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Data-Driven Modeling of Normal and Pathological Oscillations in the Hippocampus

  • Ivan RaikovEmail author
  • Ivan Soltesz
Chapter
Part of the Springer Series in Cognitive and Neural Systems book series (SSCNS, volume 13)

Abstract

Epilepsy is a disorder caused by abnormalities at all levels of neural organization that often have complex and poorly understood interactions. Physiologically detailed computational models provide valuable tools for evaluation of possible clinical treatments of neural disorders because every parameter can be changed and many experimentally inaccessible variables can be observed. We present our recently developed full-scale model of the CA1 subfield in the rodent hippocampus and highlight its role in the study of biophysical neural oscillations, which are important biomarkers of cognitive processes as well as abnormal neural dynamics in epilepsy. This model provides an integrative framework that unifies experimentally derived knowledge about the hippocampus on multiple scales and can yield insight into the neurophysiological mechanisms underlying the dynamical regimes of the brain. Such a framework can be useful in studying cellular mechanisms of multitarget pharmacological treatments of neural disorders.

Keywords

Hippocampus CA1 Theta oscillations Gamma oscillations Epilepsy High-frequency oscillations Fast ripples 

Notes

Acknowledgments

The authors are supported by NIH NINDS under award number 1U19NS104590. Access to supercomputers for simulations of the CA1 model was provided by the Extreme Science and Engineering Discovery Environment (XSEDE; NSF grant number ACI-1053575), XSEDE Research Allocation grant TG-IBN140007 to I.S., and the Blue Waters sustained-petascale computing project (supported by NSF Awards OCI-0725070 and ACI-1238993 and the state of Illinois), NSF PRAC Awards 1614622, 1811597 to I.S.

References

  1. 1.
    Akam T, Kullmann D (2012) Efficient communication through coherence requires oscillations structured to minimize interference between signals. PLoS Comput Biol 8:e1002760CrossRefPubMedPubMedCentralGoogle Scholar
  2. 2.
    Amilhon B, Huh C, Manseau F et al (2015) Parvalbumin interneurons of hippocampus tune population activity at theta frequency. Neuron 86:1277–1289CrossRefGoogle Scholar
  3. 3.
    Atallah B, Scanziani M (2009) Instantaneous modulation of gamma oscillation frequency by balancing excitation with inhibition. Neuron 62:566–577CrossRefPubMedPubMedCentralGoogle Scholar
  4. 4.
    Bezaire M, Raikov I, Burk K et al (2016) Interneuronal mechanisms of hippocampal theta oscillations in a full-scale model of the rodent CA1 circuit. elife 5:e18566CrossRefPubMedPubMedCentralGoogle Scholar
  5. 5.
    Bezaire M, Soltesz I (2013) Quantitative assessment of CA1 local circuits: knowledge base for interneuron-pyramidal cell connectivity. Hippocampus 23:751–785CrossRefPubMedPubMedCentralGoogle Scholar
  6. 6.
    Bragin A, Benassi S, Kheiri F, Engel J (2011) Further evidence that pathologic high-frequency oscillations are bursts of population spikes derived from recordings of identified cells in dentate gyrus. Epilepsia 52:45–52CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    Bragin A, Engel J, Staba R (2010) High-frequency oscillations in epileptic brain. Curr Opin Neurol 23:151–156CrossRefPubMedPubMedCentralGoogle Scholar
  8. 8.
    Bragin A, Engel J, Wilson C et al (1999) Hippocampal and entorhinal cortex high-frequency oscillations (100–500 Hz) in human epileptic brain and in kainic acid-treated rats with chronic seizures. Epilepsia 40:127–137CrossRefGoogle Scholar
  9. 9.
    Bragin A, Jando G, Nadasdy Z et al (1995) Gamma (40–100 Hz) oscillation in the hippocampus of the behaving rat. J Neurosci 15:47–60CrossRefGoogle Scholar
  10. 10.
    Bragin A, Wilson C, Engel J (2003) Spatial stability over time of brain areas generating fast ripples in the epileptic rat. Epilepsia 44:1233–1237CrossRefGoogle Scholar
  11. 11.
    Bui A, Nguyen T, Limouse C et al (2017) Dentate gyrus mossy cells control spontaneous convulsive seizures and spatial memory. Science 359:787–790CrossRefGoogle Scholar
  12. 12.
    Butler J, Mendonca P, Robinson H, Paulsen O (2016) Intrinsic cornu ammonis area 1 theta-nested gamma oscillations induced by optogenetic theta frequency stimulation. J Neurosci 36:4155–4169CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    Buzsaki G (2002) Theta oscillations in the hippocampus. Neuron 33:325–340CrossRefGoogle Scholar
  14. 14.
    Buzsaki G (2015) Hippocampal sharp wave-ripple: a cognitive biomarker for episodic memory and planning. Hippocampus 25:1073–1188CrossRefPubMedPubMedCentralGoogle Scholar
  15. 15.
    Buzsaki G (1996) The hippocampo-neocortical dialogue. Cereb Cortex 6:81–92CrossRefGoogle Scholar
  16. 16.
    Buzsaki G, Buhl D, Harris K et al (2003) Hippocampal network patterns of activity in the mouse. Neuroscience 116:201–211CrossRefGoogle Scholar
  17. 17.
    Buzsaki G, Moser E (2013) Memory, navigation and theta rhythm in the hippocampal-entorhinal system. Nat Neurosci 16:130–138CrossRefPubMedPubMedCentralGoogle Scholar
  18. 18.
    Colgin L (2013) Mechanisms and functions of theta rhythms. Ann Rev Neurosci 36:295–312CrossRefGoogle Scholar
  19. 19.
    Colgin L (2016) Rhythms of the hippocampal network. Nat Rev Neurosci 17(4):239–249CrossRefPubMedPubMedCentralGoogle Scholar
  20. 20.
    Colgin L, Moser E (2010) Gamma oscillations in the hippocampus. Physiology 25:319–329CrossRefGoogle Scholar
  21. 21.
    Csicsvari J, Hirase H, Czurko A et al (1999) Oscillatory coupling of hippocampal pyramidal cells and interneurons in the behaving rat. J Neurosci 19:274–287CrossRefGoogle Scholar
  22. 22.
    Dyhrfjeld-Johnsen J, Santhakumar V, Morgan RJ et al (2007) Topological determinants of epileptogenesis in large-scale structural and functional models of the dentate gyrus derived from experimental data. J Neurophysiol 97:1566–1587CrossRefGoogle Scholar
  23. 23.
    Dzhala V, Kuchibhotla K, Glykys J et al (2010) Progressive nKCC1-dependent neuronal chloride accumulation during neonatal seizures. J Neurosci 30:11745–11761CrossRefPubMedPubMedCentralGoogle Scholar
  24. 24.
    Engel JJ, Bragin A, Staba R, Mody I (2009) High-frequency oscillations: what is normal and what is not? Epilepsia 50:598–604CrossRefGoogle Scholar
  25. 25.
    Engel JJ, Thompson P, Stern JM et al (2013) Connectomics and epilepsy. Curr Opin Neurol 26:186–194CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    Fisher R, van Emde Boas W, Blume W et al (2004) Epileptic seizures and epilepsy: definitions proposed by the international league against epilepsy (ILAE) and the International Bureau for Epilepsy (IBE). Epilepsia 46:470–472CrossRefGoogle Scholar
  27. 27.
    Fries P (2015) Rhythms for cognition: communication through coherence. Neuron 88:220–235CrossRefPubMedPubMedCentralGoogle Scholar
  28. 28.
    Goutagny R, Jackson J, Williams S (2009) Self-generated theta oscillations in the hippocampus. Nat Neurosci 12:1491–1493CrossRefGoogle Scholar
  29. 29.
    Jacobs J, Staba R, Asano E et al (2012) High-frequency oscillations (hFOs) in clinical epilepsy. Prog Neurobiol 98:302–315CrossRefPubMedPubMedCentralGoogle Scholar
  30. 30.
    Jensen O, Colgin L (2007) Cross-frequency coupling between neuronal oscillations. Trends Cogn Sci 11:267–269CrossRefGoogle Scholar
  31. 31.
    Jirsa V, Stacey W, Quilichini P et al (2014) On the nature of seizure dynamics. Brain 137:2210–2230CrossRefPubMedPubMedCentralGoogle Scholar
  32. 32.
    Jirsch J, Urrestarazu E, LeVan P et al (2006) High-frequency oscillations during human focal seizures. Brain 129:1593–1608CrossRefGoogle Scholar
  33. 33.
    Klausberger T, Magill P, Marton L et al (2003) Brain-state- and cell-type-specific firing of hippocampal interneurons in vivo. Nature 421:844–848CrossRefPubMedPubMedCentralGoogle Scholar
  34. 34.
    Kobayashi E, Grova C, Tyvaert L et al (2009) Structures involved at the time of temporal lobe spikes revealed by interindividual group analysis of EEG/fMRI data. Epilepsia 50:2549–2556CrossRefPubMedPubMedCentralGoogle Scholar
  35. 35.
    Krook-Magnuson E, Szabo G, Armstrong C et al (2014) Cerebellar directed optogenetic intervention inhibits spontaneous hippocampal seizures in a mouse model of temporal lobe epilepsy. eNeuro 1:Google Scholar
  36. 36.
    Le Van Quyen M, Khalilov I, Ben-Ari Y (2006) The dark side of high-frequency oscillations in the developing brain. Trends Neurosci 29:419–427CrossRefGoogle Scholar
  37. 37.
    Lee M, Chrobak J, Sik A et al (1994) Hippocampal theta activity following selective lesion of the septal cholinergic system. Neuroscience 62:1033–1047CrossRefPubMedPubMedCentralGoogle Scholar
  38. 38.
    Lopes da Silva F, Blanes W, Kalitzin S et al (2003) Dynamical diseases of brain systems: different routes to epileptic seizures. IEEE Trans Biomed Eng 50:540–548CrossRefPubMedPubMedCentralGoogle Scholar
  39. 39.
    Lytton W (2017) Multiscale modeling in the clinic: diseases of the brain and nervous system. Brain Inform 4:219–230CrossRefPubMedPubMedCentralGoogle Scholar
  40. 40.
    Lytton W (2008) Computer modelling of epilepsy. Nat Rev Neurosci 9:626–637CrossRefPubMedPubMedCentralGoogle Scholar
  41. 41.
    Maris E, Fries P, van Ede F (2016) Diverse phase relations among neuronal rhythms and their potential function. Trends Neurosci 39:86–99CrossRefGoogle Scholar
  42. 42.
    Morgan R, Soltesz I (2008) Nonrandom connectivity of the epileptic dentate gyrus predicts a major role for neuronal hubs in seizures. Proc Natl Acad Sci USA 105:6179–6184CrossRefGoogle Scholar
  43. 43.
    Moser E, Kropff E, Moser M-B (2008) Place cells, grid cells, and the brain’s spatial representation system. Annu Rev Neurosci 31:69–89CrossRefGoogle Scholar
  44. 44.
    Rogawski M, Cavazos J (2015) Mechanisms of action of antiepileptic drugs. In: Wyllie E (ed) Wyllie’s treatment of epilepsy: principles and practice, 6th edn. Wolters Kluwer Health, PhiladelphiaGoogle Scholar
  45. 45.
    Rogawski M, Loscher W (2004) The neurobiology of antiepileptic drugs. Nat Rev Neurosci 5:554–564CrossRefGoogle Scholar
  46. 46.
    Rubinov M, Sporns O (2010) Complex network measures of brain connectivity: uses and interpretations. NeuroImage 52:2059–2069CrossRefGoogle Scholar
  47. 47.
    Santhakumar V, Aradi I, Soltesz I (2005) Role of mossy fiber sprouting and mossy cell loss in hyperexcitability: a network model of the dentate gyrus incorporating cell types and axonal topography. J Neurophysiol 93:437–453CrossRefGoogle Scholar
  48. 48.
    Schneider C, Cuntz H, Soltesz I (2014) Linking macroscopic with microscopic neuroanatomy using synthetic neuronal populations. PLoS Comput Biol 10:e1003921CrossRefPubMedPubMedCentralGoogle Scholar
  49. 49.
    Schomburg E, Anastassiou C, Buzsaki G, Koch C (2012) The spiking component of oscillatory extracellular potentials in the rat hippocampus. J Neurosci 32:11798–11811CrossRefPubMedPubMedCentralGoogle Scholar
  50. 50.
    Soltesz I, Deschenes M (1993) Low-and high-frequency membrane potential oscillations during theta activity in CA1 and CA3 pyramidal neurons of the rat hippocampus under ketamine-xylazine anesthesia. J Neurophysiol 70:97–97CrossRefGoogle Scholar
  51. 51.
    Sperk G, Drexel M, Pirker S (2009) Neuronal plasticity in animal models and the epileptic human hippocampus. Epilepsia 50(Suppl 12):29–31CrossRefPubMedPubMedCentralGoogle Scholar
  52. 52.
    Sporns O (2012) Discovering the human connectome. MIT Press, Cambridge, MACrossRefGoogle Scholar
  53. 53.
    Staba R, Wilson C, Bragin A et al (2002) Quantitative analysis of high-frequency oscillations (80–500 hz) recorded in human epileptic hippocampus and entorhinal cortex. J Neurophysiol 88:1743–1752CrossRefGoogle Scholar
  54. 54.
    Stark E, Roux L, Eichler R et al (2014) Pyramidal cell-interneuron interactions underlie hippocampal ripple oscillations. Neuron 83:467–480CrossRefPubMedPubMedCentralGoogle Scholar
  55. 55.
    Szucs A (1998) Applications of the spike density function in analysis of neuronal firing patterns. J Neurosci Methods 81:159–167CrossRefGoogle Scholar
  56. 56.
    Taylor P, Kaiser M, Dauwels J (2014) Structural connectivity based whole brain modelling in epilepsy. J Neurosci Methods 246:51–57CrossRefGoogle Scholar
  57. 57.
    Varga C, Golshani P, Soltesz I (2012) Frequency-invariant temporal ordering of interneuronal discharges during hippocampal oscillations in awake mice. Proc Natl Acad Sci 109:E2726–E2734CrossRefGoogle Scholar
  58. 58.
    Varga C, Oijala M, Lish J, Szabo GG, Bezaire M, Marchionni I, Golshani P, Soltesz I (2014) Functional fission of parvalbumin interneuron classes during fast network events. Elife 3. https://doi.org/10.7554/eLife.04006
  59. 59.
    Viayna E, Sola I, Di Pietro O, Munoz-Torrero D (2013) Human disease and drug pharmacology, complex as real life. Curr Med Chem 20:1623–1634CrossRefGoogle Scholar
  60. 60.
    Ylinen A, Bragin A, Nadasdy Z et al (1995) Sharp wave-associated high-frequency oscillation (200 Hz) in the intact hippocampus: network and intracellular mechanisms. J Neurosci 15:30–46CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Department of NeurosurgeryStanford UniversityStanfordUSA

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