Brain and Nonlinear Dynamics: Slow-Wave Sleep Regulates to the Edge of Chaos

Chapter
Part of the Springer Series in Cognitive and Neural Systems book series (SSCNS, volume 11)

Abstract

We present a theoretical modeling study that predicts that the EEG waveforms observed during the passage from wake through the stages of deepening natural sleep arise from the evolving interactions between symmetry-breaking transitions in the brain. These non-equilibrium transitions are brought on by modulations from naturally occurring neurotransmitters, primarily acetylcholine and GABA, whose concentrations vary dynamically during sleep. In particular, we find that the slow-wave oscillations of deepest nonREM sleep are fundamentally chaotic in nature, arising spontaneously from a competitive interaction between Turing (spatial) and Hopf (temporal) instabilities. We show that by introducing an activity-based regulation of inhibitory gap-junction diffusion, the sleeping cortex can move towards the edge of chaos defined by the boundary between the disordered slow-wave state and a pathologically ordered seizure-like state. We suggest that such self-organization could allow the brain to dwell in a state that is optimized for pruning and consolidation of memories.

Keywords

Slow-wave sleep EEG Spatiotemporal instability Birfurcation Non-equilibrium states Hopf oscillations Turing patterns Self-organization Edge of chaos 

References

  1. Bak P, Paczuski M (1995) Complexity, contingency, and criticality. Proc Natl Acad Sci U S A 92:6689–6696CrossRefPubMedPubMedCentralGoogle Scholar
  2. Beggs JM (2008) The criticality hypothesis: how local cortical networks might optimize information processing. Philos Trans A Math Phys Eng Sci 366(1864):329–343CrossRefPubMedGoogle Scholar
  3. Bennett MV, Zukin RS (2004) Electrical coupling and neuronal synchronization in the mammalian brain. Neuron 41:495–511CrossRefPubMedGoogle Scholar
  4. Bertschinger N, Natschläger T (2004) Real-time computation at the edge of chaos in recurrent neural networks. Neural Comput 16(7):1413–1436CrossRefPubMedGoogle Scholar
  5. Bienenstock E, Lehmann D (1998) Regulated criticality in the brain? Adv Complex Syst 1:361–384CrossRefGoogle Scholar
  6. Boedecker J, Obst O, Lizier JT, Mayer NM, Asada M (2012) Information processing in echo state networks at the edge of chaos. Theory Biosci 131(3):205–213CrossRefPubMedGoogle Scholar
  7. Bornholdt S, Röhl T (2003) Self-organized critical neural networks. Phys Rev E 67(6 Pt 2):066118CrossRefGoogle Scholar
  8. Costa MS, Born J, Claussen JC, Martinetz T (2016) Modeling the effect of sleep regulation on a neural mass model. J Comput Neurosci 41(1):15–28CrossRefPubMedGoogle Scholar
  9. Diniz Behn CG, Booth V (2010) Simulating microinjection experiments in a novel model of the rat sleep-wake regulatory network. J Neurophysiol 103(4):1937–1953CrossRefPubMedGoogle Scholar
  10. Freyer F, Roberts JA, Becker R, Robinson PA, Ritter P, Breakspear M (2011) Biophysical mechanisms of multistability in resting-state cortical rhythms. J Neurosci 31(17):6353–6361CrossRefPubMedGoogle Scholar
  11. Fukuda T, Kosaka T, Singer W, Galuske RAW (2006) Gap junctions among dendrites of cortical GABAergic neurons establish a dense and widespread intercolumnar network. J Neurosci 26:3434–3443CrossRefPubMedGoogle Scholar
  12. Galarreta M, Hestrin S (2001) Electrical synapses between GABA-releasing interneurons. Nat Rev Neurosci 2(6):425–433CrossRefPubMedGoogle Scholar
  13. Hasselmo ME (1995) Neuromodulation and cortical function: modeling the physiological basis of behavior. Behav Brain Res 67(1):1–27CrossRefPubMedGoogle Scholar
  14. Kramer MA, Kirsch HE, Szeri AJ (2005) Pathological pattern formation and cortical propagation of epileptic seizures. J R Soc Lond Interface 2:113–207CrossRefGoogle Scholar
  15. Langton CG (1990) Computation at the edge of chaos: phase transitions and emergent computation. Physica D: Nonlinear Phenomena 42:12–37CrossRefGoogle Scholar
  16. Liley DTJ, Bojak I (2005) Understanding the transition to seizure by modeling the epileptiform activity of general anesthetic agents. J Clin Neurophysiol 22(5):300–313PubMedGoogle Scholar
  17. Loddenkemper T, Fernández IS, Peters JM (2011) Continuous spike and waves during sleep and electrical status epilepticus in sleep. J Clin Neurophysiol 28(2):154–164CrossRefPubMedGoogle Scholar
  18. Massimini M, Huber R, Ferrarelli F, Hill S, Tononi G (2004) The sleep slow oscillation as a traveling wave. J Neurosci 24(31):6862–6870CrossRefPubMedGoogle Scholar
  19. McCarley RW, Hobson JA (1975) Neuronal excitability modulation over the sleep cycle: a structural and mathematical model. Science 189(4196):58–60CrossRefPubMedGoogle Scholar
  20. Meisel C, Olbrich E, Shriki O, Achermann P (2013) Fading signatures of critical brain dynamics during sustained wakefulness in humans. J Neurosci 33(44):17363–17372CrossRefPubMedPubMedCentralGoogle Scholar
  21. Murphy M, Bruno M-A, Riedner BA, Boveroux P, Noirhomme Q, Landsness EC, Brichant J-F, Phillips C, Massimini M, Laureys S, Tononi G, Boly M (2011) Propofol anesthesia and sleep: a high-density EEG study. Sleep 34(3):283–291ACrossRefPubMedPubMedCentralGoogle Scholar
  22. Palacios-Prado N, Hoge G, Marandykina A, Rimkute L, Chapuis S, Paulauskas N, Skeberdis VA, O’Brien J, Pereda AE, Bennett MVL, Bukauskas FF (2013) Intracellular magnesium-dependent modulation of gap junction channels formed by neuronal connexin36. J Neurosci 33(11):4741–4753CrossRefPubMedPubMedCentralGoogle Scholar
  23. Pearlmutter BA, Houghton CJ (2009) A new hypothesis for sleep: tuning for criticality. Neural Comput 21(6):1622–1641CrossRefPubMedGoogle Scholar
  24. Phillips AJK, Robinson PA (2007) A quantitative model of sleep-wake dynamics based on the physiology of the brainstem ascending arousal system. J Biol Rhythms 22(2):167–179CrossRefPubMedGoogle Scholar
  25. Priesemann V, Valderrama M, Wibral M, Le Van Quyen M (2013) Neuronal avalanches differ from wakefulness to deep sleep–evidence from intracranial depth recordings in humans. PLoS Comput Biol 9(3):e1002985CrossRefPubMedPubMedCentralGoogle Scholar
  26. Rechtschaffen A, Kale A (1968) A manual of standardized terminology, techniques, and scoring system for sleep stages of human subjects. U.S. Govt Printing Office, Washington, DCGoogle Scholar
  27. Robinson PA, Rennie CJ, Wright JJ (1997) Propagation and stability of waves of electrical activity in the cerebral cortex. Phys Rev E 56:826–840CrossRefGoogle Scholar
  28. Robinson PA, Rennie CJ, Wright JJ, Bahramali H, Gordon E, Rowe DL (2001) Prediction of electroencephalographic spectra from neurophysiology. Phys Rev E Stat Nonlin Soft Matter Phys 63(2 Pt 1):021903CrossRefPubMedGoogle Scholar
  29. Saper CB, Chou TC, Scammell TE (2001) The sleep switch: hypothalamic control of sleep and wakefulness. Trends Neurosci 24(12):726–731CrossRefPubMedGoogle Scholar
  30. Steriade M (2004) Acetylcholine systems and rhythmic activities during the waking–sleep cycle. Prog Brain Res 145:179–196CrossRefPubMedGoogle Scholar
  31. Steriade M, Amzica F (1998) Slow sleep oscillation, rhythmic K-complexes, and their paroxysmal developments. J Sleep Res 7(Suppl 1):30–35CrossRefPubMedGoogle Scholar
  32. Steyn-Ross ML, Steyn-Ross DA, Sleigh JW, Liley DTJ (1999) Theoretical electroencephalogram stationary spectrum for a white-noise-driven cortex: evidence for a general anesthetic-induced phase transition. Phys Rev E 60(6 Pt B):7299–7311Google Scholar
  33. Steyn-Ross ML, Steyn-Ross DA, Wilson MT, Sleigh JW (2007) Gap junctions mediate large-scale Turing structures in a mean-field cortex driven by subcortical noise. Phys Rev E 76:011916CrossRefGoogle Scholar
  34. Steyn-Ross ML, Steyn-Ross DA, Wilson MT, Sleigh JW (2009) Modeling brain activation patterns for the default and cognitive states. NeuroImage 45:298–311CrossRefPubMedGoogle Scholar
  35. Steyn-Ross ML, Steyn-Ross DA, Sleigh JW (2012) Gap junctions modulate seizures in a mean-field model of general anesthesia for the cortex. Cogn Neurodyn 6(3):215–225CrossRefPubMedPubMedCentralGoogle Scholar
  36. Steyn-Ross ML, Steyn-Ross DA, Sleigh JW (2013) Interacting Turing-Hopf instabilities drive symmetry-breaking transitions in a mean-field model of the cortex: a mechanism for the slow oscillation. Phys Rev X 3(2):021005Google Scholar
  37. Tononi G, Cirelli C (2006) Sleep function and synaptic homeostasis. Sleep Med Rev 10(1):49–62CrossRefPubMedGoogle Scholar
  38. Toyoizumi T, Abbott LF (2011) Beyond the edge of chaos: amplification and temporal integration by recurrent networks in the chaotic regime. Phys Rev E 84(5 Pt 1):051908CrossRefGoogle Scholar
  39. Vanini G, Lydic R, Baghdoyan HA (2012) GABA-to-ACh ratio in basal forebrain and cerebral cortex varies significantly during sleep. Sleep 35(10):1325–1334CrossRefPubMedPubMedCentralGoogle Scholar
  40. Walker MP, Stickgold R (2004) Sleep-dependent learning and memory consolidation. Neuron 44(1):121–133CrossRefPubMedGoogle Scholar
  41. Wang Y, Barakat A, Zhou H (2010) Electrotonic coupling between pyramidal neurons in the neocortex. PLoS One 5(4):e10253CrossRefPubMedPubMedCentralGoogle Scholar
  42. Wentlandt K, Samoilova M, Carlen PL, El Beheiry H (2006) General anesthetics inhibit gap junction communication in cultured organotypic hippocampal slices. Anesth Analg 102(6):1692–1698CrossRefPubMedGoogle Scholar
  43. Wilson MT, Sleigh JW, Steyn-Ross DA, Steyn-Ross ML (2006) General anesthetic-induced seizures can be explained by a mean-field model of cortical dynamics. Anesthesiology 104:588–593CrossRefPubMedGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2017

Authors and Affiliations

  1. 1.School of EngineeringUniversity of WaikatoHamiltonNew Zealand

Personalised recommendations