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.

Subscribe

Logo for

Science 302 (5652): 1981-1984

Copyright © 2003 by the American Association for the Advancement of Science

High-Probability Uniquantal Transmission at Excitatory Synapses in Barrel Cortex

R. Angus Silver,1*{dagger} Joachim Lübke,2 Bert Sakmann,3 Dirk Feldmeyer3*

Abstract: The number of vesicles released at excitatory synapses and the number of release sites per synaptic connection are key determinants of information processing in the cortex, yet they remain uncertain. Here we show that the number of functional release sites and the number of anatomically identified synaptic contacts are equal at connections between spiny stellate and pyramidal cells in rat barrel cortex. Moreover, our results indicate that the amount of transmitter released per synaptic contact is independent of release probability and the intrinsic release probability is high. These properties suggest that connections between layer 4and layer 2/3 are tuned for reliable transmission of spatially distributed, timing-based signals.

1 Department of Physiology, University College London, Gower Street, London WC1E 6BT, U.K.
2 Forschungszentrum Jülich GmbH, Institut für Medizin, D-52425 Jülich, Germany.
3 Max-Planck Institut für Medizinische Forschung, Abteilung Zellphysiologie, Jahnstrasse 29, D-69120 Heidelberg, Germany.

Back to Top

* These authors contributed equally to the work.

{dagger} To whom correspondence should be addressed. E-mail: a.silver{at}ucl.ac.uk


THIS ARTICLE HAS BEEN CITED BY OTHER ARTICLES:
Pansynaptic Enlargement at Adult Cortical Connections Strengthened by Experience.
C. E. J. Cheetham, S. J. Barnes, G. Albieri, G. W. Knott, and G. T. Finnerty (2014)
Cereb Cortex 24, 521-531
   Abstract »    Full Text »    PDF »
Contribution of Intracolumnar Layer 2/3-to-Layer 2/3 Excitatory Connections in Shaping the Response to Whisker Deflection in Rat Barrel Cortex.
L. Sarid, D. Feldmeyer, A. Gidon, B. Sakmann, and I. Segev (2013)
Cereb Cortex
   Abstract »    Full Text »    PDF »
Activation of Extrasynaptic NMDARs at Individual Parallel Fiber-Molecular Layer Interneuron Synapses in Cerebellum.
B. Nahir and C. E. Jahr (2013)
J. Neurosci. 33, 16323-16333
   Abstract »    Full Text »    PDF »
A Barrel-Related Interneuron in Layer 4 of Rat Somatosensory Cortex with a High Intrabarrel Connectivity.
C. Koelbl, M. Helmstaedter, J. Lubke, and D. Feldmeyer (2013)
Cereb Cortex
   Abstract »    Full Text »    PDF »
Adaptation of Granule Cell to Purkinje Cell Synapses to High-Frequency Transmission.
A. M. Valera, F. Doussau, B. Poulain, B. Barbour, and P. Isope (2012)
J. Neurosci. 32, 3267-3280
   Abstract »    Full Text »    PDF »
Intrinsic morphological diversity of thick-tufted layer 5 pyramidal neurons ensures robust and invariant properties of in silico synaptic connections.
S. Ramaswamy, S. L. Hill, J. G. King, F. Schurmann, Y. Wang, and H. Markram (2012)
J. Physiol. 590, 737-752
   Abstract »    Full Text »    PDF »
Receptor saturation controls short-term synaptic plasticity at corticothalamic synapses.
Y.-G. Sun and M. Beierlein (2011)
J Neurophysiol 105, 2319-2329
   Abstract »    Full Text »    PDF »
Multivesicular Release Differentiates the Reliability of Synaptic Transmission between the Visual Cortex and the Somatosensory Cortex.
C.-H. Huang, J. Bao, and T. Sakaba (2010)
J. Neurosci. 30, 11994-12004
   Abstract »    Full Text »    PDF »
Modulation and function of the autaptic connections of layer V fast spiking interneurons in the rat neocortex.
W. M. Connelly and G. Lees (2010)
J. Physiol. 588, 2047-2063
   Abstract »    Full Text »    PDF »
Quantal Analysis Reveals a Functional Correlation between Presynaptic and Postsynaptic Efficacy in Excitatory Connections from Rat Neocortex.
N. R. Hardingham, J. C. A. Read, A. J. Trevelyan, J. C. Nelson, J. J. B. Jack, and N. J. Bannister (2010)
J. Neurosci. 30, 1441-1451
   Abstract »    Full Text »    PDF »
Maximization of the connectivity repertoire as a statistical principle governing the shapes of dendritic arbors.
Q. Wen, A. Stepanyants, G. N. Elston, A. Y. Grosberg, and D. B. Chklovskii (2009)
PNAS 106, 12536-12541
   Abstract »    Full Text »    PDF »
Synaptic Output of Individual Layer 4 Neurons in Guinea Pig Visual Cortex.
I. Saez and M. J. Friedlander (2009)
J. Neurosci. 29, 4930-4944
   Abstract »    Full Text »    PDF »
Circuit and Plasticity Defects in the Developing Somatosensory Cortex of Fmr1 Knock-Out Mice.
I. Bureau, G. M. G. Shepherd, and K. Svoboda (2008)
J. Neurosci. 28, 5178-5188
   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-Independent and Nicotinic Receptor-Mediated Concerted Release of Multiple Quanta at Hippocampal CA3-Mossy Fiber Synapses.
G. Sharma, M. Grybko, and S. Vijayaraghavan (2008)
J. Neurosci. 28, 2563-2575
   Abstract »    Full Text »    PDF »
Pathway-specific use-dependent dynamics of excitatory synaptic transmission in rat intracortical circuits.
S. R. Williams and S. E. Atkinson (2007)
J. Physiol. 585, 759-777
   Abstract »    Full Text »    PDF »
Spatial Organization of Neuronal Population Responses in Layer 2/3 of Rat Barrel Cortex.
J. N. D. Kerr, C. P. J. de Kock, D. S. Greenberg, R. M. Bruno, B. Sakmann, and F. Helmchen (2007)
J. Neurosci. 27, 13316-13328
   Abstract »    Full Text »    PDF »
Modeling a layer 4-to-layer 2/3 module of a single column in rat neocortex: Interweaving in vitro and in vivo experimental observations.
L. Sarid, R. Bruno, B. Sakmann, I. Segev, and D. Feldmeyer (2007)
PNAS 104, 16353-16358
   Abstract »    Full Text »    PDF »
Developmental Switch in the Contribution of Presynaptic and Postsynaptic NMDA Receptors to Long-Term Depression.
R. Corlew, Y. Wang, H. Ghermazien, A. Erisir, and B. D. Philpot (2007)
J. Neurosci. 27, 9835-9845
   Abstract »    Full Text »    PDF »
Statistical Analysis of Visual Fits: Answer to J. Ninio.
A. Mallet, D. S. Faber, and H. Korn (2007)
J Neurophysiol 98, 1836-1840
   Full Text »    PDF »
Binomial parameters differ across neocortical layers and with different classes of connections in adult rat and cat neocortex.
A. Bremaud, D. C. West, and A. M. Thomson (2007)
PNAS 104, 14134-14139
   Abstract »    Full Text »    PDF »
Layer- and Cell-Type-Specific Effects of Neonatal Whisker-Trimming in Adult Rat Barrel Cortex.
S.-H. Lee, P. W. Land, and D. J. Simons (2007)
J Neurophysiol 97, 4380-4385
   Abstract »    Full Text »    PDF »
Multivesicular release and saturation of glutamatergic signalling at retinal ribbon synapses.
J. H. Singer (2007)
J. Physiol. 580, 23-29
   Abstract »    Full Text »    PDF »
Modified Sensory Processing in the Barrel Cortex of the Adult Mouse After Chronic Whisker Stimulation.
C. Quairiaux, M. Armstrong-James, and E. Welker (2007)
J Neurophysiol 97, 2130-2147
   Abstract »    Full Text »    PDF »
Release Probability-Dependent Scaling of the Postsynaptic Responses at Single Hippocampal GABAergic Synapses.
A. A. Biro, N. B. Holderith, and Z. Nusser (2006)
J. Neurosci. 26, 12487-12496
   Abstract »    Full Text »    PDF »
Efficacy and connectivity of intracolumnar pairs of layer 2/3 pyramidal cells in the barrel cortex of juvenile rats.
D. Feldmeyer, J. Lubke, and B. Sakmann (2006)
J. Physiol. 575, 583-602
   Abstract »    Full Text »    PDF »
Background synaptic activity is sparse in neocortex..
J. Waters and F. Helmchen (2006)
J. Neurosci. 26, 8267-8277
   Abstract »    Full Text »    PDF »
N-cadherin transsynaptically regulates short-term plasticity at glutamatergic synapses in embryonic stem cell-derived neurons..
K. Jungling, V. Eulenburg, R. Moore, R. Kemler, V. Lessmann, and K. Gottmann (2006)
J. Neurosci. 26, 6968-6978
   Abstract »    Full Text »    PDF »
Extracellular calcium regulates postsynaptic efficacy through group 1 metabotropic glutamate receptors..
N. R. Hardingham, N. J. Bannister, J. C. A. Read, K. D. Fox, G. E. Hardingham, and J. J. B. Jack (2006)
J. Neurosci. 26, 6337-6345
   Abstract »    Full Text »    PDF »
Multivesicular Release at Schaffer Collateral-CA1 Hippocampal Synapses.
J. M. Christie and C. E. Jahr (2006)
J. Neurosci. 26, 210-216
   Abstract »    Full Text »    PDF »
Map Plasticity in Somatosensory Cortex.
D. E. Feldman and M. Brecht (2005)
Science 310, 810-815
   Abstract »    Full Text »    PDF »
Short-Term Synaptic Depression Causes a Non-Monotonic Response to Correlated Stimuli.
J. de la Rocha and N. Parga (2005)
J. Neurosci. 25, 8416-8431
   Abstract »    Full Text »    PDF »
Rapid Vesicular Release, Quantal Variability, and Spillover Contribute to the Precision and Reliability of Transmission at a Glomerular Synapse.
P. B. Sargent, C. Saviane, T. A. Nielsen, D. A. DiGregorio, and R. A. Silver (2005)
J. Neurosci. 25, 8173-8187
   Abstract »    Full Text »    PDF »
Auditory Thalamocortical Transmission Is Reliable and Temporally Precise.
H. J. Rose and R. Metherate (2005)
J Neurophysiol 94, 2019-2030
   Abstract »    Full Text »    PDF »
Adaptation at Synaptic Connections to Layer 2/3 Pyramidal Cells in Rat Visual Cortex.
O. Beck, M. Chistiakova, K. Obermayer, and M. Volgushev (2005)
J Neurophysiol 94, 363-376
   Abstract »    Full Text »    PDF »
Encoding and Decoding of Dendritic Excitation during Active States in Pyramidal Neurons.
S. R. Williams (2005)
J. Neurosci. 25, 5894-5902
   Abstract »    Full Text »    PDF »
{gamma}-Protocadherins, Presenilin-mediated Release of C-terminal Fragment Promotes Locus Expression.
B. Hambsch, V. Grinevich, P. H. Seeburg, and M. K. Schwarz (2005)
J. Biol. Chem. 280, 15888-15897
   Abstract »    Full Text »    PDF »
The neocortical microcircuit as a tabula rasa.
N. Kalisman, G. Silberberg, and H. Markram (2005)
PNAS 102, 880-885
   Abstract »    Full Text »    PDF »
Quantal Size Is Independent of the Release Probability at Hippocampal Excitatory Synapses.
A. A. Biro, N. B. Holderith, and Z. Nusser (2005)
J. Neurosci. 25, 223-232
   Abstract »    Full Text »    PDF »
The Kinetic Profile of Intracellular Calcium Predicts Long-Term Potentiation and Long-Term Depression.
I. Ismailov, D. Kalikulov, T. Inoue, and M. J. Friedlander (2004)
J. Neurosci. 24, 9847-9861
   Abstract »    Full Text »    PDF »
Functional Connectivity in Layer IV Local Excitatory Circuits of Rat Somatosensory Cortex.
A. I. Cowan and C. Stricker (2004)
J Neurophysiol 92, 2137-2150
   Abstract »    Full Text »    PDF »
Probability of Transmitter Release at Neocortical Synapses at Different Temperatures.
M. Volgushev, I. Kudryashov, M. Chistiakova, M. Mukovski, J. Niesmann, and U. T. Eysel (2004)
J Neurophysiol 92, 212-220
   Abstract »    Full Text »    PDF »
Sensory Neuron Signaling to the Brain: Properties of Transmitter Release from Olfactory Nerve Terminals.
G. J. Murphy, L. L. Glickfeld, Z. Balsen, and J. S. Isaacson (2004)
J. Neurosci. 24, 3023-3030
   Abstract »    Full Text »    PDF »

To Advertise     Find Products


Science Signaling. ISSN 1937-9145 (online), 1945-0877 (print). Pre-2008: Science's STKE. ISSN 1525-8882