Dynamics of a Memory Trace: Effects of Sleep on Consolidation
Open accessAbstract
Background There is evidence that sleep is important for memory consolidation, but the underlying neuronal changes are not well understood. We studied the effect of sleep modulation on memory and on neuronal activity in a memory system of the domestic chick brain after the learning process of imprinting. Neurons in this system become, through imprinting, selectively responsive to a training (imprinting) stimulus and so possess the properties of a memory trace.Results The proportion of neurons responsive to the training stimulus reaches a maximum the day after training. We demonstrate that sleep is necessary for this maximum to be achieved, that sleep stabilizes the initially unstable, selective responses of neurons to the imprinting stimulus, and that for sleep to be effective, it must occur during a particular period of time after training. During this period, there is a time-dependent increase in EEG activity in the 5-6 Hz band, that is, in the lower range of the theta bandwidth. The effects of sleep disturbance on consolidation cannot be attributed to fatigue or to stress.Conclusions We establish that long-term trace consolidation requires sleep within a restricted period shortly after learning. Undisturbed sleep is necessary for the stabilization of long-term memory, measured at the behavioral and neuronal levels, and of long-term but not short-term neuronal responsiveness to the training stimulus.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
A more recent study compellingly demonstrated a critical involvement of sleep in consolidation of the imprinting stimulus.
“Results from a more recent study compellingly demonstrated a critical involvement of sleep in the consolidation of the imprinting stimulus (600).”
From About Sleep's Role in Memory (2013) · cites this paper as [600]
Chicks with disturbed sleep in the first 6-h interval after training and undisturbed sleep in the second interval showed no significant memory for the imprinting stimulus and a strong decrease in responsive IMM neurons.
“In contrast, chicks that experienced disturbed sleep in the first 6-h interval after training and undisturbed sleep in the second 6-h interval, at final testing did not exhibit any significant memory for the imprinting stimulus and showed a strong decrease in the number of IMM neurons responsive to the imprinting stimulus.”
From About Sleep's Role in Memory (2013) · cites this paper as [600]
Tracking of individual IMM neurons suggested that sleep shortly after imprinting stabilizes the memory representation by supporting recovery of responsiveness of cells that had ceased to respond, with this effect requiring some hours.
“Interestingly, tracking of individual IMM neurons revealed a pattern suggesting that sleep shortly after imprinting training stabilizes the memory representation by supporting the recovery of responsiveness of cells that for any reasons had ceased to respond to the imprinting stimulus in the course of training or shortly afterwards, with this effect requiring some hours to occur (600, 1150).”
From About Sleep's Role in Memory (2013) · cites this paper as [600]
In that study, final testing after the second sleep period revealed stable memory for the imprinting stimulus and an overall doubled number of IMM neurons responding to the imprinting stimulus compared with before sleep.
“Final testing after the second sleep period revealed a stable memory for the imprinting stimulus together with an overall doubled number of IMM neurons responding to the imprinting stimulus (compared to imprinting training before sleep).”
From About Sleep's Role in Memory (2013) · cites this paper as [600]
Chicks with undisturbed sleep after imprinting displayed an increase in EEG SWA covering the 0-6 Hz frequency band during this period.
“In addition, chicks with undisturbed sleep after imprinting displayed an increase in EEG SWA covering the 0 -6 Hz frequency band during this period.”
From About Sleep's Role in Memory (2013) · cites this paper as [600]
Given that the IMM receives significant hippocampal input, such inputs during sleep may drive stabilization of IMM representations, although hippocampal neurons do not appear to selectively respond to the imprinting stimulus after training.
“Given that the IMM corresponds to parts of the mammalian neocortex receiving significant input from the hippocampus (819, 979), such inputs during sleep may drive the stabilization of IMM representations, although hippocampal neurons do not appear to selectively respond to the imprinting stimulus after training (600, 858).”
From About Sleep's Role in Memory (2013) · cites this paper as [600]
Cites
Statistical principles in experimental design.
Winer, B. J. (1962) · McGraw-Hill Book Company · doi:10.1037/11774-000 · Cited by 27,137 · see citing works
Memory - A century of consolidation
McGaugh, J. L. (2000) · Science · doi:10.1126/science.287.5451.248 · Cited by 4,250 · see citing works
Theta oscillations in the hippocampus
Buzsáki, G. (2002) · Neuron · doi:10.1016/s0896-6273(02)00586-x · Cited by 3,332 · see citing works
The organization of recent and remote memories
Frankland, P. W., & Bontempi, B. (2005) · Nature Reviews Neuroscience · doi:10.1038/nrn1607 · Cited by 2,138 · see citing works
Turner, B. D., & Crawley, M. J. (1994) · Journal of Ecology · doi:10.2307/2261403 · Cited by 2,083 · see citing works
Plasticity of ocular dominance columns in monkey striate cortex
Hubel, D. H., Wiesel, T. N., LeVay, S., Barlow, H. B., & Gaze, R. M. (1977) · Philosophical transactions of the Royal Society of London. Series B, Biological sciences · doi:10.1098/rstb.1977.0050 · Cited by 1,642 · see citing works
Revised nomenclature for avian telencephalon and some related brainstem nuclei
Reiner, A., Perkel, D. J., Bruce, L. L., Butler, A. B., Csillag, A., Kuenzel, W., Medina, L., Paxinos, G., Shimizu, T., Striedter, G., et al. (2004) · Journal of Comparative Neurology · doi:10.1002/cne.20118 · Cited by 1,148 · cited 1× · see citing works
“The IMM probably corresponds to part of the mammalian neocortex [41], receiving sensory inputs from other forebrain areas as well as a projection from the hippocampal region [33, 42].”
BackgroundSleep-Dependent Learning and Memory Consolidation
Walker, M. P., & Stickgold, R. (2004) · Neuron · doi:10.1016/j.neuron.2004.08.031 · Cited by 1,113 · cited 2× · see citing works
“In mammals [2, 3] and birds [4, 5], this process is influenced by periods of sleep.”
BackgroundPolyneuronal innervation of skeletal muscle in new‐born rats and its elimination during maturation.
Brown, M. C., Jansen, J., & van Essen, D. V. (1976) · Journal of Physiology · doi:10.1113/jphysiol.1976.sp011565 · Cited by 789 · see citing works
Self-citationSong presentation induces gene expression in the songbird forebrain.
Mello, C. V., Vicario, D. S., & Clayton, D. F. (1992) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.89.15.6818 · Cited by 615 · see citing works
Sleep Enhances Plasticity in the Developing Visual Cortex
Frank, M. G., Issa, N. P., & Stryker, M. P. (2001) · Neuron · doi:10.1016/s0896-6273(01)00279-3 · Cited by 523 · see citing works
A refined model of sleep and the time course of memory formation
Walker, M. P. (2005) · Behavioral and Brain Sciences · doi:10.1017/s0140525x05000026 · Cited by 466 · see citing works
Song 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
Sleep transforms the cerebral trace of declarative memories
Gais, S., Albouy, G., Boly, M., Dang-Vu, T. T., Darsaud, A., Desseilles, M., Rauchs, G., Schabus, M., Sterpenich, V., Vandewalle, G., et al. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0705454104 · Cited by 412 · see citing works
Vocalization of farm animals as a measure of welfare
Manteuffel, G., Puppe, B., & Schön, P. C. (2004) · Applied Animal Behaviour Science · doi:10.1016/j.applanim.2004.02.012 · Cited by 399 · see citing works
Compartmentalized Synthesis and Degradation of Proteins in Neurons
Steward, O., & Schuman, E. M. (2003) · Neuron · doi:10.1016/s0896-6273(03)00635-4 · Cited by 377 · see citing works
Neural mechanisms of birdsong memory
Bolhuis, J. J., & Gahr, M. L. (2006) · Nature reviews. Neuroscience · doi:10.1038/nrn1904 · Cited by 373 · see citing works
MECHANISMS OF AVIAN IMPRINTING: A REVIEW
Bolhuis, J. J. (1991) · Biological reviews/Biological reviews of the Cambridge Philosophical Society · doi:10.1111/j.1469-185x.1991.tb01145.x · Cited by 359 · see citing works
Memory, Imprinting, and the Brain
Horn, G. (1985) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780198521563.001.0001 · Cited by 344 · see citing works
Self-citationThe Spectrographic Analysis of Sound Signals of the Domestic Fowl
Collias, N. E., & Joos, M. (1953) · Behaviour · doi:10.1163/156853953x00104 · Cited by 329 · see citing works
How sleep affects the developmental learning of bird song
Derégnaucourt, S., Mitra, P. P., Fehér, O., Pytte, C., & Tchernichovski, O. (2005) · Nature · doi:10.1038/nature03275 · Cited by 320 · see citing works
Pathways of the Past: the Imprint of Memory
Horn, G. (2004) · Nature reviews. Neuroscience · doi:10.1038/nrn1324 · Cited by 308 · see citing works
Self-citationMcCabe, B. J., & Horn, G. (1988) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.85.8.2849 · Cited by 298 · see citing works
Self-citationIntegration of biochemical signalling in spines
Kennedy, M. B., Beale, H. C., Carlisle, H. J., & Washburn, L. R. (2005) · Nature Reviews Neuroscience · doi:10.1038/nrn1685 · Cited by 286 · see citing works
Development of Brain and Behaviour in the Chicken
Rogers, L. J. (1995) · CABI eBooks · doi:10.1079/9780851989242.0000 · Cited by 270 · see citing works
AMPA receptor trafficking and long-term potentiation
Malinow, R. (2003) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2002.1233 · Cited by 248 · see citing works
The GLIM System Release 3: Generalized Linear Interactive Modeling.
McCullagh, P. J., Baker, R. J., & Nelder, J. A. (1979) · Journal of the American Statistical Association · doi:10.2307/2286440 · Cited by 231 · see citing works
Half-awake to the risk of predation
Rattenborg, N. C., Lima, S. L., & Amlaner, C. J. (1999) · Nature · doi:10.1038/17037 · Cited by 222 · see citing works
God's Organism? The Chick as a Model System for Memory StudiesPreprint
Rose, S. P. R. (2000) · Learning & Memory · doi:10.1101/lm.7.1.1 · Cited by 209 · see citing works
Changes in the structure of synapses associated with learning
Horn, G., Bradley, P. M., & Bj, M. (1985) · Journal of Neuroscience · doi:10.1523/jneurosci.05-12-03161.1985 · Cited by 155 · see citing works
Self-citationMcCabe, B. J., Horn, G., & Bateson, P. P. G. (1981) · Brain Research · doi:10.1016/0006-8993(81)90717-4 · Cited by 153 · see citing works
Self-citationActivity-Induced Rapid Synaptic Maturation Mediated by Presynaptic Cdc42 Signaling
Shen, W., Wu, B., Zhang, Z., Dou, Y., Rao, Z., Chen, Y., & Duan, S. (2006) · Neuron · doi:10.1016/j.neuron.2006.03.017 · Cited by 133 · see citing works
Imprinting: An electron microscopic study of chick hyperstriatum ventrale
Bradley, P., Horn, G., & Bateson, P. (1981) · Experimental Brain Research · doi:10.1007/bf00236600 · Cited by 125 · see citing works
Self-citation‘Deaf, mute and whispering’ silent synapses: their role in synaptic plasticity
Voronin, L. L., & Cherubini, E. (2004) · The Journal of Physiology · doi:10.1113/jphysiol.2003.058966 · Cited by 125 · see citing works
The Effects of Prior Exposure To Light On the Imprinting Process in Domestic Chicks
Bateson, P., & Wainwright, A. A. P. (1972) · Behaviour · doi:10.1163/156853972x00310 · Cited by 114 · see citing works
McCabe, B. J., Cipolla‐Neto, J., Horn, G., & Bateson, P. (1982) · Experimental Brain Research · doi:10.1007/bf00239568 · Cited by 110 · see citing works
Self-citationVocalisation in chicks (Gallus gallus dom.) during stepwise social isolation
Marx, G., Leppelt, J., & Ellendorff, F. (2001) · Applied Animal Behaviour Science · doi:10.1016/s0168-1591(01)00180-0 · Cited by 101 · see citing works
Norman, K. A., Newman, E. L., & Perotte, R. (2005) · Neural Networks · doi:10.1016/j.neunet.2005.08.010 · Cited by 90 · see citing works
McCabe, B. J., & Horn, G. (1991) · Behavioral Neuroscience · doi:10.1037//0735-7044.105.2.289 · Cited by 64 · see citing works
Self-citationNicol, A. U., Brown, M. W., & Horn, G. (1995) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.1995.tb00680.x · Cited by 63 · see citing works
Self-citationThe development of brain and behaviour in the chicken
Bolhuis, J. J. (1995) · Trends in Neurosciences · doi:10.1016/0166-2236(95)90051-9 · Cited by 62 · see citing works
Horn, G., Nicol, A. U., & Brown, M. W. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.091094798 · Cited by 61 · see citing works
Self-citationBrown, M. W., & Horn, G. (1994) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.1994.tb01009.x · Cited by 59 · see citing works
Self-citationMcCabe, B. J., & Horn, G. (1991) · Behavioral Neuroscience · doi:10.1037/0735-7044.105.2.289 · Cited by 59 · see citing works
Self-citationSilent synapses: what are they telling us about long-term potentiation?
Kullmann, D. M. (2003) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2002.1229 · Cited by 51 · see citing works
Neural cell adhesion molecules, learning, and memory in the domestic chick.
Solomonia, R. O., McCabe, B. J., & Horn, G. (1998) · Behavioral Neuroscience · doi:10.1037/0735-7044.112.3.646 · Cited by 49 · see citing works
Self-citationLight exposure of the chick embryo influences monocular sleep
Bobbo, D., Galvani, F., Mascetti, G. G., & Vallortígara, G. (2002) · Behavioural Brain Research · doi:10.1016/s0166-4328(02)00059-1 · Cited by 36 · see citing works
Solomonia, R. O., Morgan, K., Kotorashvili, A., McCabe, B. J., Jackson, A. P., & Horn, G. (2003) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2003.02539.x · Cited by 32 · see citing works
Self-citationDavies, D. C., & Horn, G. (1983) · Neuroscience Letters · doi:10.1016/0304-3940(83)90024-1 · Cited by 29 · see citing works
Self-citationNeural encoding of subject–object distance in a visual recognition system
Nicol, Brown, & Horn (1998) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.1998.00002.x · Cited by 15 · see citing works
The electroencephalogram and sleep in the domestic chicken
Ookawa, T. (2004) · Avian and Poultry Biology Reviews · doi:10.3184/147020604783637453 · Cited by 13 · see citing works
Bredenkötter, M., & Braun, K. (2000) · Neurobiology of Learning and Memory · doi:10.1006/nlme.1999.3923 · Cited by 12 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Rasch, B., & Born, J. (2013) · Physiological Reviews · doi:10.1152/physrev.00032.2012 · Cited by 2,783 · see citing works
“Interestingly, tracking of individual IMM neurons revealed a pattern suggesting that sleep shortly after imprinting training stabilizes the memory representation by supporting the recovery of responsiveness of cells that for any reasons had ceased to respond to the imprinting stimulus in the course of training or shor…”
BackgroundInfluentialSleep 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
Decoding material-specific memory reprocessing during sleep in humans
Schönauer, M., Alizadeh, S., Jamalabadi, H., Abraham, A., Pawlizki, A., & Gais, S. (2017) · Nature Communications · doi:10.1038/ncomms15404 · Cited by 139 · see citing works
Rattenborg, N. C., Martı́nez-González, D., & Lesku, J. A. (2008) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2008.08.010 · Cited by 134 · see citing works
Poe, G. R. (2017) · Journal of Neuroscience · doi:10.1523/jneurosci.0820-16.2017 · Cited by 130 · see citing works
Yang, G., & Gan, W. (2011) · Developmental Neurobiology · doi:10.1002/dneu.20996 · Cited by 123 · see citing works
Steinmeyer, C., Schielzeth, H., Mueller, J. C., & Kempenaers, B. (2010) · Animal Behaviour · doi:10.1016/j.anbehav.2010.08.005 · Cited by 122 · see citing works
Hippocampal memory consolidation during sleep: a comparison of mammals and birds
Rattenborg, N. C., Martı́nez-González, D., Roth, T. C., & Витальевич, П. В. (2010) · Biological reviews/Biological reviews of the Cambridge Philosophical Society · doi:10.1111/j.1469-185x.2010.00165.x · Cited by 121 · see citing works
Sleep, clocks, and synaptic plasticity
Frank, M. G., & Cantera, R. (2014) · Trends in Neurosciences · doi:10.1016/j.tins.2014.06.005 · Cited by 118 · see citing works
Local sleep homeostasis in the avian brain: convergence of sleep function in mammals and birds?
Lesku, J. A., Vyssotski, A. L., Martinez-Gonzalez, D., Wilzeck, C., & Rattenborg, N. C. (2011) · Proceedings of the Royal Society B: Biological Sciences · doi:10.1098/rspb.2010.2316 · Cited by 112 · see citing works
Sleep function: current questions and new approaches
Vassalli, A., & Dijk, D. (2009) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2009.06767.x · Cited by 110 · see citing works
Sleep, synaptic connectivity, and hippocampal memory during early development
Huber, R., & Jan Born, A. (2014) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2013.12.005 · Cited by 101 · see citing works
Sara, S. J. (2017) · Journal of Neuroscience · doi:10.1523/jneurosci.0297-16.2017 · Cited by 100 · see citing works
Sleep, plasticity, and sensory neurodevelopment
Blumberg, M. S., Dooley, J. C., & Tiriac, A. (2022) · Neuron · doi:10.1016/j.neuron.2022.08.005 · Cited by 93 · see citing works
Memory in the making: localized brain activation related to song learning in young songbirds
Gobes, S. M. H., Zandbergen, M. A., & Bolhuis, J. J. (2010) · Proceedings of the Royal Society B: Biological Sciences · doi:10.1098/rspb.2010.0870 · Cited by 91 · see citing works
Birdsong memory and the brain: In search of the template
Bolhuis, J. J., & Moorman, S. (2014) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2014.11.019 · Cited by 84 · see citing works
The ecological relevance of sleep: the trade-off between sleep, memory and energy conservation
Roth, T. C., Rattenborg, N. C., & Витальевич, П. В. (2010) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2009.0209 · Cited by 79 · see citing works
Honeybees consolidate navigation memory during sleep
Beyaert, L., Greggers, U., & Menzel, R. (2012) · Journal of Experimental Biology · doi:10.1242/jeb.075499 · Cited by 60 · see citing works
Visual Imprinting in Birds: Behavior, Models, and Neural Mechanisms
McCabe, B. J. (2019) · Frontiers in Physiology · doi:10.3389/fphys.2019.00658 · Cited by 55 · see citing works
Self-citationSleep-Dependent Consolidation of Auditory Discrimination Learning in Adult Starlings
Brawn, T. P., Nusbaum, H. C., & Margoliash, D. (2010) · The Journal of Neuroscience · doi:10.1523/jneurosci.4237-09.2010 · Cited by 55 · see citing works
In search of a recognition memory engram
Brown, M. W., & Banks, P. J. (2014) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2014.09.016 · Cited by 56 · see citing works
Self-citationMcCabe, B. J. (2013) · Wiley Interdisciplinary Reviews Cognitive Science · doi:10.1002/wcs.1231 · Cited by 52 · see citing works
Self-citationThe Ontogenesis of Mammalian Sleep: Form and Function
Frank, M. G. (2020) · Current Sleep Medicine Reports · doi:10.1007/s40675-020-00190-y · Cited by 55 · see citing works
Molecular mechanisms of memory in imprinting
Solomonia, R. O., & McCabe, B. J. (2014) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2014.09.013 · Cited by 46 · see citing works
Self-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
Sleep loss impairs cognitive performance and alters song output in Australian magpies
Johnsson, R. D., Connelly, F., Mussoi, J. G., Vyssotski, A. L., Cain, K. E., Roth, T. C., & Lesku, J. A. (2022) · Scientific Reports · doi:10.1038/s41598-022-10162-7 · Cited by 39 · see citing works
Memory-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
Self-citationLearning-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
An 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
Avian Versus Mammalian Sleep: the Fruits of Comparing Apples and Oranges
Rattenborg, N. C., & Martı́nez-González, D. (2014) · Current Sleep Medicine Reports · doi:10.1007/s40675-014-0001-9 · Cited by 23 · see citing works
Wellmann, A. E., & Downs, C. T. (2008) · Animal Behaviour · doi:10.1016/j.anbehav.2008.09.010 · Cited by 22 · 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
Stability and individual variability of social attachment in imprinting
Lemaire, B., Rucco, D., Josserand, M., Vallortígara, G., & Versace, E. (2021) · Scientific Reports · doi:10.1038/s41598-021-86989-3 · Cited by 20 · see citing works
Mitochondrial proteins, learning and memory: biochemical specialization of a memory system
Solomonia, R. O., Kunelauri, N., Mikautadze, E., Apkhazava, D., McCabe, B. J., & Horn, G. (2011) · Neuroscience · doi:10.1016/j.neuroscience.2011.07.053 · Cited by 20 · see citing works
Self-citationOffline Improvement in Learning to Read a Novel Orthography Depends on Direct Letter Instruction
Bitan, T., & Booth, J. R. (2012) · Cognitive Science · doi:10.1111/j.1551-6709.2012.01234.x · Cited by 19 · see citing works
Taylor, L. A., Thawley, C. J., Pertuit, O. R., Dennis, A. J., Carson, I. R., Tang, C., & Johnson, M. A. (2022) · Physiology & Behavior · doi:10.1016/j.physbeh.2022.113992 · Cited by 18 · see citing works
Solomonia, R. O., Meparishvili, M., Mikautadze, E., Kunelauri, N., Aphkhazava, D., & McCabe, B. J. (2013) · Experimental Brain Research · doi:10.1007/s00221-013-3435-2 · Cited by 18 · see citing works
Self-citationDecomposing 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
Ontogenetic development of magnetic compass orientation in domestic chickens ( Gallus gallus )
Denzau, S., Nießner, C., Rogers, L. J., & Wiltschko, W. (2013) · Journal of Experimental Biology · doi:10.1242/jeb.088815 · Cited by 14 · see citing works
Sleep-dependent reconsolidation after memory destabilization in starlings
Brawn, T. P., Nusbaum, H. C., & Margoliash, D. (2018) · Nature Communications · doi:10.1038/s41467-018-05518-5 · Cited by 14 · see citing works
Liu, C., Zhou, J., Yang, X., Lv, J., Shi, Y., & Zeng, X. (2015) · PubMed Central · Cited by 14 · see citing works
Neuronal Plasticity and Multisensory Integration in Filial Imprinting
Town, S. M., & McCabe, B. J. (2011) · PLoS ONE · doi:10.1371/journal.pone.0017777 · Cited by 12 · see citing works
Self-citationZanon, M., Lemaire, B., & Vallortígara, G. (2021) · Biological Cybernetics · doi:10.1007/s00422-021-00886-6 · Cited by 12 · see citing works
Does artificial light pollution impair problem‐solving success in peafowl?
Yorzinski, J. L., Ordonez, K., & Chema, K. T. (2017) · Ethology · doi:10.1111/eth.12658 · Cited by 12 · see citing works
Importance of sleep for avian vocal communication
Mussoi, J. G., Stanley, M. C., & Cain, K. E. (2022) · Biology Letters · doi:10.1098/rsbl.2022.0223 · Cited by 12 · see citing works
Rapid induction of the immediate early gene c-fos in a chick forebrain system involved in memory
Suge, R., Kato, H., & McCabe, B. (2009) · Experimental Brain Research · doi:10.1007/s00221-009-2006-z · Cited by 11 · see citing works
Self-citationA Review on Agronomic, Phytochemical and Pharmacological Aspects of Cannabis (Cannabis sativa L.)
Asadi, S., Moghadam, H., Badi, H. N., Badi, H. N., Naghavi, M. R., & Salami, S. O. (2019) · Journal of Medicinal Plants · doi:10.29252/jmp.2.70.1 · Cited by 11 · see citing works
Olfactory bulb encoding during learning under anesthesia
Nicol, A. U., Sánchez-Andrade, G., Collado, P., Segonds-Pichon, A., & Kendrick, K. M. (2014) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2014.00193 · Cited by 10 · see citing works
Self-citationSleep, memory, and molecular neurobiology
Smith, C. T., & Peters, K. R. (2010) · Handbook of clinical neurology · doi:10.1016/b978-0-444-52006-7.00017-4 · Cited by 11 · see citing works
Neural mechanisms of vocal imitation: The role of sleep replay in shaping mirror neurons
Giret, N., Edeline, J., & Negro, C. D. (2017) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2017.01.051 · Cited by 11 · see citing works
Sleep: The Ebb and Flow of Memory Consolidation
Stickgold, R. (2008) · Current Biology · doi:10.1016/j.cub.2008.03.022 · Cited by 10 · see citing works
Divergent neuronal activity patterns in the avian hippocampus and nidopallium
van der Meij, J., Rattenborg, N. C., & Beckers, G. J. L. (2020) · European Journal of Neuroscience · doi:10.1111/ejn.14675 · Cited by 10 · see citing works
Aton, S., Seibt, J., & Frank, M. G. (2009) · Wiley eBooks · doi:10.1002/9780470015902.a0021395 · Cited by 10 · see citing works
Aton, S. J., Seibt, J., & Frank, M. G. (2014) · Wiley eBooks · doi:10.1002/9780470015902.a0021395.pub2 · Cited by 8 · see citing works
Yeganegi, H., & Ondracek, J. M. (2023) · Scientific Reports · doi:10.1038/s41598-023-35160-1 · Cited by 7 · see citing works
A bird's-eye view of the function of sleep
Rattenborg, N. C., & Amlaner, C. J. (2001) · Cambridge University Press eBooks · doi:10.1017/cbo9780511642074.008 · Cited by 7 · see citing works
Mechanisms of recognition in birds and social Hymenoptera: from detection to information processing
Rossi, N., & Derégnaucourt, S. (2020) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2019.0483 · Cited by 6 · see citing works
Evolution of sleep in relation to memory – a birds’ brain view
van der Meij, J., Ungurean, G., Rattenborg, N. C., & Beckers, G. J. L. (2020) · Current Opinion in Behavioral Sciences · doi:10.1016/j.cobeha.2019.12.004 · Cited by 5 · see citing works
The Role of Sleep in Song Learning Processes in Songbird
Giret, N. (2019) · Handbook of behavioral neuroscience · doi:10.1016/b978-0-12-813743-7.00026-8 · Cited by 5 · see citing works
The influence of sleep disruption on learning and memory in fish
Sowersby, W., Kobayashi, T., Awata, S., Sogawa, S., & Kohda, M. (2025) · Journal of Sleep Research · doi:10.1111/jsr.70005 · Cited by 4 · see citing works
The effects of sleep disturbance on a songbird’s vocal performance
Mussoi, J. G., MacQueen, R. A., Stanley, M. C., Li, S., Quann, C. T., & Cain, K. E. (2025) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2025.1409 · Cited by 4 · see citing works
The effect of food quality during growth on spatial memory consolidation in adult pigeons
Scriba, M. F., Gasparini, J., Jacquin, L., Mettke‐Hofmann, C., Rattenborg, N. C., & Roulin, A. (2016) · Journal of Experimental Biology · doi:10.1242/jeb.152454 · Cited by 4 · see citing works
A Role for Neuronal Oscillations of Sleep in Memory and Cognition
Marshall, L. (2020) · Springer eBooks · doi:10.1007/978-1-0716-0653-7_7 · Cited by 4 · see citing works
Bird Brains Key to the Functions of Sleep
Gobes, S. M. H., & Bolhuis, J. J. (2008) · Science · doi:10.1126/science.322.5909.1789a · Cited by 3 · see citing works
Sleep is required for odor exposure to consolidate memory and remodel olfactory synapsesPreprint
Chandra, R., Farah, F., Muñoz-Lobato, F., Bokka, A., Benedetti, K. L., Brueggemann, C., Saifuddin, F. A., Miller, J. M., Li, J., Chang, E., et al. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.11.24.395228 · Cited by 3 · see citing works
Bolhuis, J. J., & Johnson, M. H. (2012) · Current Biology · doi:10.1016/j.cub.2012.10.050 · Cited by 2 · see citing works
Brain, memory and development: The imprint of Gabriel Horn
Bolhuis, J. J., Brown, M. W., & Johnson, M. H. (2015) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2015.02.001 · Cited by 2 · see citing works
Self-citationQuercia, A., Bobbo, D., & Mascetti, G. G. (2017) · Laterality Asymmetries of Body Brain and Cognition · doi:10.1080/1357650x.2017.1347180 · Cited by 2 · see citing works
Understanding Sleep and Memory in the Avian Brain
Ondracek, J. M. (2026) · Journal of Integrative Neuroscience · doi:10.31083/jin50421 · Cited by 1 · see citing works
The role of REM sleep in maintaining neuronal excitability and its possible mechanism of action
Madan, V., & Mallick, B. N. (2011) · Cambridge University Press eBooks · doi:10.1017/cbo9780511921179.038 · Cited by 1 · see citing works
Svarnik, О. E., Alexandrov, Y. I., & Anokhin, K. V. (2015) · Journal of Behavioral and Brain Science · doi:10.4236/jbbs.2015.53006 · Cited by 1 · see citing works
Sleep sculpts circuits in every species studied
Poe, G. R., & Donlea, J. M. (2023) · Cell · doi:10.1016/j.cell.2023.05.042 · Cited by 1 · see citing works
Animal models for cognitive deficits induced by sleep deprivation
Seugnet, L., & Salin, P. A. (2013) · Cambridge University Press eBooks · doi:10.1017/cbo9781139649469.019 · Cited by 1 · see citing works
Hippocampal neural firing dynamics during sleep
Grosmark, A. (2014) · doi:10.7282/t3k072j1 · Cited by 1 · see citing works
Effects of Sleep Fragmentation on the Immune System of Zebra Finches Using Cytokine Gene Expression
Cooper, L. N. (2016) · TopSCHOLAR (Western Kentucky University) · Cited by 1 · see citing works
Ungurean, G., Lesku, J. A., & Rattenborg, N. C. (2021) · Elsevier eBooks · doi:10.1016/b978-0-12-822963-7.00081-5 · Cited by 1 · see citing works
Lesku, J. A., & Rattenborg, N. C. (2013) · Elsevier eBooks · doi:10.1016/b978-0-12-378610-4.00012-7 · Cited by 1 · see citing works
Sleepphysiology and homeostasis
Shaw, P. J., Tafti, M., & Thorpy, M. J. (2013) · Cambridge University Press eBooks · doi:10.1017/cbo9781139649469.016
Taylor, L. A. (2020) · Digital Commons - Trinity University (Trinity University)
(2017) · Routledge eBooks · doi:10.1201/b22117-11
Neural Mechanisms of Imprinting
McCabe, B. J. (2020) · Elsevier eBooks · doi:10.1016/b978-0-12-809324-5.23954-0
Self-citationBolhuis, J. J. (2010) · The Corsini Encyclopedia of Psychology · doi:10.1002/9780470479216.corpsy0435
Developmental and comparative insights into the origins and functions of sleep
BLUMBERG, M. S., Ungurean, G., & Rattenborg, N. C. (2025) · Elsevier eBooks · doi:10.1016/b978-0-443-27380-3.00031-2
Johnsson, R. D., Semenov, G. А., Rice, A. M., Taylor, S. A., & Roth, T. C. (2025) · Biological reviews/Biological reviews of the Cambridge Philosophical Society · doi:10.1111/brv.70083
The Role of Vision on Neural Mechanisms for Sensory Processing and Spatial Representation
Vitali, H., & Gori, M. (2025) · Signals and communication technology · doi:10.1007/978-3-031-91550-5_5
Filial Imprinting: Behaviour and Neurobiology
McCabe, B. J. (2026) · Behavioral Sciences · doi:10.3390/bs16050741
Self-citation
- Authors
- Jackson, C., McCabe, B. J., Nicol, A. U., Grout, A. S., Brown, M. W., & Horn, G.
- Affiliations
- University of Cambridge (GB)
- Babraham Institute (GB)
- University of Bristol (GB)
- Corresponding author
- McCabe, Brian J.
- Venue
- Current Biology
- Publisher
- Elsevier BV
- Published
- 2008-03
- Volume
- 18
- Issue
- 6
- Pages
- 393-400
- ISSN
- 0960-9822 (ISSN-L)
- OpenAlex
- W2067697035
- Cited by
- 88
- References
- 52
- Citations by year
- 2026: 2 · 2025: 5 · 2023: 2 · 2022: 4 · 2021: 4 · 2020: 8 · 2019: 4 · 2018: 1 · 2017: 7 · 2016: 3 · 2015: 4 · 2014: 13 · 2013: 7 · 2012: 4
- FWCI
- 3.27
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Current Biology (publishedVersion)
- PubMed (publishedVersion)
- Explore Bristol Research (submittedVersion)
- Bristol Research (University of Bristol) (submittedVersion)
- Funders
- Biotechnology and Biological Sciences Research Council (S18043)
- 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, memory consolidation, memory traces, imprinting, domestic chicks, neuronal responsiveness, theta oscillations, sleep timing, sleep disorders, long-term memory
- MeSH terms
- Animals, Chickens, Electroencephalography, Imprinting, Psychological, Neurons, Sleep, Time Factors, Vocalization, Animal, Recognition, Psychology
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
