Skip to main content
Log in

The dynamic structure underlying subthreshold oscillatory activity and the onset of spikes in a model of medial entorhinal cortex stellate cells

  • Published:
Journal of Computational Neuroscience Aims and scope Submit manuscript

Abstract

Medial entorhinal cortex layer II stellate cells display subthreshold oscillations (STOs). We study a single compartment biophysical model of such cells which qualitatively reproduces these STOs. We argue that in the subthreshold interval (STI) the seven-dimensional model can be reduced to a three-dimensional system of equations with well differentiated times scales. Using dynamical systems arguments we provide a mechanism for generations of STOs. This mechanism is based on the “canard structure,” in which relevant trajectories stay close to repelling manifolds for a significant interval of time. We also show that the transition from subthreshold oscillatory activity to spiking (“canard explosion”) is controlled in the STI by the same structure. A similar mechanism is invoked to explain why noise increases the robustness of the STO regime. Taking advantage of the reduction of the dimensionality of the full stellate cell system, we propose a nonlinear artificially spiking (NAS) model in which the STI reduced system is supplemented with a threshold for spiking and a reset voltage. We show that the synchronization properties in networks made up of the NAS cells are similar to those of networks using the full stellate cell models.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Acker CD, Kopell N, White JA (2003) Synchronization of strongly coupled excitatory neurons: Relating network behavior to biophysics. J. Comput. Neurosci. 15: 71–90.

    Google Scholar 

  • 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.

  • Alonso AA, Klink R (1993) Differential electroresponsiveness of stellate and pyramidal-like cells of medial entorhinal cortex layer II. J. Neurophysiol. 70: 144–157.

    Google Scholar 

  • Alonso AA, Llinás RR (1989) Subthreshold Na+-dependent theta like rhythmicity in stellate cells of entorhinal cortex layer II. Nature 342: 175–177.

    Google Scholar 

  • Baer SM, Erneux T, Rinzel J (1989) The slow passage through a Hopf bifurcation: delay, memory effects, and resonance. SIAM J. Appl. Math. 49: 55–71.

    Google Scholar 

  • Benoit E, Callot JL, Dienner F, MD (1980) Chasse au Canard. IRMA, Strasbourg.

  • Brons M, Krupa M, Wechselberger M (2005) Mixed mode oscillations due to the generalized canard phenomenon. Submitted.

  • Burden RL, Faires JD (1980) Numerical Analysis. PWS Publishing Company, Boston.

  • Buzsáki G (1989) Two-stage model of memory trace formation: A role for ‘noisy’ brain states. Neuroscience 31: 551–570.

    Google Scholar 

  • Buzsáki G, Draguhn (2004) Neuronal oscillations in cortical networks. Science 304: 1926–1929.

  • Chow CC, White JA (1996) Spontaneous action potentials due to channel fluctuation. Bioph. J. 71: 3013–3021.

    Google Scholar 

  • Clewley R, Rotstein HG, Kopell N (2005) A computational tool for the reduction of nonlinear ode systems possening multiple scales. SIAM J. Multiscale Model. Sim. (in press).

  • Dayan P, Abbott LF (2001) Theoretical Neuroscience. The MIT Press.

  • Destexhe A, Mainen ZF, Sejnowski TJ (1994) Synthesis of models for excitable membranes, synaptic transmission and neuromodulation using a common kinetic formalism 3: 195–230.

  • Dickson CT, Magistretti J, Shalinsky M, Hamam B, Alonso AA (2000a) Oscillatory activity in entorhinal neurons and circuits. Ann. NY Acad. Sci. 911: 127–150.

    Google Scholar 

  • Dickson CT, Magistretti J, Shalinsky MH, Fransén E, Hasselmo M, Alonso AA (2000b) Properties and role of I h in the pacing of subthreshold oscillation in entorhinal cortex layer II neurons. J. Neurophysiol. 83: 2562–2579.

    Google Scholar 

  • 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.

    Google Scholar 

  • Dumortier F, Roussarie R (1996) Canard cycles and center manifolds. Mem. Am. Math. Soc. 121 (577).

  • Eckhaus W (1983) Relaxation oscillations including a standard chase on french ducks. In Lecture Notes in Mathematics, Springer-Verlag 985: 449–497.

  • Erchova I, Kreck G, Heinemann U, Herz AVM (2004) Dynamics of rat entorhinal cortex layer II and III cells: characteristics of membrane potential resonance ar rest predict oscillation properties near threshold. J. Physiol. 560: 89–110.

    Google Scholar 

  • Fenichel N (1971) Persistence and smoothness of invariant manifolds for flows. Ind. Univ. Math. J. 21: 193–225.

    Google Scholar 

  • Fransén E, Alonso AA, Dickson CT, Magistretti J, Hasselmo ME (2004) Ionic mechanisms in the generation of subthreshold oscillations and action potential clustering in entorhinal layer II stellate neurons. Hippocampus 14: 368–384.

    Google Scholar 

  • Fransén E, Dickson CT, Magistretti J, Alonso AA, Hasselmo ME (1998) Modeling the generation of subthreshold membrane potential oscillations of entorhinal cortex layer II stellate cells. Soc. Neurosci. Abstr. 24: 814–815.

    Google Scholar 

  • Fransén E, Wallestein GV, Alonso AA, Dickson CT, Hasselmo ME (1999) A biophysical simulation of intrinsic and network properties of entorhinal cortex. Neurocomputing 26–27: 375–380

  • Gillies MJ, Traub RD, LeBeau FEN, Davies CH, Gloveli T, Buhl EH, Whittington MA (2002) A model of atropine-resistant theta oscillations in rat hippocampal area CA1. J. Physiol. 543.3: 779–793.

    Google Scholar 

  • Hutcheon B, Miura RM, Puil E (1996) Subthreshold membrane resonance in neocortical neurons. J. Neurophysiol. 76: 683–697.

    Google Scholar 

  • Hutcheon B, Yarom Y (2000) Resonance oscillations and the intrinsic frequency preferences in neurons. Trends Neurosci. 23: 216–222.

    Google Scholar 

  • Izhikevich E (2005) Dynamical Systems in Neuroscience. (http://www.nsi.edu/users/izhikevich/publications/index.htm), Section 5.1.4. MIT Press.

  • Izhikevich EM (2001) Resonate-and-fire neurons. Neural Netw. 14: 883–894.

    Google Scholar 

  • Jalics J, Kispersky T, Dickson C, Kopell N (2004) Neuronal ensembles and modules: Modeling dynamics in medial entorhinal cortex. Soc. Neurosci. Abstr. 517.1.

  • Jalics J, Rotstein HG, Kopell N (2005) Unpublished data.

  • 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.

    Google Scholar 

  • Klink RM, Alonso A (1993) Ionic mechanisms for the subthreshold oscillations and differential electroresponsiveness of medial entorhinal cortex layer II neurons. J. Neurophysiol. 70: 128–143.

    Google Scholar 

  • Klink RM, Alonso AA (1997) Ionic mechanisms of muscarinic depolarization in entorhinal cortex layer II neurons. J. Neurophysiol. 77: 1829–1843.

    Google Scholar 

  • Koch C (1999) Biophysics of Computation. Oxford University Press.

  • Kopell N, LeMasson G (1994) Rhythmogenesis, amplitude modulation, and multiplexing in a cortical architecture. Proc. Natl. Acad. Sci. USA 91: 10586–10590.

    Google Scholar 

  • Krupa M, Szmolyan P (2001) Relaxation oscillation and canard explosion. J. Diff. Eq. 174: 312–368.

    Google Scholar 

  • Llinás RR, Yarom Y (1981) Electrophysiology of mammalian inferior olivary neurons in vitro different types of voltage-dependent ionic conductances. J. Physiol. 315: 549–567.

    Google Scholar 

  • Llinás RR, Yarom Y (1986) Oscillatory properties of guinea pig olivary neurons and their pharmachological modulation: An in vitro study. J. Physiol. 376: 163–182.

    Google Scholar 

  • Magistretti J, Alonso AA (1999) Biophysical properties and slow valtage-dependent inactivation of a sustained sodium current in entorhinal cortex layer-II principal neurons. a whole-cell and single-channel study. J. Gen. Physiol. 114(4): 491–509.

    Google Scholar 

  • Magistretti J, Ragsdale DS (1999) High conductance sustained single-channel activity responsible for the low-threshold persistent Na+ current in entorhinal cortex neurons. J. Neurosci. 19(17): 7334–7341.

    Google Scholar 

  • Makarov VA, Nekorkin VI, Velarde MG (2001) Spiking behavior in a noise-driven system combining oscillatory and excitatory properties. Phys. Rev. Lett. 15: 3031–3034.

    Google Scholar 

  • Neishtadt AI (1987) Persistence of stability loss for dynamical bifurcations I. Diff. Eqs. 23: 1385–1391.

    Google Scholar 

  • Neishtadt AI (1988) Persistence of stability loss for dynamical bifurcations II. Diff. Eqs. 24: 171–176.

    Google Scholar 

  • Netoff T, Banks M, White J (2003) Bridging single cell and network dynamics. Soc. Neurosci. Abstr. 32: 171.7.

    Google Scholar 

  • Netoff T, Pervouchine D, Kopell N, White J (2004) Oscillation frequency switches in model and hybrid networks of the hippocampus. Soc. Neurosci. Abstr. *32*. In press.

  • Pervouchine DD, Netoff TI, Rotstein HG, White JA, Kopell N (2005) Low-dimensional maps encoding dynamics in entorhinal cortex and hippocampus. In revision.

  • Richardson MJE, Brunel N, Hakim V (2003) From subthreshold to firing-rate resonance. J. Neurophysiol. 89: 2538–2554.

    Google Scholar 

  • Rinzel J (1985) Excitation dynamics: Insights from simplified membrane models. Fed. Proc. 44: 2944–2946.

    Google Scholar 

  • Rotstein HG, Clewley R, Wechselberger M, Kopell N (2005a) Reduction of dimensions and dynamics of a medial entorhinal cortex layer II stellate cell model. In preparation.

  • Rotstein HG, Pervouchine D, Gillies MJ, Acker CD, White JA, Buhl EH, Whittington MA, Kopell N (2005b) 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • Shalinsky JH, Magistretti J, Ma L, Alonso AA (2002) Muscarinic activation of a cation current and associated current noise in entorhinal-cortex layer-II neurons. J. Neurophysiol. 88: 1197–1211.

    Google Scholar 

  • Spain WJ, Schwindt PC, Crill WE (1987) Anomalous rectification in neurons from cat sensorimotor cortex in vitro. J. Neurophysiol. 57: 1555–1576.

    Google Scholar 

  • Szmolyan P, Wechselberger M (2001) Canards in R 3. J. Diff. Eq. 177: 419–453.

  • Wechselberger M (2005) Existence and bifurcation of canards in R 3 in the case of a folded node. SIAM J. Appl. Dyn. Syst. 4: 101–139.

    Google Scholar 

  • White JA, Budde T, Kay ARA (1995) A bifurcation analysis of neuronal subthreshold oscillations. Biophysical. J. 69: 1203–1217.

    Google Scholar 

  • White JA, Klink R, Alonso A, Kay ARA (1998) Noise from voltage-gated ion channels may influence neuronal dynamics in the entorhinal cortex. J. Neurophysiol. 80: 262–269.

    Google Scholar 

  • White JA, Rubinstein JT, Kay AA (2000) Channel noise in neurons. Trends Neurosci. 23(3): 131–137.

    Google Scholar 

  • Winson J (1978) Loss of hippocampal theta rhythm results in spatial memory deficit in the rat. Science 201: 160–163.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Additional information

In memory of Angel A. Alonso

Rights and permissions

Reprints and permissions

About this article

Cite this article

Rotstein, H.G., Oppermann, T., White, J.A. et al. The dynamic structure underlying subthreshold oscillatory activity and the onset of spikes in a model of medial entorhinal cortex stellate cells. J Comput Neurosci 21, 271–292 (2006). https://doi.org/10.1007/s10827-006-8096-8

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10827-006-8096-8

Keywords

Navigation