Sleep-Dependent Consolidation of Auditory Discrimination Learning in Adult Starlings
Open accessAbstract
Memory consolidation is widely believed to benefit from sleep. Sleep-dependent memory consolidation has been established broadly in humans, appearing in declarative and procedural tasks. Animal studies have indicated a variety of mechanisms that could potentially serve as the neural basis of sleep-dependent consolidation, such as the offline replay of waking neural activity and the modulation of specific sleep parameters or synaptic strength during sleep. Memory consolidation, however, cannot be inferred from neuronal events alone, and the behavioral demonstration of sleep-dependent consolidation has been limited in animals. Here we investigated whether adult animals undergo sleep-dependent memory consolidation comparable to that of humans. European starlings (Sturnus vulgaris) were trained to discriminate between segments of novel starling song and retested after retention periods that included a regular night of sleep or consisted only of wakefulness. Auditory discrimination performance improved significantly after retention periods that included sleep but not after time spent awake, and the performance changes following sleep were significantly greater than after comparable periods of wakefulness. Thus, sleep produces a pattern of memory benefits in adult starlings that is fundamentally similar to the patterns of sleep-dependent consolidation observed in humans, suggesting a common sleep-dependent mechanism works across many vertebrate species to consolidate memories and establishing a robust animal model for this phenomenon.
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Reactivations during sleep may also strengthen the song template.
“In addition to modifying sensorimotor representations, reactivations during sleep may also strengthen the song template (136).”
From About Sleep's Role in Memory (2013) · cites this paper as [136]
The Introduction and Discussion propose that neural reactivation during sleep could strengthen memory traces, and the Discussion notes that reactivation has been observed in zebra finches. The paper does not specifically identify the song template as the trace being strengthened; its own experiment concerns auditory discrimination in adult starlings. (LLM, conf=0.83)
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Huber, R., Felice Ghilardi, M., Massimini, M., & Tononi, G. (2004) · Nature · doi:10.1038/nature02663 · Cited by 1,854 · see citing works
The contribution of sleep to hippocampus-dependent memory consolidation
Marshall, L., & Born, J. (2007) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2007.09.001 · Cited by 667 · see citing works
Consolidation during sleep of perceptual learning of spoken language
Fenn, K. M., Nusbaum, H. C., & Margoliash, D. (2003) · Nature · doi:10.1038/nature01951 · Cited by 463 · see citing works
Self-citationSong replay during sleep and computational rules for sensorimotor vocal learning
Dave, A. S., & Margoliash, D. (2000) · Science · doi:10.1126/science.290.5492.812 · Cited by 458 · see citing works
Self-citationWidespread Changes in Synaptic Markers as a Function of Sleep and Wakefulness in <i>Drosophila</i>
Gilestro, G. F., Tononi, G., & Cirelli, C. (2009) · Science · doi:10.1126/science.1166673 · Cited by 360 · see citing works
Sustained increase in hippocampal sharp-wave ripple activity during slow-wave sleep after learning
Eschenko, O., Ramadan, W., Mölle, M., Born, J., & Sara, S. J. (2008) · Learning & Memory · doi:10.1101/lm.726008 · Cited by 277 · see citing works
Mechanisms of sleep-dependent consolidation of cortical plasticity
Aton, S. J., Seibt, J., Dumoulin, M., Jha, S. K., Steinmetz, N., Coleman, T., Naidoo, N., & Frank, M. G. (2009) · Neuron · doi:10.1016/j.neuron.2009.01.007 · Cited by 244 · see citing works
Sleep and sensorimotor integration during early vocal learning in a songbird
Shank, S. S., & Margoliash, D. (2009) · Nature · doi:10.1038/nature07615 · Cited by 178 · cited 4× · see citing works
“…zebra finches was shown to deteriorate immediately after sleep and then improve during intense morning singing, with the magnitude of nightly deterioration correlating with a more accurate tutor song imitation at the end of development (Derégnaucourt et al., 2005; Shank and Margoliash, 2009).”
BackgroundInfluentialSelf-citationHippocampal Sharp Wave/Ripples during Sleep for Consolidation of Associative Memory
Ramadan, W., Eschenko, O., & Sara, S. J. (2009) · PLoS ONE · doi:10.1371/journal.pone.0006697 · Cited by 173 · see citing works
Dynamics of a Memory Trace: Effects of Sleep on Consolidation
Jackson, C., McCabe, B. J., Nicol, A. U., Grout, A. S., Brown, M. W., & Horn, G. (2008) · Current Biology · doi:10.1016/j.cub.2008.01.062 · Cited by 88 · see citing works
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Research works printed but not linked: 23
- Brawn TP Fenn KM Nusbaum HC Margoliash D 2008 Consolidation of sensorimotor learning during sleep Learn Mem 15 815 819 18984561
- Cai DJ Shuman T Gorman MR Sage JR Anagnostaras SG 2009 Sleep selectively enhances hippocampus-dependent memory in mice Behav Neuro 123 713 719 19634928
- Datta S 2000 Avoidance task training potentiates phasic pontine-wave density in the rat: A mechanism for sleep-dependent plasticity J Neurosci 20 8607 8613 11069969 PMC6773158
- Deregnaucourt S Mitra PP Feher O Pytte C Tchernichovski O 2004 How sleep affects the developmental learning of bird song Nature 433 710 716 15716944
- Ellenbogen JM Hulbert JC Stickgold R Dinges DF Thompson-Schill SL 2006 Interfering with theories of sleep and memory: Sleep, declarative memory, and associative interference Curr Biol 16 1290 1294 16824917
- Eschenko O Molle M Born J Sara SJ 2006 Elevated sleep spindle density after learning or after retrieval in rats J Neurosci 26 12914 12920 17167082 PMC6674950
- Fenn KM Gallo DA Margoliash D Roediger HL Nusbaum HC 2009 Reduced false memory after sleep Learn Mem 16 509 513 19706833
- Gais S Plihal W Wagner U Born J 2000 Early sleep triggers memory for early visual discrimination skills Nat Neurosci 3 1335 1339 11100156
- Gentner TQ Margoliash D 2003 Neuronal populations and single cells representing learned auditory objects Nature 424 669 674 12904792 PMC2631575
- Hennevin E Huetz C Edeline JM 2007 Neural representations during sleep: From sensory processing to memory traces Neurobiol Learn Mem 87 416 440 17178239
- Ji D Wilson MA 2007 Coordinated memory replay in the visual cortex and hippocampus during sleep Nat Neurosci 10 100 107 17173043
- Korman M Doyon J Doljanksy J Carrier J Dagan Y Karni A 2007 Daytime sleep condenses the time course of motor memory consolidation Nat Neurosci 10 1206 1213 17694051
- Peigneux P Laureys S Fuchs S Collette F Perrin F Reggers J Phillips C Degueldre C Del Fiore G Aerts J Luxen A Maquet P 2004 Are spatial memories strengthened in the human hippocampus during slow wave sleep? Neuron 44 535 545 15504332
- Peyrache A Khamassi M Benchenane K Wiener SI Battaglia FP 2009 Replay of rule-learning related neural patterns in the prefrontal cortex during sleep Nat Neurosci 12 919 926 19483687
- Rasch B Born J 2007 Maintaining memories by reactivation Curr Opin Neurobiol 17 698 703 18222688
- Robertson EM Pascual-Leone A Press DZ 2004 Awareness modifies the skill-learning benefits of sleep Curr Biol 14 208 212 14761652
- Siegel JM 2001 The REM sleep-memory consolidation hypothesis Science 294 1058 1063 11691984 PMC8760621
- Smith C 1995 Sleep states and memory processes Behav Brain Res 69 137 145 7546305
- Talarmini LM Nieuwenhuis ILC Takashima A Jensen O 2008 Sleep directly following learning benefits consolidation of spatial associative memory Learn Mem 15 233 237 18391183
- Tononi G Cirelli C 2006 Sleep function and synaptic homeostasis Sleep Med Rev 10 49 62 16376591
- Walker MP Brakefield T Morgan A Hobson JA Stickgold R 2002 Practice with sleep makes perfect: Sleep-dependent motor skill learning Neuron 35 205 211 12123620
- Walker MP 2005 A refined model of sleep and the time course of memory formation Behav Brain Sci 28 51 64 16047457
- Wilson MA McNaughton BL 1994 Reactivation of hippocampal ensemble memories during sleep Science 265 676 679 8036517
Cited by
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Rasch, B., & Born, J. (2013) · Physiological Reviews · doi:10.1152/physrev.00032.2012 · Cited by 2,783 · see citing works
“modifying sensorimotor representations, reactivations during sleep may also strengthen the song template (136).”
BackgroundConsolidating the Effects of Waking and Sleep on Motor-Sequence Learning
Brawn, T. P., Fenn, K. M., Nusbaum, H. C., & Margoliash, D. (2010) · The Journal of Neuroscience · doi:10.1523/jneurosci.3295-10.2010 · Cited by 181 · see citing works
Self-citationSleep and memory in mammals, birds and invertebrates
Vorster, A. P., & Born, J. (2015) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2014.09.020 · Cited by 169 · see citing works
- Authors
- Brawn, T. P., Nusbaum, H. C., & Margoliash, D.
- Affiliations
- University of Chicago (US)
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2010-01-13
- Volume
- 30
- Issue
- 2
- Pages
- 609-613
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC2824332
- OpenAlex
- W1964221523
- Cited by
- 55
- References
- 10
- Citations by year
- 2026: 2 · 2025: 4 · 2024: 2 · 2023: 1 · 2022: 3 · 2021: 1 · 2020: 1 · 2019: 2 · 2018: 3 · 2017: 7 · 2016: 1 · 2015: 2 · 2014: 7 · 2013: 7 · 2012: 4
- FWCI
- 3.69
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institute on Deafness and Other Communication Disorders (R01DC007206, DC 007206)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Sleep and Wakefulness Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory Processes and Influences
- Keywords
- sleep-dependent memory consolidation, auditory discrimination learning, Sturnus vulgaris, sleep versus wakefulness, memory retention
- MeSH terms
- Acoustic Stimulation, Animals, Auditory Perception, Behavior, Animal, Discrimination Learning, Memory, Sleep, Time Factors, Wakefulness, Starlings
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