Sleep and sensorimotor integration during early vocal learning in a songbird
Open accessAbstract
Behavioural studies widely implicate sleep in memory consolidation in the learning of a broad range of behaviours. During sleep, brain regions are reactivated, and specific patterns of neural activity are replayed, consistent with patterns observed in previous waking behaviour. Birdsong learning is a paradigmatic model system for skill learning. Song development in juvenile zebra finches (Taeniopygia guttata) is characterized by sleep-dependent circadian fluctuations in singing behaviour, with immediate post-sleep deterioration in song structure followed by recovery later in the day. In sleeping adult birds, spontaneous bursting activity of forebrain premotor neurons in the robust nucleus of the arcopallium (RA) carries information about daytime singing. Here we show that, in juvenile zebra finches, playback during the day of an adult 'tutor' song induced profound and tutor-song-specific changes in bursting activity of RA neurons during the following night of sleep. The night-time neuronal changes preceded tutor-song-induced changes in singing, first observed the following day. Interruption of auditory feedback greatly reduced sleep bursting and prevented the tutor-song-specific neuronal remodelling. Thus, night-time neuronal activity is shaped by the interaction of the song model (sensory template) and auditory feedback, with changes in night-time activity preceding the onset of practice associated with vocal learning. We hypothesize that night-time bursting induces adaptive changes in premotor networks during sleep as part of vocal learning. By this hypothesis, adaptive changes driven by replay of sensory information at night and by evaluation of sensory feedback during the day interact to produce the complex circadian patterns seen early in vocal development.
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The sequence structure of spiking within bursts during sleep was significantly correlated with that observed while the bird listened to the tutor song during the preceding wake phase.
“Moreover, the sequence structure of spiking within bursts identified during sleep was significantly correlated with that observed while the bird was listening to the tutor song during the preceding wake phase.”
From About Sleep's Role in Memory (2013) · cites this paper as [1063]
The passage on emerging RA bursting activity (section labelled Abstract; page not provided) reports that sleep inter-spike-interval distributions were more similar among birds that heard the same tutor song. The paper's reported correlations compare sleep distributions across birds, not sleep spike sequences with spiking recorded while a bird listened to the tutor song during the preceding wake phase. (LLM, conf=0.88)
Experimental — accuracy not yet measuredIn juvenile zebra finches, first exposure to a tutor song enhanced high-frequency bursting in RA neurons during subsequent sleep, with corresponding changes in singing occurring the following day.
“Thus, in juvenile zebra finches, the first exposure to a tutor song distinctly enhanced high-frequency bursting in RA neurons during subsequent sleep, with corresponding changes in singing occurring not until the following day (1063).”
From About Sleep's Role in Memory (2013) · cites this paper as [1063]
Increases in RA burst occurrence and burst structure after initial tutor song exposure required auditory feedback from the bird's own singing, as they were reduced by auditory feedback deprivation or surgical muting.
“Both the increase in burst occurrence and burst structure in RA after initial exposure to the tutor song also required that the bird receive auditory feedback from its own singing, as these increases were drastically reduced when the birds were experimentally deprived from auditory feedback or were surgically muted.”
From About Sleep's Role in Memory (2013) · cites this paper as [1063]
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Sleep Consolidation of Interfering Auditory Memories in Starlings
Brawn, T. P., Nusbaum, H. C., & Margoliash, D. (2013) · Psychological Science · doi:10.1177/0956797612457391 · Cited by 44 · see citing works
“…of sleep reactivation have not been conducted in starlings, reactivation during sleep has been observed in adult zebra finches (Dave & Margoliash, 2000), and sleep-dependent changes in neural activity have been associated with song learning in juvenile zebra finches (Shank & Margoliash, 2009).”
BackgroundSelf-citationLight, Sleep and Performance in Diurnal Birds
Aulsebrook, A. E., Johnsson, R. D., & Lesku, J. A. (2021) · Clocks & Sleep · doi:10.3390/clockssleep3010008 · Cited by 42 · see citing works
Applications of Avian Transgenesis
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Sleep loss impairs cognitive performance and alters song output in Australian magpies
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Dynamic variation in forebrain estradiol levels during song learning
Chao, A., Paon, A., & Remage‐Healey, L. (2014) · Developmental Neurobiology · doi:10.1002/dneu.22228 · Cited by 37 · see citing works
“These two features have previously been documented to reflect changes in song that occur following tutoring during the sensorimotor stage (Der egnaucourt et al., 2005; Shank and Margoliash, 2009).”
BackgroundMaul, K. K., Voss, H. U., Parra, L. C., Salgado‐Commissariat, D., Ballon, D., Tchernichovski, O., & Helekar, S. A. (2009) · Developmental Neurobiology · doi:10.1002/dneu.20751 · Cited by 36 · see citing works
“For example, brief exposure to songs causes strong changes in (presumably sensory) activity in the song system during the first night after exposure—before vocal changes have occurred (Shank and Margoliash, 2009).”
BackgroundSet and setting: How behavioral state regulates sensory function and plasticity
Aton, S. J. (2013) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2013.06.007 · Cited by 36 · see citing works
“Sleephasbeenshowntoplayanessentialroleinbothsongdiscriminationlearninginadultsongbirds(Brawn,Nusbaum,&Margoliash ,2010b)andininitiallearningofatutor'ssonginjuvenile birds(Shank&Margoliash,2009).”
Melatonin affects the temporal pattern of vocal signatures in birds
Derégnaucourt, S., Saar, S., & Gahr, M. L. (2012) · Journal of Pineal Research · doi:10.1111/j.1600-079x.2012.00993.x · Cited by 34 · see citing works
“Some studies have demonstrated the active role of sleep on the developmental learning of birdsong [34, 42].”
BackgroundMemory-related brain lateralisation in birds and humans
Moorman, S., & Nicol, A. U. (2014) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2014.07.006 · Cited by 32 · see citing works
Learning-related brain hemispheric dominance in sleeping songbirds
Moorman, S., Gobes, S. M. H., van de Kamp, F. C., Zandbergen, M. A., & Bolhuis, J. J. (2015) · Scientific Reports · doi:10.1038/srep09041 · Cited by 32 · see citing works
Adret, P., Meliza, C. D., & Margoliash, D. (2012) · Journal of Neurophysiology · doi:10.1152/jn.00905.2011 · Cited by 32 · see citing works
“shown to shape spontaneous activity in RA neurons, downstream from HVC (Shank and Margoliash 2009).”
BackgroundSelf-citationNeuron-Specific Cholinergic Modulation of a Forebrain Song Control Nucleus
Shea, S. D., Koch, H., Baleckaitis, D. D., Ramirez, J., & Margoliash, D. (2009) · Journal of Neurophysiology · doi:10.1152/jn.00803.2009 · Cited by 31 · see citing works
Self-citationRegulation of learned vocal behavior by an auditory motor cortical nucleus in juvenile zebra finches
Naie, K., & Hahnloser, R. H. R. (2011) · Journal of Neurophysiology · doi:10.1152/jn.01035.2010 · Cited by 31 · see citing works
“The combined driver roles of NIf during sleep and singing point to a possible involvement of NIf in shaping the developing premotor circuitry by driving activity during sleep as a function of auditory experience during the day (Roberts et al. 2010; Shank and Margoliash 2009).”
BackgroundRauske, P. L., Chi, Z., Dave, A. S., & Margoliash, D. (2010) · The Journal of Neuroscience · doi:10.1523/jneurosci.3112-09.2010 · Cited by 31 · see citing works
“, 2009), the emergence of song system neuronal bursting in juvenile birds at the onset of song learning (Shank and Margoliash, 2009), and experience-dependent changes in the correlations of activity patterns of rat hippocampal neurons (Poe et al.”
BackgroundInfluentialSelf-citationPlumes of neuronal activity propagate in three dimensions through the nuclear avian brain
Beckers, G. J. L., van der Meij, J., Lesku, J. A., & Rattenborg, N. C. (2014) · BMC Biology · doi:10.1186/1741-7007-12-16 · Cited by 30 · see citing works
“Finally, our findings may have implications for the interpretation of sleep-related neuronal activity in the song system of sleeping zebra finches, a prominent model for investigating sleep’s role in memory consolidation [45].”
Derégnaucourt, S. (2011) · Interaction Studies Social Behaviour and Communication in Biological and Artificial Systems · doi:10.1075/is.12.2.07der · Cited by 29 · see citing works
Memory circuits for vocal imitation
Ikeda, M. Z., Trusel, M., & Roberts, T. F. (2019) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2019.11.002 · Cited by 29 · see citing works
“Indeed, Shank and Margoliash examined the inter-spike interval (ISI) in high frequency burst firing in RA following tutoring experience and remarkably found that ISI distributions across birds clustered based on the song of their tutor (Shank and Margoliash, 2009).”
BackgroundResultInfluentialAutism-linked gene FoxP1 selectively regulates the cultural transmission of learned vocalizations
García‐Oscos, F., Koch, T. M., Pancholi, H., Trusel, M., Daliparthi, V., Co, M., Park, S.-H. E., Ayhan, F., Alam, D. H., Holdway, J. E., et al. (2021) · Science Advances · doi:10.1126/sciadv.abd2827 · Cited by 29 · see citing works
“Acquisition of tutor-song memories is correlated with the rapid emergence of prolonged patterns of bursting activity in HVC and in RA (17, 18, 48).”
BackgroundHormonal acceleration of song development illuminates motor control mechanism in canaries
Alliende, J. A., Méndez, J. M., Goller, F., & Mindlin, G. B. (2010) · Developmental Neurobiology · doi:10.1002/dneu.20835 · Cited by 29 · see citing works
“Exposure to song and subsequent song production coincides with a change in the spontaneous firing rate of RA neurons (Shank and Margoliash, 2009).”
BackgroundInfluentialRapid encoding of an internal model for imitative learning
Deshpande, M., Pirlepesov, F., & Lints, T. (2014) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2013.2630 · Cited by 29 · see citing works
“Ninety-fifth percentile EV values have been used as a measure for the most structured song elements being produced in the given time-window [14].”
BackgroundMethodInfluentialBoerma, T., ter Haar, S. M., Ganga, R., Wijnen, F. N. K., Blom, E., & Wierenga, C. J. (2023) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2023.105398 · Cited by 29 · see citing works
“In starlings, sleep improved auditory memory (Brawn et al., 2013) and sleep-related vocal changes have been shown in juvenile zebra finches during song learning (Der ´ egnaucourt et al., 2005; Shank and Margoliash, 2009).”
Motor circuits help encode auditory memories of vocal models used to guide vocal learning
Roberts, T. F., & MOONEY, R. D. (2013) · Hearing Research · doi:10.1016/j.heares.2013.01.009 · Cited by 28 · see citing works
“Additionally, complex spontaneous action potential activity also emerges shortly after tutoring in RA (Shank and Margoliash, 2009), presumably reflecting augmented drive from HVC, and the temporal profile of”
InfluentialNeurophysiological Basis of Sleep’s Function on Memory and Cognition
Spencer, R. M. C. (2013) · ISRN Physiology · doi:10.1155/2013/619319 · Cited by 28 · see citing works
“Brawn TP, Nusbaum HC, Margoliash D. Sleep-dependent consolidation of auditory discrimination learning in adult starlings.”
InfluentialBuilding a state space for song learning
Mackevicius, E. L., & Fee, M. S. (2017) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2017.12.001 · Cited by 28 · see citing works
“In support of the latter idea, sleep replay in the song motor system is believed to be important for song learning [63–65], is driven by the auditory system [66,67], and increases dramatically following exposure to tutor song [52].”
BackgroundTokarev, K., Тиунова, А. А., Scharff, C., & Anokhin, K. V. (2011) · PLoS ONE · doi:10.1371/journal.pone.0021157 · Cited by 26 · see citing works
“there is spontaneous bursting activity reminiscent of that during singing [59].”
BackgroundReproductive and diurnal rhythms regulate vocal motor plasticity in a teleost fish
Rubow, T. K., & Bass, A. H. (2009) · Journal of Experimental Biology · doi:10.1242/jeb.032748 · Cited by 26 · see citing works
“, 1998; Schmidt and Konishi, 1998), as well as the role of sleep in song learning (Shank and Margoliash, 2008).”
BackgroundShort Bouts of Vocalization Induce Long-Lasting Fast Gamma Oscillations in a Sensorimotor Nucleus
Lewandowski, B. C., & Schmidt, M. F. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.6809-10.2011 · Cited by 26 · see citing works
“During the first night following exposure to the tutor song, RA neurons transition from being tonically active to becoming more phasic in nature, with a dramatic increase in interspike intervals in the fast gamma range (Shank and Margoliash, 2009).”
BackgroundBudgerigars have complex sleep structure similar to that of mammals
Canavan, S. V., & Margoliash, D. (2020) · PLoS Biology · doi:10.1371/journal.pbio.3000929 · Cited by 25 · see citing works
“…demonstrate a relation between sleep and zebra finch song learning [34,35], studies in adult starlings demonstrate a role of sleep in memory (re)consolidation [37,38], and zebra finch electrophysiological studies demonstrate neuronal bursting [113] and song replay [33,35,36,113] during sleep.”
Self-citationAn in depth view of avian sleep
Beckers, G. J. L., & Rattenborg, N. C. (2014) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2014.07.019 · Cited by 24 · see citing works
van Hasselt, S. J., Rusche, M., Vyssotski, A. L., Verhulst, S., Rattenborg, N. C., & Meerlo, P. (2019) · SLEEP · doi:10.1093/sleep/zsz311 · Cited by 24 · see citing works
“Indeed, there are numerous studies showing that sleep may support the formation of specific memories, not only in mammals but in birds as well [57–59], particularly in relation to song learning [60, 61].”
BackgroundPerformance-Dependent Consolidation of Learned Vocal Changes in Adult Songbirds
Tachibana, R. O., Lee, D., Kai, K., & Kojima, S. (2022) · Journal of Neuroscience · doi:10.1523/jneurosci.1942-21.2021 · Cited by 24 · see citing works
Circuit reactivation dynamically regulates synaptic plasticity in neocortex
Kruskal, P. B., Li, L., & MacLean, J. N. (2013) · Nature Communications · doi:10.1038/ncomms3574 · Cited by 24 · see citing works
“We set out to evaluate the effect of the CDP rule, defined as a scaling factor for STDP determined by the membrane voltage 25ms before a synaptic input (see Methods) on three metrics: (1) the progression of an assembly phase sequence, (2) synaptic potentiation and (3) overall synaptic ‘footprint’ of an assembly.”
MethodHippocampal Contributions to Declarative Memory Consolidation During Sleep
Antony, J. W., & Paller, K. A. (2017) · Springer eBooks · doi:10.1007/978-3-319-50406-3_9 · Cited by 23 · see citing works
“2000); and (4) auditory perceptual learning (Brawn et al. 2010b, 2013; Fenn et al. 2003; Gaab et al. 2004; Shank and Margoliash 2009).”
BackgroundBrain Damage - Bridging Between Basic Research and Clinics
González-Quevedo, A. (2012) · InTech eBooks · doi:10.5772/2174 · Cited by 21 · see citing works
Intrinsic plasticity and birdsong learning
Daou, A., & Margoliash, D. (2021) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2021.107407 · Cited by 24 · see citing works
“A prior study of RA neurons found that extracellular activity changed overnight in a tutor song specific manner following first exposure to the tutor song, and these changes could be suppressed as long as a bird was prevented from hearing feedback from his own singing (Shank and Margoliash, 2009).”
BackgroundSelf-citationvan der Kant, A., Derégnaucourt, S., Gahr, M. L., der Linden, A. V., & Poirier, C. (2013) · PLoS ONE · doi:10.1371/journal.pone.0061764 · Cited by 21 · see citing works
“Playback of tutor song during the day has also been found to induce in juvenile birds specific changes in bursting activity of neurons during the following night of sleep, suggesting again that memory consolidation processes took place during the night [47].”
BackgroundNeuronal Intrinsic Physiology Changes During Development of a Learned Behavior
Ross, M. T., Flores, D., Bertram, R., Johnson, F., & Hyson, R. L. (2017) · eNeuro · doi:10.1523/eneuro.0297-17.2017 · Cited by 21 · see citing works
“There is also evidence that there are developmental changes in synaptic connectivity in RA (Wang and Hessler, 2006; Shank and Margoliash, 2009).”
BackgroundAlcaro, A., & Carta, S. M. (2019) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2018.00522 · Cited by 22 · see citing works
A biological perspective on memory
Crystal, J. D., & Glanzman, D. L. (2013) · Current Biology · doi:10.1016/j.cub.2013.07.082 · Cited by 21 · see citing works
A Bird’s Eye View of Sleep-Dependent Memory Consolidation
Brawn, T. P., & Margoliash, D. (2014) · Current topics in behavioral neurosciences · doi:10.1007/7854_2014_349 · Cited by 20 · see citing works
“A number of recent studies have explored the interaction between interference and sleep consolidation (e.g., Walker et al. 2003; Ellenbogen et al. 2006, 2009; Korman et al. 2007; Drosopoulos et al. 2007; Diekelmann et al. 2011; Alger et al. 2012; Sheth et al. 2012).”
BackgroundSelf-citationFusani, L., & Gahr, M. (2014) · Brain, Behavior and Evolution · doi:10.1159/000367984 · Cited by 20 · see citing works
“song deteriorates after sleep and is recovered during the day, allowing modifications of learned motor patterns [Shank and Margoliash, 2008; Deregnaucourt et al., 2012].”
BackgroundBehavioral state-dependent reconfiguration of song-related network activity and cholinergic systems
Shea, S., & Margoliash, D. (2009) · Journal of Chemical Neuroanatomy · doi:10.1016/j.jchemneu.2009.10.002 · Cited by 15 · see citing works
“Indeed, the developmental appearance of sleep bursting activity in the song motor pathway is conspicuously correlated with exposure to a model song, and first appears on the night before the initiation of imitative learning (Shank and Margoliash, 2009).”
BackgroundSelf-citationNeural Representation of a Target Auditory Memory in a Cortico-Basal Ganglia Pathway
Achiro, J. M., & Bottjer, S. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.0710-13.2013 · Cited by 39 · see citing works
Adult zebra finches rehearse highly variable song patterns during sleep.
Young, B., Mindlin, G. B., Arneodo, E. M., & Goller, F. (2017) · PubMed Central · doi:10.7717/peerj.4052 · Cited by 17 · see citing works
“…of spontaneous Young et al. (2017), PeerJ, DOI 10.7717/peerj.4052 11/18 activity during sleep can be matched to activity during song performance, the absence of spikes and non-matching bursts are difficult to interpret (Dave & Margoliash, 2000; Shank & Margoliash, 2009; Rauske et al., 2010).”
BackgroundInfluentialDaily and developmental modulation of “premotor” activity in the birdsong system
Day, N. F., Kinnischtzke, A. K., Adam, M., & Nick, T. A. (2009) · Developmental Neurobiology · doi:10.1002/dneu.20739 · Cited by 18 · see citing works
“Is sleep required for the resetting of HVC activity, or does it result from a circadian rhythm? Developmental analysis of song behavior has revealed that sleep can reset the song entropy variance (Deregnaucourt et al., 2005; Shank and Margoliash, 2009), which suggests that sleep may be involved in the resetting of HVC…”
BackgroundInfluentialRenaud, J., Dumont, F., Khelfaoui, M., Reibel, S., Letourneur, F., Bienvenu, T., Khwaja, O., Dorseuil, O., & Billuart, P. (2015) · Neuroscience · doi:10.1016/j.neuroscience.2015.08.066 · Cited by 16 · see citing works
Vocal Learning in Songbirds and Humans: A Retrospective in Honor of Peter Marler
Soha, J. A., & Peters, S. S. (2015) · Ethology · doi:10.1111/eth.12415 · Cited by 16 · see citing works
Piristine, H. C., Choetso, T., & Gobes, S. M. H. (2016) · Developmental Neurobiology · doi:10.1002/dneu.22384 · Cited by 15 · see citing works
“Nocturnal bursting activity in the descending motor pathway is driven by the thalamic nucleus Uva and propagates through Nif to HVC and RA (Dave and Margoliash, 2000; Hahnloser et al., 2006; Hahnloser and Fee, 2007; Hahnloser et al., 2008; Shank and Margoliash, 2009; Rauske et al., 2010).”
BackgroundDecomposing the Evolution of Sleep: Comparative and Developmental Approaches
BLUMBERG, M. S., & Rattenborg, N. C. (2016) · Elsevier eBooks · doi:10.1016/b978-0-12-804042-3.00100-7 · Cited by 15 · see citing works
“…song learning, juvenile males attempt to reproduce the song of their father, a gradual process that spans months; interestingly, the quality of the song actually degrades during nightly sleep and improves with waking practice during the day (Deregnaucourt et al., 2005; Shank and Margoliash, 2009).”
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Maximized song learning of juvenile male zebra finches following BDNF expression in the HVC
Dittrich, F., Maat, A. T., Jansen, R. F., Pieneman, A. W., Hertel, M., Frankl‐Vilches, C., & Gahr, M. L. (2013) · European Journal of Neuroscience · doi:10.1111/ejn.12329 · Cited by 15 · see citing works
“Further, enhanced neuronal plasticity at the onset of vocal learning was reported in parts of the descending song production pathway, in the robust nucleus of the arcopallium (RA; Shank & Margoliash, 2009; Sizemore & Perkel, 2011) and in the HVC (letter-based name; Roberts et al., 2010).”
BackgroundA bird's eye view of neural circuit formation
Ölveczky, B. P., & Gardner, T. J. (2010) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2010.08.001 · Cited by 15 · see citing works
“RA neurons during sleep [61 ].”
Hayase, S., & Wada, K. (2018) · European Journal of Neuroscience · doi:10.1111/ejn.14057 · Cited by 14 · see citing works
- Authors
- Shank, S. S., & Margoliash, D.
- Affiliations
- University of Chicago (US)
- Corresponding author
- Margoliash, Daniel
- ORCID
- Margoliash, Daniel
- Venue
- Nature
- Published
- 2008-12-14
- Volume
- 458
- Issue
- 7234
- Pages
- 73-77
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- PMC
- PMC2651989
- OpenAlex
- W1985290816
- Cited by
- 178
- References
- 35
- Citations by year
- 2026: 5 · 2025: 3 · 2024: 13 · 2023: 4 · 2022: 8 · 2021: 7 · 2020: 6 · 2019: 9 · 2018: 3 · 2017: 12 · 2016: 3 · 2015: 8 · 2014: 16 · 2013: 19 · 2012: 12
- FWCI
- 12.19
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- Funders
- National Institute of Mental Health (R01MH059831)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Developmental Biology › Animal Vocal Communication and Behavior
- Life Sciences › Neuroscience › Cognitive Neuroscience › Sleep and Wakefulness Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Keywords
- songbird song, zebra finch, sleep-dependent learning, auditory feedback, tutor song, robust nucleus of the arcopallium, premotor neurons, neuronal bursting, sensorimotor integration, memory consolidation
- MeSH terms
- Acoustic Stimulation, Action Potentials, Animals, Circadian Rhythm, Darkness, Female, Learning, Male, Models, Neurological, Neurons, Mental Recall, Sleep, Vocalization, Animal, Prosencephalon, Entropy, Feedback, Physiological, Finches
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