Error message

No crossref credentials set for sci

Target Cell-Dependent Normalization of Transmitter Release at Neocortical Synapses

Science, 6 May 2005
Vol. 308, Issue 5723, p. 863-866
DOI: 10.1126/science.1100815

Target Cell-Dependent Normalization of Transmitter Release at Neocortical Synapses

  1. Helmut J. Koester1,2,*,,
  2. Daniel Johnston2,*
  1. 1 Abteilung Zellphysiologie, Max-Planck-Institut für Medizinische Forschung, Jahnstraße 29, D-69120 Heidelberg, Germany.
  2. 2 Department of Neuroscience, Baylor College of Medicine, One Baylor Plaza, Houston, TX 77030, USA.
  1. To whom correspondence should be addressed. E-mail: HKoester{at}
  • Published online 17 March 2005;

  • Include this information when citing this paper.

  • * Present address: Center for Learning and Memory, University of Texas at Austin, Austin, TX 78712, USA.


The efficacy and short-term modification of neocortical synaptic connections vary with the type of target neuron. We investigated presynaptic Ca2+ and release probability at single synaptic contacts between pairs of neurons in layer 2/3 of the rat neocortex. The amplitude of Ca2+ signals in boutons of pyramids contacting bitufted or multipolar interneurons or other pyramids was dependent on the target cell type. Optical quantal analysis at single synaptic contacts suggested that release probabilities are also target cell-specific. Both the Ca2+ signal and the release probability of different boutons of a pyramid contacting the same target cell varied little. We propose that the mechanisms that regulate the functional properties of boutons of a pyramid normalize the presynaptic Ca2+ influx and release probability for all those boutons that innervate the same target cell.

    • Received for publication 27 May 2004.
    • Accepted for publication 10 February 2005.


    H. J. Koester and D. Johnston, Target Cell-Dependent Normalization of Transmitter Release at Neocortical Synapses. Science 308, 863-866 (2005).

    Input-specific maturation of synaptic dynamics of parvalbumin interneurons in primary visual cortex
    J. Lu, J. Tucciarone, Y. Lin, and Z. J. Huang
    Proc. Natl. Acad. Sci. USA 111, 16895-16900 (25 November 2014)

    Elfn1 Regulates Target-Specific Release Probability at CA1-Interneuron Synapses
    E. L. Sylwestrak, and A. Ghosh
    Science 338, 536-540 (26 October 2012)

    Decoding the Neuronal Tower of Babel
    C. J. McBain, and A. Ghosh
    Science 338, 482-483 (26 October 2012)

    Determinants of synaptic strength vary across an axon arbor
    X. Peng, T. D. Parsons, and R. J. Balice-Gordon
    J. Neurophysiol. 107, 2430-2441 (1 May 2012)

    Dendritic position is a major determinant of presynaptic strength
    A. P. H. de Jong, S. K. Schmitz, R. F. G. Toonen, and M. Verhage
    JCB 197, 327-337 (16 April 2012)

    Slow oscillating population activity in developing cortical networks: models and experimental results
    T. Baltz, A. Herzog, and T. Voigt
    J. Neurophysiol. 106, 1500-1514 (1 September 2011)

    Specificity of Synaptic Connectivity between Layer 1 Inhibitory Interneurons and Layer 2/3 Pyramidal Neurons in the Rat Neocortex
    C. Wozny, and S. R. Williams
    Cereb Cortex 21, 1818-1826 (1 August 2011)

    CB1 modulation of temporally distinct synaptic facilitation among local circuit interneurons mediated by N-type calcium channels in CA1
    A. B. Ali, and S. R. Williams
    J. Neurophysiol. 105, 1051-1062 (1 March 2011)

    Postsynaptic GluA1 enables acute retrograde enhancement of presynaptic function to coordinate adaptation to synaptic inactivity
    M. Lindskog, L. Li, R. D. Groth, D. Poburko, T. C. Thiagarajan, X. Han, and R. W. Tsien
    Proc. Natl. Acad. Sci. USA 107, 21806-21811 (14 December 2010)

    Multivesicular Release Differentiates the Reliability of Synaptic Transmission between the Visual Cortex and the Somatosensory Cortex
    C.-H. Huang, J. Bao, and T. Sakaba
    J. Neurosci. 30, 11994-12004 (8 September 2010)

    Rapid structural alterations of the active zone lead to sustained changes in neurotransmitter release
    J. Matz, A. Gilyan, A. Kolar, T. McCarvill, and S. R. Krueger
    Proc. Natl. Acad. Sci. USA 107, 8836-8841 (11 May 2010)

    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
    J. Neurosci. 30, 1441-1451 (27 January 2010)

    Neuromodulation at Single Presynaptic Boutons of Cerebellar Parallel Fibers Is Determined by Bouton Size and Basal Action Potential-Evoked Ca Transient Amplitude
    W. Zhang, and D. J. Linden
    J. Neurosci. 29, 15586-15594 (9 December 2009)

    Long-Term Potentiation of Excitatory Synapses on Neocortical Somatostatin-Expressing Interneurons
    H.-X. Chen, M. Jiang, D. Akakin, and S. N. Roper
    J. Neurophysiol. 102, 3251-3259 (1 December 2009)

    Endocannabinoid-Dependent Homeostatic Regulation of Inhibitory Synapses by Miniature Excitatory Synaptic Activities
    S.-y. Zhang, M. Xu, Q.-l. Miao, M.-m. Poo, and X.-h. Zhang
    J. Neurosci. 29, 13222-13231 (21 October 2009)

    Embedding Multiple Trajectories in Simulated Recurrent Neural Networks in a Self-Organizing Manner
    J. K. Liu, and D. V. Buonomano
    J. Neurosci. 29, 13172-13181 (21 October 2009)

    Calcium-Permeable Presynaptic Kainate Receptors Involved in Excitatory Short-Term Facilitation Onto Somatostatin Interneurons During Natural Stimulus Patterns
    H. Y. Sun, A. F. Bartley, and L. E. Dobrunz
    J. Neurophysiol. 101, 1043-1055 (1 February 2009)

    Firing-Pattern-Dependent Specificity of Cortical Excitatory Feed-Forward Subnetworks
    T. Otsuka, and Y. Kawaguchi
    J. Neurosci. 28, 11186-11195 (29 October 2008)

    Fidelity of Complex Spike-Mediated Synaptic Transmission between Inhibitory Interneurons
    M. T. Roberts, K. J. Bender, and L. O. Trussell
    J. Neurosci. 28, 9440-9450 (17 September 2008)

    Efficient Recruitment of Layer 2/3 Interneurons by Layer 4 Input in Single Columns of Rat Somatosensory Cortex
    M. Helmstaedter, J. F. Staiger, B. Sakmann, and D. Feldmeyer
    J. Neurosci. 28, 8273-8284 (13 August 2008)

    Synapse-Specific Expression of Functional Presynaptic NMDA Receptors in Rat Somatosensory Cortex
    D. J. Brasier, and D. E. Feldman
    J. Neurosci. 28, 2199-2211 (27 February 2008)

    Robust but delayed thalamocortical activation of dendritic-targeting inhibitory interneurons
    Z. Tan, H. Hu, Z. J. Huang, and A. Agmon
    Proc. Natl. Acad. Sci. USA 105, 2187-2192 (12 February 2008)

    Monosynaptic Connections between Pairs of L5A Pyramidal Neurons in Columns of Juvenile Rat Somatosensory Cortex
    A. Frick, D. Feldmeyer, M. Helmstaedter, and B. Sakmann
    Cereb Cortex 18, 397-406 (1 February 2008)

    Target Cell-Specific Involvement of Presynaptic Mitochondria in Post-Tetanic Potentiation at Hippocampal Mossy Fiber Synapses
    D. Lee, K.-H. Lee, W.-K. Ho, and S.-H. Lee
    J. Neurosci. 27, 13603-13613 (12 December 2007)

    Spike-Timing-Dependent Plasticity of Neocortical Excitatory Synapses on Inhibitory Interneurons Depends on Target Cell Type
    J.-t. Lu, C.-y. Li, J.-P. Zhao, M.-m. Poo, and X.-h. Zhang
    J. Neurosci. 27, 9711-9720 (5 September 2007)

    Reliability and Heterogeneity of Calcium Signaling at Single Presynaptic Boutons of Cerebellar Granule Cells
    S. D. Brenowitz, and W. G. Regehr
    J. Neurosci. 27, 7888-7898 (25 July 2007)

    Presynaptic Efficacy Directs Normalization of Synaptic Strength in Layer 2/3 Rat Neocortex After Paired Activity
    N. R. Hardingham, G. E. Hardingham, K. D. Fox, and J. J. B. Jack
    J. Neurophysiol. 97, 2965-2975 (1 April 2007)

    Strategies for Odor Coding in the Piriform Cortex
    J. H. Brann, S. R. Saideman, M. T. Valley, and D. Wiedl
    J. Neurosci. 27, 1237-1238 (7 February 2007)

    Retrograde Regulation of GABA Transmission by the Tonic Release of Oxytocin and Endocannabinoids Governs Postsynaptic Firing
    S. H. R. Oliet, D. V. Baimoukhametova, R. Piet, and J. S. Bains
    J. Neurosci. 27, 1325-1333 (7 February 2007)

    An Increase in Calcium Influx Contributes to Post-Tetanic Potentiation at the Rat Calyx of Held Synapse
    R. L. P. Habets, and J. G. G. Borst
    J. Neurophysiol. 96, 2868-2876 (1 December 2006)

    Neural Coding by Two Classes of Principal Cells in the Mouse Piriform Cortex.
    N. Suzuki, and J. M. Bekkers
    J. Neurosci. 26, 11938-11947 (15 November 2006)

    Presynaptic kainate receptor activation is a novel mechanism for target cell-specific short-term facilitation at schaffer collateral synapses.
    H. Y. Sun, and L. E. Dobrunz
    J. Neurosci. 26, 10796-10807 (18 October 2006)

    Active zone assembly and synaptic release
    R. J. Kittel, S. Hallermann, S. Thomsen, C. Wichmann, S. J. Sigrist, and M. Heckmann
    Biochm. Soc. Trans. 34, 939-941 (1 October 2006)

    Ca2+-Dependent Mechanisms of Presynaptic Control at Central Synapses
    D. A. Rusakov, S. Hallermann, S. Thomsen, C. Wichmann, S. J. Sigrist, and M. Heckmann
    Neuroscientist 12, 317-326 (1 August 2006)

    The Role of Nitric Oxide and GluR1 in Presynaptic and Postsynaptic Components of Neocortical Potentiation
    N. Hardingham, and K. Fox
    J. Neurosci. 26, 7395-7404 (12 July 2006)

    Main Determinants of Presynaptic Ca2+ Dynamics at Individual Mossy Fiber-CA3 Pyramidal Cell Synapses
    R. Scott, and D. A. Rusakov
    J. Neurosci. 26, 7071-7081 (28 June 2006)

    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
    J. Neurosci. 26, 6337-6345 (7 June 2006)

    Dendritic Branch Typing and Spine Expression Patterns in Cortical Nonpyramidal Cells
    Y. Kawaguchi, F. Karube, and Y. Kubota
    Cereb Cortex 16, 696-711 (1 May 2006)

    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
    Cereb Cortex 16, 541-552 (1 April 2006)

    Interglomerular Center-Surround Inhibition Shapes Odorant-Evoked Input to the Mouse Olfactory Bulb In Vivo
    D. Vucinic, L. B. Cohen, and E. K. Kosmidis
    J. Neurophysiol. 95, 1881-1887 (1 March 2006)

    Highlights from the Literature
    L. B. Cohen, and E. K. Kosmidis
    Physiology 20, 369-373 (1 December 2005)

    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
    J. Neurosci. 25, 8173-8187 (7 September 2005)

    NEUROSCIENCE: Matching at the Synapse
    S. M. Thompson, C. Saviane, T. A. Nielsen, D. A. DiGregorio, and R. A. Silver
    Science 308, 800-801 (6 May 2005)

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