Literature DB >> 21102988

Coping with sleep deprivation: shifts in regional brain activity and learning strategy.

Roelina Hagewoud1, Robbert Havekes, Paula A Tiba, Arianna Novati, Koen Hogenelst, Pim Weinreder, Eddy A Van der Zee, Peter Meerlo.   

Abstract

STUDY
OBJECTIVES: dissociable cognitive strategies are used for place navigation. Spatial strategies rely on the hippocampus, an area important for flexible integration of novel information. Response strategies are more rigid and involve the dorsal striatum. These memory systems can compensate for each other in case of temporal or permanent damage. Sleep deprivation has adverse effects on hippocampal function. However, whether the striatal memory system can compensate for sleep-deprivation-induced hippocampal impairments is unknown.
DESIGN: with a symmetrical maze paradigm for mice, we examined the effect of sleep deprivation on learning the location of a food reward (training) and on learning that a previously nonrewarded arm was now rewarded (reversal training). MEASUREMENTS AND
RESULTS: five hours of sleep deprivation after each daily training session did not affect performance during training. However, in contrast with controls, sleep-deprived mice avoided a hippocampus-dependent spatial strategy and preferentially used a striatum-dependent response strategy. In line with this, the training-induced increase in phosphorylation of the transcription factor cAMP response-element binding protein (CREB) shifted from hippocampus to dorsal striatum. Importantly, although sleep-deprived mice performed well during training, performance during reversal training was attenuated, most likely due to rigidity of the striatal system they used.
CONCLUSIONS: together, these findings suggest that the brain compensates for negative effects of sleep deprivation on the hippocampal memory system by promoting the use of a striatal memory system. However, effects of sleep deprivation can still appear later on because the alternative learning mechanisms and brain regions involved may result in reduced flexibility under conditions requiring adaptation of previously formed memories.

Entities:  

Keywords:  CREB; Sleep restriction; hippocampus; memory formation; reversal learning; striatum

Mesh:

Substances:

Year:  2010        PMID: 21102988      PMCID: PMC2954696          DOI: 10.1093/sleep/33.11.1465

Source DB:  PubMed          Journal:  Sleep        ISSN: 0161-8105            Impact factor:   5.849


  47 in total

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Journal:  Cell       Date:  1997-03-07       Impact factor: 41.582

2.  Ethosecretogram: relation of behavior to plasma corticosterone in freely moving rats.

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3.  Inactivation of hippocampus or caudate nucleus with lidocaine differentially affects expression of place and response learning.

Authors:  M G Packard; J L McGaugh
Journal:  Neurobiol Learn Mem       Date:  1996-01       Impact factor: 2.877

4.  Antisense oligodeoxynucleotide-mediated disruption of hippocampal cAMP response element binding protein levels impairs consolidation of memory for water maze training.

Authors:  J F Guzowski; J L McGaugh
Journal:  Proc Natl Acad Sci U S A       Date:  1997-03-18       Impact factor: 11.205

5.  Validation of open:closed arm entries in an elevated plus-maze as a measure of anxiety in the rat.

Authors:  S Pellow; P Chopin; S E File; M Briley
Journal:  J Neurosci Methods       Date:  1985-08       Impact factor: 2.390

6.  Dependence on REM sleep of overnight improvement of a perceptual skill.

Authors:  A Karni; D Tanne; B S Rubenstein; J J Askenasy; D Sagi
Journal:  Science       Date:  1994-07-29       Impact factor: 47.728

7.  Hippocampal function and spatial memory: evidence from functional neuroimaging in healthy participants and performance of patients with medial temporal lobe resections.

Authors:  Véronique D Bohbot; Giuseppe Iaria; Michael Petrides
Journal:  Neuropsychology       Date:  2004-07       Impact factor: 3.295

8.  Interaction between the human hippocampus and the caudate nucleus during route recognition.

Authors:  Nicol C Voermans; Karl Magnus Petersson; Leonie Daudey; Bernd Weber; Karel P Van Spaendonck; Hubertus P H Kremer; Guillén Fernández
Journal:  Neuron       Date:  2004-08-05       Impact factor: 17.173

9.  Evidence for a paradoxical sleep window for place learning in the Morris water maze.

Authors:  C Smith; G M Rose
Journal:  Physiol Behav       Date:  1996-01

10.  Deficient long-term memory in mice with a targeted mutation of the cAMP-responsive element-binding protein.

Authors:  R Bourtchuladze; B Frenguelli; J Blendy; D Cioffi; G Schutz; A J Silva
Journal:  Cell       Date:  1994-10-07       Impact factor: 41.582

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  36 in total

1.  Prevention by Regular Exercise of Acute Sleep Deprivation-Induced Impairment of Late Phase LTP and Related Signaling Molecules in the Dentate Gyrus.

Authors:  Munder A Zagaar; An T Dao; Ibrahim A Alhaider; Karim A Alkadhi
Journal:  Mol Neurobiol       Date:  2015-04-23       Impact factor: 5.590

2.  Acute Sleep Deprivation Blocks Short- and Long-Term Operant Memory in Aplysia.

Authors:  Harini C Krishnan; Catherine E Gandour; Joshua L Ramos; Mariah C Wrinkle; Joseph J Sanchez-Pacheco; Lisa C Lyons
Journal:  Sleep       Date:  2016-12-01       Impact factor: 5.849

3.  Sleep Consolidates Motor Learning of Complex Movement Sequences in Mice.

Authors:  Hirotaka Nagai; Luisa de Vivo; Michele Bellesi; Maria Felice Ghilardi; Giulio Tononi; Chiara Cirelli
Journal:  Sleep       Date:  2017-02-01       Impact factor: 5.849

4.  Sleep deprivation during a specific 3-hour time window post-training impairs hippocampal synaptic plasticity and memory.

Authors:  Toni-Moi Prince; Mathieu Wimmer; Jennifer Choi; Robbert Havekes; Sara Aton; Ted Abel
Journal:  Neurobiol Learn Mem       Date:  2013-12-28       Impact factor: 2.877

5.  Free recall of word lists under total sleep deprivation and after recovery sleep.

Authors:  Gislaine de Almeida Valverde Zanini; Sérgio Tufik; Monica Levy Andersen; Raquel Cristina Martins da Silva; Orlando Francisco Amodeo Bueno; Camila Cruz Rodrigues; Sabine Pompéia
Journal:  Sleep       Date:  2012-02-01       Impact factor: 5.849

6.  Effects of acute sleep deprivation on motor and reversal learning in mice.

Authors:  Andrew W Varga; Mihwa Kang; Priyanka V Ramesh; Eric Klann
Journal:  Neurobiol Learn Mem       Date:  2014-07-18       Impact factor: 2.877

7.  Antidepressant suppression of non-REM sleep spindles and REM sleep impairs hippocampus-dependent learning while augmenting striatum-dependent learning.

Authors:  Alain Watts; Howard J Gritton; Jamie Sweigart; Gina R Poe
Journal:  J Neurosci       Date:  2012-09-26       Impact factor: 6.167

Review 8.  About sleep's role in memory.

Authors:  Björn Rasch; Jan Born
Journal:  Physiol Rev       Date:  2013-04       Impact factor: 37.312

9.  Sleep deprivation impairs synaptic tagging in mouse hippocampal slices.

Authors:  Christopher G Vecsey; Ted Huang; Ted Abel
Journal:  Neurobiol Learn Mem       Date:  2018-03-15       Impact factor: 2.877

10.  A PILOT STUDY ON THE ENCODING OF A PERCEPTUAL LEARNING TASK FOLLOWING SLEEP DEPRIVATION.

Authors:  Kelly K McWhirter; Anne S Morrow; Beth A Lee; Shrinivas Bishu; Alan J Zametkin; Thomas J Balkin; Carolyn B Smith; Dante Picchioni
Journal:  Percept Mot Skills       Date:  2015-07-30
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