The mechanism of abrupt transition between theta and hyper-excitable spiking activity in medial entorhinal cortex layer II stellate cells

PLoS ONE

Volumn 5, Issue 11, 2010, Pages

  Kispersky, Tilman ^a   White, John A ^b   Rotstein, Horacio G ^c  

^a BOSTON UNIVERSITY   (United States)

^b Department of Electrical and Computer Engineering   (United States)

^c NEW JERSEY INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMPA RECEPTOR; POTASSIUM CHANNEL KCNQ5;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; ARTIFICIAL NEURAL NETWORK; CELL ISOLATION; CONTROLLED STUDY; ENTORHINAL CORTEX; EPILEPSY; HYPERPOLARIZATION; IN VITRO STUDY; MATHEMATICAL MODEL; NERVE CELL EXCITABILITY; NERVE CELL MEMBRANE POTENTIAL; NERVE CELL NETWORK; NONHUMAN; POTASSIUM CURRENT; PREDICTION; PROCESS MODEL; RAT; SPIKE WAVE; STELLATE CELL; SYNAPTIC INHIBITION; SYNAPTIC POTENTIAL; SYNAPTIC TRANSMISSION; THETA RHYTHM; ACTION POTENTIAL; ALGORITHM; ANIMAL; BIOLOGICAL MODEL; CELL MEMBRANE POTENTIAL; CYTOLOGY; LONG EVANS RAT; NERVE CELL; PATCH CLAMP; PHYSIOLOGY;

ANIMALIA;

ACTION POTENTIALS; ALGORITHMS; ANIMALS; ENTORHINAL CORTEX; MEMBRANE POTENTIALS; MODELS, NEUROLOGICAL; NERVE NET; NEURONS; PATCH-CLAMP TECHNIQUES; RATS; RATS, LONG-EVANS; THETA RHYTHM;

EID: 78149481436     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0013697     Document Type: Article

References (63)

1. Johnston D, Amaral DG (2004) Hippocampus. In The Synaptic Organization of the Brain GMShepherd, ed. (Oxford University Press). pp 455-498.
2. Amaral DG, Witter MP (1995) The hippocampus. In: Paxinos G, ed. The Rat Nervous System, 2nd ed. New York: Academic Press. pp 443-493.
3. Scharfman HE, Witter MP, Schwarcz R (2000) The Parahippocampal region: Implications for neurological and psychiatric diseases. Annals of the New York Academy of Sciences, V. 911.
4. Dickson CT, Magistretti J, Shalinsky MH, Fransén E, Hasselmo M, et al. (2000) Properties and role of Ih in the pacing of subthreshold oscillation in entorhinal cortex layer II neurons. J Neurophysiol 83: 2562-2579.
5. Haas JS, White JA (2002) Frequency selectivity of layer II stellate cells in the medial entorhinal cortex. J Neurophysiol 88: 2422-2429.
6. Schreiber S, Erchova I, Heinemann U, Herz AV (2004) Subthreshold resonance explains the frequency-dependent integration of periodic as well as random stimuli in the entorhinal cortex. J Neurophysiol 92: 408-415.
7. Engel TA, Schimansky-Geier L, Herz AV, Schreiber S, Erchova I (2008) Subthreshold membrane-potential resonances shape spike-train patterns in the entorhinal cortex. J Neurophysiol 100: 1576-1588.
8. Acker CD, Kopell N, White JA (2003) Synchronization of strongly coupled excitatory neurons: relating network behavior to biophysics. Journal of Computational Neuroscience 15: 71-90.
9. Dudman JT, Nolan MF (2009) Stochastically gating ion channels enable patterned spike firing through activity-dependent modulation of spike probability. PLoS Computational Biology 5: e1000290.
10. Rotstein HG, Oppermann T, White JA, Kopell N (2006) A reduced model for medial entorhinal cortex stellate cells: subthreshold oscillations, spiking and synchronization. Journal of Computational Neuroscience 21: 271-292.
11. Rotstein HG, Wechselberger M, Kopell N (2008) Canard induced mixed-mode oscillations in a medial entorhinal cortex layer II stellate cell model. SIAM J Appl Dyn Sys 7: 1582-1611.
12. + -dependent theta like rhythmicity in stellate cells of entorhinal cortex layer II. Nature 342: 175-177.
13. Alonso AA, García Austt E (1987) Neuronal sources of theta rhythm in the entorhinal cortex of the rat. II. phase relations between unit discharges and theta field potentials. Exp Brain Res 67: 493-501.
14. Fernandez R, White JA (2008) Artificial synaptic conductances reduce subthreshold oscillations and periodic firing in stellate cells of the entorhinal cortex. J Neurosci 28: 3790-3803.
15. Winson J (1978) Loss of hippocampal theta rhythm results in spatial memory deficit in the rat. Science 201: 160-163.
16. Buzsáki G (1989) Two-stage model of memory trace formation: a role for 'noisy' brain states. 31: 551-570.
17. Kahana MJ, Sekuler R, Caplan JB, Kirschen M, Madsen JR (1999) Human theta oscillations exhibit task dependence during virtual maze navigation. Nature 399: 781-784.
18. Rutishauser U, Ross IB, Mamelak AN, Schuman EM (2010) Human memory strength is predicted by theta-frequency phase-locking of single neurons. Nature 464: 903-907.
19. Fyhn M, Molden S, Witter MP, I ME, Moser MB (2004) Spatial representation in the entorhinal cortex. Science 305: 1258-1264.
20. Sargolini F, Fyhn M, Hafting T, McNaughton B, Witter MP, et al. (2006) Conjunctive representation of position, direction, and velocity in the entorhinal cortex. Science 312: 758-762.
21. Moser E, M-B.M (2008) A metric for space. Hippocampus 18: 1142-1156.
22. Hafting T, Fyhn M, Molden S, Moser MB, Moser EI (2005) Microstructure of a spatial map in the entorhinal cortex. Nature 436: 801-806.
23. Bear J, Fountain NB, Lothman EW (1996) Responses of superficial entorhinal cortex in vitro slices from naive and chronically epileptic rats. J Neurophysiol 76: 2928-2940.
24. Scharfman HE, Goodman JH, Du F, Schwarcz R (1998) Chronic changes in synaptic responses of entorhinal hippocampal neurons after amino-oxyacetic acid (AOAA)-induced entorhinal cortical neuron loss. J Neurophysiol 80: 3031-3046.
25. Tolner EA, Klosterman F, van Vliet EA, Witter MP, Lopes da Silva FH, et al. (2005) Presubiculum stimulation in vivo evokes distinct oscillations in superficial and deep entorhinal cortex layers in chronic epileptic rats. J Neurosci 25: 8755-8765.
26. Sloviter RS (1987) Decreased hippocampal inhibition and a selective loos of interneurons in experimental epilepsy. Science 235: 73-76.
27. Bekenstein JW, Lothman EW (1993) Dormancy of inhibitory interneurons in a model of temporal lobe epilepsy. Science 259: 97-100.
28. Du F, Eid T, Lothman EE, Køler C, Schwarcz R (1995) Preferntial neuronal loss in layer III of the medial entorhinal cortex in rat models of temporal lobe epilepsy. J Neurosci 15: 6301-6313.
29. Eid T, Schwarcz R, Ottersen OP (1999) Ultrastructure and immunocytochemical distribution in layer III of the rat medial entorhinal cortex following aminooxyacetic acid-induced seizures. Exp Brain Res 125: 463-475.
30. Schwarcz R, Tore E, Du F (2000) Neurons in layer III of the entorhinal cortex: A role in epileptogenesis and epilepsy? Ann NY Acad Sci 911: 328-342.
31. Kumar SS, Buckmaster PS (2006) Hyperexcitability, interneurons, and loss of GABAergic synapses in entorhinal cortex in a model of temporal lobe epilepsy. J Neurosci 26: 4613-4623.
32. Kumar SS, Jin X, Buckmaster PS, Huguenard JR (2007) Recurrent circuits in layer II of medial entorhinal cortex in a model of temporal lobe epilepsy. J Neurosci 27: 1239-1246.
33. Fransén E, Alonso AA, Dickson CT, Magistretti ME, Hasselmo J (2004) Ionic mechanisms in the generation of subthreshold oscillations and action potential clustering in entorhinal layer II stellate neurons. Hippocampus 14: 368-384.
34. White JA, Budde T, Kay AR (1995) A bifurcation analysis of neuronal subthreshold oscillations. Biophysical J 69: 1203-1217.
35. White JA, Klink R, Alonso A, Kay AR (1998) Noise from voltage-gated ion channels may influence neuronal dynamics in the entorhinal cortex. J Neurophysiol 80: 262-269.
36. Wang XJ (1999) Synaptic basis of cortical persistent activity: the importance of NMDA receptos to working memory. J Neurosci 19: 9587-9603.
37. Middleton S, Jalics J, Kispersky T, LeBeau FEN, Roopun AK, et al. (2008) NMDA receptor-dependent switching between different gamma rhythmgenerating microcircuits in entorhinal cortex. Proc Natl Acad Sci USA 105: 18572-18577.
38. Rotstein HG, Pervouchine D, Gillies MJ, Acker CD, White JA, et al. (2005) Slow and fast inhibition and h-current interact to create a theta rhythm in a model of CA1 interneuron networks. J Neurophysiol 94: 1509-1518.
39. Sutherland C, Doiron B, Longtin A (2009) Feedback-induced gain control in stochastic spiking networks. 100: 475-489.
40. Drover J, Rubin J, Su J, Ermentrout B (2004) Analysis of a canard mechanism by which excitatory synaptic coupling can synchronize neurons at low firing frequencies. SIAM J Appl Math 65: 69-92.
41. Krupa M, Szmolyan P (2001) Extending geometric singular perturbation theory to nonhyperbolic points - fold and canard points in two dimensions. SIAM J Math Anal 33(2): 286-314.
42. Baer SM, Erneux T (1992) Singular Hopf bifurcation to relaxation oscillations. SIAM J Appl Math 52: 1651-1664.
43. Traub RD, Miles R, Wong RK (1989) Model of the origin of rhythmic population oscillations in the hippocampal slice. Science 243: 1319-1325.
44. Traub RD, Miles R, Wong RK (1987) Models of synchronized hippocampal bursts in the presence of inhibition. I. single population events. J Neurophysiol 58: 739-751.
45. Traub RD, Miles R, Wong SLSRK, Schneiderman JH (1987) Models of synchronized hippocampal bursts in the presence of inhibition. I. ongoing spontaneous populations events. J Neurophysiol 58: 752-764.
46. Traub RD, Miles R, Wong RK (1988) Models of synchronous firing in longitudinal slices from the CA3 region of the hippocampus. J Neurophysiol 60: 1481-1496.
47. Wechselberger M (2005) Existence and bifurcation of canards in R3 in the case of a folded node. SIAM J Appl Dyn Syst 4: 101-139.
48. Yoshida M, Alonso A (2007) Cell-type-specific modulation of intrinsic firing properties and subthreshold membrane oscillations by the M(Kv7)-currents in neurons of the entorhinal cortex. J Neurophysiol 98: 2779-2994.
49. Brown DA, Adams PR (1980) Muscarinic supression of novel voltage-sensitive K+ current in a vertebrate neurone. Nature 283: 673-676.
50. Yue C, Yaari Y (2004) KCNQ/M channels control spike afterdepolarization and burst generation in hippocampal neurons. J Neurosci 24: 4614-1624.
51. Jalics J, Krupa M, Rotstein HG (2010) A novel mechanism for mixed-mode oscillations in a neuronal model. Dynamical Systems: An International Journal iFirst. pp 1-38.
52. Kobayashi M, Buckmaster PS (2003) Reduced inhibition of dentate granule cells in a model of temporal lobe epilepsy. J Neurosci 23: 2440-2452.
53. White JA, Haas JS (2001) Intrinsic noise from voltage-gated ion channels: effects on dynamics and reliability in intrinsically oscillatory neurons. In Handbook of Biological Physics 4: 257-278.
54. Netoff TI, Banks MI, Dorval AD, Acker CD, Haas JS, et al. (2005) Synchronization in hybrid neuronal networks of the hippocampal formation. J Neurophysiol 93: 1197-1208.
55. Ben-Menachem E (2007) Retigabine: Has the orphan found a home? Epilepsy Curr 7: 153-154.
56. Wang XJ, Buzsáki G (1996) Gamma oscillations by synaptic inhibition in an interneuronal network model. J Neurosci 16: 6402-6413.
57. Ermentrout GB (2002) Simulating, analyzing, and animating dynamical systems. A guide to XPPAUT for researchers and students. Society for Industrial and Applied Mathematics (Philadelphia, PA, USA).
58. Burden RL, Faires JD (1980) Numerical analysis PWS Publishing Company - Boston.
59. Richardson MJE, Brunel N, Hakim V (2003) From subthreshold to firing-rate resonance. J Neurophysiol 89: 2538-2554.
60. Izhikevich EM (2001) Resonate-and-fire neurons. Neural Networks 14: 883-894.
61. Klink RM, Alonso AA (1997) Ionic mechanisms of muscarinic depolarization in entorhinal cortex layer II neurons. J Neurophysiol 77: 1829-1843.
62. Dorval ADJ, White JA (2005) Channel noise is essential for perithreshold oscillations in entorhinal stellate neurons. J Neurosci 25: 10025-10028.
63. Destexhe A, Mainen ZF, Sejnowski TJ (1994) Synthesis of models for excitable membranes, synaptic transmission and neuromodulation using a common kinetic formalism. Journal of Computational Neuroscience 3: 195-230.