Note to users. If you're seeing this message, it means that your browser cannot find this page's style/presentation instructions -- or possibly that you are using a browser that does not support current Web standards. Find out more about why this message is appearing, and what you can do to make your experience of our site the best it can be.

Site Tools

  • AAAS
  • Subscribe
  • Feedback

Site Search

Search Advanced

Science 17 October 1997:
Vol. 278. no. 5337, pp. 463 - 467
DOI: 10.1126/science.278.5337.463

Reports

Forward and Backward Propagation of Dendritic Impulses and Their Synaptic Control in Mitral Cells

Wei R. Chen, * Jens Midtgaard, Gordon M. Shepherd

The site of impulse initiation is crucial for the integrative actions of mammalian central neurons, but this question is currently controversial. Some recent studies support classical evidence that the impulse always arises in the soma-axon hillock region, with back-propagation through excitable dendrites, whereas others indicate that the dendrites are sufficiently excitable to initiate impulses that propagate forward along the dendrite to the soma-axon hillock. This issue has been addressed in the olfactory mitral cell, in which excitatory synaptic input is restricted to the distal tuft of a single primary dendrite. In rat olfactory bulb slices, dual whole cell recordings were made at or near the soma and from distal sites on the primary dendrite. The results show that the impulse can be initiated in either the soma-axon hillock or in the distal primary dendrite, and that the initiation site is controlled physiologically by the excitatory synaptic inputs to the distal tuft and inhibitory synaptic inputs near the soma.

W. R. Chen and G. M. Shepherd, Section of Neurobiology, Yale University School of Medicine, New Haven, CT 06510, USA.
J. Midtgaard, Department of Medical Physiology, University of Copenhagen, DK-2200 N, Copenhagen, Denmark.
*   To whom correspondence should be addressed.


Read the Full Text


THIS ARTICLE HAS BEEN CITED BY OTHER ARTICLES:
The Origin of the Complex Spike in Cerebellar Purkinje Cells.
J. T. Davie, B. A. Clark, and M. Hausser (2008)
J. Neurosci. 28, 7599-7609
   Abstract »    Full Text »    PDF »
Extending Cable Theory to Heterogeneous Dendrites.
C. Meunier and B. L. d'Incamps (2008)
Neural Comput. 20, 1732-1775
   Abstract »    Full Text »    PDF »
Dendritic Action Potential Initiation in Hypothalamic Gonadotropin-Releasing Hormone Neurons.
C. B. Roberts, R. E. Campbell, A. E. Herbison, and K. J. Suter (2008)
Endocrinology 149, 3355-3360
   Abstract »    Full Text »    PDF »
Functional Structure of the Mitral Cell Dendritic Tuft in the Rat Olfactory Bulb.
M. Djurisic, M. Popovic, N. Carnevale, and D. Zecevic (2008)
J. Neurosci. 28, 4057-4068
   Abstract »    Full Text »    PDF »
Dendritic Excitability and Synaptic Plasticity.
P. J. Sjostrom, E. A. Rancz, A. Roth, and M. Hausser (2008)
Physiol Rev 88, 769-840
   Abstract »    Full Text »    PDF »
Action potential initiation and propagation in hippocampal mossy fibre axons.
C. Schmidt-Hieber, P. Jonas, and J. Bischofberger (2008)
J. Physiol. 586, 1849-1857
   Abstract »    Full Text »    PDF »
An Energy Budget for the Olfactory Glomerulus.
J. C. Nawroth, C. A. Greer, W. R. Chen, S. B. Laughlin, and G. M. Shepherd (2007)
J. Neurosci. 27, 9790-9800
   Abstract »    Full Text »    PDF »
Synaptic Activation of Dendritic AMPA and NMDA Receptors Generates Transient High-Frequency Firing in Substantia Nigra Dopamine Neurons In Vitro.
S. N. Blythe, J. F. Atherton, and M. D. Bevan (2007)
J Neurophysiol 97, 2837-2850
   Abstract »    Full Text »    PDF »
Dendritic Processing of Excitatory Synaptic Input in Hypothalamic Gonadotropin Releasing-Hormone Neurons.
C. B. Roberts, J. A. Best, and K. J. Suter (2006)
Endocrinology 147, 1545-1555
   Abstract »    Full Text »    PDF »
Branch-Specific Ca2+ Influx from Na+-Dependent Dendritic Spikes in Olfactory Granule Cells.
T. Zelles, J. D. Boyd, A. B. Hardy, and K. R. Delaney (2006)
J. Neurosci. 26, 30-40
   Abstract »    Full Text »    PDF »
Constraining Compartmental Models Using Multiple Voltage Recordings and Genetic Algorithms.
N. Keren, N. Peled, and A. Korngreen (2005)
J Neurophysiol 94, 3730-3742
   Abstract »    Full Text »    PDF »
SK Channel Regulation of Dendritic Excitability and Dendrodendritic Inhibition in the Olfactory Bulb.
B. J. Maher and G. L. Westbrook (2005)
J Neurophysiol 94, 3743-3750
   Abstract »    Full Text »    PDF »
Complementary Roles of Cholecystokinin- and Parvalbumin-Expressing GABAergic Neurons in Hippocampal Network Oscillations.
T. Klausberger, L. F. Marton, J. O'Neill, J. H. J. Huck, Y. Dalezios, P. Fuentealba, W. Y. Suen, E. Papp, T. Kaneko, M. Watanabe, et al. (2005)
J. Neurosci. 25, 9782-9793
   Abstract »    Full Text »    PDF »
Imaging of Spiking and Subthreshold Activity of Mitral Cells with Voltage-Sensitive Dyes.
M. DJURISIC and D. ZECEVIC (2005)
Ann. N.Y. Acad. Sci. 1048, 92-102
   Abstract »    Full Text »    PDF »
Tuft Calcium Spikes in Accessory Olfactory Bulb Mitral Cells.
N. N. Urban and J. B. Castro (2005)
J. Neurosci. 25, 5024-5028
   Abstract »    Full Text »    PDF »
Dendritic Sodium Spikelets and Low-Threshold Calcium Spikes in Turtle Olfactory Bulb Granule Cells.
G. Pinato and J. Midtgaard (2005)
J Neurophysiol 93, 1285-1294
   Abstract »    Full Text »    PDF »
Synaptically Recruited Apical Currents Are Required to Initiate Axonal and Apical Spikes in Hippocampal Pyramidal Cells: Modulation by Inhibition.
S. Canals, L. Lopez-Aguado, and O. Herreras (2005)
J Neurophysiol 93, 909-918
   Abstract »    Full Text »    PDF »
Information Processing in the Mammalian Olfactory System.
P.-M. Lledo, G. Gheusi, and J.-D. Vincent (2005)
Physiol Rev 85, 281-317
   Abstract »    Full Text »    PDF »
On the Initiation and Propagation of Dendritic Spikes in CA1 Pyramidal Neurons.
S. Gasparini, M. Migliore, and J. C. Magee (2004)
J. Neurosci. 24, 11046-11056
   Abstract »    Full Text »    PDF »
Action Potential Backpropagation and Multiglomerular Signaling in the Rat Vomeronasal System.
J. Ma and G. Lowe (2004)
J. Neurosci. 24, 9341-9352
   Abstract »    Full Text »    PDF »
Inhibitory Interneurons in the Olfactory Bulb: From Development to Function.
P.-M. Lledo, A. Saghatelyan, and M. Lemasson (2004)
Neuroscientist 10, 292-303
   Abstract »    PDF »
Voltage Imaging from Dendrites of Mitral Cells: EPSP Attenuation and Spike Trigger Zones.
M. Djurisic, S. Antic, W. R. Chen, and D. Zecevic (2004)
J. Neurosci. 24, 6703-6714
   Abstract »    Full Text »    PDF »
Endoplasmic Reticulum Export Site Formation and Function in Dendrites.
M. Aridor, A. K. Guzik, A. Bielli, and K. N. Fish (2004)
J. Neurosci. 24, 3770-3776
   Abstract »    Full Text »    PDF »
Sodium Channels and Dendritic Spike Initiation at Excitatory Synapses in Globus Pallidus Neurons.
J. E. Hanson, Y. Smith, and D. Jaeger (2004)
J. Neurosci. 24, 329-340
   Abstract »    Full Text »    PDF »
Action Potential Initiation and Propagation in Layer 5 Pyramidal Neurons of the Rat Prefrontal Cortex: Absence of Dopamine Modulation.
A. T. Gulledge and G. J. Stuart (2003)
J. Neurosci. 23, 11363-11372
   Abstract »    Full Text »    PDF »
Regulation of Granule Cell Excitability by a Low-Threshold Calcium Spike in Turtle Olfactory Bulb.
G. Pinato and J. Midtgaard (2003)
J Neurophysiol 90, 3341-3351
   Abstract »    Full Text »    PDF »
Supralinear Ca2+ Influx into Dendritic Tufts of Layer 2/3 Neocortical Pyramidal Neurons In Vitro and In Vivo.
J. Waters, M. Larkum, B. Sakmann, and F. Helmchen (2003)
J. Neurosci. 23, 8558-8567
   Abstract »    Full Text »    PDF »
Dendrodendritic Inhibition and Simulated Odor Responses in a Detailed Olfactory Bulb Network Model.
A. P. Davison, J. Feng, and D. Brown (2003)
J Neurophysiol 90, 1921-1935
   Abstract »    Full Text »    PDF »
Action Potential Propagation in Dendrites of Rat Mitral Cells In Vivo.
F. Debarbieux, E. Audinat, and S. Charpak (2003)
J. Neurosci. 23, 5553-5560
   Abstract »    Full Text »    PDF »
Branching Out: A New Idea for Dendritic Function. Focus on "Coincidence Detection in Pyramidal Neurons Is Tuned by Their Dendritic Branching Pattern".
N. Spruston (2003)
J Neurophysiol 89, 2887-2888
   Full Text »    PDF »
Regulation of Backpropagating Action Potentials in Mitral Cell Lateral Dendrites by A-Type Potassium Currents.
J. M. Christie and G. L. Westbrook (2003)
J Neurophysiol 89, 2466-2472
   Abstract »    Full Text »    PDF »
A Dynamic Dendritic Refractory Period Regulates Burst Discharge in the Electrosensory Lobe of Weakly Electric Fish.
L. Noonan, B. Doiron, C. Laing, A. Longtin, and R. W. Turner (2003)
J. Neurosci. 23, 1524-1534
   Abstract »    Full Text »    PDF »
Multiple Modes of Action Potential Initiation and Propagation in Mitral Cell Primary Dendrite.
W. R. Chen, G. Y. Shen, G. M. Shepherd, M. L. Hines, and J. Midtgaard (2002)
J Neurophysiol 88, 2755-2764
   Abstract »    Full Text »    PDF »
Structural Inhomogeneities Differentially Modulate Action Currents and Population Spikes Initiated in the Axon or Dendrites.
L. Lopez-Aguado, J. M. Ibarz, P. Varona, and O. Herreras (2002)
J Neurophysiol 88, 2809-2820
   Abstract »    Full Text »    PDF »
Signaling of Layer 1 and Whisker-Evoked Ca2+ and Na+ Action Potentials in Distal and Terminal Dendrites of Rat Neocortical Pyramidal Neurons In Vitro and In Vivo.
M. E. Larkum and J. J. Zhu (2002)
J. Neurosci. 22, 6991-7005
   Abstract »    Full Text »    PDF »
Functional Inhibition in Direction-Selective Retinal Ganglion Cells: Spatiotemporal Extent and Intralaminar Interactions.
S. F. Stasheff and R. H. Masland (2002)
J Neurophysiol 88, 1026-1039
   Abstract »    Full Text »    PDF »
Inhibition of Backpropagating Action Potentials in Mitral Cell Secondary Dendrites.
G. Lowe (2002)
J Neurophysiol 88, 64-85
   Abstract »    Full Text »    PDF »
Differential Effects of Serotonin Enhance Activity of an Electrically Coupled Neural Network.
B. D. Burrell, C. L. Sahley, and K. J. Muller (2002)
J Neurophysiol 87, 2889-2895
   Abstract »    Full Text »    PDF »
Dichotomy of Action-Potential Backpropagation in CA1 Pyramidal Neuron Dendrites.
N. L. Golding, W. L. Kath, and N. Spruston (2001)
J Neurophysiol 86, 2998-3010
   Abstract »    Full Text »    PDF »
Multiple Sites of Action Potential Initiation Increase Neuronal Firing Rate.
S. A. Baccus, C. L. Sahley, and K. J. Muller (2001)
J Neurophysiol 86, 1226-1236
   Abstract »    Full Text »    PDF »
Membrane Bistability in Olfactory Bulb Mitral Cells.
P. Heyward, M. Ennis, A. Keller, and M. T. Shipley (2001)
J. Neurosci. 21, 5311-5320
   Abstract »    Full Text »    PDF »
Dendritic Glutamate Autoreceptors Modulate Signal Processing in Rat Mitral Cells.
P.-A. Salin, P.-M. Lledo, J.-D. Vincent, and S. Charpak (2001)
J Neurophysiol 85, 1275-1282
   Abstract »    Full Text »    PDF »
Propagation of Action Potentials in Dendrites Depends on Dendritic Morphology.
P. Vetter, A. Roth, and M. Hausser (2001)
J Neurophysiol 85, 926-937
   Abstract »    Full Text »    PDF »
Odor-evoked calcium signals in dendrites of rat mitral cells.
S. Charpak, J. Mertz, E. Beaurepaire, L. Moreaux, and K. Delaney (2001)
PNAS
   Abstract »    Full Text »
The Contribution of Dendritic Kv3 K+ Channels to Burst Threshold in a Sensory Neuron.
A. J. Rashid, E. Morales, R. W. Turner, and R. J. Dunn (2001)
J. Neurosci. 21, 125-135
   Abstract »    Full Text »    PDF »
Action potential propagation in mitral cell lateral dendrites is decremental and controls recurrent and lateral inhibition in the mammalian olfactory bulb.
T. W. Margrie, B. Sakmann, and N. N. Urban (2000)
PNAS
   Abstract »    Full Text »
Diversity and Dynamics of Dendritic Signaling.
M. Häusser, N. Spruston, and G. J. Stuart (2000)
Science 290, 739-744
   Abstract »    Full Text »
Tonic and Synaptically Evoked Presynaptic Inhibition of Sensory Input to the Rat Olfactory Bulb Via GABAB Heteroreceptors.
V. Aroniadou-Anderjaska, F.-M. Zhou, C. A. Priest, M. Ennis, and M. T. Shipley (2000)
J Neurophysiol 84, 1194-1203
   Abstract »    Full Text »    PDF »
Conditional Spike Backpropagation Generates Burst Discharge in a Sensory Neuron.
N. Lemon and R. W. Turner (2000)
J Neurophysiol 84, 1519-1530
   Abstract »    Full Text »    PDF »
Macroscopic and Subcellular Factors Shaping Population Spikes.
P. Varona, J. M. Ibarz, L. Lopez-Aguado, and O. Herreras (2000)
J Neurophysiol 83, 2192-2208
   Abstract »    Full Text »    PDF »
Action Potential Reflection and Failure at Axon Branch Points Cause Stepwise Changes in EPSPs in a Neuron Essential for Learning.
S. A. Baccus, B. D. Burrell, C. L. Sahley, and K. J. Muller (2000)
J Neurophysiol 83, 1693-1700
   Abstract »    Full Text »    PDF »
Long-Lasting Depolarizations in Mitral Cells of the Rat Olfactory Bulb.
G. C. Carlson, M. T. Shipley, and A. Keller (2000)
J. Neurosci. 20, 2011-2021
   Abstract »    Full Text »    PDF »
Distal Initiation and Active Propagation of Action Potentials in Interneuron Dendrites.
M. Martina, I. Vida, and P. Jonas (2000)
Science 287, 295-300
   Abstract »    Full Text »
Computational Analysis of Action Potential Initiation in Mitral Cell Soma and Dendrites Based on Dual Patch Recordings.
G. Y. Shen, W. R. Chen, J. Midtgaard, G. M. Shepherd, and M. L. Hines (1999)
J Neurophysiol 82, 3006-3020
   Abstract »    Full Text »    PDF »
Signal Transfer in Passive Dendrites with Nonuniform Membrane Conductance.
M. London, C. Meunier, and I. Segev (1999)
J. Neurosci. 19, 8219-8233
   Abstract »    Full Text »    PDF »
Physiological Properties of Macaque V1 Neurons are Correlated With Extracellular Spike Amplitude, Duration, and Polarity.
M. Gur, A. Beylin, and D. M. Snodderly (1999)
J Neurophysiol 82, 1451-1464
   Abstract »    Full Text »    PDF »
The Role of Dendritic Filtering in Associative Long-Term Synaptic Plasticity.
V. Sourdet and D. Debanne (1999)
Learn. Mem. 6, 422-447
   Abstract »    Full Text »
Action Potentials in the Dendrites of Retinal Ganglion Cells.
T. J. Velte and R. H. Masland (1999)
J Neurophysiol 81, 1412-1417
   Abstract »    Full Text »    PDF »
Current-Source Density Analysis in the Rat Olfactory Bulb: Laminar Distribution of Kainate/AMPA- and NMDA-Receptor-Mediated Currents.
V. Aroniadou-Anderjaska, M. Ennis, and M. T. Shipley (1999)
J Neurophysiol 81, 15-28
   Abstract »    Full Text »    PDF »
Dendrodendritic Inhibition in the Olfactory Bulb Is Driven by NMDA Receptors.
N. E. Schoppa, J. M. Kinzie, Y. Sahara, T. P. Segerson, and G. L. Westbrook (1998)
J. Neurosci. 18, 6790-6802
   Abstract »    Full Text »    PDF »
Synaptic facilitation by reflected action potentials: Enhancement of transmission when nerve impulses reverse direction at axon branch points.
S. A. Baccus (1998)
PNAS 95, 8345-8350
   Abstract »    Full Text »    PDF »
Action potential propagation in mitral cell lateral dendrites is decremental and controls recurrent and lateral inhibition in the mammalian olfactory bulb.
T. W. Margrie, B. Sakmann, and N. N. Urban (2001)
PNAS 98, 319-324
   Abstract »    Full Text »    PDF »
Odor-evoked calcium signals in dendrites of rat mitral cells.
S. Charpak, J. Mertz, E. Beaurepaire, L. Moreaux, and K. Delaney (2001)
PNAS 98, 1230-1234
   Abstract »    Full Text »    PDF »



ADVERTISEMENT
Click Me!

ADVERTISEMENT
Click Me!

To Advertise     Find Products


Science. ISSN 0036-8075 (print), 1095-9203 (online)