Skip to main content
Log in

Beyond Two-Cell Networks: Experimental Measurement of Neuronal Responses to Multiple Synaptic Inputs

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

Abstract

Oscillations of large populations of neurons are thought to be important in the normal functioning of the brain. We have used phase response curve (PRC) methods to characterize the dynamics of single neurons and predict population dynamics. Our past experimental work was limited to special circumstances (e.g., 2-cell networks of periodically firing neurons). Here, we explore the feasibility of extending our methods to predict the synchronization properties of stellate cells (SCs) in the rat entorhinal cortex under broader conditions. In particular, we test the hypothesis that PRCs in SCs scale linearly with changes in synaptic amplitude, and measure how well responses to Poisson process-driven inputs can be predicted in terms of PRCs. Although we see nonlinear responses to excitatory and inhibitory inputs, we find that models based on weak coupling account for scaling and Poisson process-driven inputs reasonably accurately.

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

Access this article

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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

Instant access to the full article PDF.

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 A, Llina’s RR (1989) Subthreshold Na+-dependent theta-like rhythmicity in stellate cells of entorhinal cortex layer II. Nature 342: 175–177.

    Google Scholar 

  • Alonso A, Klink R (1993) Differential electroresponsiveness of stellate and pyramidal-like cells of medial entorhinal cortex layer II. J. Neurophysiol. 70: 128–143.

    Google Scholar 

  • Berretta N, Jones RS (1996) A comparison of spontaneous EPSCs in layer II and layer IV-V neurons of the rat entorhinal cortex in vitro. J. Neurophysiol. 76: 1089–1100.

    Google Scholar 

  • Bland BH, Colom LV (1993) Extrinsic and intrinsic properties underlying oscillation and synchrony in limbic cortex. Progress In Neurobiology 41: 157–208.

    Google Scholar 

  • Canavier CC, Butera RJ, Dror RO, Baxter DA, Clark JW, Byrne JH (1997) Phase response characteristics of model neurons determine which patterns are expressed in a ring circuit model of gait generation. Biol. Cybern. 77: 367–380.

    Google Scholar 

  • Charpak S, Pare D, Llinas R (1995) The entorhinal cortex entrains fast CA1 hippocampal oscillations in the anaesthetized guinea-pig: Role of the monosynaptic component of the perforant path. Eur. J. Neurosci. 7: 1548–1557.

    Google Scholar 

  • Chow CC, White JA, Ritt J, Kopell N (1998) Frequency control in synchronized networks of inhibitory neurons. J. Comput. Neurosci. 5: 407–420.

    Google Scholar 

  • Chrobak JJ, Buzsa’ki G (1998) Gamma oscillations in the entorhinal cortex of the freely behaving rat. J. Neurosci. 18: 388–398.

    Google Scholar 

  • Demir SS, Butera RJ, Jr., DeFranceschi AA, Clark JW, Jr., Byrne JH (1997) Phase sensitivity and entrainment in a modeled bursting neuron. Biophys. J. 72: 579–594.

    Google Scholar 

  • Dorval AD, Christini DJ, White JA (2001) Real-Time linux dynamic clamp: A fast and flexible way to construct virtual ion channels in living cells. Ann. Biomed. Eng. 29: 897–907.

    Google Scholar 

  • Ermentrout B (1996) Type I membranes, phase resetting curves, and synchrony. Neural. Comput. 8: 979–1001.

    Google Scholar 

  • Fries P, Roelfsema PR, Engel AK, Konig P, Singer W (1997) Synchronization of oscillatory responses in visual cortex correlates with perception in interocular rivalry. Proc. Natl. Acad. Sci. USA 94: 12699–12704.

    Google Scholar 

  • Gray CM, Konig P, Engel AK, Singer W (1989) Oscillatory responses in cat visual cortex exhibit inter-columnar synchronization which reflects global stimulus properties. Nature 338: 334– 337.

    Google Scholar 

  • Hansel D, Mato G, Meunier C (1995) Synchrony in excitatory neural networks. Neural. Comput. 7: 307–337.

    Google Scholar 

  • Kopell N, Ermentrout GB (2002) Mechanisms of phase-locking and frequency control in pairs of coupled neural oscillators. In: B Fiedler, ed. Handbook on Dynamical Systems. Elsevier, New York, pp. 3–54.

    Google Scholar 

  • Netoff TI, Banks MI, Dorval AD, Acker CD, Haas JS, Kopell N, White JA (2005) Synchronization in Hybrid Neuronal Networks of the Hippocampal Formation. J. Neurophysiol. (in press).

  • O’Keefe J (1993) Hippocampus, theta, and spatial memory. Current Opinion in Neurobiology 3: 917–924.

    Google Scholar 

  • Oprisan SA, Canavier CC (2001) Stability analysis of rings of pulse-coupled oscillators: The effect of phase-resetting in the second cycle after the pulse is important at synchrony and for long pulses. Differential Equations and Dynamical Systems 9: 243–258.

    Google Scholar 

  • Oprisan SA, Canavier CC (2002) The influence of limit cycle topology on the phase resetting curve. Neural. Comput. 14: 1027–1057.

    Google Scholar 

  • Oprisan SA, Thirumalai V, Canavier CC (2003) Dynamics from a time series: Can we extract the phase resetting curve from a time series? Biophys. J. 84: 2919–2928.

    Google Scholar 

  • Oprisan SA, Prinz AA, Canavier CC (2004) Phase resetting and phase locking in hybrid circuits of one model and one biological neuron. Biophys. J. 87: 2283–2298.

    Google Scholar 

  • Press WH, Teukolsky SA, Vetterling WT, Flannery BP (1992) Numerical recipes in C: The Art of Scientific Computing, 2nd edition. Cambridge University Press, Cambridge [Cambridgeshire], New York.

    Google Scholar 

  • Reyes AD, Fetz EE (1993) Two modes of interspike interval shortening by brief transient depolarizations in cat neocortical neurons. J. Neurophysiol. 69: 1661–1672.

    Google Scholar 

  • Roelfsema PR, Engel AK, Konig P, Singer W (1997) Visuomotor integration is associated with zero time-lag synchronization among cortical areas. Nature 385: 157–161.

    Google Scholar 

  • Singer W (1999) Neurobiology. Striving for coherence [news; comment]. Nature 397: 391, 393.

    Google Scholar 

  • Skaggs WE, McNaughton BL, Wilson MA, Barnes CA (1996) Theta phase precession in hippocampal neuronal populations and the compression of temporal sequences. Hippocampus 6: 149–172.

    Article  CAS  PubMed  Google Scholar 

  • Squire LR, Zola-Morgan S (1991) The medial temporal lobe memory system. Science 253: 1380–1386.

    Google Scholar 

  • Stewart M, Fox SE (1990) Do septal neurons pace the hippocampal theta rhythm? Trends Neurosci. 13: 163–168.

    Google Scholar 

  • Van Vreeswijk C, Abbott LF, Ermentrout GB (1994) When inhibition not excitation synchronizes neural firing. J. Comput. Neurosci. 1: 313–321.

    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

Corresponding author

Correspondence to Theoden I. Netoff.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Netoff, T.I., Acker, C.D., Bettencourt, J.C. et al. Beyond Two-Cell Networks: Experimental Measurement of Neuronal Responses to Multiple Synaptic Inputs. J Comput Neurosci 18, 287–295 (2005). https://doi.org/10.1007/s10827-005-0336-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10827-005-0336-9

Keywords

Navigation