Awake, Offline Processing During Associative Learning

Overview

Journal PLoS One

Specialties General Medicine
Science

Date 2016 Apr 28

PMID 27119345

Citations 4

Authors

James K Bursley

Adrian Nestor

Michael J Tarr

J David Creswell

Affiliations

Soon will be listed here.

Abstract

Offline processing has been shown to strengthen memory traces and enhance learning in the absence of conscious rehearsal or awareness. Here we evaluate whether a brief, two-minute offline processing period can boost associative learning and test a memory reactivation account for these offline processing effects. After encoding paired associates, subjects either completed a distractor task for two minutes or were immediately tested for memory of the pairs in a counterbalanced, within-subjects functional magnetic resonance imaging study. Results showed that brief, awake, offline processing improves memory for associate pairs. Moreover, multi-voxel pattern analysis of the neuroimaging data suggested reactivation of encoded memory representations in dorsolateral prefrontal cortex during offline processing. These results signify the first demonstration of awake, active, offline enhancement of associative memory and suggest that such enhancement is accompanied by the offline reactivation of encoded memory representations.

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References

Krause B, Schmidt D, Mottaghy F, Taylor J, Halsband U, Herzog H . Episodic retrieval activates the precuneus irrespective of the imagery content of word pair associates. A PET study. Brain. 1999; 122 ( Pt 2):255-63. DOI: 10.1093/brain/122.2.255. View

Mottaghy F, Shah N, Krause B, Schmidt D, Halsband U, Jancke L . Neuronal correlates of encoding and retrieval in episodic memory during a paired-word association learning task: a functional magnetic resonance imaging study. Exp Brain Res. 1999; 128(3):332-42. DOI: 10.1007/s002210050853. View

Fischer S, Hallschmid M, Elsner A, Born J . Sleep forms memory for finger skills. Proc Natl Acad Sci U S A. 2002; 99(18):11987-91. PMC: 129381. DOI: 10.1073/pnas.182178199. View

Lundstrom B, Ingvar M, Petersson K . The role of precuneus and left inferior frontal cortex during source memory episodic retrieval. Neuroimage. 2005; 27(4):824-34. DOI: 10.1016/j.neuroimage.2005.05.008. View

Stickgold R . Sleep-dependent memory consolidation. Nature. 2005; 437(7063):1272-8. DOI: 10.1038/nature04286. View

Cohen D, Pascual-Leone A, Press D, Robertson E . Off-line learning of motor skill memory: a double dissociation of goal and movement. Proc Natl Acad Sci U S A. 2005; 102(50):18237-41. PMC: 1312380. DOI: 10.1073/pnas.0506072102. View

Cavanna A, Trimble M . The precuneus: a review of its functional anatomy and behavioural correlates. Brain. 2006; 129(Pt 3):564-83. DOI: 10.1093/brain/awl004. View

Blumenfeld R, Ranganath C . Dorsolateral prefrontal cortex promotes long-term memory formation through its role in working memory organization. J Neurosci. 2006; 26(3):916-25. PMC: 6675388. DOI: 10.1523/JNEUROSCI.2353-05.2006. View

Turk-Browne N, Yi D, Chun M . Linking implicit and explicit memory: common encoding factors and shared representations. Neuron. 2006; 49(6):917-27. DOI: 10.1016/j.neuron.2006.01.030. View

10.

Peigneux P, Orban P, Balteau E, Degueldre C, Luxen A, Laureys S . Offline persistence of memory-related cerebral activity during active wakefulness. PLoS Biol. 2006; 4(4):e100. PMC: 1413571. DOI: 10.1371/journal.pbio.0040100. View

11.

Summerfield C, Greene M, Wager T, Egner T, Hirsch J, Mangels J . Neocortical connectivity during episodic memory formation. PLoS Biol. 2006; 4(5):e128. PMC: 1436028. DOI: 10.1371/journal.pbio.0040128. View

12.

Foerde K, Knowlton B, Poldrack R . Modulation of competing memory systems by distraction. Proc Natl Acad Sci U S A. 2006; 103(31):11778-83. PMC: 1544246. DOI: 10.1073/pnas.0602659103. View

13.

Staresina B, Davachi L . Differential encoding mechanisms for subsequent associative recognition and free recall. J Neurosci. 2006; 26(36):9162-72. PMC: 6674493. DOI: 10.1523/JNEUROSCI.2877-06.2006. View

14.

Aminoff E, Gronau N, Bar M . The parahippocampal cortex mediates spatial and nonspatial associations. Cereb Cortex. 2006; 17(7):1493-503. DOI: 10.1093/cercor/bhl078. View

15.

Ellenbogen J, Payne J, Stickgold R . The role of sleep in declarative memory consolidation: passive, permissive, active or none?. Curr Opin Neurobiol. 2006; 16(6):716-22. DOI: 10.1016/j.conb.2006.10.006. View

16.

Brown R, Robertson E . Inducing motor skill improvements with a declarative task. Nat Neurosci. 2007; 10(2):148-9. PMC: 1831714. DOI: 10.1038/nn1836. View

17.

Rasch B, Buchel C, Gais S, Born J . Odor cues during slow-wave sleep prompt declarative memory consolidation. Science. 2007; 315(5817):1426-9. DOI: 10.1126/science.1138581. View

18.

Stickgold R, Walker M . Sleep-dependent memory consolidation and reconsolidation. Sleep Med. 2007; 8(4):331-43. PMC: 2680680. DOI: 10.1016/j.sleep.2007.03.011. View

19.

Blumenfeld R, Ranganath C . Prefrontal cortex and long-term memory encoding: an integrative review of findings from neuropsychology and neuroimaging. Neuroscientist. 2007; 13(3):280-91. DOI: 10.1177/1073858407299290. View

20.

Brown R, Robertson E . Off-line processing: reciprocal interactions between declarative and procedural memories. J Neurosci. 2007; 27(39):10468-75. PMC: 6673170. DOI: 10.1523/JNEUROSCI.2799-07.2007. View