Learning-induced ribosomal RNA is required for memory consolidation in mice-Evidence of differentially ex-pressed rRNA variants in learning and memory

Kim D. Allen, Matthew J. Regier, Changchi Hsieh, Panayiotis Tsokas, Maya Barnard, Shwetha Phatarpekar, Jason Wolk, Todd C. Sacktor, Andre Fenton, A. Iván Hernández

Research output: Contribution to journalArticle

Abstract

The transition from short-term to long-term forms of synaptic plasticity requires protein synthesis and new gene expression. Most efforts to understand experience-induced changes in neuronal gene expression have focused on the transcription products of RNA polymerase II-primarily mRNAs and the proteins they encode. We recently showed that nucleolar integrity and activity-dependent ribosomal RNA (rRNA) synthesis are essential for the maintenance of hippocampal long-term potentiation (LTP). Consequently, the synaptic plasticity and memory hypothesis predicts that nucleolar integrity and activity dependent rRNA synthesis would be required for Long-term memory (LTM). We tested this prediction using the hippocampus-dependent, Active Place Avoidance (APA) spatial memory task and found that training induces de novo rRNA synthesis in mouse dorsal hippocampus. This learning-induced increase in nucleolar activity and rRNA synthesis persists at least 24 h after training. In addition, intra-hippocampal injection of the Pol I specific inhibitor, CX-5461 prior to training, revealed that de novo rRNA synthesis is required for 24 h memory, but not for learning. Using qPCR to assess activity-dependent changes in gene expression, we found that of seven known rRNA expression variants (v-rRNAs), only one, v-rRNA IV, is significantly upregulated right after training. These data indicate that learning induced v-rRNAs are crucial for LTM, and constitute the first evidence that differential rRNA gene expression plays a role in memory.

Original languageEnglish (US)
Pages (from-to)e0203374
JournalPLoS One
Volume13
Issue number10
DOIs
StatePublished - Jan 1 2018

Fingerprint

Ribosomal RNA
Consolidation
learning
ribosomal RNA
Learning
Data storage equipment
Gene expression
mice
Gene Expression
Neuronal Plasticity
Long-Term Memory
synthesis
Hippocampus
Plasticity
gene expression
hippocampus
Long-Term Potentiation
rRNA Genes
Transcription
Memory Consolidation

ASJC Scopus subject areas

  • Biochemistry, Genetics and Molecular Biology(all)
  • Agricultural and Biological Sciences(all)

Cite this

Learning-induced ribosomal RNA is required for memory consolidation in mice-Evidence of differentially ex-pressed rRNA variants in learning and memory. / Allen, Kim D.; Regier, Matthew J.; Hsieh, Changchi; Tsokas, Panayiotis; Barnard, Maya; Phatarpekar, Shwetha; Wolk, Jason; Sacktor, Todd C.; Fenton, Andre; Hernández, A. Iván.

In: PLoS One, Vol. 13, No. 10, 01.01.2018, p. e0203374.

Research output: Contribution to journalArticle

Allen, KD, Regier, MJ, Hsieh, C, Tsokas, P, Barnard, M, Phatarpekar, S, Wolk, J, Sacktor, TC, Fenton, A & Hernández, AI 2018, 'Learning-induced ribosomal RNA is required for memory consolidation in mice-Evidence of differentially ex-pressed rRNA variants in learning and memory', PLoS One, vol. 13, no. 10, pp. e0203374. https://doi.org/10.1371/journal.pone.0203374
Allen, Kim D. ; Regier, Matthew J. ; Hsieh, Changchi ; Tsokas, Panayiotis ; Barnard, Maya ; Phatarpekar, Shwetha ; Wolk, Jason ; Sacktor, Todd C. ; Fenton, Andre ; Hernández, A. Iván. / Learning-induced ribosomal RNA is required for memory consolidation in mice-Evidence of differentially ex-pressed rRNA variants in learning and memory. In: PLoS One. 2018 ; Vol. 13, No. 10. pp. e0203374.
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