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.

Science 14 January 2000:
Vol. 287. no. 5451, pp. 295 - 300
DOI: 10.1126/science.287.5451.295
Prev | Table of Contents | Next

Reports

Distal Initiation and Active Propagation of Action Potentials in Interneuron Dendrites

Marco Martina, 1 Imre Vida, 2 Peter Jonas 1*

Fast and reliable activation of inhibitory interneurons is critical for the stability of cortical neuronal networks. Active conductances in dendrites may facilitate interneuron activation, but direct experimental evidence was unavailable. Patch-clamp recordings from dendrites of hippocampal oriens-alveus interneurons revealed high densities of voltage-gated sodium and potassium ion channels. Simultaneous recordings from dendrites and somata suggested that action potential initiation occurs preferentially in the axon with long threshold stimuli, but can be shifted to somatodendritic sites when brief stimuli are applied. After initiation, action potentials propagate over the somatodendritic domain with constant amplitude, high velocity, and reliability, even during high-frequency trains.

1 Physiologisches Institut der Universität Freiburg,
2 Anatomisches Institut der Universität Freiburg, D-79104 Freiburg, Germany.
*   To whom correspondence should be addressed. E-mail: jonasp{at}ruf.uni-freiburg.de

Read the Full Text


THIS ARTICLE HAS BEEN CITED BY OTHER ARTICLES:
Somatic Spikes Regulate Dendritic Signaling in Small Neurons in the Absence of Backpropagating Action Potentials.
M. H. Myoga, M. Beierlein, and W. G. Regehr (2009)
J. Neurosci. 29, 7803-7814
   Abstract »    Full Text »    PDF »
Activity-Dependent Compartmentalized Regulation of Dendritic Ca2+ Signaling in Hippocampal Interneurons.
L. Topolnik, S. Chamberland, J.-G. Pelletier, I. Ran, and J.-C. Lacaille (2009)
J. Neurosci. 29, 4658-4663
   Abstract »    Full Text »    PDF »
Experimentally guided modelling of dendritic excitability in rat neocortical pyramidal neurones.
N. Keren, D. Bar-Yehuda, and A. Korngreen (2009)
J. Physiol. 587, 1413-1437
   Abstract »    Full Text »    PDF »
Quantitative Assessment of the Distributions of Membrane Conductances Involved in Action Potential Backpropagation Along Basal Dendrites.
C. D. Acker and S. D. Antic (2009)
J Neurophysiol 101, 1524-1541
   Abstract »    Full Text »    PDF »
Synaptic and Cellular Properties of the Feedforward Inhibitory Circuit within the Input Layer of the Cerebellar Cortex.
R. T. Kanichay and R. A. Silver (2008)
J. Neurosci. 28, 8955-8967
   Abstract »    Full Text »    PDF »
Divergent sodium channel defects in familial hemiplegic migraine.
K. M. Kahlig, T. H. Rhodes, M. Pusch, T. Freilinger, J. M. Pereira-Monteiro, M. D. Ferrari, A. M. J. M. van den Maagdenberg, M. Dichgans, and A. L. George Jr. (2008)
PNAS 105, 9799-9804
   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 »
Coincidence detection of convergent perforant path and mossy fibre inputs by CA3 interneurons.
E. Calixto, E. J. Galvan, J. P. Card, and G. Barrionuevo (2008)
J. Physiol. 586, 2695-2712
   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 »
Synaptic Kainate Receptors Tune Oriens-Lacunosum Moleculare Interneurons to Operate at Theta Frequency.
M. Goldin, J. Epsztein, I. Jorquera, A. Represa, Y. Ben-Ari, V. Crepel, and R. Cossart (2007)
J. Neurosci. 27, 9560-9572
   Abstract »    Full Text »    PDF »
Intrinsic properties and mechanisms of spontaneous firing in mouse cerebellar unipolar brush cells.
M. J. Russo, E. Mugnaini, and M. Martina (2007)
J. Physiol. 581, 709-724
   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 »
The Linear Computational Algorithm of Cerebellar Purkinje Cells.
J. T. Walter and K. Khodakhah (2006)
J. Neurosci. 26, 12861-12872
   Abstract »    Full Text »    PDF »
Somatodendritic Kv7/KCNQ/M Channels Control Interspike Interval in Hippocampal Interneurons..
J. J. Lawrence, F. Saraga, J. F. Churchill, J. M. Statland, K. E. Travis, F. K. Skinner, and C. J. McBain (2006)
J. Neurosci. 26, 12325-12338
   Abstract »    Full Text »    PDF »
Role for the Subthreshold Currents ILeak and IH in the Homeostatic Control of Excitability in Neocortical Somatostatin-Positive Inhibitory Neurons.
J. R. Gibson, A. F. Bartley, and K. M. Huber (2006)
J Neurophysiol 96, 420-432
   Abstract »    Full Text »    PDF »
On the Origin of the Extracellular Action Potential Waveform: A Modeling Study.
C. Gold, D. A. Henze, C. Koch, and G. Buzsaki (2006)
J Neurophysiol 95, 3113-3128
   Abstract »    Full Text »    PDF »
Gap junctions among dendrites of cortical GABAergic neurons establish a dense and widespread intercolumnar network..
T. Fukuda, T. Kosaka, W. Singer, and R. A. W. Galuske (2006)
J. Neurosci. 26, 3434-3443
   Abstract »    Full Text »    PDF »
Distal Gap Junctions and Active Dendrites Can Tune Network Dynamics.
F. Saraga, L. Ng, and F. K. Skinner (2006)
J Neurophysiol 95, 1669-1682
   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 »
Cell type-specific dependence of muscarinic signalling in mouse hippocampal stratum oriens interneurones.
J. J. Lawrence, J. M. Statland, Z. M. Grinspan, and C. J. McBain (2006)
J. Physiol. 570, 595-610
   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 »
Differential Expression of TASK Channels between Horizontal Interneurons and Pyramidal Cells of Rat Hippocampus.
S. Taverna, T. Tkatch, A. E. Metz, and M. Martina (2005)
J. Neurosci. 25, 9162-9170
   Abstract »    Full Text »    PDF »
Coupled Networks of Parvalbumin-Immunoreactive Interneurons in the Rat Basolateral Amygdala.
J. F. Muller, F. Mascagni, and A. J. McDonald (2005)
J. Neurosci. 25, 7366-7376
   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 »
Functional Properties of Electrical Synapses Between Inhibitory Interneurons of Neocortical Layer 4.
J. R. Gibson, M. Beierlein, and B. W. Connors (2005)
J Neurophysiol 93, 467-480
   Abstract »    Full Text »    PDF »
Dendritic spike back propagation in the electrosensory lobe of Gnathonemus petersii.
L. Gomez, M. Kanneworff, R. Budelli, and K. Grant (2005)
J. Exp. Biol. 208, 141-155
   Abstract »    Full Text »    PDF »
Stratum oriens horizontal interneurone diversity and hippocampal network dynamics.
G. Maccaferri (2005)
J. Physiol. 562, 73-80
   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 »
Electrotonic coupling between stratum oriens interneurones in the intact in vitro mouse juvenile hippocampus.
X.-L. Zhang, L. Zhang, and P. L. Carlen (2004)
J. Physiol. 558, 825-839
   Abstract »    Full Text »    PDF »
Somatic Localization of a Specific Large-Conductance Calcium-Activated Potassium Channel Subtype Controls Compartmentalized Ethanol Sensitivity in the Nucleus Accumbens.
G. Martin, S. Puig, A. Pietrzykowski, P. Zadek, P. Emery, and S. Treistman (2004)
J. Neurosci. 24, 6563-6572
   Abstract »    Full Text »    PDF »
Global dendritic calcium spikes in mouse layer 5 low threshold spiking interneurones: implications for control of pyramidal cell bursting.
J. H. Goldberg, C. O. Lacefield, and R. Yuste (2004)
J. Physiol. 558, 465-478
   Abstract »    Full Text »    PDF »
Synaptic Efficacy during Repetitive Activation of Excitatory Inputs in Primate Dorsolateral Prefrontal Cortex.
G. Gonzalez-Burgos, L. S. Krimer, N. N. Urban, G. Barrionuevo, and D. A. Lewis (2004)
Cereb Cortex 14, 530-542
   Abstract »    Full Text »    PDF »
Distance-Dependent Scaling of Calcium Transients Evoked by Backpropagating Spikes and Synaptic Activity in Dendrites of Hippocampal Interneurons.
B. Rozsa, T. Zelles, E. S. Vizi, and B. Lendvai (2004)
J. Neurosci. 24, 661-670
   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 »
Active dendrites and spike propagation in multicompartment models of oriens-lacunosum/moleculare hippocampal interneurons.
F Saraga, C P Wu, L Zhang, and F K Skinner (2003)
J. Physiol. 552, 673-689
   Abstract »    Full Text »    PDF »
Distance-Dependent Modifiable Threshold for Action Potential Back-Propagation in Hippocampal Dendrites.
C. Bernard and D. Johnston (2003)
J Neurophysiol 90, 1807-1816
   Abstract »    Full Text »    PDF »
Ca2+ imaging of mouse neocortical interneurone dendrites: Ia-type K+ channels control action potential backpropagation.
J. H Goldberg, G. Tamas, and R. Yuste (2003)
J. Physiol. 551, 49-65
   Abstract »    Full Text »    PDF »
Excitatory Inputs to CA1 Interneurons Show Selective Synaptic Dynamics.
C. J. Wierenga and W. J. Wadman (2003)
J Neurophysiol 90, 811-821
   Abstract »    Full Text »    PDF »
Properties and Functional Role of Voltage-Dependent Potassium Channels in Dendrites of Rat Cerebellar Purkinje Neurons.
M. Martina, G. L. Yao, and B. P. Bean (2003)
J. Neurosci. 23, 5698-5707
   Abstract »    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 »
Kv3 Potassium Conductance is Necessary and Kinetically Optimized for High-Frequency Action Potential Generation in Hippocampal Interneurons.
C.-C. Lien and P. Jonas (2003)
J. Neurosci. 23, 2058-2068
   Abstract »    Full Text »    PDF »
Selective modulation of excitatory and inhibitory microcircuits by dopamine.
W.-J. Gao and P. S. Goldman-Rakic (2003)
PNAS 100, 2836-2841
   Abstract »    Full Text »    PDF »
Selective Depression by General Anesthetics of Glutamate Versus GABA Release from Isolated Cortical Nerve Terminals.
R. I. Westphalen and H. C. Hemmings Jr. (2003)
J. Pharmacol. Exp. Ther. 304, 1188-1196
   Abstract »    Full Text »    PDF »
Functional Autaptic Neurotransmission in Fast-Spiking Interneurons: A Novel Form of Feedback Inhibition in the Neocortex.
A. Bacci, J. R. Huguenard, and D. A. Prince (2003)
J. Neurosci. 23, 859-866
   Abstract »    Full Text »    PDF »
Electrical Synapses Mediate Signal Transmission in the Rod Pathway of the Mammalian Retina.
M. L. Veruki and E. Hartveit (2002)
J. Neurosci. 22, 10558-10566
   Abstract »    Full Text »    PDF »
Stimulus-Evoked Modulation of Sensorimotor Pyramidal Neuron EPSPs.
A. Kohn, C. Metz, M. A. Tommerdahl, and B. L. Whitsel (2002)
J Neurophysiol 88, 3331-3347
   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 »
Role of Dendritic Spines in Action Potential Backpropagation: A Numerical Simulation Study.
D. Tsay and R. Yuste (2002)
J Neurophysiol 88, 2834-2845
   Abstract »    Full Text »    PDF »
Fast synaptic inhibition promotes synchronized gamma oscillations in hippocampal interneuron networks.
M. Bartos, I. Vida, M. Frotscher, A. Meyer, H. Monyer, J. R. P. Geiger, and P. Jonas (2002)
PNAS 99, 13222-13227
   Abstract »    Full Text »    PDF »
Distally Directed Dendrotoxicity Induced by Kainic Acid in Hippocampal Interneurons of Green Fluorescent Protein-Expressing Transgenic Mice.
A. A. Oliva Jr, T. T. Lam, and J. W. Swann (2002)
J. Neurosci. 22, 8052-8062
   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 »
The minicolumn hypothesis in neuroscience.
D. P. Buxhoeveden and M. F. Casanova (2002)
Brain 125, 935-951
   Abstract »    Full Text »    PDF »
A fundamental oscillatory state of isolated rodent hippocampus.
C. Wu, H. Shen, W. P. Luk, and L. Zhang (2002)
J. Physiol. 540, 509-527
   Abstract »    Full Text »    PDF »
Gating, modulation and subunit composition of voltage-gated K+ channels in dendritic inhibitory interneurones of rat hippocampus.
C.-C. Lien, M. Martina, J. H Schultz, H. Ehmke, and P. Jonas (2002)
J. Physiol. 538, 405-419
   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 »
Self-Organized Synaptic Plasticity Contributes to the Shaping of gamma and beta Oscillations In Vitro.
A. Bibbig, H. J. Faulkner, M. A. Whittington, and R. D. Traub (2001)
J. Neurosci. 21, 9053-9067
   Abstract »    Full Text »    PDF »
RNA-Binding Protein Musashi2: Developmentally Regulated Expression in Neural Precursor Cells and Subpopulations of Neurons in Mammalian CNS.
S.-i. Sakakibara, Y. Nakamura, H. Satoh, and H. Okano (2001)
J. Neurosci. 21, 8091-8107
   Abstract »    Full Text »    PDF »
Dendrites.
Y.-N. Jan and L. Y. Jan (2001)
Genes & Dev. 15, 2627-2641
   Full Text »    PDF »
Back-propagating action potentials mediate calcium signalling in dendrites of bitufted interneurons in layer 2/3 of rat somatosensory cortex.
K. M M Kaiser, Y Zilberter, and B Sakmann (2001)
J. Physiol. 535, 17-31
   Abstract »    Full Text »    PDF »
A hebbian form of long-term potentiation dependent on mGluR1a in hippocampal inhibitory interneurons.
Y. Perez, F. Morin, and J.-C. Lacaille (2001)
PNAS
   Abstract »    Full Text »    PDF »
Spike Transmission and Synchrony Detection in Networks of GABAergic Interneurons.
M. Galarreta and S. Hestrin (2001)
Science 292, 2295-2299
   Abstract »    Full Text »    PDF »
Prefrontal Microcircuits: Membrane Properties and Excitatory Input of Local, Medium, and Wide Arbor Interneurons.
L. S. Krimer and P. S. Goldman-Rakic (2001)
J. Neurosci. 21, 3788-3796
   Abstract »    Full Text »    PDF »
Rapid Signaling at Inhibitory Synapses in a Dentate Gyrus Interneuron Network.
M. Bartos, I. Vida, M. Frotscher, J. R. P. Geiger, and P. Jonas (2001)
J. Neurosci. 21, 2687-2698
   Abstract »    Full Text »    PDF »
Genetically altered AMPA-type glutamate receptor kinetics in interneurons disrupt long-range synchrony of gamma oscillation.
E. C. Fuchs, H. Doheny, H. Faulkner, A. Caputi, R. D. Traub, A. Bibbig, N. Kopell, M. A. Whittington, and H. Monyer (2001)
PNAS 98, 3571-3576
   Abstract »    Full Text »    PDF »
Synaptic and Nonsynaptic Contributions to Giant IPSPs and Ectopic Spikes Induced by 4-Aminopyridine in the Hippocampus In Vitro.
R. D. Traub, R. Bibbig, A. Piechotta, R. Draguhn, and D. Schmitz (2001)
J Neurophysiol 85, 1246-1256
   Abstract »    Full Text »    PDF »
Differential Expression of Synaptic and Nonsynaptic Mechanisms Underlying Stimulus-Induced Gamma Oscillations In Vitro.
M. A. Whittington, H. C. Doheny, R. D. Traub, F. E. N. LeBeau, and E. H. Buhl (2001)
J. Neurosci. 21, 1727-1738
   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 »
Associative Long-Term Depression in the Hippocampus Is Dependent on Postsynaptic N-Type Ca2+ Channels.
C. Normann, D. Peckys, C. H. Schulze, J. Walden, P. Jonas, and J. Bischofberger (2000)
J. Neurosci. 20, 8290-8297
   Abstract »    Full Text »    PDF »
Diversity and Dynamics of Dendritic Signaling.
M. Häusser, N. Spruston, and G. J. Stuart (2000)
Science 290, 739-744
   Abstract »    Full Text »
Deficit of Striatal Parvalbumin-Reactive GABAergic Interneurons and Decreased Basal Ganglia Output in a Genetic Rodent Model of Idiopathic Paroxysmal Dystonia.
M. Gernert, M. Hamann, M. Bennay, W. Loscher, and A. Richter (2000)
J. Neurosci. 20, 7052-7058
   Abstract »    Full Text »    PDF »
A hebbian form of long-term potentiation dependent on mGluR1a in hippocampal inhibitory interneurons.
Y. Perez, F. Morin, and J.-C. Lacaille (2001)
PNAS 98, 9401-9406
   Abstract »    Full Text »    PDF »


To Advertise     Find Products

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