
        • Yang Y.
        • Fischer Q.S.
        • Daw N.W.
        • Strittmatter S.M.
        Experience-driven plasticity of visual cortex limited by myelin and Nogo receptor.
        Science. 2005; 309: 2222-2226
        • Syken J.
        • Grandpre T.
        • Kanold P.O.
        • Shatz C.J.
        PirB restricts ocular-dominance plasticity in visual cortex.
        Science. 2006; 313: 1795-1800
        • Stark K.L.
        • Xu B.
        • Bagchi A.
        • Lai W.S.
        • Liu H.
        • Hsu R.
        • et al.
        Altered brain microRNA biogenesis contributes to phenotypic deficits in a 22q11-deletion mouse model.
        Nat Genet. 2008; 40: 751-760
        • Takesian A.E.
        • Hensch T.K.
        Balancing plasticity/stability across brain development.
        Prog Brain Res. 2013; 207: 3-34