The non-coding RNA BC1 regulates experience-dependent structural plasticity and learning

Victor Briz, Leonardo Restivo, Emanuela Pasciuto, Konrad Juczewski, Valentina Mercaldo, Adrian C Lo, Pieter Baatsen, Natalia V Gounko, Antonella Borreca, Tiziana Girardi, Rossella Luca, Julie Nys, Rogier B Poorthuis, Huibert D Mansvelder, Gilberto Fisone, Martine Ammassari-Teule, Lutgarde Arckens, Patrik Krieger, Rhiannon Meredith, Claudia Bagni

Research output: Contribution to JournalArticleAcademicpeer-review

Abstract

The brain cytoplasmic (BC1) RNA is a non-coding RNA (ncRNA) involved in neuronal translational control. Absence of BC1 is associated with altered glutamatergic transmission and maladaptive behavior. Here, we show that pyramidal neurons in the barrel cortex of BC1 knock out (KO) mice display larger excitatory postsynaptic currents and increased spontaneous activity in vivo. Furthermore, BC1 KO mice have enlarged spine heads and postsynaptic densities and increased synaptic levels of glutamate receptors and PSD-95. Of note, BC1 KO mice show aberrant structural plasticity in response to whisker deprivation, impaired texture novel object recognition and altered social behavior. Thus, our study highlights a role for BC1 RNA in experience-dependent plasticity and learning in the mammalian adult neocortex, and provides insight into the function of brain ncRNAs regulating synaptic transmission, plasticity and behavior, with potential relevance in the context of intellectual disabilities and psychiatric disorders.Brain cytoplasmic (BC1) RNA is a non-coding RNA that has been implicated in translational regulation, seizure, and anxiety. Here, the authors show that in the cortex, BC1 RNA is required for sensory deprivation-induced structural plasticity of dendritic spines, as well as for correct sensory learning and social behaviors.

Original languageEnglish
Pages (from-to)293
JournalNature Communications
Volume8
Issue number1
DOIs
Publication statusPublished - 17 Aug 2017

Fingerprint

Untranslated RNA
knockout mice
plastic properties
learning
Plasticity
Knockout Mice
Learning
brain
Brain
spine
cortexes
Social Behavior
sensory deprivation
Sensory Deprivation
anxiety
deprivation
seizures
disabilities
Post-Synaptic Density
Vibrissae

Keywords

  • Animals
  • Base Sequence
  • Cells, Cultured
  • Dendritic Spines
  • Excitatory Postsynaptic Potentials
  • In Situ Hybridization, Fluorescence
  • Learning
  • Male
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Microscopy, Electron
  • Neocortex
  • Neuronal Plasticity
  • Pyramidal Cells
  • RNA, Small Cytoplasmic
  • Sensory Deprivation
  • Sequence Homology, Nucleic Acid
  • Social Behavior
  • Synaptic Transmission
  • Vibrissae
  • Journal Article
  • Research Support, Non-U.S. Gov't

Cite this

Briz, V., Restivo, L., Pasciuto, E., Juczewski, K., Mercaldo, V., Lo, A. C., ... Bagni, C. (2017). The non-coding RNA BC1 regulates experience-dependent structural plasticity and learning. Nature Communications, 8(1), 293. https://doi.org/10.1038/s41467-017-00311-2
Briz, Victor ; Restivo, Leonardo ; Pasciuto, Emanuela ; Juczewski, Konrad ; Mercaldo, Valentina ; Lo, Adrian C ; Baatsen, Pieter ; Gounko, Natalia V ; Borreca, Antonella ; Girardi, Tiziana ; Luca, Rossella ; Nys, Julie ; Poorthuis, Rogier B ; Mansvelder, Huibert D ; Fisone, Gilberto ; Ammassari-Teule, Martine ; Arckens, Lutgarde ; Krieger, Patrik ; Meredith, Rhiannon ; Bagni, Claudia. / The non-coding RNA BC1 regulates experience-dependent structural plasticity and learning. In: Nature Communications. 2017 ; Vol. 8, No. 1. pp. 293.
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Briz, V, Restivo, L, Pasciuto, E, Juczewski, K, Mercaldo, V, Lo, AC, Baatsen, P, Gounko, NV, Borreca, A, Girardi, T, Luca, R, Nys, J, Poorthuis, RB, Mansvelder, HD, Fisone, G, Ammassari-Teule, M, Arckens, L, Krieger, P, Meredith, R & Bagni, C 2017, 'The non-coding RNA BC1 regulates experience-dependent structural plasticity and learning' Nature Communications, vol. 8, no. 1, pp. 293. https://doi.org/10.1038/s41467-017-00311-2

The non-coding RNA BC1 regulates experience-dependent structural plasticity and learning. / Briz, Victor; Restivo, Leonardo; Pasciuto, Emanuela; Juczewski, Konrad; Mercaldo, Valentina; Lo, Adrian C; Baatsen, Pieter; Gounko, Natalia V; Borreca, Antonella; Girardi, Tiziana; Luca, Rossella; Nys, Julie; Poorthuis, Rogier B; Mansvelder, Huibert D; Fisone, Gilberto; Ammassari-Teule, Martine; Arckens, Lutgarde; Krieger, Patrik; Meredith, Rhiannon; Bagni, Claudia.

In: Nature Communications, Vol. 8, No. 1, 17.08.2017, p. 293.

Research output: Contribution to JournalArticleAcademicpeer-review

TY - JOUR

T1 - The non-coding RNA BC1 regulates experience-dependent structural plasticity and learning

AU - Briz, Victor

AU - Restivo, Leonardo

AU - Pasciuto, Emanuela

AU - Juczewski, Konrad

AU - Mercaldo, Valentina

AU - Lo, Adrian C

AU - Baatsen, Pieter

AU - Gounko, Natalia V

AU - Borreca, Antonella

AU - Girardi, Tiziana

AU - Luca, Rossella

AU - Nys, Julie

AU - Poorthuis, Rogier B

AU - Mansvelder, Huibert D

AU - Fisone, Gilberto

AU - Ammassari-Teule, Martine

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AB - The brain cytoplasmic (BC1) RNA is a non-coding RNA (ncRNA) involved in neuronal translational control. Absence of BC1 is associated with altered glutamatergic transmission and maladaptive behavior. Here, we show that pyramidal neurons in the barrel cortex of BC1 knock out (KO) mice display larger excitatory postsynaptic currents and increased spontaneous activity in vivo. Furthermore, BC1 KO mice have enlarged spine heads and postsynaptic densities and increased synaptic levels of glutamate receptors and PSD-95. Of note, BC1 KO mice show aberrant structural plasticity in response to whisker deprivation, impaired texture novel object recognition and altered social behavior. Thus, our study highlights a role for BC1 RNA in experience-dependent plasticity and learning in the mammalian adult neocortex, and provides insight into the function of brain ncRNAs regulating synaptic transmission, plasticity and behavior, with potential relevance in the context of intellectual disabilities and psychiatric disorders.Brain cytoplasmic (BC1) RNA is a non-coding RNA that has been implicated in translational regulation, seizure, and anxiety. Here, the authors show that in the cortex, BC1 RNA is required for sensory deprivation-induced structural plasticity of dendritic spines, as well as for correct sensory learning and social behaviors.

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KW - Learning

KW - Male

KW - Mice, Inbred C57BL

KW - Mice, Knockout

KW - Microscopy, Electron

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KW - Pyramidal Cells

KW - RNA, Small Cytoplasmic

KW - Sensory Deprivation

KW - Sequence Homology, Nucleic Acid

KW - Social Behavior

KW - Synaptic Transmission

KW - Vibrissae

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JO - Nature Communications

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SN - 2041-1723

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