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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; DOI: 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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    Figure 1.

    Viral expression of DmOctβR1 is restricted to excitatory neurons of the hippocampus. A, Mice were injected with pAAV9-CaMKIIα0.4-EGFP or pAAV9-CaMKIIα0.4-DmOctβ1R-HA to drive expression of EGFP or the Gαs-coupled DmOctβ1R in hippocampal excitatory neurons. B, Activation of the DmOctβ1R by its ligand octopamine (OCT) stimulates adenylyl cyclase activity, which synthesizes cAMP. C, D, Representative low-magnification images of EGFP and DmOctβ1R expression in coronal brain sections. Scale bar, 570 μm. E, F, Representative images EGFP and DmOctβ1R expression in all three major hippocampal subregions. Scale bar, 200 μm. G–L, Higher-magnification images of area CA1 (E, H), CA3 (F, I), and dentate gyrus (G, J). Scale bar, 20 μm. AC, Adenyl cyclase; ITR, inverted terminal repeats.

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    Figure 2.

    Activation of the DmOctβ1R in hippocampal neurons leads to increased cAMP levels selectively in the hippocampus. A, A systemic injection with octopamine (1 mg/kg) increased hippocampal cAMP levels 30 min after injection (*p = 0.034, t test) in mice expressing DmOctβ1R. B, Systemic injection with octopamine (1 mg/kg) did not alter cAMP levels in the prefrontal cortex 30 min after injection in mice expressing DmOctβ1R (p = 0.668, t test). All data are expressed as the mean ± SEM.

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    Figure 3.

    Increasing neuronal cAMP levels in hippocampal neurons prevents memory deficits caused by sleep deprivation. A, A diagram illustrating the training schedule and time points at which all animals received intraperitonal injections with octopamine. B, Viral expression of the Gαs-coupled DmOctβ1R in hippocampal neurons does not affect object exploration levels during training in the object–place recognition task (effect of virus: F(1,35) = 1.640, p = 0.209). All groups showed decreased total object exploration time during consecutive training sessions in a similar fashion (effect of session: F(2,70) = 58.723, p = 0.0001; interaction effect: F(2,70) = 0.936, p = 0.397). C, Mice expressing EGFP or DmOctβ1R were trained in the hippocampus-dependent object–place recognition task and sleep deprived for 5 h immediately after training [sleep-deprived (SD) animals] or were left undisturbed [non-sleep-deprived (NSD) animals]. Mice received systemic injections with octopamine directly after training and 2.5 h into sleep deprivation. Boosting cAMP signaling by activating the of DmOctβ1R prevents memory deficits caused by sleep deprivation (n = 9–10; effect of sleep deprivation: F(1,35) = 6.603, p = 0.015; effect of virus: F(1,35) = 20.256, p < 0.001; interaction effect: F(1,35) = 4.565, p = 0.04; EGFP SD group vs other groups, p < 0.05). Dotted line indicates chance performance. Error bars denote SEM. *p < 0.05. All data are expressed as the mean ± SEM.

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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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