Activity-Dependent Gating of Parvalbumin Interneuron Function by the Perineuronal Net Protein Brevican

Activity-dependent neuronal plasticity is a fundamental mechanism through which the nervous system adapts to sensory experience. Several lines of evidence suggest that parvalbumin (PV+) interneurons are essential in this process, but the molecular mechanisms underlying the influence of experience on interneuron plasticity remain poorly understood. Perineuronal nets (PNNs) enwrapping PV+ cells are long-standing candidates for playing such a role, yet their precise contribution has remained elusive. We show that the PNN protein Brevican is a critical regulator of interneuron plasticity. We find that Brevican simultaneously controls cellular and synaptic forms of plasticity in PV+ cells by regulating the localization of potassium channels and AMPA receptors, respectively. By modulating Brevican levels, experience introduces precise molecular and cellular modifications in PV+ cells that are required for learning and memory. These findings uncover a molecular program through which a PNN protein facilitates appropriate behavioral responses to experience by dynamically gating PV+ interneuron function.

[1]  Ken Sugino,et al.  Transcriptional and Electrophysiological Maturation of Neocortical Fast-Spiking GABAergic Interneurons , 2009, The Journal of Neuroscience.

[2]  S. Arber,et al.  A Developmental Switch in the Response of DRG Neurons to ETS Transcription Factor Signaling , 2005, PLoS biology.

[3]  Fiona E. N. LeBeau,et al.  Recruitment of Parvalbumin-Positive Interneurons Determines Hippocampal Function and Associated Behavior , 2007, Neuron.

[4]  Richard J Weinberg,et al.  Perineuronal Nets Suppress Plasticity of Excitatory Synapses on CA2 Pyramidal Neurons , 2016, The Journal of Neuroscience.

[5]  J. Fawcett,et al.  Composition of Perineuronal Net Extracellular Matrix in Rat Brain , 2006, Journal of Biological Chemistry.

[6]  Helge Ewers,et al.  Dual-color 3D superresolution microscopy by combined spectral-demixing and biplane imaging. , 2015, Biophysical journal.

[7]  B. Rudy,et al.  Developmental expression and functional characterization of the potassium-channel subunit Kv3.1b in parvalbumin-containing interneurons of the rat hippocampus , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[8]  Pico Caroni,et al.  Parvalbumin-expressing basket-cell network plasticity induced by experience regulates adult learning , 2013, Nature.

[9]  Ben A. Barres,et al.  Emerging roles of astrocytes in neural circuit development , 2013, Nature Reviews Neuroscience.

[10]  Siu Kang,et al.  Bidirectional plasticity in fast-spiking GABA circuits by visual experience , 2009, Nature.

[11]  R. Frischknecht,et al.  Neural ECM molecules in axonal and synaptic homeostatic plasticity. , 2014, Progress in brain research.

[12]  C. Müller,et al.  Postnatal development and localization of an N‐acetylgalactosamine containing glycoconjugate associated with nonpyramidal neurons in cat visual cortex , 1993, The Journal of comparative neurology.

[13]  C. Garner,et al.  Brevican, a Chondroitin Sulfate Proteoglycan of Rat Brain, Occurs as Secreted and Cell Surface Glycosylphosphatidylinositol-anchored Isoforms (*) , 1995, The Journal of Biological Chemistry.

[14]  Andreas Lüthi,et al.  Perineuronal Nets Protect Fear Memories from Erasure , 2009, Science.

[15]  Ethan M. Goldberg,et al.  K+ Channels at the Axon Initial Segment Dampen Near-Threshold Excitability of Neocortical Fast-Spiking GABAergic Interneurons , 2008, Neuron.

[16]  G. Turrigiano Homeostatic synaptic plasticity: local and global mechanisms for stabilizing neuronal function. , 2012, Cold Spring Harbor perspectives in biology.

[17]  S. Hockfield,et al.  A surface antigen expressed by a subset of neurons in the vertebrate central nervous system. , 1983, Proceedings of the National Academy of Sciences of the United States of America.

[18]  M. Kreutz,et al.  Brevican isoforms associate with neural membranes , 2002, Journal of neurochemistry.

[19]  M. Stryker,et al.  Local GABA circuit control of experience-dependent plasticity in developing visual cortex. , 1998, Science.

[20]  P. H. Seeburg,et al.  Spatial memory dissociations in mice lacking GluR1 , 2002, Nature Neuroscience.

[21]  Roger Y Tsien,et al.  Very long-term memories may be stored in the pattern of holes in the perineuronal net , 2013, Proceedings of the National Academy of Sciences.

[22]  K. Deisseroth,et al.  Parvalbumin neurons and gamma rhythms enhance cortical circuit performance , 2009, Nature.

[23]  L. Maffei,et al.  Reactivation of Ocular Dominance Plasticity in the Adult Visual Cortex , 2002, Science.

[24]  M. Scanziani,et al.  Equalizing Excitation-Inhibition Ratios across Visual Cortical Neurons , 2014, Nature.

[25]  Nathan R. Wilson,et al.  Division and subtraction by distinct cortical inhibitory networks in vivo , 2012, Nature.

[26]  P. Somogyi,et al.  Neuronal Diversity and Temporal Dynamics: The Unity of Hippocampal Circuit Operations , 2008, Science.

[27]  Mark A Good,et al.  Enhanced long-term and impaired short-term spatial memory in GluA1 AMPA receptor subunit knockout mice: evidence for a dual-process memory model. , 2009, Learning & memory.

[28]  Takao K Hensch,et al.  Balancing plasticity/stability across brain development. , 2013, Progress in brain research.

[29]  F. Asztély,et al.  Brevican-Deficient Mice Display Impaired Hippocampal CA1 Long-Term Potentiation but Show No Obvious Deficits in Learning and Memory , 2002, Molecular and Cellular Biology.

[30]  B. Alger,et al.  Synaptic Cross Talk between Perisomatic-Targeting Interneuron Classes Expressing Cholecystokinin and Parvalbumin in Hippocampus , 2009, The Journal of Neuroscience.

[31]  C. McBain,et al.  Developmental origin dictates interneuron AMPA and NMDA receptor subunit composition and plasticity , 2013, Nature Neuroscience.

[32]  Peter Jonas,et al.  Fast-spiking, parvalbumin+ GABAergic interneurons: From cellular design to microcircuit function , 2014, Science.

[33]  Yue Zhang,et al.  The Loop Position of shRNAs and Pre-miRNAs Is Critical for the Accuracy of Dicer Processing In Vivo , 2012, Cell.

[34]  J. Rawlins,et al.  Deletion of glutamate receptor-A (GluR-A) AMPA receptor subunits impairs one-trial spatial memory. , 2007, Behavioral neuroscience.

[35]  H. Ewers,et al.  A simple method for GFP- and RFP-based dual color single-molecule localization microscopy. , 2015, ACS chemical biology.

[36]  J. Lippincott-Schwartz,et al.  Imaging Intracellular Fluorescent Proteins at Nanometer Resolution , 2006, Science.

[37]  J R Wolff,et al.  Perineuronal nets provide a polyanionic, glia‐associated form of microenvironment around certain neurons in many parts of the rat brain , 1993, Glia.

[38]  S. Hockfield,et al.  A Family of Activity-Dependent Neuronal Cell-Surface Chondroitin Sulfate Proteoglycans in Cat Visual Cortex , 1997, The Journal of Neuroscience.

[39]  M. Greenberg,et al.  The activity-dependent transcription factor NPAS4 regulates domain-specific inhibition , 2013, Nature.

[40]  Ken Mackie,et al.  Presynaptically Located CB1 Cannabinoid Receptors Regulate GABA Release from Axon Terminals of Specific Hippocampal Interneurons , 1999, The Journal of Neuroscience.

[41]  H. Morishita,et al.  Regulating Critical Period Plasticity: Insight from the Visual System to Fear Circuitry for Therapeutic Interventions , 2013, Front. Psychiatry.

[42]  Michael Lagler,et al.  Divisions of Identified Parvalbumin-Expressing Basket Cells during Working Memory-Guided Decision Making , 2016, Neuron.

[43]  Jessica A. Cardin,et al.  Driving fast-spiking cells induces gamma rhythm and controls sensory responses , 2009, Nature.

[44]  R. Froemke Plasticity of cortical excitatory-inhibitory balance. , 2015, Annual review of neuroscience.

[45]  R. Frischknecht,et al.  Hyaluronan-based extracellular matrix under conditions of homeostatic plasticity , 2014, Philosophical Transactions of the Royal Society B: Biological Sciences.

[46]  X. Zhuang,et al.  Superresolution Imaging of Chemical Synapses in the Brain , 2010, Neuron.

[47]  J. Yates,et al.  Unbiased Discovery of Glypican as a Receptor for LRRTM4 in Regulating Excitatory Synapse Development , 2013, Neuron.

[48]  A. Engel,et al.  The Extracellular Matrix Molecule Hyaluronic Acid Regulates Hippocampal Synaptic Plasticity by Modulating Postsynaptic L-Type Ca2+ Channels , 2010, Neuron.

[49]  J. Henley,et al.  Synaptic AMPA receptor composition in development, plasticity and disease , 2016, Nature Reviews Neuroscience.

[50]  Oscar Marín,et al.  Tuning of fast-spiking interneuron properties by an activity-dependent transcriptional switch , 2015, Science.

[51]  Daniel Choquet,et al.  Brain extracellular matrix affects AMPA receptor lateral mobility and short-term synaptic plasticity , 2009, Nature Neuroscience.

[52]  Lacey J. Kitch,et al.  Entorhinal Cortical Ocean Cells Encode Specific Contexts and Drive Context-Specific Fear Memory , 2015, Neuron.