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Articles, Behavioral/Cognitive

Transiently Increasing cAMP Levels Selectively in Hippocampal Excitatory Neurons during Sleep Deprivation Prevents Memory Deficits Caused by Sleep Loss

Robbert Havekes, Vibeke M. Bruinenberg, Jennifer C. Tudor, Sarah L. Ferri, Arnd Baumann, Peter Meerlo and Ted Abel
Journal of Neuroscience 19 November 2014, 34 (47) 15715-15721; https://doi.org/10.1523/JNEUROSCI.2403-14.2014
Robbert Havekes
1Department of Biology, University of Pennsylvania, Philadelphia, Pennsylvania 19104,
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Vibeke M. Bruinenberg
1Department of Biology, University of Pennsylvania, Philadelphia, Pennsylvania 19104,
2Center for Behavior and Neurosciences, University of Groningen, Groningen, The Netherlands, and
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Jennifer C. Tudor
1Department of Biology, University of Pennsylvania, Philadelphia, Pennsylvania 19104,
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Sarah L. Ferri
1Department of Biology, University of Pennsylvania, Philadelphia, Pennsylvania 19104,
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Arnd Baumann
3Forschungszentrum Jülich, Institute of Complex Systems, Zelluläre Biophysik (ICS-4), D-52425 Jülich, Germany
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Peter Meerlo
2Center for Behavior and Neurosciences, University of Groningen, Groningen, The Netherlands, and
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Ted Abel
1Department of Biology, University of Pennsylvania, Philadelphia, Pennsylvania 19104,
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Abstract

The hippocampus is particularly sensitive to sleep loss. Although previous work has indicated that sleep deprivation impairs hippocampal cAMP signaling, it remains to be determined whether the cognitive deficits associated with sleep deprivation are caused by attenuated cAMP signaling in the hippocampus. Further, it is unclear which cell types are responsible for the memory impairments associated with sleep deprivation. Transgenic approaches lack the spatial resolution to manipulate specific signaling pathways selectively in the hippocampus, while pharmacological strategies are limited in terms of cell-type specificity. Therefore, we used a pharmacogenetic approach based on a virus-mediated expression of a Gαs-coupled Drosophila octopamine receptor selectively in mouse hippocampal excitatory neurons in vivo. With this approach, a systemic injection with the receptor ligand octopamine leads to increased cAMP levels in this specific set of hippocampal neurons. We assessed whether transiently increasing cAMP levels during sleep deprivation prevents memory consolidation deficits associated with sleep loss in an object–location task. Five hours of total sleep deprivation directly following training impaired the formation of object–location memories. Transiently increasing cAMP levels in hippocampal neurons during the course of sleep deprivation prevented these memory consolidation deficits. These findings demonstrate that attenuated cAMP signaling in hippocampal excitatory neurons is a critical component underlying the memory deficits in hippocampus-dependent learning tasks associated with sleep deprivation.

  • hippocampus
  • learning
  • memory
  • pharmacogenetics
  • sleep
  • sleep disruption
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The Journal of Neuroscience: 34 (47)
Journal of Neuroscience
Vol. 34, Issue 47
19 Nov 2014
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Transiently Increasing cAMP Levels Selectively in Hippocampal Excitatory Neurons during Sleep Deprivation Prevents Memory Deficits Caused by Sleep Loss
Robbert Havekes, Vibeke M. Bruinenberg, Jennifer C. Tudor, Sarah L. Ferri, Arnd Baumann, Peter Meerlo, Ted Abel
Journal of Neuroscience 19 November 2014, 34 (47) 15715-15721; DOI: 10.1523/JNEUROSCI.2403-14.2014

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Transiently Increasing cAMP Levels Selectively in Hippocampal Excitatory Neurons during Sleep Deprivation Prevents Memory Deficits Caused by Sleep Loss
Robbert Havekes, Vibeke M. Bruinenberg, Jennifer C. Tudor, Sarah L. Ferri, Arnd Baumann, Peter Meerlo, Ted Abel
Journal of Neuroscience 19 November 2014, 34 (47) 15715-15721; DOI: 10.1523/JNEUROSCI.2403-14.2014
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Keywords

  • hippocampus
  • learning
  • memory
  • pharmacogenetics
  • sleep
  • sleep disruption

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