Cited by 117Neuroscience and Neuropharmacology ResearchNeurogenesis and neuroplasticity mechanismsVisual perception and processing mechanisms

Neuregulin-1/ErbB4 Signaling Regulates Visual Cortical Plasticity

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Sun, Yanjun, Ikrar, Taruna, Davis, Melissa F., Gong, Nian, Zheng, Xiaoting, Luo, Z. David, Lai, Cary, Mei, Lin +3 more·2016·Neuron

Abstract

Experience alters cortical networks through neural plasticity mechanisms. During a developmental critical period, the most dramatic consequence of occluding vision through one eye (monocular deprivation) is a rapid loss of excitatory synaptic inputs to parvalbumin-expressing (PV) inhibitory neurons in visual cortex. Subsequent cortical disinhibition by reduced PV cell activity allows for excitatory ocular dominance plasticity. However, the molecular mechanisms underlying critical period synaptic plasticity are unclear. Here we show that brief monocular deprivation during the critical period downregulates neuregulin-1(NRG1)/ErbB4 signaling in PV neurons, causing retraction of excitatory inputs to PV neurons. Exogenous NRG1 rapidly restores excitatory inputs onto deprived PV cells through downstream PKC-dependent activation and AMPA receptor exocytosis, thus enhancing PV neuronal inhibition to excitatory neurons. NRG1 treatment prevents the loss of deprived eye visual cortical responsiveness in vivo. Our findings reveal molecular, cellular, and circuit mechanisms of NRG1/ErbB4 in regulating the initiation of critical period visual cortical plasticity.

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Crossref · 10.1016/j.neuron.2016.08.033

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  • Sensory manipulations or drug treatments that inhibit PV cells may result in PV-mediated cortical disinhibition that creates a permissive state for ODP in the presence of visual experience.

    “Sensory manipulations or drug treatments that inhibit PV cells may result in PV-mediated cortical disinhibition that creates a permissive state for ODP to occur in the presence of visual experience (Kuhlman et al., 2013;Gu et al., 2016;Sun et al., 2016;Grieco et al., 2020;Sadahiro et al., 2020).”

    From Psychedelics and Neural Plasticity: Therapeutic Implications (2022) · cites this paper as Sun et al., 2016

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Research works printed but not linked: 39

  1. Abe Y Namba H Kato T Iwakura Y Nawa H 2011 Neuregulin-1 signals from the periphery regulate AMPA receptor sensitivity and expression in GABAergic interneurons in developing neocortex J Neurosci 31 5699 5709 21490211 PMC6622838
  2. Bekhite MM Finkensieper A Binas S Muller J Wetzker R Figulla HR Sauer H Wartenberg M 2011 VEGF-mediated PI3K class IA and PKC signaling in cardiomyogenesis and vasculogenesis of mouse embryonic stem cells J Cell Sci 124 1819 1830 21540297
  3. Berardi N Pizzorusso T Ratto GM Maffei L 2003 Molecular basis of plasticity in the visual cortex Trends Neurosci 26 369 378 12850433
  4. Chen C Xu R Clarke IJ Ruan M Loneragan K Roh SG 2000 Diverse intracellular signalling systems used by growth hormone-releasing hormone in regulating voltage-gated Ca2+ or K channels in pituitary somatotropes Immunol Cell Biol 78 356 368 10947860
  5. Chen YJ Zhang M Yin DM Wen L Ting A Wang P Lu YS Zhu XH Li SJ Wu CY 2010 ErbB4 in parvalbumin-positive interneurons is critical for neuregulin 1 regulation of long-term potentiation Proc Natl Acad Sci U S A 107 21818 21823 21106764 PMC3003111
  6. D'Amour J A Froemke RC 2015 Inhibitory and excitatory spike-timing-dependent plasticity in the auditory cortex Neuron 86 514 528 25843405 PMC4409545
  7. Eilam R Pinkas-Kramarski R Ratzkin BJ Segal M Yarden Y 1998 Activity-dependent regulation of Neu differentiation factor/neuregulin expression in rat brain Proc Natl Acad Sci U S A 95 1888 1893 9465112 PMC19208
  8. Feldman DE 2012 The spike-timing dependence of plasticity Neuron 75 556 571 22920249 PMC3431193
  9. Frey RS Gao X Javaid K Siddiqui SS Rahman A Malik AB 2006 Phosphatidylinositol 3-kinase gamma signaling through protein kinase Czeta induces NADPH oxidase-mediated oxidant generation and NF-kappaB activation in endothelial cells J Biol Chem 281 16128 16138 16527821
  10. Gogtay N Vyas NS Testa R Wood SJ Pantelis C 2011 Age of onset of schizophrenia: perspectives from structural neuroimaging studies Schizophr Bull 37 504 513 21505117 PMC3080674
  11. Gu Y Huang S Chang MC Worley P Kirkwood A Quinlan EM 2013 Obligatory role for the immediate early gene NARP in critical period plasticity Neuron 79 335 346 23889936 PMC3804028
  12. Hensch TK 2005 Critical period plasticity in local cortical circuits Nat Rev Neurosci 6 877 888 16261181
  13. Hippenmeyer S Vrieseling E Sigrist M Portmann T Laengle C Ladle DR Arber S 2005 A developmental switch in the response of DRG neurons to ETS transcription factor signaling PLoS Biol 3 e159 15836427 PMC1084331
  14. Huang YZ Won S Ali DW Wang Q Tanowitz M Du QS Pelkey KA Yang DJ Xiong WC Salter MW 2000 Regulation of neuregulin signaling by PSD-95 interacting with ErbB4 at CNS synapses Neuron 26 443 455 10839362
  15. Huang ZJ Kirkwood A Pizzorusso T Porciatti V Morales B Bear MF Maffei L Tonegawa S 1999 BDNF regulates the maturation of inhibition and the critical period of plasticity in mouse visual cortex Cell 98 739 755 10499792
  16. Huber KM Kayser MS Bear MF 2000 Role for rapid dendritic protein synthesis in hippocampal mGluR-dependent long-term depression Science 288 1254 1257 10818003
  17. Iwakura Y Nawa H 2013 ErbB1-4-dependent EGF/neuregulin signals and their cross talk in the central nervous system: pathological implications in schizophrenia and Parkinson's disease Frontiers in cellular neuroscience 7 4 23408472 PMC3570895
  18. Kalatsky VA Stryker MP 2003 New paradigm for optical imaging: temporally encoded maps of intrinsic signal Neuron 38 529 545 12765606
  19. Li Q Roberts AC Glanzman DL 2005 Synaptic facilitation and behavioral dishabituation in Aplysia: dependence on release of Ca2+ from postsynaptic intracellular stores, postsynaptic exocytosis, and modulation of postsynaptic AMPA receptor efficacy J Neurosci 25 5623 5637 15944390 PMC6724986
  20. Liu X Bates R Yin DM Shen C Wang F Su N Kirov SA Luo Y Wang JZ Xiong WC 2011 Specific regulation of NRG1 isoform expression by neuronal activity J Neurosci 31 8491 8501 21653853 PMC3154699
  21. Livak KJ Schmittgen TD 2001 Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method Methods 25 402 408 11846609
  22. Long W Wagner KU Lloyd KC Binart N Shillingford JM Hennighausen L Jones FE 2003 Impaired differentiation and lactational failure of Erbb4-deficient mammary glands identify ERBB4 as an obligate mediator of STAT5 Development 130 5257 5268 12954715
  23. Lu W Man H Ju W Trimble WS MacDonald JF Wang YT 2001 Activation of synaptic NMDA receptors induces membrane insertion of new AMPA receptors and LTP in cultured hippocampal neurons Neuron 29 243 254 11182095
  24. Ma WP Li YT Tao HW 2013 Downregulation of cortical inhibition mediates ocular dominance plasticity during the critical period J Neurosci 33 11276 11280 23825430 PMC3718365
  25. Madisen L Mao T Koch H Zhuo JM Berenyi A Fujisawa S Hsu YW Garcia AJ 3rd Gu X Zanella S 2012 A toolbox of Cre-dependent optogenetic transgenic mice for light-induced activation and silencing Nat Neurosci 15 793 802 22446880 PMC3337962
  26. Madisen L Zwingman Ta Sunkin SM Oh SW Zariwala Ha Gu H Ng LL Palmiter RD Hawrylycz MJ Jones AR 2010 A robust and high-throughput Cre reporting and characterization system for the whole mouse brain Nature neuroscience 13 133 140 20023653 PMC2840225
  27. Maffei A Lambo ME Turrigiano GG 2010 Critical period for inhibitory plasticity in rodent binocular V1 J Neurosci 30 3304 3309 20203190 PMC2848504
  28. Mei L Xiong WC 2008 Neuregulin 1 in neural development, synaptic plasticity and schizophrenia Nat Rev Neurosci 9 437 452 18478032 PMC2682371
  29. Ozaki M Itoh K Miyakawa Y Kishida H Hashikawa T 2004 Protein processing and releases of neuregulin-1 are regulated in an activity-dependent manner J Neurochem 91 176 188 15379898
  30. Sato M Stryker MP 2008 Distinctive features of adult ocular dominance plasticity J Neurosci 28 10278 10286 18842887 PMC2851628
  31. Sawtell NB Frenkel MY Philpot BD Nakazawa K Tonegawa S Bear MF 2003 NMDA receptor-dependent ocular dominance plasticity in adult visual cortex Neuron 38 977 985 12818182
  32. Smith SL Trachtenberg JT 2007 Experience-dependent binocular competition in the visual cortex begins at eye opening Nat Neurosci 10 370 375 17293862
  33. Sternson SM Roth BL 2014 Chemogenetic tools to interrogate brain functions Annu Rev Neurosci 37 387 407 25002280
  34. Tamura H Kawata M Hamaguchi S Ishikawa Y Shiosaka S 2012 Processing of neuregulin-1 by neuropsin regulates GABAergic neuron to control neural plasticity of the mouse hippocampus J Neurosci 32 12657 12672 22972991 PMC6703812
  35. Vullhorst D Neddens J Karavanova I Tricoire L Petralia RS McBain CJ Buonanno A 2009 Selective expression of ErbB4 in interneurons, but not pyramidal cells, of the rodent hippocampus J Neurosci 29 12255 12264 19793984 PMC2774835
  36. Wen L Lu YS Zhu XH Li XM Woo RS Chen YJ Yin DM Lai C Terry AV Jr Vazdarjanova A 2010 Neuregulin 1 regulates pyramidal neuron activity via ErbB4 in parvalbumin-positive interneurons Proc Natl Acad Sci U S A 107 1211 1216 20080551 PMC2824309
  37. Woo RS Li XM Tao Y Carpenter-Hyland E Huang YZ Weber J Neiswender H Dong XP Wu J Gassmann M 2007 Neuregulin-1 enhances depolarization-induced GABA release Neuron 54 599 610 17521572
  38. Xu X Olivas ND Ikrar T Peng T Holmes TC Nie Q Shi Y 2016 Primary visual cortex shows laminar specific and balanced circuit organization of excitatory and inhibitory synaptic connectivity J Physiol PMC4818606 26844927
  39. Zhou P Zhang Y Ma Q Gu F Day DS He A Zhou B Li J Stevens SM Romo D 2013 Interrogating translational efficiency and lineage-specific transcriptomes using ribosome affinity purification Proc Natl Acad Sci U S A 110 15395 15400 24003143 PMC3780890

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Authors
Sun, Y., Ikrar, T., Davis, M. F., Gong, N., Zheng, X., Luo, Z. D., Lai, C., Mei, L., Holmes, T. C., Gandhi, S. P., & Xu, X.
Affiliations
  • University of California, Irvine (US)
  • Indiana University Bloomington (US)
  • Augusta University (US)
Corresponding author
Xu, Xiangmin
Venue
Neuron
Publisher
Elsevier BV
Published
2016-10
Volume
92
Issue
1
Pages
160-173
ISSN
0896-6273 (ISSN-L)
OpenAlex
W2520836933
Cited by
117
References
11
Citations by year
2026: 7 · 2025: 9 · 2024: 5 · 2023: 10 · 2022: 13 · 2021: 9 · 2020: 18 · 2019: 14 · 2018: 18 · 2017: 12 · 2016: 2
FWCI
8.63
Type
journal article
Language
en
Open access
Locations
  • Neuron (publishedVersion)
  • PubMed (publishedVersion)
  • PubMed Central (acceptedVersion)
  • eScholarship (California Digital Library) (submittedVersion)
Funders
  • National Institute of Mental Health (R01MH105427)
  • National Institute on Drug Abuse (R00DA023700)
  • National Eye Institute (DP2EY024504)
  • National Cancer Institute (P30CA062203)
  • National Institute of General Medical Sciences (R01GM107405, R01GM102965)
  • National Institute of Neurological Disorders and Stroke (R01NS078434)
Topics
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
  • Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Visual perception and processing mechanisms
Keywords
neuregulin-1, ERBB4 signaling, visual cortical plasticity, critical period, monocular deprivation, ocular dominance, parvalbumin interneurons, cortical disinhibition, PKC signaling, visual cortex
MeSH terms
Animals, Critical Period, Psychological, Female, Male, Neural Inhibition, Neuronal Plasticity, Neurons, Parvalbumins, Sensory Deprivation, Visual Cortex, Down-Regulation, Neuregulin-1, Dominance, Ocular, Mice, Receptor, ErbB-4

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