Modeling the effect of sleep regulation on a neural mass model
In mammals, sleep is categorized by two main sleep stages, rapid eye movement (REM) and non-REM (NREM) sleep that are known to fulfill different functional roles, the most notable being the consolidation of memory. While REM sleep is characterized by brain activity similar to wakefulness, the EEG activity changes drastically with the emergence of K-complexes, sleep spindles and slow oscillations during NREM sleep. These changes are regulated by circadian and ultradian rhythms, which emerge from an intricate interplay between multiple neuronal populations in the brainstem, forebrain and hypothalamus and the resulting varying levels of neuromodulators. Recently, there has been progress in the understanding of those rhythms both from a physiological as well as theoretical perspective. However, how these neuromodulators affect the generation of the different EEG patterns and their temporal dynamics is poorly understood. Here, we build upon previous work on a neural mass model of the sleeping cortex and investigate the effect of those neuromodulators on the dynamics of the cortex and the corresponding transition between wakefulness and the different sleep stages. We show that our simplified model is sufficient to generate the essential features of human EEG over a full day. This approach builds a bridge between sleep regulatory networks and EEG generating neural mass models and provides a valuable tool for model validation.
KeywordsNeural mass EEG Sleep regulation Neuromodulators Sleep Sleep rhythms
- Benita, J.M., Guillamon, A., Deco, G., & Sanchez-Vives, M.V. (2012). Synaptic depression and slow oscillatory activity in a biophysical network model of the cerebral cortex. Frontiers in computational neuroscience, 6 (64). doi:10.3389/fncom.2012.00064.
- Benoıt, E., Callot, J.L., Diener, F., & Diener, M. (1981). Chasse au canard. Collectanea Mathematica, 31-32(1-3), 37–119.Google Scholar
- Borbély, A.A. (1982). A two process model of sleep regulation Human neurobiology.Google Scholar
- Brown, R.E., McKenna, J.T., Winston, S., Basheer, R., Yanagawa, Y., Thakkar, M.M., & McCarley, R.W. (2008). Characterization of GABAergic neurons in rapid-eye-movement sleep controlling regions of the brainstem reticular formation in GAD67-green fluorescent protein knock-in mice. European Journal of Neuroscience, 27(2), 352–363. doi:10.1111/j.1460-9568.2008.06024.x.CrossRefPubMedPubMedCentralGoogle Scholar
- Daan, S., Beersma, D.G.M., & Borbély, A.A. (1984). Timing of human sleep: recovery process gated by a circadian pacemaker. The American Journal of Physiology, 246(2 Pt 2), 161– 183.Google Scholar
- Datta, S., & MacLean, R.R. (2007). Neurobiological Mechanisms for the Regulation of Mammalian Sleep-Wake Behavior: Reinterpretation of Historical Evidence and Inclusion of Contemporary Cellular and Molecular Evidence. Neuroscience Biobehavior Reviews, 31(5), 775–824. doi:10.1016/j.biotechadv.2011.08.021.Secreted.CrossRefGoogle Scholar
- Fleshner, M., Booth, V., Forger, D.B., & Diniz Behn, C.G. (2011). Circadian regulation of sleep-wake behaviour in nocturnal rats requires multiple signals from suprachiasmatic nucleus. Philosophical Transactions of the Royal Society A: Mathematical, physical, and engineering sciences, 369(1952), 3855–3883. doi:10.1098/rsta.2011.0085.CrossRefGoogle Scholar
- Iber, C., Ancoli-Israel, S., Chesson Jr., A.L., & Quan, S.F. (2007). The AASM Manual for the Scoring of Sleep and Associated Events: Rules Terminology and Technical Specifications 1st ed.Google Scholar
- Jansen, B.H., Zouridakis, G., & Brandt, M.E. (1993). A neurophysiologically-based mathematical model of flash visual evoked potentials. Electrical Engineering, 283, 275–283.Google Scholar
- Kales, A., & Rechtschaffen, A. (1968). Rechtschaffen, A.: A manual of standardized terminology, techniques and scoring system for sleep stages of human subjects. U. S. National Institute of Neurological Diseases and Blindness, Neurological Information Network.Google Scholar
- Léna, I., Parrot, S., Deschaux, O., Muffat-Joly, S., Sauvinet, V., Renaud, B., Suaud-Chagny, M.F., & Gottesmann, C. (2005). Variations in extracellular levels of dopamine, noradrenaline, glutamate, and aspartate across the sleep–wake cycle in the medial prefrontal cortex and nucleus accumbens of freely moving rats. Journal of Neuroscience Research, 81(6), 891–899. doi:10.1002/jnr.20602.CrossRefPubMedGoogle Scholar
- Luppi, P.H., Gervasoni, D., Verret, L., Goutagny, R., Peyron, C., Salvert, D., Leger, L., & Fort, P. (2006). Paradoxical (REM) sleep genesis: The switch from an aminergic-cholinergic to a GABAergic-glutamatergic hypothesis. Journal of Physiology Paris, 100(5-6), 271–283. doi:10.1016/j.jphysparis.2007.05.006.CrossRefGoogle Scholar
- Peyron, C., Tighe, D.K., Van den Pol, A.N., de Lecea, L., Heller, H.C., Sutcliffe, J.G., & Kilduff, T.S. (1998). Neurons containing hypocretin (orexin) project to multiple neuronal systems. The Journal of Neuroscience, 015(23), 9996–10.Google Scholar
- Sapin, E., Lapray, D., Bérod, A., Goutagny, R., Léger, L., Ravassard, P., Clément, O., Hanriot, L., Fort, P., & Luppi, P.H. (2009). Localization of the brainstem GABAergic neurons controlling Paradoxical (REM) sleep. PLoS One, 4(1). doi:10.1371/journal.pone.0004272.
- Schellenberger Costa, M. (2006a). Simulation routine of the model. https://github.com/miscco/NM_Cortex_SR.
- Soma, S., & Shimegi, S. (2016). Cholinergic modulation of response gain in the primary visual cortex of the macaque. Journal of Neurophysiology, 107, 283–291. doi:10.1152/jn.00330.2011.