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Science 311 (5765): 1290-1293

Copyright © 2006 by the American Association for the Advancement of Science

Combined Analog and Action Potential Coding in Hippocampal Mossy Fibers

Henrik Alle, and Jörg R. P. Geiger*

Abstract: In the mammalian cortex, it is generally assumed that the output information of neurons is encoded in the number and the timing of action potentials. Here, we show, by using direct patchclamp recordings from presynaptic hippocampal mossy fiber boutons, that axons transmit analog signals in addition to action potentials. Excitatory presynaptic potentials result from subthreshold dendritic synaptic inputs, which propagate several hundreds of micrometers along the axon and modulate action potential–evoked transmitter release at the mossy fiber–CA3 synapse. This combined analog and action potential coding represents an additional mechanism for information transmission in a major hippocampal pathway.

Independent Hertie Research Group, Max Planck Institute for Brain Research, D-60528 Frankfurt, Germany.

* To whom correspondence should be addressed. E-mail: geiger{at}mpih-frankfurt.mpg.de


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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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S. R. Williams and S. E. Atkinson (2007)
J. Physiol. 585, 759-777
   Abstract »    Full Text »    PDF »
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J. Neurosci. 27, 13420-13429
   Abstract »    Full Text »    PDF »
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P. Krieger, T. Kuner, and B. Sakmann (2007)
J. Neurosci. 27, 11473-11482
   Abstract »    Full Text »    PDF »
Structural Determinants of Transmission at Large Hippocampal Mossy Fiber Synapses.
A. Rollenhagen, K. Satzler, E. P. Rodriguez, P. Jonas, M. Frotscher, and J. H. R. Lubke (2007)
J. Neurosci. 27, 10434-10444
   Abstract »    Full Text »    PDF »
Activation of Presynaptic GABAA Receptors Induces Glutamate Release from Parallel Fiber Synapses.
B. M. Stell, P. Rostaing, A. Triller, and A. Marty (2007)
J. Neurosci. 27, 9022-9031
   Abstract »    Full Text »    PDF »
Subthreshold Dendritic Signal Processing and Coincidence Detection in Dentate Gyrus Granule Cells.
C. Schmidt-Hieber, P. Jonas, and J. Bischofberger (2007)
J. Neurosci. 27, 8430-8441
   Abstract »    Full Text »    PDF »
Selective control of cortical axonal spikes by a slowly inactivating K+ current.
Y. Shu, Y. Yu, J. Yang, and D. A. McCormick (2007)
PNAS 104, 11453-11458
   Abstract »    Full Text »    PDF »
Action Potential Initiation and Propagation in CA3 Pyramidal Axons.
J. P. Meeks and S. Mennerick (2007)
J Neurophysiol 97, 3460-3472
   Abstract »    Full Text »    PDF »
Synapses in the Fly Motion-Vision Pathway: Evidence for a Broad Range of Signal Amplitudes and Dynamics.
U. Beckers, M. Egelhaaf, and R. Kurtz (2007)
J Neurophysiol 97, 2032-2041
   Abstract »    Full Text »    PDF »
GABAergic Spill-Over Transmission onto Hippocampal Mossy Fiber Boutons.
H. Alle and J. R. P. Geiger (2007)
J. Neurosci. 27, 942-950
   Abstract »    Full Text »    PDF »
Properties of Action-Potential Initiation in Neocortical Pyramidal Cells: Evidence From Whole Cell Axon Recordings.
Y. Shu, A. Duque, Y. Yu, B. Haider, and D. A. McCormick (2007)
J Neurophysiol 97, 746-760
   Abstract »    Full Text »    PDF »
Electrophysiological Mechanisms of Delayed Excitotoxicity: Positive Feedback Loop Between NMDA Receptor Current and Depolarization-Mediated Glutamate Release.
C. M. Norris, E. M. Blalock, O. Thibault, L. D. Brewer, G. V. Clodfelter, N. M. Porter, and P. W. Landfield (2006)
J Neurophysiol 96, 2488-2500
   Abstract »    Full Text »    PDF »
Kv7/KCNQ/M-channels in rat glutamatergic hippocampal axons and their role in regulation of excitability and transmitter release.
K. Vervaeke, N. Gu, C. Agdestein, H. Hu, and J. F. Storm (2006)
J. Physiol. 576, 235-256
   Abstract »    Full Text »    PDF »
Main determinants of presynaptic Ca2+ dynamics at individual mossy fiber-CA3 pyramidal cell synapses..
R. Scott and D. A. Rusakov (2006)
J. Neurosci. 26, 7071-7081
   Abstract »    Full Text »    PDF »
Analogue brains.
W. A. Wells (2006)
J. Cell Biol. 172, 958
   Full Text »    PDF »

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