• This record comes from PubMed

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

. 2024 Sep ; 21 () : . [epub] 20240603

Status PubMed-not-MEDLINE Language English Country Netherlands Media print-electronic

Document type Journal Article

Grant support
R01 MH125557 NIMH NIH HHS - United States
R01 NS109553 NINDS NIH HHS - United States
RF1 NS132913 NINDS NIH HHS - United States

Understanding the function of sleep and its associated neural rhythms is an important goal in neuroscience. While many theoretical models of neural dynamics during sleep exist, few include the effects of neuromodulators on sleep oscillations and describe transitions between sleep and wake states or different sleep stages. Here, we started with a C++-based thalamocortical network model that describes characteristic thalamic and cortical oscillations specific to sleep. This model, which includes a biophysically realistic description of intrinsic and synaptic channels, allows for testing the effects of different neuromodulators, intrinsic cell properties, and synaptic connectivity on neural dynamics during sleep. We present a complete reimplementation of this previously-published sleep model in the standardized NEURON/Python framework, making it more accessible to the wider scientific community.

See more in PubMed

Girardeau G, Lopes-Dos-Santos V, Brain neural patterns and the memory function of sleep, Science 374 (6567) (2021) 560–564. PubMed PMC

Fernandez LM, Lüthi A, Sleep spindles: mechanisms and functions, Physiol. Rev 100 (2) (2020) 805–868. PubMed

Fultz NE, Bonmassar G, Setsompop K, Stickgold RA, Rosen BR, Polimeni JR, Lewis LD, Coupled electrophysiological, hemodynamic, and cerebrospinal fluid oscillations in human sleep, Science 366 (6465) (2019) 628–631. PubMed PMC

Timofeev I, Chauvette S, Sleep slow oscillation and plasticity, Curr. Opin. Neurobiol 44 (2017) 116–126. PubMed

Ngo H-V, Fell J, Staresina B, Sleep spindles mediate hippocampal-neocortical coupling during long-duration ripples, ELife 9 (2020) e57011. PubMed PMC

Born J, Slow-wave sleep and the consolidation of long-term memory, World J. Biol. Psychiatry 11 (sup1) (2010) 16–21. PubMed

Picchioni D, Özbay PS, Mandelkow H, de Zwart JA, Wang Y, van Gelderen P, Duyn JH, Autonomic arousals contribute to brain fluid pulsations during sleep, Neuroimage 249 (2022) 118888. PubMed PMC

McCormick DA, Neurotransmitter actions in the thalamus and cerebral cortex and their role in neuromodulation of thalamocortical activity, Prog. Neurobiol 39 (4) (1992) 337–388. PubMed

Samanta A, Alonso A, Genzel L, Memory reactivations and consolidation: considering neuromodulators across wake and sleep, Curr. Opin. Physiol 15 (2020) 120–127.

Falup-Pecurariu C, Diaconu S, Tint D, Falup-Pecurariu O, Neurobiology of sleep, Exp. Therapeutic Med 21 (3) (2021) 1–1. PubMed PMC

Krishnan GP, Chauvette S, Shamie I, Soltani S, Timofeev I, Cash SS, Halgren E, Bazhenov M, Cellular and neurochemical basis of sleep stages in the thalamocortical network, ELife 5 (2016) e18607. PubMed PMC

Bazhenov M, Timofeev I, Steriade M, Sejnowski TJ, Model of thalamocortical slow-wave sleep oscillations and transitions to activated states, J. Neurosci 22 (19) (2002) 8691–8704. PubMed PMC

Fuentealba P, Timofeev I, Bazhenov M, Sejnowski TJ, Steriade M, Membrane bistability in thalamic reticular neurons during spindle oscillations, J. Neurophysiol 93 (1) (2005) 294–304. PubMed PMC

Bazhenov M, Timofeev I, Intrinsic and synaptic mechanisms of cortical active states generation during slow-wave sleep, in: Mechanisms of Spontaneous Active States in the Neocortex, 2007, pp. 1–22.

Bonjean M, Baker T, Lemieux M, Timofeev I, Sejnowski T, Bazhenov M, Corticothalamic feedback controls sleep spindle duration in vivo, J. Neurosci 31 (25) (2011) 9124–9134. PubMed PMC

Bazhenov M, Lonjers P, Skorheim S, Bedard C, Destexhe A, Non-homogeneous extracellular resistivity affects the current-source density profiles of up-down state oscillations, Phil. Trans. R. Soc. A 369 (1952) (2011) 3802–3819. PubMed PMC

Bonjean M, Baker T, Bazhenov M, Cash S, Halgren E, Sejnowski T, Interactions between core and matrix thalamocortical projections in human sleep spindle synchronization, J. Neurosci 32 (15) (2012) 5250–5263. PubMed PMC

Chen J-Y, Chauvette S, Skorheim S, Timofeev I, Bazhenov M, Interneuron-mediated inhibition synchronizes neuronal activity during slow oscillation, J. Physiol 590 (16) (2012) 3987–4010. PubMed PMC

Lemieux M, Chen J-Y, Lonjers P, Bazhenov M, Timofeev I, The impact of cortical deafferentation on the neocortical slow oscillation, J. Neurosci 34 (16) (2014) 5689–5703. PubMed PMC

Chen J-Y, Lonjers P, Lee C, Chistiakova M, Volgushev M, Bazhenov M, Heterosynaptic plasticity prevents runaway synaptic dynamics, J. Neurosci 33 (40) (2013) 15915–15929. PubMed PMC

Mak-McCully RA, Deiss SR, Rosen BQ, Jung K-Y, Sejnowski TJ, Bastuji H, Rey M, Cash SS, Bazhenov M, Halgren E, Synchronization of isolated downstates (K-complexes) may be caused by cortically-induced disruption of thalamic spindling, PLoS Comput. Biol 10 (9) (2014) e1003855. PubMed PMC

Volgushev M, Chen J-Y, Ilin V, Goz R, Chistiakova M, Bazhenov M, Partial breakdown of input specificity of STDP at individual synapses promotes new learning, J. Neurosci 36 (34) (2016) 8842–8855. PubMed PMC

Bannon NM, Chistiakova M, Chen J-Y, Bazhenov M, Volgushev M, Adenosine shifts plasticity regimes between associative and homeostatic by modulating heterosynaptic changes, J. Neurosci 37 (6) (2017) 1439–1452. PubMed PMC

Krishnan GP, Rosen BQ, Chen J-Y, Muller L, Sejnowski TJ, Cash SS, Halgren E, Bazhenov M, Thalamocortical and intracortical laminar connectivity determines sleep spindle properties, PLoS Comput. Biol 14 (6) (2018) e1006171. PubMed PMC

Wei Y, Krishnan GP, Bazhenov M, Synaptic mechanisms of memory consolidation during sleep slow oscillations, J. Neurosci 36 (15) (2016) 4231–4247. PubMed PMC

Wei Y, Krishnan GP, Komarov M, Bazhenov M, Differential roles of sleep spindles and sleep slow oscillations in memory consolidation, PLoS Comput. Biol 14 (7) (2018) e1006322. PubMed PMC

Rosen BQ, Krishnan G, Sanda P, Komarov M, Sejnowski T, Rulkov N, Ulbert I, Eross L, Madsen J, Devinsky O, et al., Simulating human sleep spindle MEG and EEG from ion channel and circuit level dynamics, J. Neurosci. Methods 316 (2019) 46–57. PubMed PMC

Wei Y, Krishnan GP, Marshall L, Martinetz T, Bazhenov M, Stimulation augments spike sequence replay and memory consolidation during slow-wave sleep, J. Neurosci 40 (4) (2020) 811–824. PubMed PMC

González OC, Sokolov Y, Krishnan GP, Delanois JE, Bazhenov M, Can sleep protect memories from catastrophic forgetting? ELife 9 (2020) e51005. PubMed PMC

Sanda P, Malerba P, Jiang X, Krishnan GP, Gonzalez-Martinez J, Halgren E, Bazhenov M, Bidirectional interaction of hippocampal ripples and cortical slow waves leads to coordinated spiking activity during nrem sleep, Cerebral Cortex 31 (1) (2021) 324–340. PubMed PMC

Hines M, Davison AP, Muller E, Neuron and python, Front. Neuroinform 3 (2009) 391. PubMed PMC

Lytton WW, Seidenstein AH, Dura-Bernal S, McDougal RA, Schürmann F, Hines ML, Simulation neurotechnologies for advancing brain research: parallelizing large networks in neuron, Neural Comput. 28 (10) (2016) 2063–2090. PubMed PMC

Sivagnanam S, Majumdar A, Yoshimoto K, Astakhov V, Bandrowski AE, Martone ME, Carnevale NT, et al., Introducing the neuroscience gateway, IWSG 993 (2013). PubMed PMC

Marru S, Pierce M, Plale B, Pamidighantam S, Wannipurage D, Christie M, Ranawaka I, Abeysinghe E, Quick R, Tajkhorshid E, et al., Cybershuttle: An end-to-end cyberinfrastructure continuum to accelerate discovery in science and engineering, in: Practice and Experience in Advanced Research Computing, 2023, pp. 26–34.

Lindén H, Hagen E, Leski S, Norheim ES, Pettersen KH, Einevoll GT, LFPy: a tool for biophysical simulation of extracellular potentials generated by detailed model neurons, Front. Neuroinform 7 (2014) 41. PubMed PMC

Staresina BP, Coupled sleep rhythms for memory consolidation, Trends in Cognitive Sciences (2024). PubMed

Petzka M, Chatburn A, Charest I, Balanos GM, Staresina BP, Sleep spindles track cortical learning patterns for memory consolidation, Curr. Biol 32 (11) (2022) 2349–2356. PubMed PMC

Yordanova J, Kirov R, Verleger R, Kolev V, Dynamic coupling between slow waves and sleep spindles during slow wave sleep in humans is modulated by functional pre-sleep activation, Sci. Rep 7 (1) (2017) 14496. PubMed PMC

Golden R, Delanois JE, Sanda P, Bazhenov M, Sleep prevents catastrophic forgetting in spiking neural networks by forming a joint synaptic weight representation, PLoS Comput. Biol 18 (11) (2022) e1010628. PubMed PMC

Durán E, Pandinelli M, Logothetis NK, Eschenko O, Altered norepinephrine transmission after spatial learning impairs sleep-mediated memory consolidation in rats, Sci. Rep 13 (1) (2023) 4231. PubMed PMC

de Quervain D, Schwabe L, Roozendaal B, Stress, glucocorticoids and memory: implications for treating fear-related disorders, Nat. Rev. Neurosci 18 (1) (2017) 7–19. PubMed

Power JM, Sah P, Nuclear calcium signaling evoked by cholinergic stimulation in hippocampal CA1 pyramidal neurons, J. Neurosci 22 (9) (2002) 3454–3462. PubMed PMC

Hasselmo ME, Alexander AS, Hoyland A, Robinson JC, Bezaire MJ, Chapman GW, Saudargiene A, Carstensen LC, Dannenberg H, The unexplored territory of neural models: Potential guides for exploring the function of metabotropic neuromodulation, Neuroscience 456 (2021) 143–158. PubMed PMC

Kumbhar P, Hines M, Fouriaux J, Ovcharenko A, King J, Delalondre F, Schürmann F, Coreneuron: An optimized compute engine for the neuron simulator, Front. Neuroinform 13 (2019) 63. PubMed PMC

Mainen ZF, Sejnowski TJ, Influence of dendritic structure on firing pattern in model neocortical neurons, Nature 382 (6589) (1996) 363–366. PubMed

Find record

Citation metrics

Loading data ...

Archiving options

Loading data ...