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 10 August 2001:
Vol. 293. no. 5532, pp. 1159 - 1163
DOI: 10.1126/science.1060342
Prev | Table of Contents | Next

Reports

Enforcement of Temporal Fidelity in Pyramidal Cells by Somatic Feed-Forward Inhibition

Frédéric Pouille, Massimo Scanziani*

The temporal resolution of neuronal integration depends on the time window within which excitatory inputs summate to reach the threshold for spike generation. Here, we show that in rat hippocampal pyramidal cells this window is very narrow (less than 2 milliseconds). This narrowness results from the short delay with which disynaptic feed-forward inhibition follows monosynaptic excitation. Simultaneous somatic and dendritic recordings indicate that feed-forward inhibition is much stronger in the soma than in the dendrites, resulting in a broader integration window in the latter compartment. Thus, the subcellular partitioning of feed-forward inhibition enforces precise coincidence detection in the soma, while allowing dendrites to sum incoming activity over broader time windows.

Brain Research Institute, University of Zurich, Winterthurerstrasse 190, CH-8057 Zurich, Switzerland.
*   To whom correspondence should be addressed. E-mail: massimo{at}hifo.unizh.ch

Read the Full Text


THIS ARTICLE HAS BEEN CITED BY OTHER ARTICLES:
GABAB Receptor Modulation of Feedforward Inhibition through Hippocampal Neurogliaform Cells.
C. J. Price, R. Scott, D. A. Rusakov, and M. Capogna (2008)
J. Neurosci. 28, 6974-6982
   Abstract »    Full Text »    PDF »
Cortical Transformation of Wide-Field (Multiwhisker) Sensory Responses.
A. Hirata and M. A. Castro-Alamancos (2008)
J Neurophysiol 100, 358-370
   Abstract »    Full Text »    PDF »
Rate-specific synchrony: Using noisy oscillations to detect equally active neurons.
D. A. Markowitz, F. Collman, C. D. Brody, J. J. Hopfield, and D. W. Tank (2008)
PNAS 105, 8422-8427
   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 »
Complementary Modulation of Somatic Inhibition by Opioids and Cannabinoids.
L. L. Glickfeld, B. V. Atallah, and M. Scanziani (2008)
J. Neurosci. 28, 1824-1832
   Abstract »    Full Text »    PDF »
Gamma Oscillations and Stimulus Selection.
C. Borgers and N. J. Kopell (2008)
Neural Comput. 20, 383-414
   Abstract »    Full Text »    PDF »
Differential Tonic GABA Conductances in Striatal Medium Spiny Neurons.
K. K. Ade, M. J. Janssen, P. I. Ortinski, and S. Vicini (2008)
J. Neurosci. 28, 1185-1197
   Abstract »    Full Text »    PDF »
Learning-related long-term potentiation of inhibitory synapses in the cerebellar cortex.
B. Scelfo, B. Sacchetti, and P. Strata (2008)
PNAS 105, 769-774
   Abstract »    Full Text »    PDF »
GABAA Receptor {gamma}2 Subunit Mutations Linked to Human Epileptic Syndromes Differentially Affect Phasic and Tonic Inhibition.
E. Eugene, C. Depienne, S. Baulac, M. Baulac, J. M. Fritschy, E. Le Guern, R. Miles, and J. C. Poncer (2007)
J. Neurosci. 27, 14108-14116
   Abstract »    Full Text »    PDF »
Synaptic heterogeneity between mouse paracapsular intercalated neurons of the amygdala.
R. Geracitano, W. A. Kaufmann, G. Szabo, F. Ferraguti, and M. Capogna (2007)
J. Physiol. 585, 117-134
   Abstract »    Full Text »    PDF »
The transience of interneuron circuit diversity just "sped" up.
E. Krook-Magnuson and M. M. Huntsman (2007)
PNAS 104, 16723-16724
   Full Text »    PDF »
Development of gerbil medial superior olive: integration of temporally delayed excitation and inhibition at physiological temperature.
F. V. Chirila, K. C. Rowland, J. M. Thompson, and G. A. Spirou (2007)
J. Physiol. 584, 167-190
   Abstract »    Full Text »    PDF »
Immunoreactivity for the GABAA Receptor {alpha}1 Subunit, Somatostatin and Connexin36 Distinguishes Axoaxonic, Basket, and Bistratified Interneurons of the Rat Hippocampus.
A. Baude, C. Bleasdale, Y. Dalezios, P. Somogyi, and T. Klausberger (2007)
Cereb Cortex 17, 2094-2107
   Abstract »    Full Text »    PDF »
Temporal Patterning of Saccadic Eye Movement Signals.
D. L. Kimmel and T. Moore (2007)
J. Neurosci. 27, 7619-7630
   Abstract »    Full Text »    PDF »
Recruitment of an inhibitory hippocampal network after bursting in a single granule cell.
M. Mori, B. H. Gahwiler, and U. Gerber (2007)
PNAS 104, 7640-7645
   Abstract »    Full Text »    PDF »
Electrophysiological Differences Between Neurogliaform Cells From Monkey and Rat Prefrontal Cortex.
N. V. Povysheva, A. V. Zaitsev, S. Kroner, O. A. Krimer, D. C. Rotaru, G. Gonzalez-Burgos, D. A. Lewis, and L. S. Krimer (2007)
J Neurophysiol 97, 1030-1039
   Abstract »    Full Text »    PDF »
Networks of Parvalbumin-Positive Interneurons in the Basolateral Amygdala.
A. R. Woodruff and P. Sah (2007)
J. Neurosci. 27, 553-563
   Abstract »    Full Text »    PDF »
Unitary IPSPs enhance hilar mossy cell gain in the rat hippocampus.
A. M. Kerr and M. Capogna (2007)
J. Physiol. 578, 451-470
   Abstract »    Full Text »    PDF »
Correlation Between Axonal Morphologies and Synaptic Input Kinetics of Interneurons from Mouse Visual Cortex.
D. Dumitriu, R. Cossart, J. Huang, and R. Yuste (2007)
Cereb Cortex 17, 81-91
   Abstract »    Full Text »    PDF »
Postsynaptic origin of CB1-dependent tonic inhibition of GABA release at cholecystokinin-positive basket cell to pyramidal cell synapses in the CA1 region of the rat hippocampus.
A. Neu, C. Foldy, and I. Soltesz (2007)
J. Physiol. 578, 233-247
   Abstract »    Full Text »    PDF »
Event-driven simulation scheme for spiking neural networks using lookup tables to characterize neuronal dynamics..
E. Ros, R. Carrillo, E. M. Ortigosa, B. Barbour, and R. Agis (2006)
Neural Comput. 18, 2959-2993
   Abstract »    Full Text »    PDF »
GABAergic Excitation in the Basolateral Amygdala..
A. R. Woodruff, H. Monyer, and P. Sah (2006)
J. Neurosci. 26, 11881-11887
   Abstract »    Full Text »    PDF »
GABAergic Input onto CA3 Hippocampal Interneurons Remains Shunting throughout Development..
T. G. Banke and C. J. McBain (2006)
J. Neurosci. 26, 11720-11725
   Abstract »    Full Text »    PDF »
Active and Passive Membrane Properties and Intrinsic Kinetics Shape Synaptic Inhibition in Hippocampal CA1 Pyramidal Neurons..
J. B. Hardie and R. A. Pearce (2006)
J. Neurosci. 26, 8559-8569
   Abstract »    Full Text »    PDF »
Specific Subtypes of GABAA Receptors Mediate Phasic and Tonic Forms of Inhibition in Hippocampal Pyramidal Neurons.
G. A. Prenosil, E. M. Schneider Gasser, U. Rudolph, R. Keist, J.-M. Fritschy, and K. E. Vogt (2006)
J Neurophysiol 96, 846-857
   Abstract »    Full Text »    PDF »
Integrative spike dynamics of rat CA1 neurons: a multineuronal imaging study.
T. Sasaki, R. Kimura, M. Tsukamoto, N. Matsuki, and Y. Ikegaya (2006)
J. Physiol. 574, 195-208
   Abstract »    Full Text »    PDF »
Temperature-dependent shift of balance among the components of short-term plasticity in hippocampal synapses..
V. A. Klyachko and C. F. Stevens (2006)
J. Neurosci. 26, 6945-6957
   Abstract »    Full Text »    PDF »
Depolarizing GABAergic conductances regulate the balance of excitation to inhibition in the developing retinotectal circuit in vivo..
C. J. Akerman and H. T. Cline (2006)
J. Neurosci. 26, 5117-5130
   Abstract »    Full Text »    PDF »
Rapid, activity-dependent plasticity in timing precision in neonatal barrel cortex..
M. I. Daw, N. V. Bannister, and J. T. R. Isaac (2006)
J. Neurosci. 26, 4178-4187
   Abstract »    Full Text »    PDF »
Cortical inputs and GABA interneurons imbalance projection neurons in the striatum of parkinsonian rats..
N. Mallet, B. Ballion, C. Le Moine, and F. Gonon (2006)
J. Neurosci. 26, 3875-3884
   Abstract »    Full Text »    PDF »
Properties of Excitatory Synaptic Responses in Fast-spiking Interneurons and Pyramidal Cells from Monkey and Rat Prefrontal Cortex.
N.V. Povysheva, G. Gonzalez-Burgos, A.V. Zaitsev, S. Kroner, G. Barrionuevo, D.A. Lewis, and L.S. Krimer (2006)
Cereb Cortex 16, 541-552
   Abstract »    Full Text »    PDF »
Coincidence detection of synaptic inputs is facilitated at the distal dendrites after long-term potentiation induction..
N.-l. Xu, C.-q. Ye, M.-m. Poo, and X.-h. Zhang (2006)
J. Neurosci. 26, 3002-3009
   Abstract »    Full Text »    PDF »
Balanced Excitation and Inhibition Determine Spike Timing during Frequency Adaptation.
M. J. Higley and D. Contreras (2006)
J. Neurosci. 26, 448-457
   Abstract »    Full Text »    PDF »
Maturation of glycinergic inhibition in the gerbil medial superior olive after hearing onset.
A. K Magnusson, C. Kapfer, B. Grothe, and U. Koch (2005)
J. Physiol. 568, 497-512
   Abstract »    Full Text »    PDF »
Factors determining the precision of the correlated firing generated by a monosynaptic connection in the cat visual pathway.
F. J Veredas, F. J Vico, and J.-M. Alonso (2005)
J. Physiol. 567, 1057-1078
   Abstract »    Full Text »    PDF »
Time-Dependent Activation of Feed-Forward Inhibition in a Looming-Sensitive Neuron.
F. Gabbiani, I. Cohen, and G. Laurent (2005)
J Neurophysiol 94, 2150-2161
   Abstract »    Full Text »    PDF »
Spike Timing in CA3 Pyramidal Cells During Behavior: Implications for Synaptic Transmission.
M. Frerking, J. Schulte, S. P. Wiebe, and U. Staubli (2005)
J Neurophysiol 94, 1528-1540
   Abstract »    Full Text »    PDF »
Background Synaptic Conductance and Precision of EPSP-Spike Coupling at Pyramidal Cells.
V. Zsiros and S. Hestrin (2005)
J Neurophysiol 93, 3248-3256
   Abstract »    Full Text »    PDF »
Integration Time in a Subset of Spinal Lamina I Neurons Is Lengthened by Sodium and Calcium Currents Acting Synergistically to Prolong Subthreshold Depolarization.
S. A. Prescott and Y. De Koninck (2005)
J. Neurosci. 25, 4743-4754
   Abstract »    Full Text »    PDF »
Stimulus-Dependent Changes in Spike Threshold Enhance Feature Selectivity in Rat Barrel Cortex Neurons.
W. B. Wilent and D. Contreras (2005)
J. Neurosci. 25, 2983-2991
   Abstract »    Full Text »    PDF »
Feed-forward inhibition shapes the spike output of cerebellar Purkinje cells.
W. Mittmann, U. Koch, and M. Hausser (2005)
J. Physiol. 563, 369-378
   Abstract »    Full Text »    PDF »
The HVC Microcircuit: The Synaptic Basis for Interactions between Song Motor and Vocal Plasticity Pathways.
R. Mooney and J. F. Prather (2005)
J. Neurosci. 25, 1952-1964
   Abstract »    Full Text »    PDF »
Differential Postnatal Maturation of GABAA, Glycine Receptor, and Mixed Synaptic Currents in Renshaw Cells and Ventral Spinal Interneurons.
D. Gonzalez-Forero and F. J. Alvarez (2005)
J. Neurosci. 25, 2010-2023
   Abstract »    Full Text »    PDF »
Synaptic Integration in Rat Frontal Cortex Shaped by Network Activity.
J.-F. Leger, E. A. Stern, A. Aertsen, and D. Heck (2005)
J Neurophysiol 93, 281-293
   Abstract »    Full Text »    PDF »
Timing and Balance of Inhibition Enhance the Effect of Long-Term Potentiation on Cell Firing.
C. P. Marder and D. V. Buonomano (2004)
J. Neurosci. 24, 8873-8884
   Abstract »    Full Text »    PDF »
Intrinsic and Circuit Properties Favor Coincidence Detection for Decoding Oscillatory Input.
J. Perez-Orive, M. Bazhenov, and G. Laurent (2004)
J. Neurosci. 24, 6037-6047
   Abstract »    Full Text »    PDF »
Behavioral Context and Coherent Oscillations in the Supplementary Motor Area.
D. Lee (2004)
J. Neurosci. 24, 4453-4459
   Abstract »    Full Text »    PDF »
Coincidence detection enhances appropriate wiring of the nervous system.
N. C. Spitzer (2004)
PNAS 101, 5311-5312
   Full Text »    PDF »
Intrinsic cellular currents and the temporal precision of EPSP-action potential coupling in CA1 pyramidal cells.
N. Axmacher and R. Miles (2004)
J. Physiol. 555, 713-725
   Abstract »    Full Text »    PDF »
Specific GABAA Circuits for Visual Cortical Plasticity.
M. Fagiolini, J.-M. Fritschy, K. Low, H. Mohler, U. Rudolph, and T. K. Hensch (2004)
Science 303, 1681-1683
   Abstract »    Full Text »    PDF »
Dynamic Influences on Coincidence Detection in Neocortical Pyramidal Neurons.
L. A. Grande, G. A. Kinney, G. L. Miracle, and W. J. Spain (2004)
J. Neurosci. 24, 1839-1851
   Abstract »    Full Text »    PDF »
Long-Term Enhancement of Neuronal Excitability and Temporal Fidelity Mediated by Metabotropic Glutamate Receptor Subtype 5.
V. Sourdet, M. Russier, G. Daoudal, N. Ankri, and D. Debanne (2003)
J. Neurosci. 23, 10238-10248
   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 »
Rapid Critical Period Induction by Tonic Inhibition in Visual Cortex.
Y. Iwai, M. Fagiolini, K. Obata, and T. K. Hensch (2003)
J. Neurosci. 23, 6695-6702
   Abstract »    Full Text »    PDF »
Coherent Oscillations in Neuronal Activity of the Supplementary Motor Area during a Visuomotor Task.
D. Lee (2003)
J. Neurosci. 23, 6798-6809
   Abstract »    Full Text »    PDF »
Gene Expression Deficits in a Subclass of GABA Neurons in the Prefrontal Cortex of Subjects with Schizophrenia.
T. Hashimoto, D. W. Volk, S. M. Eggan, K. Mirnics, J. N. Pierri, Z. Sun, A. R. Sampson, and D. A. Lewis (2003)
J. Neurosci. 23, 6315-6326
   Abstract »    Full Text »    PDF »
Synapse Density Regulates Independence at Unitary Inhibitory Synapses.
L. S. Overstreet and G. L. Westbrook (2003)
J. Neurosci. 23, 2618-2626
   Abstract »    Full Text »    PDF »
A Fast-Conducting, Stochastic Integrative Mode for Neocortical Neurons InVivo.
M. Rudolph and A. Destexhe (2003)
J. Neurosci. 23, 2466-2476
   Abstract »    Full Text »    PDF »
Timing and Precision of Spike Initiation in Layer V Pyramidal Cells of the Rat Somatosensory Cortex.
T. Berger and H.-R. Luscher (2003)
Cereb Cortex 13, 274-281
   Abstract »    Full Text »    PDF »
Differential Effects of Short- and Long-Term Potentiation on Cell Firing in the CA1 Region of the Hippocampus.
C. P. Marder and D. V. Buonomano (2003)
J. Neurosci. 23, 112-121
   Abstract »    Full Text »    PDF »
Development of GABAA Receptor-Mediated Inhibitory Postsynaptic Currents in Hippocampus.
M. I. Banks, J. B. Hardie, and R. A. Pearce (2002)
J Neurophysiol 88, 3097-3107
   Abstract »    Full Text »    PDF »
Temporal Organization of Activity in the Cerebellar Cortex: A Manifesto for Synchrony.
P. ISOPE, S. DIEUDONNE, and B. BARBOUR (2002)
Ann. N.Y. Acad. Sci. 978, 164-174
   Abstract »    Full Text »    PDF »
Thalamocortical Bursts Trigger Recurrent Activity in Neocortical Networks: Layer 4 as a Frequency-Dependent Gate.
M. Beierlein, C. P. Fall, J. Rinzel, and R. Yuste (2002)
J. Neurosci. 22, 9885-9894
   Abstract »    Full Text »    PDF »
Oscillations and Sparsening of Odor Representations in the Mushroom Body.
J. Perez-Orive, O. Mazor, G. C. Turner, S. Cassenaer, R. I. Wilson, and G. Laurent (2002)
Science 297, 359-365
   Abstract »    Full Text »    PDF »
Control of Feedforward Dendritic Inhibition by NMDA Receptor-Dependent Spike Timing in Hippocampal Interneurons.
G. Maccaferri and R. Dingledine (2002)
J. Neurosci. 22, 5462-5472
   Abstract »    Full Text »    PDF »


ADVERTISEMENT
Click Me!

ADVERTISEMENT
Click Me!

To Advertise     Find Products

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