Pentraxins Coordinate Excitatory Synapse Maturation and Circuit Integration of Parvalbumin Interneurons
Circuit computation requires precision in the timing, extent, and synchrony of principal cell (PC) firing that is largely enforced by parvalbumin-expressing, fast-spiking interneurons (PVFSIs). To reliably coordinate network activity, PVFSIs exhibit specialized synaptic and membrane properties that...
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| Published in | Neuron (Cambridge, Mass.) Vol. 85; no. 6; pp. 1257 - 1272 |
|---|---|
| Main Authors | , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Elsevier Inc
18.03.2015
Elsevier Limited |
| Subjects | |
| Online Access | Get full text |
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| Abstract | Circuit computation requires precision in the timing, extent, and synchrony of principal cell (PC) firing that is largely enforced by parvalbumin-expressing, fast-spiking interneurons (PVFSIs). To reliably coordinate network activity, PVFSIs exhibit specialized synaptic and membrane properties that promote efficient afferent recruitment such as expression of high-conductance, rapidly gating, GluA4-containing AMPA receptors (AMPARs). We found that PVFSIs upregulate GluA4 during the second postnatal week coincident with increases in the AMPAR clustering proteins NPTX2 and NPTXR. Moreover, GluA4 is dramatically reduced in NPTX2−/−/NPTXR−/− mice with consequent reductions in PVFSI AMPAR function. Early postnatal NPTX2−/−/NPTXR−/− mice exhibit delayed circuit maturation with a prolonged critical period permissive for giant depolarizing potentials. Juvenile NPTX2−/−/NPTXR−/− mice display reduced feedforward inhibition yielding a circuit deficient in rhythmogenesis and prone to epileptiform discharges. Our findings demonstrate an essential role for NPTXs in controlling network dynamics highlighting potential therapeutic targets for disorders with inhibition/excitation imbalances such as schizophrenia.
•GluA4 is undetectable in neonatal PVFSIs, then increases and plateaus by P15•NPTX2−/−/NPTXR−/− mice have profound loss of GluA4•PVFSI AMPAR function and recruitment are compromised in NPTX2−/−/NPTXR−/− mice•I/E imbalances in NPTX2−/−/NPTXR−/− mice impair rhythmogenesis and working memory
Pelkey et al. demonstrate a critical role for neuronal pentraxins 2 and receptor (NPTX2/R) in regulating GluA4 expression within parvalbumin fast-spiking interneurons (PVFSIs). Circuit recruitment of PVFSIs is compromised in NPTX2−/−/NPTXR−/− mice, with consequent deficits in network rhythmogenesis and behavior. |
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| AbstractList | Circuit computation requires precision in the timing, extent, and synchrony of principal cell (PC) firing that is largely enforced by parvalbumin-expressing, fast-spiking interneurons (PVFSIs). To reliably coordinate network activity, PVFSIs exhibit specialized synaptic and membrane properties that promote efficient afferent recruitment such as expression of high-conductance, rapidly gating, GluA4-containing AMPA receptors (AMPARs). We found that PVFSIs upregulate GluA4 during the second postnatal week coincident with increases in the AMPAR clustering proteins NPTX2 and NPTXR. Moreover, GluA4 is dramatically reduced in NPTX2−/−/NPTXR−/− mice with consequent reductions in PVFSI AMPAR function. Early postnatal NPTX2−/−/NPTXR−/− mice exhibit delayed circuit maturation with a prolonged critical period permissive for giant depolarizing potentials. Juvenile NPTX2−/−/NPTXR−/− mice display reduced feedforward inhibition yielding a circuit deficient in rhythmogenesis and prone to epileptiform discharges. Our findings demonstrate an essential role for NPTXs in controlling network dynamics highlighting potential therapeutic targets for disorders with inhibition/excitation imbalances such as schizophrenia.
•GluA4 is undetectable in neonatal PVFSIs, then increases and plateaus by P15•NPTX2−/−/NPTXR−/− mice have profound loss of GluA4•PVFSI AMPAR function and recruitment are compromised in NPTX2−/−/NPTXR−/− mice•I/E imbalances in NPTX2−/−/NPTXR−/− mice impair rhythmogenesis and working memory
Pelkey et al. demonstrate a critical role for neuronal pentraxins 2 and receptor (NPTX2/R) in regulating GluA4 expression within parvalbumin fast-spiking interneurons (PVFSIs). Circuit recruitment of PVFSIs is compromised in NPTX2−/−/NPTXR−/− mice, with consequent deficits in network rhythmogenesis and behavior. Circuit computation requires precision in the timing, extent, and synchrony of principal cell (PC) firing that is largely enforced by parvalbumin-expressing, fast-spiking interneurons (PVFSIs). To reliably coordinate network activity, PVFSIs exhibit specialized synaptic and membrane properties that promote efficient afferent recruitment such as expression of high-conductance, rapidly gating, GluA4-containing AMPA receptors (AMPARs). We found that PVFSIs upregulate GluA4 during the second postnatal week coincident with increases in the AMPAR clustering proteins NPTX2 and NPTXR. Moreover, GluA4 is dramatically reduced inNPTX2-/-/NPTXR-/-mice with consequent reductions in PVFSI AMPAR function. Early postnatalNPTX2-/-/NPTXR-/-mice exhibit delayed circuit maturation with a prolonged critical period permissive for giant depolarizing potentials. JuvenileNPTX2-/-/NPTXR-/-mice display reduced feedforward inhibition yielding a circuit deficient in rhythmogenesis and prone to epileptiform discharges. Our findings demonstrate an essential role for NPTXs in controlling network dynamics highlighting potential therapeutic targets for disorders with inhibition/excitation imbalances such as schizophrenia. Circuit computation requires precision in the timing, extent, and synchrony of principal cell (PC) firing that is largely enforced by parvalbumin-expressing, fast-spiking interneurons (PVFSIs). To reliably coordinate network activity PVFSIs exhibit specialized synaptic and membrane properties that promote efficient afferent recruitment such as expression of high-conductance, rapidly gating, GluA4-containing AMPA receptors (AMPARs). We found that PVFSIs upregulate GluA4 during the second postnatal week coincident with increases in the AMPAR clustering proteins NPTX2 and NPTXR. Moreover, GluA4 is dramatically reduced in NPTX2 −/− /NPTXR −/− mice with consequent reductions in PVFSI AMPAR function. Early postnatal NPTX2 −/− /NPTXR −/− mice exhibit delayed circuit maturation with a prolonged critical period permissive for giant depolarizing potentials. Juvenile NPTX2 −/− /NPTXR −/− mice display reduced feedforward inhibition yielding a circuit deficient in rhythmogenesis and prone to epileptiform discharges. Our findings demonstrate an essential role for NPTXs in controlling network dynamics highlighting potential therapeutic targets for disorders with inhibition/excitation imbalances such as schizophrenia. Circuit computation requires precision in the timing, extent, and synchrony of principal cell (PC) firing that is largely enforced by parvalbumin-expressing, fast-spiking interneurons (PVFSIs). To reliably coordinate network activity, PVFSIs exhibit specialized synaptic and membrane properties that promote efficient afferent recruitment such as expression of high-conductance, rapidly gating, GluA4-containing AMPA receptors (AMPARs). We found that PVFSIs upregulate GluA4 during the second postnatal week coincident with increases in the AMPAR clustering proteins NPTX2 and NPTXR. Moreover, GluA4 is dramatically reduced in NPTX2-/-/NPTXR-/- mice with consequent reductions in PVFSI AMPAR function. Early postnatal NPTX2-/-/NPTXR-/- mice exhibit delayed circuit maturation with a prolonged critical period permissive for giant depolarizing potentials. Juvenile NPTX2-/-/NPTXR-/- mice display reduced feedforward inhibition yielding a circuit deficient in rhythmogenesis and prone to epileptiform discharges. Our findings demonstrate an essential role for NPTXs in controlling network dynamics highlighting potential therapeutic targets for disorders with inhibition/excitation imbalances such as schizophrenia. |
| Author | Wyeth, Megan S. Pelkey, Kenneth A. Sukumaran, Madhav McBain, Chris J. Cameron, Heather A. Yuan, Xiaoqing Chittajallu, Ramesh Barksdale, Elizabeth Vargish, Geoffrey A. Petralia, Ronald S. Mitchell, Robert M. Colonnese, Matthew T. Karlsson, Rose-Marie Worley, Paul F. Murata, Yasunobu Craig, Michael T. |
| AuthorAffiliation | 2 Advanced Imaging Core, NIDCD, NIH, 35 Lincoln Dr. Bethesda, Maryland, 20892 USA 3 Section on Neuroplasticity, Mood and Anxiety Disorders Program, NIMH, NIH, 35 Lincoln Dr. Bethesda, MD, 20892 USA 5 The Solomon H. Snyder Dept. of Neurosci., JHU, 725 N. Wolfe St. Baltimore, Maryland, 21205 USA 1 PDN, Eunice Kennedy-Shriver NICHD, NIH, 35 Lincoln Dr. Bethesda, Maryland 20892 USA 4 Dept. of Pharm. and Physiol., and Inst. for Neurosci., GWU, 2300 Eye St. NW Washington, DC, 20037 USA |
| AuthorAffiliation_xml | – name: 4 Dept. of Pharm. and Physiol., and Inst. for Neurosci., GWU, 2300 Eye St. NW Washington, DC, 20037 USA – name: 2 Advanced Imaging Core, NIDCD, NIH, 35 Lincoln Dr. Bethesda, Maryland, 20892 USA – name: 5 The Solomon H. Snyder Dept. of Neurosci., JHU, 725 N. Wolfe St. Baltimore, Maryland, 21205 USA – name: 3 Section on Neuroplasticity, Mood and Anxiety Disorders Program, NIMH, NIH, 35 Lincoln Dr. Bethesda, MD, 20892 USA – name: 1 PDN, Eunice Kennedy-Shriver NICHD, NIH, 35 Lincoln Dr. Bethesda, Maryland 20892 USA |
| Author_xml | – sequence: 1 givenname: Kenneth A. surname: Pelkey fullname: Pelkey, Kenneth A. email: pelkeyk2@mail.nih.gov organization: Program in Developmental Neuroscience, Eunice Kennedy-Shriver National Institute of Child Health and Human Development, National Institutes of Health, 35 Lincoln Drive, Bethesda, MD 20892, USA – sequence: 2 givenname: Elizabeth surname: Barksdale fullname: Barksdale, Elizabeth organization: Program in Developmental Neuroscience, Eunice Kennedy-Shriver National Institute of Child Health and Human Development, National Institutes of Health, 35 Lincoln Drive, Bethesda, MD 20892, USA – sequence: 3 givenname: Michael T. surname: Craig fullname: Craig, Michael T. organization: Program in Developmental Neuroscience, Eunice Kennedy-Shriver National Institute of Child Health and Human Development, National Institutes of Health, 35 Lincoln Drive, Bethesda, MD 20892, USA – sequence: 4 givenname: Xiaoqing surname: Yuan fullname: Yuan, Xiaoqing organization: Program in Developmental Neuroscience, Eunice Kennedy-Shriver National Institute of Child Health and Human Development, National Institutes of Health, 35 Lincoln Drive, Bethesda, MD 20892, USA – sequence: 5 givenname: Madhav surname: Sukumaran fullname: Sukumaran, Madhav organization: Program in Developmental Neuroscience, Eunice Kennedy-Shriver National Institute of Child Health and Human Development, National Institutes of Health, 35 Lincoln Drive, Bethesda, MD 20892, USA – sequence: 6 givenname: Geoffrey A. surname: Vargish fullname: Vargish, Geoffrey A. organization: Program in Developmental Neuroscience, Eunice Kennedy-Shriver National Institute of Child Health and Human Development, National Institutes of Health, 35 Lincoln Drive, Bethesda, MD 20892, USA – sequence: 7 givenname: Robert M. surname: Mitchell fullname: Mitchell, Robert M. organization: Program in Developmental Neuroscience, Eunice Kennedy-Shriver National Institute of Child Health and Human Development, National Institutes of Health, 35 Lincoln Drive, Bethesda, MD 20892, USA – sequence: 8 givenname: Megan S. surname: Wyeth fullname: Wyeth, Megan S. organization: Program in Developmental Neuroscience, Eunice Kennedy-Shriver National Institute of Child Health and Human Development, National Institutes of Health, 35 Lincoln Drive, Bethesda, MD 20892, USA – sequence: 9 givenname: Ronald S. surname: Petralia fullname: Petralia, Ronald S. organization: Advanced Imaging Core National Institute of Deafness and Other Communication Disorders, National Institutes of Health, 35 Lincoln Drive, Bethesda, MD 20892, USA – sequence: 10 givenname: Ramesh surname: Chittajallu fullname: Chittajallu, Ramesh organization: Program in Developmental Neuroscience, Eunice Kennedy-Shriver National Institute of Child Health and Human Development, National Institutes of Health, 35 Lincoln Drive, Bethesda, MD 20892, USA – sequence: 11 givenname: Rose-Marie surname: Karlsson fullname: Karlsson, Rose-Marie organization: Section on Neuroplasticity, Mood and Anxiety Disorders Program, National Institute of Mental Health, National Institutes of Health, 35 Lincoln Drive, Bethesda, MD 20892, USA – sequence: 12 givenname: Heather A. surname: Cameron fullname: Cameron, Heather A. organization: Section on Neuroplasticity, Mood and Anxiety Disorders Program, National Institute of Mental Health, National Institutes of Health, 35 Lincoln Drive, Bethesda, MD 20892, USA – sequence: 13 givenname: Yasunobu surname: Murata fullname: Murata, Yasunobu organization: Department of Pharmacology and Physiology, and Institute for Neuroscience, George Washington University, 2300 Eye Street, Washington, DC 20037, USA – sequence: 14 givenname: Matthew T. surname: Colonnese fullname: Colonnese, Matthew T. organization: Department of Pharmacology and Physiology, and Institute for Neuroscience, George Washington University, 2300 Eye Street, Washington, DC 20037, USA – sequence: 15 givenname: Paul F. surname: Worley fullname: Worley, Paul F. organization: The Solomon H. Snyder Department of Neuroscience, Johns Hopkins University, 725 N. Wolfe Street, Baltimore, MD 21205, USA – sequence: 16 givenname: Chris J. surname: McBain fullname: McBain, Chris J. organization: Program in Developmental Neuroscience, Eunice Kennedy-Shriver National Institute of Child Health and Human Development, National Institutes of Health, 35 Lincoln Drive, Bethesda, MD 20892, USA |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/25754824$$D View this record in MEDLINE/PubMed |
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| Copyright | 2015 Elsevier Inc. Copyright © 2015 Elsevier Inc. All rights reserved. Copyright Elsevier Limited Mar 18, 2015 2015 Published by Elsevier Inc. 2015 |
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| SubjectTerms | Action Potentials - physiology Animals Animals, Newborn Behavior C-Reactive Protein - deficiency C-Reactive Protein - metabolism Disease Models, Animal Experiments Interneurons - metabolism Mice Mice, Knockout Nerve Net - growth & development Nerve Tissue Proteins - deficiency Nerve Tissue Proteins - metabolism Parvalbumins - metabolism Physiology Recruitment Rodents Synapses - metabolism |
| Title | Pentraxins Coordinate Excitatory Synapse Maturation and Circuit Integration of Parvalbumin Interneurons |
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