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Abstract

Memory consolidation has been described as a process to strengthen newly formed memories and to stabilize them against interference from similar learning experiences. Sleep facilitates memory consolidation in humans, improving memory performance and protecting against interference encountered after sleep. The European starling, a songbird, has also manifested sleep-dependent memory consolidation when trained on an auditory-classification task. Here, we examined how memory for two similar classification tasks is consolidated across waking and sleep in starlings. We demonstrated for the first time that the learning of each classification reliably interferes with the retention of the other classification across waking retention but that sleep enhances and stabilizes the memory of both classifications even after performance is impaired by interference. These observations demonstrate that sleep consolidation enhances retention of interfering experiences, facilitating opportunistic daytime learning and the subsequent formation of stable long-term memories.

Keywords

memory sleep-wake cycle comparative psychology learning forgetting

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References

Brawn

T. P.

Fenn

K. M.

Nusbaum

H. C.

Margoliash

(2008). Consolidation of sensorimotor learning during sleep. Learning & Memory, 15, 815–819.

Brawn

T. P.

Fenn

K. M.

Nusbaum

H. C.

Margoliash

(2010). Consolidating the effects of waking and sleep on motor-sequence learning. Journal of Neuroscience, 30, 13977–13982.

Brawn

T. P.

Nusbaum

H. C.

Margoliash

(2010). Sleep-dependent consolidation of auditory discrimination learning in adult starlings. Journal of Neuroscience, 30, 609–613.

Dave

A. S.

Margoliash

(2000). Song replay during sleep and computational rules for sensorimotor vocal learning. Science, 290, 812–816.

Diekelmann

Born

Wagner

(2010). Sleep enhances false memories depending on general memory performance. Behavioural Brain Research, 208, 425–429.

Diekelmann

Büchel

Born

Rasch

(2011). Labile or stable: Opposing consequences for memory when reactivated during waking or sleep. Nature Neuroscience, 14, 381–386.

Diekelmann

Wilhelm

Born

(2009). The whats and whens of sleep-dependent memory consolidation. Sleep Medicine Reviews, 13, 309–321.

Drosopoulos

Schulze

Fischer

Born

(2007). Sleep’s function in the spontaneous recovery and consolidation of memories. Journal of Experimental Psychology: General, 136, 169–183.

Ellenbogen

J. M.

Hulbert

J. C.

Jiang

Stickgold

(2009). The sleeping brain’s influence on verbal memory: Boosting resistance to interference. PLoS ONE, 4(1), e4117. Retrieved from http://www.plosone.org/article/info%3Adoi%2F10.1371%2Fjournal.pone.0004117

10.

Ellenbogen

J. M.

Hulbert

J. C.

Stickgold

Dinges

D. F.

Thompson-Schill

S. L.

(2006). Interfering with theories of sleep and memory: Sleep, declarative memory, and associative interference. Current Biology, 16, 1290–1294.

11.

Fenn

K. M.

Gallo

D. A.

Margoliash

Roediger

H. L.

Nusbaum

H. C.

(2009). Reduced false memory after sleep. Learning & Memory, 16, 509–513.

12.

Fenn

K. M.

Nusbaum

H. C.

Margoliash

(2003). Consolidation during sleep of perceptual learning of spoken language. Nature, 425, 614–616.

13.

Fischer

Nitschke

M. F.

Melchert

U. H.

Erdmann

Born

(2005). Motor memory consolidation in sleep shapes more effective neuronal representations. Journal of Neuroscience, 25, 11248–11255.

14.

Gais

Lucas

Born

(2006). Sleep after learning aids memory recall. Learning & Memory, 13, 259–262.

15.

Stylos-Allan

Walker

M. P.

(2006). Sleep facilitates consolidation of emotional declarative memory. Psychological Science, 17, 891–898.

16.

Korman

Doyon

Doljansky

Carrier

Dagan

Karni

(2007). Daytime sleep condenses the time course of motor memory consolidation. Nature Neuroscience, 10, 1206–1213.

17.

Low

P. S.

Shank

S. S.

Sejnowski

T. J.

Margoliash

(2008). Mammalian-like features of sleep structure in zebra finches. Proceedings of the National Academy of Sciences, USA, 105, 9081–9086.

18.

McGaugh

J. L.

(2000). Memory: A century of consolidation. Science, 287, 248–251.

19.

Mednick

Nakayama

Stickgold

(2003). Sleep- dependent learning: A nap is as good as a night. Nature Neuroscience, 6, 697–698.

20.

Nishida

Walker

M. P.

(2007). Daytime naps, motor memory consolidation and regionally specific sleep spindles. PLoS ONE, 2(4), e341. Retrieved from http://www.plosone.org/article/info%3Adoi%2F10.1371%2Fjournal.pone.0000341

21.

O’Neill

Pleydell-Bouverie

Dupret

Csicsvari

(2010). Play it again: Reactivation of waking experience and memory. Trends in Neuroscience, 33, 220–229.

22.

Payne

J. D.

Stickgold

Swanberg

Kensinger

E. A.

(2008). Sleep preferentially enhances memory for emotional components of scenes. Psychological Science, 19, 781–788.

23.

Poe

G. R.

Walsh

C. M.

Bjorness

T. E.

(2010). Cognitive neuroscience of sleep. Progress in Brain Research, 185, 1–19.

24.

Rasch

Born

(2007). Maintaining memories by reactivation. Current Opinion in Neurobiology, 17, 698–703.

25.

Rattenborg

N. C.

Martinez-Gonzalez

Lesku

J. A.

(2009). Avian sleep homeostasis: Convergent evolution of complex brain, cognition and sleep functions in mammals and birds. Neuroscience & Biobehavioral Reviews, 233, 253–270.

26.

Rickard

T. C.

Cai

D. J.

Rieth

Jones

Ard

(2008). Sleep does not enhance motor sequence learning. Journal of Experimental Psychology: Learning, Memory, and Cognition, 34, 834–842.

27.

Scullin

M. K.

McDaniel

M. A.

(2010). Remembering to execute a goal: Sleep on it! Psychological Science, 21, 1028–1035.

28.

Shank

S. S.

Margoliash

(2009). Sleep and sensorimotor integration during early vocal learning in a songbird. Nature, 458, 73–77.

29.

Stickgold

James

Hobson

J. A.

(2000). Visual discrimination learning requires sleep after training. Nature Neuroscience, 3, 1237–1238.

30.

Tononi

Cirelli

(2003). Sleep function and synaptic homeostasis. Sleep Medicine Reviews, 10, 49–62.

31.

Tononi

Cirelli

(2006). Sleep and synaptic homeostasis: A hypothesis. Brain Research Bulletin, 62, 143–150.

32.

Walker

M. P.

Brakefield

Hobson

J. A.

Stickgold

(2003). Dissociable stages of human memory consolidation and reconsolidation. Nature, 425, 616–620.

33.

Walker

M. P.

Stickgold

(2006). Sleep, memory, and plasticity. Annual Review of Psychology, 57, 139–166.

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Sleep Consolidation of Interfering Auditory Memories in Starlings

Abstract

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