Experience-Induced Arc/Arg3.1 Primes CA1 Pyramidal Neurons for Metabotropic Glutamate Receptor-Dependent Long-Term Synaptic Depression

Vikram Jakkamsetti; Nien Pei Tsai; Christina Gross; Gemma Molinaro; Katie A. Collins; Ferdinando Nicoletti; Kuan H. Wang; Pavel Osten; Gary J. Bassell; Jay R. Gibson; Kimberly M. Huber

doi:10.1016/j.neuron.2013.07.020

Experience-Induced Arc/Arg3.1 Primes CA1 Pyramidal Neurons for Metabotropic Glutamate Receptor-Dependent Long-Term Synaptic Depression

Vikram Jakkamsetti, Nien Pei Tsai, Christina Gross, Gemma Molinaro, Katie A. Collins, Ferdinando Nicoletti, Kuan H. Wang, Pavel Osten, Gary J. Bassell, Jay R. Gibson, Kimberly M. Huber

Research output: Contribution to journal › Article › peer-review

Abstract

A novel experience induces the Arc/Arg3.1 gene as well as plasticity of CA1 neural networks. To understand how these are linked, we briefly exposed GFP reporter mice of Arc transcription to a novel environment. Excitatory synaptic function of CA1 neurons with recent invivo Arc induction (. ArcGFP+) was similar to neighboring noninduced neurons. However, in response to group 1 metabotropic glutamate receptor (mGluR) activation, ArcGFP+ neurons preferentially displayed long-term synaptic depression (mGluR-LTD) and robust increases in dendritic Arc protein. mGluR-LTD in ArcGFP+ neurons required rapid protein synthesis and Arc, suggesting that dendritic translation of Arc underlies the priming of mGluR-LTD. In support of this idea, novelty exposure increased Arc messenger RNA in CA1 dendrites and promoted mGluR-induced translation of Arc inhippocampal synaptoneurosomes. Repeated experience suppressed synaptic transmission onto ArcGFP+ neurons and occluded mGluR-LTD exvivo. mGluR-LTD priming in neurons with similar Arc activation history may contribute to encoding a novel environment

Original language	English (US)
Pages (from-to)	72-79
Number of pages	8
Journal	Neuron
Volume	80
Issue number	1
DOIs	https://doi.org/10.1016/j.neuron.2013.07.020
State	Published - Oct 2 2013
Externally published	Yes

ASJC Scopus subject areas

General Neuroscience

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10.1016/j.neuron.2013.07.020

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@article{b72b31d2da9d4f6cbbaf2fc188a345c0,

title = "Experience-Induced Arc/Arg3.1 Primes CA1 Pyramidal Neurons for Metabotropic Glutamate Receptor-Dependent Long-Term Synaptic Depression",

abstract = "A novel experience induces the Arc/Arg3.1 gene as well as plasticity of CA1 neural networks. To understand how these are linked, we briefly exposed GFP reporter mice of Arc transcription to a novel environment. Excitatory synaptic function of CA1 neurons with recent invivo Arc induction (. ArcGFP+) was similar to neighboring noninduced neurons. However, in response to group 1 metabotropic glutamate receptor (mGluR) activation, ArcGFP+ neurons preferentially displayed long-term synaptic depression (mGluR-LTD) and robust increases in dendritic Arc protein. mGluR-LTD in ArcGFP+ neurons required rapid protein synthesis and Arc, suggesting that dendritic translation of Arc underlies the priming of mGluR-LTD. In support of this idea, novelty exposure increased Arc messenger RNA in CA1 dendrites and promoted mGluR-induced translation of Arc inhippocampal synaptoneurosomes. Repeated experience suppressed synaptic transmission onto ArcGFP+ neurons and occluded mGluR-LTD exvivo. mGluR-LTD priming in neurons with similar Arc activation history may contribute to encoding a novel environment",

author = "Vikram Jakkamsetti and Tsai, {Nien Pei} and Christina Gross and Gemma Molinaro and Collins, {Katie A.} and Ferdinando Nicoletti and Wang, {Kuan H.} and Pavel Osten and Bassell, {Gary J.} and Gibson, {Jay R.} and Huber, {Kimberly M.}",

note = "Funding Information: This research was supported by the grants from the National Institutes of Health grants NS045711, HD052731 (to K.M.H.), HD056370 (to J.R.G.), and MH085617 (to G.J.B.) and Emory Neuroscience NINDS Core Facilities grant P30NS055077 (to G.J.B. and C.G.). We would like to thank Dr. John Isaac for discussions and sending us the ArcGFP-BAC mice; Darya Fakhretdinova, Lorea Ormazabal, and Nicole Cabalo for technical assistance; and members of the Huber lab for discussions and comments on the manuscript. We thank Dr. Darrin Brager and Dr. Daniel Johnston for technical assistance with whole-cell recordings in mice. ",

year = "2013",

month = oct,

day = "2",

doi = "10.1016/j.neuron.2013.07.020",

language = "English (US)",

volume = "80",

pages = "72--79",

journal = "Neuron",

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T1 - Experience-Induced Arc/Arg3.1 Primes CA1 Pyramidal Neurons for Metabotropic Glutamate Receptor-Dependent Long-Term Synaptic Depression

AU - Jakkamsetti, Vikram

AU - Tsai, Nien Pei

AU - Gross, Christina

AU - Molinaro, Gemma

AU - Collins, Katie A.

AU - Nicoletti, Ferdinando

AU - Wang, Kuan H.

AU - Osten, Pavel

AU - Bassell, Gary J.

AU - Gibson, Jay R.

AU - Huber, Kimberly M.

N1 - Funding Information: This research was supported by the grants from the National Institutes of Health grants NS045711, HD052731 (to K.M.H.), HD056370 (to J.R.G.), and MH085617 (to G.J.B.) and Emory Neuroscience NINDS Core Facilities grant P30NS055077 (to G.J.B. and C.G.). We would like to thank Dr. John Isaac for discussions and sending us the ArcGFP-BAC mice; Darya Fakhretdinova, Lorea Ormazabal, and Nicole Cabalo for technical assistance; and members of the Huber lab for discussions and comments on the manuscript. We thank Dr. Darrin Brager and Dr. Daniel Johnston for technical assistance with whole-cell recordings in mice.

PY - 2013/10/2

Y1 - 2013/10/2

N2 - A novel experience induces the Arc/Arg3.1 gene as well as plasticity of CA1 neural networks. To understand how these are linked, we briefly exposed GFP reporter mice of Arc transcription to a novel environment. Excitatory synaptic function of CA1 neurons with recent invivo Arc induction (. ArcGFP+) was similar to neighboring noninduced neurons. However, in response to group 1 metabotropic glutamate receptor (mGluR) activation, ArcGFP+ neurons preferentially displayed long-term synaptic depression (mGluR-LTD) and robust increases in dendritic Arc protein. mGluR-LTD in ArcGFP+ neurons required rapid protein synthesis and Arc, suggesting that dendritic translation of Arc underlies the priming of mGluR-LTD. In support of this idea, novelty exposure increased Arc messenger RNA in CA1 dendrites and promoted mGluR-induced translation of Arc inhippocampal synaptoneurosomes. Repeated experience suppressed synaptic transmission onto ArcGFP+ neurons and occluded mGluR-LTD exvivo. mGluR-LTD priming in neurons with similar Arc activation history may contribute to encoding a novel environment

AB - A novel experience induces the Arc/Arg3.1 gene as well as plasticity of CA1 neural networks. To understand how these are linked, we briefly exposed GFP reporter mice of Arc transcription to a novel environment. Excitatory synaptic function of CA1 neurons with recent invivo Arc induction (. ArcGFP+) was similar to neighboring noninduced neurons. However, in response to group 1 metabotropic glutamate receptor (mGluR) activation, ArcGFP+ neurons preferentially displayed long-term synaptic depression (mGluR-LTD) and robust increases in dendritic Arc protein. mGluR-LTD in ArcGFP+ neurons required rapid protein synthesis and Arc, suggesting that dendritic translation of Arc underlies the priming of mGluR-LTD. In support of this idea, novelty exposure increased Arc messenger RNA in CA1 dendrites and promoted mGluR-induced translation of Arc inhippocampal synaptoneurosomes. Repeated experience suppressed synaptic transmission onto ArcGFP+ neurons and occluded mGluR-LTD exvivo. mGluR-LTD priming in neurons with similar Arc activation history may contribute to encoding a novel environment

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U2 - 10.1016/j.neuron.2013.07.020

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VL - 80

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JO - Neuron

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ER -

Experience-Induced Arc/Arg3.1 Primes CA1 Pyramidal Neurons for Metabotropic Glutamate Receptor-Dependent Long-Term Synaptic Depression

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