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Journal of Computational Neuroscience

, Volume 18, Issue 2, pp 151–161 | Cite as

The Role of Distal Dendritic Gap Junctions in Synchronization of Mitral Cell Axonal Output

  • M. MiglioreEmail author
  • M. L. Hines
  • Gordon M. Shepherd
Article

Abstract

One of the first and most important stages of odor processing occurs in the glomerular units of the olfactory bulb and most likely involves mitral cell synchronization. Using a detailed model constrained by a number of experimental findings, we show how the intercellular coupling mediated by intraglomerular gap junctions (GJs) in the tuft dendrites could play a major role in sychronization of mitral cell action potential output in spite of their distal dendritic location. The model suggests that the high input resistance and active properties of the fine tuft dendrites are instrumental in generating local spike synchronization and an efficient forward and backpropagation of action potentials between the tuft and the soma. The model also gives insight into the physiological significance of long primary dendrites in mitral cells, and provides evidence against the use of reduced single compartmental models to investigate network properties of cortical pyramidal neurons.

Keywords

olfactory processing synchronization modeling gap junction mitral cells 

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References

  1. Bischofberger J, Jonas P, (1997) Action potential propagation into the presynaptic dendrites of rat mitral cells. J. Physiol. 504: 359–365.Google Scholar
  2. Brody CD, Hopfield JJ, (2003) Simple networks for spike-timing-based computation, with application to olfactory processing. Neuron 37: 843–852.Google Scholar
  3. Chen WR, Shen GY, Shepherd GM, Hines ML, Midtgaard J, (2002) Multiple modes of action potential initiation and propagation in mitral cell primary dendrite. J. Neurophysiol. 88: 2755– 2764.Google Scholar
  4. Chow CC, Kopell N, (2000) Dynamics of spiking neurons with electrical coupling. Neural Comput. 12: 1643–1678.Google Scholar
  5. Connors BW, Long MA, (2004) Electrical synapses in the Mammalian brain. Annu. Rev. Neurosci. 27: 393–418.Google Scholar
  6. Davison AP, Feng J, Brown D, (2003) Dendrodendritic inhibition and simulated odor responses in a detailed olfactory bulb network model. J. Neurophysiol. 90: 1921–1935.Google Scholar
  7. Debarbieux F, Audinat E, Charpak S, (2003) Action potential propagation in dendrites of rat mitral cells in vivo. J. Neurosci. 23: 5553–5560.Google Scholar
  8. Draguhn A, Traub RD, Schmitz D, Jefferys JG, (1998) Electrical coupling underlies high-frequency oscillations in the hippocampus in vitro. Nature 394: 189–192.Google Scholar
  9. Friedman D, Strowbridge BW, (2003) Both electrical and chemical synapses mediate fast network oscillations in the olfactory bulb. J. Neurophysiol. 89: 2601–2610.Google Scholar
  10. Galarreta M, Hestrin S, (2001) Electrical synapses between GABA-releasing interneurons. Nat. Rev. Neurosci. 2: 425– 433.Google Scholar
  11. Haberly LB, (2001) Parallel-distributed processing in olfactory cortex: New insights from morphological and physiological analysis of neuronal circuitry. Chem. Senses 26: 551–576.Google Scholar
  12. Hatton GI, (1998) Synaptic modulation of neuronal coupling. Cell Biol. Intern. 22: 765–780.Google Scholar
  13. Hines M, Carnevale T, (1997) The NEURON simulation environment. Neural Comp. 9: 178–209.Google Scholar
  14. Hines ML, Carnevale NT, (2001) NEURON: A tool for neuroscientists. Neuroscientist 7: 123–135.Google Scholar
  15. Hopfield JJ, Brody CD, (2000) What is a moment? “Cortical” sensory integration over a brief interval. Proc. Natl. Acad. Sci. USA 97: 13919–13924.Google Scholar
  16. Hopfield JJ, Brody CD, (2001) What is a moment? Transient synchrony as a collective mechanism for spatiotemporal integration. Proc. Natl. Acad. Sci. USA 98: 1282–1287.Google Scholar
  17. Johnston D, Wu SM, (1995) Functional properties of dendrites. In: Foundation of Neurophysiology. MIT Press, Cambridge, Ch. 4.Google Scholar
  18. Kepler TB, Marder E, Abbott LF., (1990) The effect of electrical coupling on the frequency of model neuronal oscillators. Science 248: 83–85.Google Scholar
  19. Kosaka T, Kosaka K, (2004) Neuronal gap junctions between intraglomerular mitral/tufted cell dendrites in the mouse main olfactory bulb. Neurosci. Res. 49: 373–378.Google Scholar
  20. Laurent G, Stopfer M, Friedrich RW, Rabinovich MI, Volkovskii A, Abarbanel HD, (2001) Odor encoding as an active, dynamical process: Experiments, computation, and theory. Ann. Rev. Neurosci. 24: 263–297.Google Scholar
  21. Lewis TJ, Rinzel J, (2000) Self-organized synchronous oscillations in a network of excitable cells coupled by gap junctions. Network 11: 299–320.Google Scholar
  22. Linster C, Hasselmo M, (1997) Modulation of inhibition in a model of olfactory bulb reduces overlap in the neural representation of olfactory stimuli. Behav. Brain Res. 84: 117–127.Google Scholar
  23. Llinas R, Leznik E, Makarenko VI, (2002) On the amazing olivocerebellar system Ann. N. Y. Acad. Sci. 978: 258–272.Google Scholar
  24. MacVicar BA, Dudek FE, (1982) Electrotonic coupling between granule cells of rat dentate gyrus: Physiological and anatomical evidence. J. Neurophysiol. 47: 579–592.Google Scholar
  25. Margrie TW, Schaefer AT, (2003) Theta oscillation coupled spike latencies yield computational vigour in a mammalian sensory system. J. Physiol. 546: 363–374.Google Scholar
  26. Migliore M, Hoffman DA, Magee JC, Johnston D, (1999) Role of an A-type K+ conductance in the back-propagation of action potentials in the dendrites of hippocampal pyramidal neurons. J. Comput. Neurosci. 7: 5–15.Google Scholar
  27. Moortgat KT, Bullock TH, Sejnowski TJ, (2000) Gap junction effects on precision and frequency of a model pacemaker network. J. Neurophysiol. 83: 984–997.Google Scholar
  28. Mori K, Nowycky MC, Shepherd GM, (1981) Electrophysiological analysis of mitral cells in the isolated turtle olfactory bulb. J. Physiol. 314: 281–294.Google Scholar
  29. Perez Velazquez JL, Carlen PL, (2000) Gap junctions, synchrony and seizures. Trends Neurosci. 23: 68–74.Google Scholar
  30. Pfeuty B, Mato G, Golomb D, Hansel D, (2003) Electrical synapses and synchrony: The role of intrinsic currents. J. Neurosci. 23: 6280–6294. Erratum In: J Neurosci. 23: 7237.Google Scholar
  31. Rall W, (1969) Time constants and electrotonic length of membrane cylinders and neurons. Biophys. J. 9: 1483–1508.Google Scholar
  32. Schoppa NE, Westbrook GL, (2002) AMPA autoreceptors drive correlated spiking in olfactory bulb glomeruli. Nat. Neurosci. 5: 1194–1202.Google Scholar
  33. Shepherd GM, Chen WR, Greer CA, (2004) Olfactory bulb. In The Synaptic Organization of the Brain, (Fifth Edition) ed. Shepherd, GM. New York: Oxford University Press, pp. 165–216.Google Scholar
  34. Sherman A, Rinzel J, (1992) Rhythmogenic effects of weak electrotonic coupling in neuronal models. Proc. Natl. Acad. Sci. USA 89: 2471–2474.Google Scholar
  35. Teubner B et al, (2000) Functional expression of the murine connexin 36 gene coding for a neuron-specific gap junctional protein. J. Membr. Biol. 176: 249–262.Google Scholar
  36. Traub RD, Draguhn A, Whittington MA, Baldeweg T, Bibbig A, Buhl EH, Schmitz D, (2002) Axonal gap junctions between principal neurons: A novel source of network oscillations, and perhaps epileptogenesis. Rev. Neurosci. 13: 1–30.Google Scholar
  37. Traub RD, Pais I, Bibbig A, LeBeau FE, Buhl EH, Hormuzdi SG, Monyer H, Whittington MA (2003) Contrasting roles of axonal, (pyramidal cell) and dendritic, (interneuron) electrical coupling in the generation of neuronal network oscillations. Proc. Natl. Acad. Sci. USA 100: 1370–1374.Google Scholar
  38. Urban NN, (2002) Lateral inhibition in the olfactory bulb and in olfaction. Physiol. Behav. 77: 607–612.Google Scholar
  39. Urban NN, Sakmann B, (2002) Reciprocal intraglomerular excitation and intra- and interglomerular lateral inhibition between mouse olfactory bulb mitral cells. J. Physiol. 542: 355–367.Google Scholar
  40. Vigmond EJ, Perez Velazquez JL, Valiante TA, Bardakjian BL, Carlen PL, (1997) Mechanisms of electrical coupling between pyramidal cells. J. Neurophysiol. 78: 3107–3116.Google Scholar
  41. Wang XY, McKenzie JS, Kemm RE, (1996) Whole-cell K+ currents in identified olfactory bulb output neurones of rats. J. Physiol. 490: 63–77.Google Scholar

Copyright information

© Springer Science+Business Media, Inc. 2005

Authors and Affiliations

  • M. Migliore
    • 1
    Email author
  • M. L. Hines
    • 2
  • Gordon M. Shepherd
    • 2
  1. 1.Department of NeurobiologyYale University School of MedicineNew HavenUSA
  2. 2.Department of NeurobiologyYale University School of MedicineNew HavenUSA

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