The dialogue between cortex and hippocampus is known to be crucial for sleep-dependent memory consolidation. During slow wave sleep, memory replay depends on slow oscillation (SO) and spindles in the (neo)cortex and sharp wave-ripples (SWRs) in the hippocampus. The mechanisms underlying interaction of these rhythms are poorly understood. We examined the interaction between cortical SO and hippocampal SWRs in a model of the hippocampo-cortico-thalamic network and compared the results with human intracranial recordings during sleep. We observed that ripple occurrence peaked following the onset of an Up-state of SO and that cortical input to hippocampus was crucial to maintain this relationship. A small fraction of ripples occurred during the Down-state and controlled initiation of the next Up-state. We observed that the effect of ripple depends on its precise timing, which supports the idea that ripples occurring at different phases of SO might serve different functions, particularly in the context of encoding the new and reactivation of the old memories during memory consolidation. The study revealed complex bidirectional interaction of SWRs and SO in which early hippocampal ripples influence transitions to Up-state, while cortical Up-states control occurrence of the later ripples, which in turn influence transition to Down-state.

Battelle Center for Mathematical Medicine Abigail Wexner Research Institute at Nationwide Children's Hospital Columbus OH 43215 USA

Canadian Centre for Behavioural Neuroscience University of Lethbridge Lethbridge AB T1K4G9 Canada

Department of Medicine University of California San Diego La Jolla CA 92093 USA

Department of Pediatrics and Biophysics Graduate Program Ohio State University Columbus OH 43215 USA

Department of Radiology University of California San Diego La Jolla CA 92093 USA

Epilepsy Center Cleveland Clinic Cleveland OH 44195 USA

Institute of Computer Science of the Czech Academy of Sciences Prague 18207 Czech Republic

Neurosciences Graduate Program University of California San Diego La Jolla 92093 USA

Zobrazit více v PubMed

Averbeck BB, Seo M. 2008. The statistical neuroanatomy of frontal networks in the macaque. PLoS Comput Biol. 4:e1000050. PubMed PMC

Barbas H, Blatt GJ. 1995. Topographically specific hippocampal projections target functionally distinct prefrontal areas in the rhesus monkey. Hippocampus. 5:511–533. PubMed

Battaglia FP, Sutherland GR, McNaughton BL. 2004. Hippocampal sharp wave bursts coincide with neocortical “Up-state” transitions. Learn Memory. 11:697–704. PubMed PMC

Batterink LJ, Creery JD, Paller KA. 2016. Phase of spontaneous slow oscillations during sleep influences memory-related processing of auditory cues. J Neurosci. 36:1401–1409. PubMed PMC

Bazhenov M, Timofeev I, Steriade M, Sejnowski TJ. 2002. Model of thalamocortical slow-wave sleep oscillations and transitions to activated states. J Neurosci. 22:8691–8704. PubMed PMC

Benjamini Y, Hochberg Y. 1995. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J Royal Stat Soc Ser B (Methodological). 57:289–300.

Bi GQ, Poo MM. 2001. Synaptic modification by correlated activity: Hebb’s postulate revisited. Annu Rev Neurosci. 24:139–166. PubMed

Binder S, Mölle M, Lippert M, Bruder R, Aksamaz S, Ohl F, Wiegert JS, Marshall L. 2019. Monosynaptic hippocampal–prefrontal projections contribute to spatial memory consolidation in mice. J Neurosci. 39:6978–6991. PubMed PMC

Buzsáki G. 1996. The hippocampo–neocortical dialogue. Cereb Cortex 6:81–92. PubMed

Buzsáki G. 2015. Hippocampal sharp wave-ripple: a cognitive biomarker for episodic memory and planning. Hippocampus. 25:1073–1188. PubMed PMC

Carmichael S, Price JL. 1995. Limbic connections of the orbital and medial prefrontal cortex in macaque monkeys. J Comp Neurol. 363:615–641. PubMed

Cavada C, Compañy T, Tejedor J, Cruz-Rizzolo RJ, Reinoso-Suárez F. 2000. The anatomical connections of the macaque monkey orbitofrontal cortex. A review. Cereb Cortex. 10:220–242. PubMed

Cavada C, Llamas A, Reinoso-Suárez F. 1983. Allocortical afferent connections of the prefrontal cortex of the cat. Brain Res. 260:117–120. PubMed

Cenquizca LA, Swanson LW. 2007. Spatial organization of direct hippocampal field CA1 axonal projections to the rest of the cerebral cortex. Brain Res Rev. 56:1–26. PubMed PMC

Chauvette S, Seigneur J, Timofeev I. 2012. Sleep oscillations in the thalamocortical system induce long-term neuronal plasticity. Neuron. 75:1105–1113. PubMed PMC

Chen JY, Chauvette S, Skorheim S, Timofeev I, Bazhenov M. 2012. Interneuron-mediated inhibition synchronizes neuronal activity during slow oscillation. J Physiol. 590:3987–4010. PubMed PMC

Clemens Z, Mölle M, Erőss L, Barsi P, Halász P, Born J. 2007. Temporal coupling of parahippocampal ripples, sleep spindles and slow oscillations in humans. Brain. 130:2868–2878. PubMed

Dégenètais E, Thierry AM, Glowinski J, Gioanni Y. 2003. Synaptic influence of hippocampus on pyramidal cells of the rat prefrontal cortex: an in vivo intracellular recording study. Cereb Cortex. 13:782–792. PubMed

Diekelmann S, Born J. 2010. The memory function of sleep. Nat Rev Neurosci. 11:114. PubMed

Dykstra AR, Chan AM, Quinn BT, Zepeda R, Keller CJ, Cormier J, Madsen JR, Eskandar EN, Cash SS. 2012. Individualized localization and cortical surface-based registration of intracranial electrodes. Neuroimage. 59:3563–3570. PubMed PMC

Ego-Stengel V, Wilson MA. 2010. Disruption of ripple-associated hippocampal activity during rest impairs spatial learning in the rat. Hippocampus. 20:1–10. PubMed PMC

Euston DR, Tatsuno M, McNaughton BL. 2007. Fast-forward playback of recent memory sequences in prefrontal cortex during sleep. Science. 318:1147–1150. PubMed

Ferino F, Thierry A, Glowinski J. 1987. Anatomical and electrophysiological evidence for a direct projection from ammon’s horn to the medial prefrontal cortex in the rat. Exp Brain Res. 65:421–426. PubMed

Frankland PW, Bontempi B. 2005. The organization of recent and remote memories. Nat Rev Neurosci. 6:119–130. PubMed

Gabbott P, Headlam A, Busby S. 2002. Morphological evidence that CA1 hippocampal afferents monosynaptically innervate PV-containing neurons and NADPH-diaphorase reactive cells in the medial prefrontal cortex (areas 25/32) of the rat. Brain Res. 946:314–322. PubMed

Genzel L, Kroes MC, Dresler M, Battaglia FP. 2014. Light sleep versus slow wave sleep in memory consolidation: a question of global versus local processes? Trends Neurosci. 37:10–19. PubMed

Gervasoni D, Lin SC, Ribeiro S, Soares ES, Pantoja J, Nicolelis MA. 2004. Global forebrain dynamics predict rat behavioral states and their transitions. J Neurosci. 24:11137–11147. PubMed PMC

Girardeau G, Benchenane K, Wiener SI, Buzsáki G, Zugaro MB. 2009. Selective suppression of hippocampal ripples impairs spatial memory. Nat Neurosci. 12:1222–1223. PubMed

Goldman-Rakic P, Selemon L, Schwartz M. 1984. Dual pathways connecting the dorsolateral prefrontal cortex with the hippocampal formation and parahippocampal cortex in the rhesus monkey. Neuroscience. 12:719–743. PubMed

González OC, Sokolov Y, Krishnan GP, Bazhenov M. 2020. Can sleep protect memories from catastrophic forgetting? Elife. 9:e51005. PubMed PMC

Gonzalez-Martinez J, Bulacio J, Alexopoulos A, Jehi L, Bingaman W, Najm I. 2013. Stereoelectroencephalography in the “difficult to localize” refractory focal epilepsy: early experience from a north American epilepsy center. Epilepsia. 54:323–330. PubMed

Hahn TT, Sakmann B, Mehta MR. 2007. Differential responses of hippocampal subfields to cortical up–down states. Proc Natl Acad Sci. 104:5169–5174. PubMed PMC

Hauer BE, Pagliardini S, Dickson CT. 2019. The reuniens nucleus of the thalamus has an essential role in coordinating slow-wave activity between neocortex and hippocampus. eNeuro. 6. PubMed PMC

Helfrich RF, Lendner JD, Mander BA, Guillen H, Paff M, Mnatsakanyan L, Vadera S, Walker MP, Lin JJ, Knight RT. 2019. Bidirectional prefrontal–hippocampal dynamics organize information transfer during sleep in humans. Nat Commun. 10:1–16. PubMed PMC

Hoover WB, Vertes RP. 2012. Collateral projections from nucleus reuniens of thalamus to hippocampus and medial prefrontal cortex in the rat: a single and double retrograde fluorescent labeling study. Brain Struct Funct. 217:191–209. PubMed

Inostroza M, Born J. 2013. Sleep for preserving and transforming episodic memory. Annu Rev Neurosci. 36:79–102. PubMed

Irle E, Markowitsch H. 1982. Widespread cortical projections of the hippocampal formation in the cat. Neuroscience. 7:2637–2647. PubMed

Isomura Y, Sirota A, Özen S, Montgomery S, Mizuseki K, Henze DA, Buzsáki G. 2006. Integration and segregation of activity in entorhinal–hippocampal subregions by neocortical slow oscillations. Neuron. 52:871–882. PubMed

Ito HT, Zhang SJ, Witter MP, Moser EI, Moser MB. 2015. A prefrontal–thalamo–hippocampal circuit for goal-directed spatial navigation. Nature. 522:50. PubMed

Ji D, Wilson MA. 2007. Coordinated memory replay in the visual cortex and hippocampus during sleep. Nat Neurosci. 10:100. PubMed

Jiang X, Gonzalez-Martinez J, Cash SS, Chauvel P, Gale J, Halgren E. 2020. Improved identification and differentiation from epileptiform activity of human hippocampal sharp wave ripples during NREM sleep. Hippocampus. 30:610–622. PubMed

Jiang X, Gonzalez-Martinez J, Halgren E. 2019a. Coordination of human hippocampal sharpwave ripples during NREM sleep with cortical theta bursts, spindles, downstates, and upstates. J Neurosci. 39:8744–8761. PubMed PMC

Jiang X, Gonzalez-Martinez J, Halgren E. 2019b. Posterior hippocampal spindle ripples co-occur with neocortical theta bursts and downstates-upstates, and phase-lock with parietal spindles during NREM sleep in humans. J Neurosci. 39:8949–8968. PubMed PMC

Jiang X, Shamie I, Doyle WK, Friedman D, Dugan P, Devinsky O, Eskandar E, Cash SS, Thesen T, Halgren E. 2017. Replay of large-scale spatio-temporal patterns from waking during subsequent NREM sleep in human cortex. Sci Rep. 7:1–17. PubMed PMC

Johnson LA, Euston DR, Tatsuno M, McNaughton BL. 2010. Stored-trace reactivation in rat prefrontal cortex is correlated with Down-to-Up state fluctuation density. J Neurosci. 30:2650–2661. PubMed PMC

Kim J, Gulati T, Ganguly K. 2019. Competing roles of slow oscillations and delta waves in memory consolidation versus forgetting. Cell. 179:514–526. PubMed PMC

Krishnan GP, Chauvette S, Shamie I, Soltani S, Timofeev I, Cash SS, Halgren E, Bazhenov M. 2016. Cellular and neurochemical basis of sleep stages in the thalamocortical network. Elife. 5. PubMed PMC

Kudrimoti HS, Barnes CA, McNaughton BL. 1999. Reactivation of hippocampal cell assemblies: effects of behavioral state, experience, and EEG dynamics. J Neurosci. 19:4090–4101. PubMed PMC

Laroche S, Davis S, Jay TM. 2000. Plasticity at hippocampal to prefrontal cortex synapses: dual roles in working memory and consolidation. Hippocampus. 10:438–446. PubMed

Laroche S, Jay TM, Thierry AM. 1990. Long-term potentiation in the prefrontal cortex following stimulation of the hippocampal CA1/subicular region. Neurosci Lett. 114:184–190. PubMed

Latchoumane CFV, Ngo HVV, Born J, Shin HS. 2017. Thalamic spindles promote memory formation during sleep through triple phase-locking of cortical, thalamic, and hippocampal rhythms. Neuron. 95:424–435. PubMed

Lavenex P, Amaral DG. 2000. Hippocampal–neocortical interaction: a hierarchy of associativity. Hippocampus. 10:420–430. PubMed

Lemieux M, Chen JY, Lonjers P, Bazhenov M, Timofeev I. 2014. The impact of cortical deafferentation on the neocortical slow oscillation. J Neurosci. 34:5689–5703. PubMed PMC

Levenstein D, Buzsáki G, Rinzel J. 2019. NREM sleep in the rodent neocortex and hippocampus reflects excitable dynamics. Nat Commun. 10:2478. PubMed PMC

Luczak A, Barthó P, Marguet SL, Buzsáki G, Harris KD. 2007. Sequential structure of neocortical spontaneous activity in vivo. Proc Natl Acad Sci. 104:347–352. PubMed PMC

Maingret N, Girardeau G, Todorova R, Goutierre M, Zugaro M. 2016. Hippocampo-cortical coupling mediates memory consolidation during sleep. Nat Neurosci. 19:959–964. PubMed

Mak-McCully RA, Deiss SR, Rosen BQ, Jung KY, Sejnowski TJ, Bastuji H, Rey M, Cash SS, Bazhenov M, Halgren E. 2014. Synchronization of isolated downstates (k-complexes) may be caused by cortically-induced disruption of thalamic spindling. PLoS Comput Biol. 10. PubMed PMC

Mak-McCully RA, Rosen BQ, Rolland M, Régis J, Bartolomei F, Rey M, Chauvel P, Cash SS, Halgren E. 2015. Distribution, amplitude, incidence, co-occurrence, and propagation of human k-complexes in focal transcortical recordings. eNeuro. 2. PubMed PMC

Malerba P, Bazhenov M. 2019. Circuit mechanisms of hippocampal reactivation during sleep. Neurobiol Learn Memory. 160:98–107. PubMed PMC

Malerba P, Jones MW, Bazhenov M. 2017. Defining the synaptic mechanisms that tune CA3-CA1 reactivation during sharp-wave ripples. bioRxiv. Page 164699.

Malerba P, Krishnan GP, Fellous JM, Bazhenov M. 2016. Hippocampal CA1 ripples as inhibitory transients. PLoS Comput Biol. 12: e1004880. PubMed PMC

Malerba P, Rulkov NF, Bazhenov M. 2019. Large time step discrete-time modeling of sharp wave activity in hippocampal area CA3. Commun Nonlinear Sci Numer Simul. 72:162–175. PubMed PMC

Malerba P, Tsimring K, Bazhenov M. 2018. Learning-induced sequence reactivation during sharp-wave ripples: a computational study. In Advances in the Mathematical Sciences: AWMRS 2017, vol. 15, p. 173–204. Springer.

Massimini M, Huber R, Ferrarelli F, Hill S, Tononi G. 2004. The sleep slow oscillation as a traveling wave. J Neurosci. 24:6862–6870. PubMed PMC

McClelland JL, McNaughton BL, O’Reilly RC. 1995. Why there are complementary learning systems in the hippocampus and neocortex: insights from the successes and failures of connectionist models of learning and memory. Psychol Rev. 102:419. PubMed

Mednick SC, McDevitt EA, Walsh JK, Wamsley E, Paulus M, Kanady JC, Drummond SP. 2013. The critical role of sleep spindles in hippocampal-dependent memory: a pharmacology study. J Neurosci. 33:4494–4504. PubMed PMC

Mohajerani MH, McVea DA, Fingas M, Murphy TH. 2010. Mirrored bilateral slow-wave cortical activity within local circuits revealed by fast bihemispheric voltage-sensitive dye imaging in anesthetized and awake mice. J Neurosci. 30:3745–3751. PubMed PMC

Mölle M, Yeshenko O, Marshall L, Sara SJ, Born J. 2006. Hippocampal sharp wave-ripples linked to slow oscillations in rat slow-wave sleep. J Neurophysiol. 96:62–70. PubMed

Murphy M, Riedner BA, Huber R, Massimini M, Ferrarelli F, Tononi G. 2009. Source modeling sleep slow waves. Proc Natl Acad Sci. 106:1608–1613. PubMed PMC

Nadel L, Winocur G, Ryan L, Moscovitch M. 2007. Systems consolidation and hippocampus: two views. Debate Neurosci. 1:55–66.

Nakashiba T, Buhl DL, McHugh TJ, Tonegawa S. 2009. Hippocampal CA3 output is crucial for ripple-associated reactivation and consolidation of memory. Neuron. 62:781–787. PubMed PMC

Nir Y, Staba RJ, Andrillon T, Vyazovskiy VV, Cirelli C, Fried I, Tononi G. 2011. Regional slow waves and spindles in human sleep. Neuron. 70:153–169. PubMed PMC

Parent MA, Wang L, Su J, Netoff T, Yuan LL. 2009. Identification of the hippocampal input to medial prefrontal cortex in vitro. Cereb Cortex. 20:393–403. PubMed PMC

Peyrache A, Battaglia FP, Destexhe A. 2011. Inhibition recruitment in prefrontal cortex during sleep spindles and gating of hippocampal inputs. Proc Natl Acad Sci. 108:17207–17212. PubMed PMC

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. PubMed

Preston AR, Eichenbaum H. 2013. Interplay of hippocampus and prefrontal cortex in memory. Curr Biol. 23:R764–R773. PubMed PMC

Rajasethupathy P, Sankaran S, Marshel JH, Kim CK, Ferenczi E, Lee SY, Berndt A, Ramakrishnan C, Jaffe A, Lo M, et al. . 2015. Projections from neocortex mediate top-down control of memory retrieval. Nature. 526:653. PubMed PMC

Ranganath C, Ritchey M. 2012. Two cortical systems for memory-guided behaviour. Nat Rev Neurosci. 13:713. PubMed

Redman S. 1990. Quantal analysis of synaptic potentials in neurons of the central nervous system. Physiol Rev. 70:165–198. PubMed

Rothschild G. 2019. The transformation of multi-sensory experiences into memories during sleep. Neurobiol Learn Memory. 160:58–66. PubMed

Rothschild G, Eban E, Frank LM. 2017. A cortical–hippocampal–cortical loop of information processing during memory consolidation. Nat Neurosci. 20:251. PubMed PMC

Salin PA, Prince DA. 1996. Spontaneous Gabaa receptor-mediated inhibitory currents in adult rat somatosensory cortex. J Neurophysiol. 75:1573–1588. PubMed

Sanchez-Vives MV, McCormick DA. 2000. Cellular and network mechanisms of rhythmic recurrent activity in neocortex. Nat Neurosci. 3:1027. PubMed

Sheroziya M, Timofeev I. 2014. Global intracellular slow-wave dynamics of the thalamocortical system. J Neurosci. 34:8875–8893. PubMed PMC

Siapas AG, Wilson MA. 1998. Coordinated interactions between hippocampal ripples and cortical spindles during slow-wave sleep. Neuron. 21:1123–1128. PubMed

Sirota A, Csicsvari J, Buhl D, Buzsáki G. 2003. Communication between neocortex and hippocampus during sleep in rodents. Proc Natl Acad Sci. 100:2065–2069. PubMed PMC

Sivagnanam S, Majumdar A, Yoshimoto K, Astakhov V, Bandrowski A, Martone M, Carnevale NT. 2013. Introducing the neuroscience gateway. CEUR Workshop Proceedings, CEUR-WS.org, vol. 993 of IWSG. PubMed PMC

Squire LR, Alvarez P. 1995. Retrograde amnesia and memory consolidation: a neurobiological perspective. Curr Opin Neurobiol. 5:169–177. PubMed

Staresina BP, Bergmann TO, Bonnefond M, Van Der Meij R, Jensen O, Deuker L, Elger CE, Axmacher N, Fell J. 2015. Hierarchical nesting of slow oscillations, spindles and ripples in the human hippocampus during sleep. Nat Neurosci. 18:1679–1686. PubMed PMC

Steriade M, Amzica F, et al. . 1998. Coalescence of sleep rhythms and their chronology in corticothalamic networks. Sleep Res Online. 1:1–10. PubMed

Steriade M, Nuñez A, Amzica F. 1993a. Intracellular analysis of relations between the slow (1 hz) neocortical oscillation and other sleep rhythms of the electroencephalogram. J Neurosci. 13:3266–3283. PubMed PMC

Steriade M, Nunez A, Amzica F. 1993b. A novel slow (1 hz) oscillation of neocortical neurons in vivo: depolarizing and hyperpolarizing components. J Neurosci. 13:3252–3265. PubMed PMC

Teyler TJ, DiScenna P. 1986. The hippocampal memory indexing theory. Behav Neurosci. 100:147. PubMed

Thierry AM, Gioanni Y, Dégénétais E, Glowinski J. 2000. Hippocampo-prefrontal cortex pathway: anatomical and electrophysiological characteristics. Hippocampus. 10:411–419. PubMed

Tierney PL, Dégenetais E, Thierry AM, Glowinski J, Gioanni Y. 2004. Influence of the hippocampus on interneurons of the rat prefrontal cortex. Eur J Neurosci. 20:514–524. PubMed

Timofeev I, Grenier F, Bazhenov M, Sejnowski T, Steriade M. 2000. Origin of slow cortical oscillations in deafferented cortical slabs. Cereb Cortex. 10:1185–1199. PubMed

Todorova R, Zugaro M. 2019. Isolated cortical computations during delta waves support memory consolidation. Science. 366:377–381. PubMed

Valero M, Averkin RG, Fernandez-Lamo I, Aguilar J, Lopez-Pigozzi D, Brotons-Mas JR, Cid E, Tamas G, de la Prida LM. 2017. Mechanisms for selective single-cell reactivation during offline sharp-wave ripples and their distortion by fast ripples. Neuron. 94:1234–1247. PubMed

van de Ven GM, Trouche S, McNamara CG, Allen K, Dupret D. 2016. Hippocampal offline reactivation consolidates recently formed cell assembly patterns during sharp wave-ripples. Neuron. 92:968–974. PubMed PMC

Varela C, Kumar S, Yang J, Wilson M. 2014. Anatomical substrates for direct interactions between hippocampus, medial prefrontal cortex, and the thalamic nucleus reuniens. Brain Struct Funct. 219:911–929. PubMed PMC

Vertes RP. 2006. Interactions among the medial prefrontal cortex, hippocampus and midline thalamus in emotional and cognitive processing in the rat. Neuroscience. 142:1–20. PubMed

Vertes RP, Hoover WB, Szigeti-Buck K, Leranth C. 2007. Nucleus reuniens of the midline thalamus: link between the medial prefrontal cortex and the hippocampus. Brain Res Bull. 71:601–609. PubMed PMC

Volgushev M, Chauvette S, Mukovski M, Timofeev I. 2006. Precise long-range synchronization of activity and silence in neocortical neurons during slow-wave sleep. J Neurosci. 26:5665–5672. PubMed PMC

Wang DV, Ikemoto S. 2016. Coordinated interaction between hippocampal sharp-wave ripples and anterior cingulate unit activity. J Neurosci. 36:10663–10672. PubMed PMC

Wang DV, Yau HJ, Broker CJ, Tsou JH, Bonci A, Ikemoto S. 2015. Mesopontine median raphe regulates hippocampal ripple oscillation and memory consolidation. Nat Neurosci. 18:728–735. PubMed PMC

Wei Y, Krishnan GP, Bazhenov M. 2016. Synaptic mechanisms of memory consolidation during sleep slow oscillations. J Neurosci. 36:4231–4247. PubMed PMC

Wei Y, Krishnan GP, Komarov M, Bazhenov M. 2018. Differential roles of sleep spindles and sleep slow oscillations in memory consolidation. PLoS Comput Biol. 14: e1006322. PubMed PMC

Wei Y, Krishnan GP, Marshall L, Martinetz T, Bazhenov M. 2020. Stimulation augments spike sequence replay and memory consolidation during slow-wave sleep. J Neurosci. 40:811–824. PubMed PMC

Wierzynski CM, Lubenov EV, Gu M, Siapas AG. 2009. State-dependent spike-timing relationships between hippocampal and prefrontal circuits during sleep. Neuron. 61:587–596. PubMed PMC

Wilson MA, McNaughton BL. 1994. Reactivation of hippocampal ensemble memories during sleep. Science. 265:676–679. PubMed

Winocur G, Moscovitch M, Bontempi B. 2010. Memory formation and long-term retention in humans and animals: convergence towards a transformation account of hippocampal–neocortical interactions. Neuropsychologia. 48:2339–2356. PubMed

Python/NEURON code for simulating biophysically realistic thalamocortical dynamics during sleep