Neuregulin-1/ErbB4 Signaling Regulates Visual Cortical Plasticity

Yanjun Sun, Taruna Ikrar, Melissa F. Davis, Nian Gong, Xiaoting Zheng, Z. David Luo, Cary Lai, Lin Mei, Todd C. Holmes, Sunil P. Gandhi, Xiangmin Xu

Research output: Contribution to journalArticle

35 Citations (Scopus)

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.

Original languageEnglish (US)
Pages (from-to)160-173
Number of pages14
JournalNeuron
Volume92
Issue number1
DOIs
StatePublished - Oct 5 2016

Fingerprint

Neuregulin-1
Parvalbumins
Neurons
Neuronal Plasticity
ocular Dominance
AMPA Receptors
Exocytosis
Visual Cortex
Down-Regulation
Critical Period (Psychology)

ASJC Scopus subject areas

  • Neuroscience(all)

Cite this

Sun, Y., Ikrar, T., Davis, M. F., Gong, N., Zheng, X., Luo, Z. D., ... Xu, X. (2016). Neuregulin-1/ErbB4 Signaling Regulates Visual Cortical Plasticity. Neuron, 92(1), 160-173. https://doi.org/10.1016/j.neuron.2016.08.033

Neuregulin-1/ErbB4 Signaling Regulates Visual Cortical Plasticity. / Sun, Yanjun; Ikrar, Taruna; Davis, Melissa F.; Gong, Nian; Zheng, Xiaoting; Luo, Z. David; Lai, Cary; Mei, Lin; Holmes, Todd C.; Gandhi, Sunil P.; Xu, Xiangmin.

In: Neuron, Vol. 92, No. 1, 05.10.2016, p. 160-173.

Research output: Contribution to journalArticle

Sun, Y, Ikrar, T, Davis, MF, Gong, N, Zheng, X, Luo, ZD, Lai, C, Mei, L, Holmes, TC, Gandhi, SP & Xu, X 2016, 'Neuregulin-1/ErbB4 Signaling Regulates Visual Cortical Plasticity', Neuron, vol. 92, no. 1, pp. 160-173. https://doi.org/10.1016/j.neuron.2016.08.033
Sun Y, Ikrar T, Davis MF, Gong N, Zheng X, Luo ZD et al. Neuregulin-1/ErbB4 Signaling Regulates Visual Cortical Plasticity. Neuron. 2016 Oct 5;92(1):160-173. https://doi.org/10.1016/j.neuron.2016.08.033
Sun, Yanjun ; Ikrar, Taruna ; Davis, Melissa F. ; Gong, Nian ; Zheng, Xiaoting ; Luo, Z. David ; Lai, Cary ; Mei, Lin ; Holmes, Todd C. ; Gandhi, Sunil P. ; Xu, Xiangmin. / Neuregulin-1/ErbB4 Signaling Regulates Visual Cortical Plasticity. In: Neuron. 2016 ; Vol. 92, No. 1. pp. 160-173.
@article{3842ff0a54804603b323c2b27244234b,
title = "Neuregulin-1/ErbB4 Signaling Regulates Visual Cortical Plasticity",
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.",
author = "Yanjun Sun and Taruna Ikrar and Davis, {Melissa F.} and Nian Gong and Xiaoting Zheng and Luo, {Z. David} and Cary Lai and Lin Mei and Holmes, {Todd C.} and Gandhi, {Sunil P.} and Xiangmin Xu",
year = "2016",
month = "10",
day = "5",
doi = "10.1016/j.neuron.2016.08.033",
language = "English (US)",
volume = "92",
pages = "160--173",
journal = "Neuron",
issn = "0896-6273",
publisher = "Cell Press",
number = "1",

}

TY - JOUR

T1 - Neuregulin-1/ErbB4 Signaling Regulates Visual Cortical Plasticity

AU - Sun, Yanjun

AU - Ikrar, Taruna

AU - Davis, Melissa F.

AU - Gong, Nian

AU - Zheng, Xiaoting

AU - Luo, Z. David

AU - Lai, Cary

AU - Mei, Lin

AU - Holmes, Todd C.

AU - Gandhi, Sunil P.

AU - Xu, Xiangmin

PY - 2016/10/5

Y1 - 2016/10/5

N2 - 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.

AB - 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.

UR - http://www.scopus.com/inward/record.url?scp=84992692835&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84992692835&partnerID=8YFLogxK

U2 - 10.1016/j.neuron.2016.08.033

DO - 10.1016/j.neuron.2016.08.033

M3 - Article

C2 - 27641496

AN - SCOPUS:84992692835

VL - 92

SP - 160

EP - 173

JO - Neuron

JF - Neuron

SN - 0896-6273

IS - 1

ER -