Skip to main content
SpringerLink
Log in

How do glutamatergic and GABAergic cells contribute to synchronization in the medial septum?

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

Abstract

The medial septum-diagonal band (MSDB) complex is considered as a pacemaker for the hippocampal theta rhythm. Identification of the different cell types, their electro-physiological properties and their possible function in the generation of a synchronized activity in the MSDB is a hot topic. A recent electro-physiological study showed the presence of two antiphasically firing populations of parvalbumin containing GABAergic neurons in the MSDB. Other papers described a network of cluster-firing glutamatergic neurons, which is able to generate synchronized activity in the MSDB. We propose two different computer models for the generation of synchronized population theta oscillation in the MSDB and compare their properties. In the first model GABAergic neurons are intrinsically theta periodic cluster-firing cells; while in the second model GABAergic cells are fast-firing cells and receive periodic input from local glutamatergic neurons simulated as cluster-firing cells. Using computer simulations we show that the GABAergic neurons in both models are capable of generating antiphasic theta periodic population oscillation relying on local, septal mechanisms. In the first model antiphasic theta synchrony could emerge if GABAergic neurons form two populations preferentially innervate each other. In the second model in-phase synchronization of glutamatergic neurons does not require specific network structure, and the network of these cells are able to act as a theta pacemaker for the local fast-firing GABAergic circuit. Our simulations also suggest that neurons being non-cluster-firing in vitro might exhibit clustering properties when connected into a network in vivo.

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

Access this article

Log in via an institution

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

  • Bland BH, Oddie SD, Colom, LV (1999) Mechanisms of neural synchrony in the septohippocampal pathways underlying hippocampal theta generation. J. Neurosci. 19(8): 3223–3237.

    Google Scholar 

  • Bor-hegyi Z, Varga V, Szilágyi N, Fabó D, Freund TF (2004) Phase segregation of medial septal GABA ergic neurons during hippocampal theta activity. J. Neurosci. 24(39): 8470–8479.

    Google Scholar 

  • Bower JM, Beeman D (1998) The Book of GENESIS: Exploring Realistic Neural Models with the GEneral NEural SImulation System, 2 edition. Springer–Verlag.

  • Brashear HR, Zaborszky L, Heimer L (1986) Distribution of GABAergic and cholinergic neurons in the rat diagonal band. Neuroscience 17(2): 439–451.

    Google Scholar 

  • Brazhnik ES, Fox SE (1997) Intracellular recordings from medial septal neurons during hippocampal theta rhythm. Exp. Brain. Res. 114(3): 442–453.

    Google Scholar 

  • Brazhnik ES, Fox SE (1999) Action potentials and relations to the theta rhythm of medial septal neurons in vivo. Exp. Brain Res. 127(3): 244–258.

    Google Scholar 

  • Cole AE, Nicoll RA (1984) Characterization of a slow cholinergic post-synaptic potential recorded in vitro from rat hippocampal pyramidal cells. J. Physiol. 352: 173–188.

    Google Scholar 

  • Colom LV, Castaneda MT, Reyna T, Hernandez S, Garrido-Sanabria E (2005) Characterization of medial septal glutamatergic neurons and their projection to the hippocampus. Synapse 58(3): 151–164.

    Google Scholar 

  • Destexhe A (2000) Modelling corticothalamic feedback and the gating of the thalamus by the cerebral cortex. J. Physiol. (Paris) 94: 391–410.

    Google Scholar 

  • Dragoi G, Carpi D, Recce M, Csicsvári, J, Buzsáki G (1999) Interactions between hippocampus and medial septum during sharp waves and theta oscillation in the behaving rat. J. Neurosci. 19: 6191–99.

    Google Scholar 

  • Dayan P. Abbott L (2001) Theoretical Neuroscience: Computational and Mathematical Modeling of Neural Systems. MIT Press. Chapter 1: Neural encoding: Firing rates and spike statistics.

  • Ermentrout B (2002) Simulating, Analyzing, Animating Dynami cal Systems: A Guide to XPPAUT for Researchers and Students. SIAM, Philadelphia, PA.

  • Freund TF (1989) GABAergic septohippocampal neurons contain parvalbumin. Brain Res. 478(2): 375–381.

    Google Scholar 

  • Freund TF, Antal M (1988) GABA-containing neurons in the septum control inhibitory interneurons in the hippocampus. Nature 336(6195): 170–173.

    Google Scholar 

  • Frotscher M, Leranth C (1985) Cholinergic innervation of the rat hippocampus as revealed by choline acetyltransferase immunocytochemistry: A combined light and electron microscopic study. J. Comp. Neurol. 239(2): 237–246.

    Google Scholar 

  • Garner HL, Whittington MA, Henderson Z (2005) Induction by kainate of theta frequency rhythmic activity in the rat medial septum-diagonal band complex in vitro. J. Physiol. 564(Pt 1): 83–102.

    Google Scholar 

  • Green JD, Arduini AA (1954) Hippocampal electrical activity in arousal. J. Neurophysiol 17: 533–557.

    Google Scholar 

  • Griffith W (1988) Membrane properties of cell types within guinea pig basal forebrain nuclei in vitro. J. Neurophysiol 59(5): 1590–1612.

    Google Scholar 

  • Griffith W Matthews R (1986) Electrophysiology of AChE-positive neurons in basal forebrain slices. Neurosci. Lett. 71(2): 169–174.

    Google Scholar 

  • Griffith W, Sim J, Matthews R (1991) Electrophysiologic characteristics of basal forebrain neurons in vitro. Adv. Exp. Med. Biol. 295: 143–155.

    Google Scholar 

  • Hajszan T, Alreja M, Leranth C (2004) Intrinsic vesicular glutamate transporter 2-immunoreactive input to septohippocampal parvalbumin-containing neurons: Novel glutamatergic local circuit cells. Hippocampus 14(4): 499–509.

    Google Scholar 

  • Hasselmo ME, Hay J, Ilyn M, Gorchetchnikov A (2002) Neuromodulation, theta rhythm and rat spatial navigation. Neural Netw. 15(4–6): 689–707.

    Google Scholar 

  • Henderson Z, Fiddler G, S Saha AB, Halasy K (2004) A parvalbumin-containing, axosomatic synaptic network in the rat medial septum: relevance to rhythmogenesis. Eur. J. Neurosci. 19(10): 2753–2798.

  • Henderson Z, Morris N, Grimwood P, Fiddler G, Yang H, Appenteng K (2001) Morphology of local axon collaterals of electrophysiologically characterised neurons in the rat medial septal/diagonal band complex. J. Comp. Neurol. 430(3): 410–432.

    Google Scholar 

  • King C, Recce M, O'Keefe J (1998) The rhythmicity of cells of the medial septum/diagonal band of broca in the awake freely moving rat: Relationships with behaviour and hippocampal theta. European J. Neurosci. 10: 464–477.

    Google Scholar 

  • Kiss J, Patel AJ, Baimbridge KG, Freund TF (1990) Topographical localization of neurons containing parvalbumin and choline acetyltransferase in the medial septum-diagonal band region of the rat. Neuroscience 36(1): 61–72.

    Google Scholar 

  • Knapp J, Morris N, Henderson Z, Matthews R (2000) Electrophysiological characteristics of non-bursting, glutamate decarboxylase messenger RNA-positive neurons of the medial septum/diagonal band nuclei of guinea-pig and rat. Neuroscience 98(4): 661–668.

    Google Scholar 

  • Lengyel M, Huhn Z, Erdi P (2005) Computational theories on the function of theta oscillations. Biol. Cybern. 92(6): 393–408.

    Google Scholar 

  • Leung L, Shen B (2004) Glutamatergic synaptic transmission participates in generating the hippocampal EEG. Hippocampus. 14(4):510–525.

    Google Scholar 

  • Manseau F, Danik M, Williams S (2005) A functional glutamatergic neurone network in the medial septum and diagonal band area. J. Physiol. 566(3): 865–884.

    Google Scholar 

  • Morris NP, Harris SJ, Henderson Z (1999) Parvalbumin-immunoreactive, fast-spiking neurons in the medial septum/diagonal band complex of the rat: Intracellular recordings in vitro. Neuroscience 92(2): 589–600.

    Google Scholar 

  • O'Keefe J. and Nadel L (1978) The Hippocampus as a Cognitive Map. Clarendon Press, Oxford.

  • Petsche H, Stumpf C, Gogolak G (1962) The significance of the rabbit's septum as a relay station between the mid-brain and the hippocampus. I The control of hippocampal arousal activity by the septum cells. Electroencephalogr. Clin. Neurophysiol. 14: 202–211.

    Google Scholar 

  • Puma C, Bizot JC (1999) Hippocampal theta rhythm in anesthetized rats: Role of AMPA glutamate receptors. Neuroreport 10(11): 2297–2300.

    Google Scholar 

  • Serafin M, Williams S, Khateb A, Fort P, Muhlethaler M (1996) Rhythmic firing of medial septum non-cholinergic neurons. Neuroscience 75(3): 671–675.

    Google Scholar 

  • Sotty F, Danik M, Manseau F, Quirion R, Williams S (2003) Distinct electrophysiological properties of glutamatergic, cholinergic and GABAergic rat septohippocampal neurons: Novel implications for hippocampal rhythmicity. J. Physiol. 551: 927–943.

    Google Scholar 

  • Stewart M, Fox, SE (1989) Two populations of rhythmically bursting neurons in rat medial septum are revealed by atropine. J. Neurophysiol. 61(5): 982–993.

    Google Scholar 

  • Stewart M, Fox SE (1990) Do septal neurons pace the hippocampal theta rhythm?Trends Neurosci. 13(5): 163–168.

  • Stumpf C, Petsche H, Gogolak G (1962) The significance of the rabbit's septum as a relay station between the midbrain and the hippocampus. II. The differential influence of drugs upon both the septal cell firing pattern and the hippocampus theta activity. Electroencephalogr. Clin. Neurophysiol. 14: 212–219.

    Google Scholar 

  • Vanderwolf CH (1969) Hippocampal electrical activity and voluntary movement in the rat. Electroencephalogr. Clin. Neurophysiol. 26(4): 407–418.

    Google Scholar 

  • Vértes RP, Kocsis B (1997) Brainstem-diencephalo-septohippocampal systems controlling the theta rhythm of the hippocampus. Neuroscience 81: 893–926.

    Google Scholar 

  • Vinogradova O, Brazhnik E, Karanov A, Zhadina S (1980) Neuronal activity of the septum following various types of deafferentation. Brain Res. 187(2): 353–368.

    Google Scholar 

  • Vinogradova OS (1995) Expression, control, probable functional significance of the neuronal theta-rhythm. Prog. Neurobiol. 45(6): 523–583.

    Google Scholar 

  • Wainger B, DeGennaro M, Santoro B, Siegelbaum S, Tibbs G (2001) Molecular mechanism of cAMP modulation of HCN pacemaker channels. Nature 411(6839): 805–10.

    Google Scholar 

  • Wang XJ (2002) Pacemaker neurons for the theta rhythm and their synchronization in the septohippocampal reciprocal loop. J. Neurophysiol. 87(2): 889–900.

    Google Scholar 

  • Wang XJ, Buzsáki G (1996) Gamma oscillation by synaptic inhibitionin a hippocampal interneuronl network model. J. Neurosci. 16: 6402–6413.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Biophysics, KFKI Research Institute of the Hungarian Academy of Sciences, 29–33 Konkoly-Thege street, H-1121, Budapest, Hungary

    Balázs Ujfalussy & Tamás Kiss

  2. Center for Complex Systems Studies, Kalamazoo College, Kalamazoo, MI, 49006

    Balázs Ujfalussy & Tamás Kiss

Authors
  1. Balázs Ujfalussy
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Tamás Kiss
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Balázs Ujfalussy.

Additional information

Action Editor: David Golomb

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ujfalussy, B., Kiss, T. How do glutamatergic and GABAergic cells contribute to synchronization in the medial septum?. J Comput Neurosci 21, 343–357 (2006). https://doi.org/10.1007/s10827-006-9082-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10827-006-9082-x

Keywords

Search

Navigation