Abnormal Locus Coeruleus Sleep Activity Alters Sleep Signatures of Memory Consolidation and Impairs Place Cell Stability and Spatial Memory

Kevin M. Swift, Brooks A. Gross, Michelle A. Frazer, David S. Bauer, Kyle J.D. Clark, Elena M. Vazey, Gary Aston Jones, Yong Li, Anthony E. Pickering, Susan J. Sara, Gina R. Poe

Research output: Contribution to journalArticle

3 Citations (Scopus)

Abstract

Sleep is critical for proper memory consolidation. The locus coeruleus (LC) releases norepinephrine throughout the brain except when the LC falls silent throughout rapid eye movement (REM) sleep and prior to each non-REM (NREM) sleep spindle. We hypothesize that these transient LC silences allow the synaptic plasticity that is necessary to incorporate new information into pre-existing memory circuits. We found that spontaneous LC activity within sleep spindles triggers a decrease in spindle power. By optogenetically stimulating norepinephrine-containing LC neurons at 2 Hz during sleep, we reduced sleep spindle occurrence, as well as NREM delta power and REM theta power, without causing arousals or changing sleep amounts. Stimulating the LC during sleep following a hippocampus-dependent food location learning task interfered with consolidation of newly learned locations and reconsolidation of previous locations, disrupting next-day place cell activity. The LC stimulation-induced reduction in NREM sleep spindles, delta, and REM theta and reduced ripple-spindle coupling all correlated with decreased hippocampus-dependent performance on the task. Thus, periods of LC silence during sleep following learning are essential for normal spindle generation, delta and theta power, and consolidation of spatial memories. Swift et al. show that overactivity of the locus coeruleus, the main source of norepinephrine to the forebrain, during sleep interferes with signatures of NREM sleep and REM sleep associated with sleep-dependent memory consolidation. Maladaptive LC activity can impair next day hippocampal spatial encoding, producing long-term behavioral deficits.

Original languageEnglish (US)
Pages (from-to)3599-3609.e4
JournalCurrent Biology
Volume28
Issue number22
DOIs
StatePublished - Nov 19 2018

Fingerprint

Locus Coeruleus
brain stem
sleep
Consolidation
Sleep
Data storage equipment
Eye movements
cells
REM Sleep
eyes
norepinephrine
Norepinephrine
hippocampus
Spatial Memory
Memory Consolidation
Place Cells
Hippocampus
learning
Learning
brain

All Science Journal Classification (ASJC) codes

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

Keywords

  • NREM
  • REM
  • hippocampus
  • locus coeruleus
  • optogenetic
  • reconsolidation
  • ripples
  • sleep
  • spindle
  • theta

Cite this

Swift, K. M., Gross, B. A., Frazer, M. A., Bauer, D. S., Clark, K. J. D., Vazey, E. M., ... Poe, G. R. (2018). Abnormal Locus Coeruleus Sleep Activity Alters Sleep Signatures of Memory Consolidation and Impairs Place Cell Stability and Spatial Memory. Current Biology, 28(22), 3599-3609.e4. https://doi.org/10.1016/j.cub.2018.09.054
Swift, Kevin M. ; Gross, Brooks A. ; Frazer, Michelle A. ; Bauer, David S. ; Clark, Kyle J.D. ; Vazey, Elena M. ; Aston Jones, Gary ; Li, Yong ; Pickering, Anthony E. ; Sara, Susan J. ; Poe, Gina R. / Abnormal Locus Coeruleus Sleep Activity Alters Sleep Signatures of Memory Consolidation and Impairs Place Cell Stability and Spatial Memory. In: Current Biology. 2018 ; Vol. 28, No. 22. pp. 3599-3609.e4.
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Swift, KM, Gross, BA, Frazer, MA, Bauer, DS, Clark, KJD, Vazey, EM, Aston Jones, G, Li, Y, Pickering, AE, Sara, SJ & Poe, GR 2018, 'Abnormal Locus Coeruleus Sleep Activity Alters Sleep Signatures of Memory Consolidation and Impairs Place Cell Stability and Spatial Memory', Current Biology, vol. 28, no. 22, pp. 3599-3609.e4. https://doi.org/10.1016/j.cub.2018.09.054

Abnormal Locus Coeruleus Sleep Activity Alters Sleep Signatures of Memory Consolidation and Impairs Place Cell Stability and Spatial Memory. / Swift, Kevin M.; Gross, Brooks A.; Frazer, Michelle A.; Bauer, David S.; Clark, Kyle J.D.; Vazey, Elena M.; Aston Jones, Gary; Li, Yong; Pickering, Anthony E.; Sara, Susan J.; Poe, Gina R.

In: Current Biology, Vol. 28, No. 22, 19.11.2018, p. 3599-3609.e4.

Research output: Contribution to journalArticle

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AU - Swift, Kevin M.

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AU - Li, Yong

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AU - Sara, Susan J.

AU - Poe, Gina R.

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