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.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
References
Bischofberger J, Jonas P, (1997) Action potential propagation into the presynaptic dendrites of rat mitral cells. J. Physiol. 504: 359–365.
Brody CD, Hopfield JJ, (2003) Simple networks for spike-timing-based computation, with application to olfactory processing. Neuron 37: 843–852.
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.
Chow CC, Kopell N, (2000) Dynamics of spiking neurons with electrical coupling. Neural Comput. 12: 1643–1678.
Connors BW, Long MA, (2004) Electrical synapses in the Mammalian brain. Annu. Rev. Neurosci. 27: 393–418.
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.
Debarbieux F, Audinat E, Charpak S, (2003) Action potential propagation in dendrites of rat mitral cells in vivo. J. Neurosci. 23: 5553–5560.
Draguhn A, Traub RD, Schmitz D, Jefferys JG, (1998) Electrical coupling underlies high-frequency oscillations in the hippocampus in vitro. Nature 394: 189–192.
Friedman D, Strowbridge BW, (2003) Both electrical and chemical synapses mediate fast network oscillations in the olfactory bulb. J. Neurophysiol. 89: 2601–2610.
Galarreta M, Hestrin S, (2001) Electrical synapses between GABA-releasing interneurons. Nat. Rev. Neurosci. 2: 425– 433.
Haberly LB, (2001) Parallel-distributed processing in olfactory cortex: New insights from morphological and physiological analysis of neuronal circuitry. Chem. Senses 26: 551–576.
Hatton GI, (1998) Synaptic modulation of neuronal coupling. Cell Biol. Intern. 22: 765–780.
Hines M, Carnevale T, (1997) The NEURON simulation environment. Neural Comp. 9: 178–209.
Hines ML, Carnevale NT, (2001) NEURON: A tool for neuroscientists. Neuroscientist 7: 123–135.
Hopfield JJ, Brody CD, (2000) What is a moment? “Cortical” sensory integration over a brief interval. Proc. Natl. Acad. Sci. USA 97: 13919–13924.
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.
Johnston D, Wu SM, (1995) Functional properties of dendrites. In: Foundation of Neurophysiology. MIT Press, Cambridge, Ch. 4.
Kepler TB, Marder E, Abbott LF., (1990) The effect of electrical coupling on the frequency of model neuronal oscillators. Science 248: 83–85.
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.
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.
Lewis TJ, Rinzel J, (2000) Self-organized synchronous oscillations in a network of excitable cells coupled by gap junctions. Network 11: 299–320.
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.
Llinas R, Leznik E, Makarenko VI, (2002) On the amazing olivocerebellar system Ann. N. Y. Acad. Sci. 978: 258–272.
MacVicar BA, Dudek FE, (1982) Electrotonic coupling between granule cells of rat dentate gyrus: Physiological and anatomical evidence. J. Neurophysiol. 47: 579–592.
Margrie TW, Schaefer AT, (2003) Theta oscillation coupled spike latencies yield computational vigour in a mammalian sensory system. J. Physiol. 546: 363–374.
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.
Moortgat KT, Bullock TH, Sejnowski TJ, (2000) Gap junction effects on precision and frequency of a model pacemaker network. J. Neurophysiol. 83: 984–997.
Mori K, Nowycky MC, Shepherd GM, (1981) Electrophysiological analysis of mitral cells in the isolated turtle olfactory bulb. J. Physiol. 314: 281–294.
Perez Velazquez JL, Carlen PL, (2000) Gap junctions, synchrony and seizures. Trends Neurosci. 23: 68–74.
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.
Rall W, (1969) Time constants and electrotonic length of membrane cylinders and neurons. Biophys. J. 9: 1483–1508.
Schoppa NE, Westbrook GL, (2002) AMPA autoreceptors drive correlated spiking in olfactory bulb glomeruli. Nat. Neurosci. 5: 1194–1202.
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.
Sherman A, Rinzel J, (1992) Rhythmogenic effects of weak electrotonic coupling in neuronal models. Proc. Natl. Acad. Sci. USA 89: 2471–2474.
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.
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.
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.
Urban NN, (2002) Lateral inhibition in the olfactory bulb and in olfaction. Physiol. Behav. 77: 607–612.
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.
Vigmond EJ, Perez Velazquez JL, Valiante TA, Bardakjian BL, Carlen PL, (1997) Mechanisms of electrical coupling between pyramidal cells. J. Neurophysiol. 78: 3107–3116.
Wang XY, McKenzie JS, Kemm RE, (1996) Whole-cell K+ currents in identified olfactory bulb output neurones of rats. J. Physiol. 490: 63–77.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Migliore, M., Hines, M.L. & Shepherd, G.M. The Role of Distal Dendritic Gap Junctions in Synchronization of Mitral Cell Axonal Output. J Comput Neurosci 18, 151–161 (2005). https://doi.org/10.1007/s10827-005-6556-1
Issue Date:
DOI: https://doi.org/10.1007/s10827-005-6556-1