Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Review Article
  • Published:

Short-term synaptic plasticity: a comparison of two synapses

Nature Reviews Neuroscience volume 5, pages 630–640 (2004)Cite this article

Key Points

  • Synaptic efficacy is regulated by many forms of short-term plasticity during physiological patterns of activity. Here we discuss the distinct functional consequences of short-term plasticity at two powerful synapses. The climbing fibre to cerebellar Purkinje cell synapse and the retinal ganglion cell to thalamocortical neuron (retinogeniculate) synapse share some common synaptic features. However, the climbing fibre evokes a consistent, stereotyped response in the Purkinje cell, whereas the response of the thalamocortical cell to retinal ganglion cell input is more variable.

  • Several features of transmission at the climbing fibre to Purkinje cell synapse minimize depression and allow the climbing fibre to evoke a consistent response in the Purkinje cell during physiological patterns of activity. First, postsynaptic receptor desensitization does not contribute to depression at this synapse even at short interstimulus intervals. Second, calcium that enters during the action potential accelerates recovery from depression. Finally, multivesicular release and receptor saturation make the Purkinje cell less sensitive to decreases in the amount of neurotransmitter released by the climbing fibre.

  • The retinogeniculate synapse contains both AMPA (α-amino-3-hydroxy-5-methyl-4-isoxazole propionic acid) and NMDA (N-methyl-D-aspartate) receptors, which have distinct forms of plasticity. Desensitization and depression of AMPA currents limit their efficacy, particularly during high-frequency activity. Although NMDA currents are limited by saturation, the long duration of NMDA currents results in summation and a greater NMDA contribution during sustained activity.

  • The two currents at the retinogeniculate synapse influence postsynaptic firing in distinct ways. AMPA currents elicit short-latency precisely timed action potentials. NMDA currents, however, elicit longer-latency action potentials and can elicit multiple spikes per presynaptic spike, which results in amplification. Consequently, responses can vary during the course of a train of activity and can differ between thalamocortical neurons on the basis of the relative amplitudes of AMPA and NMDA currents. So, the retinogeniculate synapse dynamically regulates transmission through the two receptor types and their distinct forms of plasticity.

  • The synapses discussed here illustrate that, despite initial similarities, synapses are specialized to serve distinct functional roles. Future work aimed at determining the contributions of multiple forms of plasticity at different synapses and how these interact with intrinsic cellular properties will be necessary to fully understand how short-term synaptic plasticity contributes to the function of synapses in the brain.

Abstract

During physiological patterns of activity, synaptic activity is regulated by many forms of short-term plasticity. Here, we compare the functional consequences of such plasticity at the synapse from the climbing fibre to the Purkinje cell in the cerebellum and at the synapse between the retinal ganglion cell and the thalamocortical relay neuron in the lateral geniculate nucleus. Despite superficial similarities between these two powerful synapses, they have distinctive synaptic plasticity. The climbing fibre synapse is highly reliable but accomplishes this through many synaptic specializations. However, the retinogeniculate synapse dynamically regulates the flow of visual information by using two types of receptor that have different types of plasticity. These synapses illustrate the important functional consequences of synaptic plasticity.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Presynaptic and postsynaptic mechanisms of short-term plasticity.
Figure 2: A comparison of the climbing fibre and retinogeniculate synapses.
Figure 3: Recovery from depression and saturation at the climbing fibre to Purkinje cell synapse.
Figure 4: AMPA and NMDA receptor contributions to retinogeniculate transmission.
Figure 5: AMPA and NMDA component amplitudes contribute to variability in response spike number and timing between different thalamocortical neurons.

Similar content being viewed by others

References

  1. Kandel, E. R., Schwartz, J. H. & Jessell, T. M. Principles of Neural Science (Elsevier, New York, 2000).

    Google Scholar 

  2. Nicholls, J. G., Martin, A. R. & Wallace, B. G. From Neuron to Brain: A Cellular and Molecular Approach to the Function of the Nervous System (Sinauer Associates, Sunderland, 1992).

    Google Scholar 

  3. Cowan, W. M., Sudhof, T. C. & Stevens, C. F. Synapses (Johns Hopkins Univ. Press, Baltimore, Maryland, 2001).

    Google Scholar 

  4. Craig, A. M. & Boudin, H. Molecular heterogeneity of central synapses: afferent and target regulation. Nature Neurosci. 4, 569–578 (2001).

    Article  CAS  PubMed  Google Scholar 

  5. Xu-Friedman, M. A. & Regehr, W. G. Structural contributions to short-term synaptic plasticity. Physiol. Rev. 84, 69–85 (2004).

    Article  CAS  PubMed  Google Scholar 

  6. Atwood, H. L. & Karunanithi, S. Diversification of synaptic strength: presynaptic elements. Nature Rev. Neurosci. 3, 497–516 (2002).

    Article  CAS  Google Scholar 

  7. Fuhrmann, G., Segev, I., Markram, H. & Tsodyks, M. Coding of temporal information by activity-dependent synapses. J. Neurophysiol. 87, 140–148 (2002). This modelling study used experimentally determined parameters of depressing and facilitating cortical synapses to examine the dependence of postsynaptic firing on the history of presynaptic firing. Depressing and facilitating synapses produce maximum information in their postsynaptic responses at different presynaptic firing frequency ranges.

    Article  PubMed  Google Scholar 

  8. Kreitzer, A. & Regehr, W. Modulation of transmission during trains at a cerebellar synapse. J. Neurosci. 20, 1348–1357 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Chen, C., Blitz, D. M. & Regehr, W. G. Contributions of receptor desensitization and saturation to plasticity at the retinogeniculate synapse. Neuron 33, 779–788 (2002). This voltage-clamp analysis revealed different short-term plasticity of the NMDA and AMPA components of the EPSC. During presynaptic bursts, pronounced AMPA receptor desensitization reduced the efficacy of the AMPA component, whereas slow kinetics and receptor saturation accentuated the efficacy of the NMDA component during such bursts.

    Article  CAS  PubMed  Google Scholar 

  10. Brenowitz, S. & Trussell, L. O. Minimizing synaptic depression by control of release probability. J. Neurosci. 21, 1857–1867 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Varela, J. A. et al. A quantitative description of short-term plasticity at excitatory synapses in layer 2/3 of rat primary visual cortex. J. Neurosci. 17, 7926–7940 (1997).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Abbott, L. F., Sen, K., Varela, J. A. & Nelson, S. B. Synaptic depression and cortical gain control. Science 275, 220–222 (1997).

    Article  CAS  PubMed  Google Scholar 

  13. Dittman, J. S., Kreitzer, A. C. & Regehr, W. G. Interplay between facilitation, depression, and residual calcium at three presynaptic terminals. J. Neurosci. 20, 1374–1385 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Markram, H., Lubke, J., Frotscher, M. & Sakmann, B. Regulation of synaptic efficacy by coincidence of postsynaptic APs and EPSPs. Science 275, 213–215 (1997).

    Article  CAS  PubMed  Google Scholar 

  15. Zucker, R. S. & Regehr, W. G. Short-term synaptic plasticity. Annu. Rev. Physiol. 64, 355–405 (2002).

    Article  CAS  PubMed  Google Scholar 

  16. von Gersdorff, H. & Borst, J. G. Short-term plasticity at the calyx of held. Nature Rev. Neurosci. 3, 53–64 (2002).

    Article  CAS  Google Scholar 

  17. Eccles, J. C., Katz, B. & Kuffler, S. W. Nature of the 'endplate potential' in curarized muscle. J. Physiol. (Lond.) 124, 574–585 (1941).

    Google Scholar 

  18. Feng, T. P. Studies on the neuromuscular junction. Chin. J. Physiol. 16, 341–372 (1941).

    CAS  Google Scholar 

  19. Katz, B. & Miledi, R. The role of calcium in neuromuscular facilitation. J. Physiol. (Lond.) 195, 481–492 (1968).

    Article  CAS  Google Scholar 

  20. Felmy, F., Neher, E. & Schneggenburger, R. Probing the intracellular calcium sensitivity of transmitter release during synaptic facilitation. Neuron 37, 801–811 (2003). There was no change in the calcium sensitivity of transmitter release during facilitation. Along with reference 21, this study provides compelling evidence for local buffer saturation as a mechanism underlying facilitation at some synapses.

    Article  CAS  PubMed  Google Scholar 

  21. Blatow, M., Caputi, A., Burnashev, N., Monyer, H. & Rozov, A. Ca2+ buffer saturation underlies paired pulse facilitation in calbindin-D28k-containing terminals. Neuron 38, 79–88 (2003). This study and reference 20 established that facilitation can result from saturation of endogenous buffers. A particularly compelling observation was that the properties of facilitation were altered markedly in mice in which the calcium-binding protein calbindin-D28k was knocked out.

    Article  CAS  PubMed  Google Scholar 

  22. Sippy, T., Cruz-Martin, A., Jeromin, A. & Schweizer, F. E. Acute changes in short-term plasticity at synapses with elevated levels of neuronal calcium sensor-1. Nature Neurosci. 6, 1031–1038 (2003). This study indicates that at some synapses the high-affinity calcium sensor NCS-1 is responsible for facilitation. This study, along with references 23 and 24, suggests that multiple mechanisms can lead to facilitation.

    Article  CAS  PubMed  Google Scholar 

  23. Atluri, P. P. & Regehr, W. G. Determinants of the time course of facilitation at the granule cell to Purkinje cell synapse. J. Neurosci. 16, 5661–5671 (1996).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Kamiya, H. & Zucker, R. S. Residual Ca2+ and short-term synaptic plasticity. Nature 371, 603–606 (1994).

    Article  CAS  PubMed  Google Scholar 

  25. Jones, M. V. & Westbrook, G. L. The impact of receptor desensitization on fast synaptic transmission. Trends Neurosci. 19, 96–101 (1996).

    Article  CAS  PubMed  Google Scholar 

  26. Sun, Y. et al. Mechanism of glutamate receptor desensitization. Nature 417, 245–253 (2002).

    Article  CAS  PubMed  Google Scholar 

  27. Trussell, L. O., Zhang, S. & Raman, I. M. Desensitization of AMPA receptors upon multiquantal neurotransmitter release. Neuron 10, 1185–1196 (1993).

    Article  CAS  PubMed  Google Scholar 

  28. Xu-Friedman, M. A. & Regehr, W. G. Ultrastructural contributions to desensitization at cerebellar mossy fiber to granule cell synapses. J. Neurosci. 23, 2182–2192 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Wadiche, J. I. & Jahr, C. E. Multivesicular release at climbing fiber-Purkinje cell synapses. Neuron 32, 301–313 (2001). A low-affinity AMPA receptor antagonist was used to show, for the first time, that multivesicular release and postsynaptic receptor saturation take place at individual release sites at the climbing fibre synapse.

    Article  CAS  PubMed  Google Scholar 

  30. Foster, K. A., Kreitzer, A. C. & Regehr, W. G. Interaction of postsynaptic receptor saturation with presynaptic mechanisms produces a reliable synapse. Neuron 36, 1115–1126 (2002). This study showed that postsynaptic receptor saturation, multivesicular release and calcium-dependent recovery from depression cause the climbing fibre to evoke a reliable response in the Purkinje cell under physiological conditions.

    Article  CAS  PubMed  Google Scholar 

  31. Harrison, J. & Jahr, C. E. Receptor occupancy limits synaptic depression at climbing fiber synapses. J. Neurosci. 23, 377–383 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Eccles, J. C., Llinas, R. & Sasaki, K. The excitatory synaptic action of climbing fibers on the Purkinje cells of the cerebellum. J. Physiol. (Lond.) 182, 268–296 (1966).

    Article  CAS  Google Scholar 

  33. Ramón y Cajal, S. Histologie du Systeme Nerveux de l'Homme et des Vertebres (Maloine, Paris, 1911).

    Google Scholar 

  34. Palay, S. L. & Chan-Palay, V. Cerebellar Cortex (Springer, New York, 1974).

    Book  Google Scholar 

  35. Eccles, J., Llinas, R. & Sasaki, K. Excitation of cerebellar Purkinje cells by the climbing fibers. Nature 203, 245–246 (1964).

    Article  CAS  PubMed  Google Scholar 

  36. Chen, C. & Regehr, W. G. Developmental remodeling of the retinogeniculate synapse. Neuron 28, 955–966 (2000).

    Article  CAS  PubMed  Google Scholar 

  37. Usrey, W. M., Reppas, J. B. & Reid, R. C. Specificity and strength of retinogeniculate connections. J. Neurophysiol. 82, 3527–3540 (1999).

    Article  CAS  PubMed  Google Scholar 

  38. Hamos, J. E., Van Horn, S. C., Raczkowski, D. & Sherman, S. M. Synaptic circuits involving an individual retinogeniculate axon in the cat. J. Comp. Neurol. 259, 165–192 (1987).

    Article  CAS  PubMed  Google Scholar 

  39. Ito, M. Cerebellar long-term depression: characterization, signal transduction, and functional roles. Physiol. Rev. 81, 1143–1195 (2001).

    Article  CAS  PubMed  Google Scholar 

  40. Carey, M. & Lisberger, S. Embarrassed, but not depressed: eye opening lessons for cerebellar learning. Neuron 35, 223–226 (2002).

    Article  CAS  PubMed  Google Scholar 

  41. Bloedel, J. R. & Bracha, V. Current concepts of climbing fiber function. Anat. Rec. 253, 118–126 (1998).

    Article  CAS  PubMed  Google Scholar 

  42. Napper, R. M. A. & Harvey, R. J. Number of parallel fiber synapses on an individual purkinje cell in the cerbellum of the rat. J. Comp. Neurol. 274, 168–177 (1988).

    Article  CAS  PubMed  Google Scholar 

  43. Napper, R. M. A. & Harvey, R. J. Quantitative study of the purkinje cell dendritic spines in the rat cerebellum. J. Comp. Neurol. 274, 158–167 (1988).

    Article  CAS  PubMed  Google Scholar 

  44. Llinas, R. & Sugimori, M. Electrophysiological properties of in vitro purkinje cell somata in mammalian cerebellar slices. J. Physiol. (Lond.) 305, 171–195 (1980).

    Article  CAS  Google Scholar 

  45. Llinas, R. & Sugimori, M. Electrophysiological properties of in vitro Purkinje cell dendrites in mammalian cerebellar slices. J. Physiol. (Lond.) 305, 197–213 (1980).

    Article  CAS  Google Scholar 

  46. Ito, M., Sakurai, M. & Tongroach, P. Climbing fibre induced depression of both mossy fibre responsiveness and glutamate sensitivity of cerebellar Purkinje cells. J. Physiol. (Lond.) 324, 113–134 (1982).

    Article  CAS  Google Scholar 

  47. Konnerth, A., Dreessen, J. & Augustine, G. J. Brief dendritic calcium signals initiate long-lasting synaptic depression in cerebellar Purkinje cells. Proc. Natl Acad. Sci. USA 89, 7051–7055 (1992).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Armstrong, D. M. & Rawson, J. A. Activity patterns of cerebellar cortical neurones and climbing fibre afferents in the awake cat. J. Physiol. (Lond.) 289, 425–448 (1979).

    Article  CAS  Google Scholar 

  49. Schwarz, C. & Welsh, J. P. Dynamic modulation of mossy fiber system throughput by inferior olive synchrony: a multielectrode study of cerebellar cortex activated by motor cortex. J. Neurophysiol. 86, 2489–2504 (2001).

    Article  CAS  PubMed  Google Scholar 

  50. Bloedel, J. R. & Ebner, T. J. Rhythmic discharge of climbing fibre afferents in response to natural peripheral stimuli in the cat. J. Physiol. (Lond.) 352, 129–146 (1984).

    Article  CAS  Google Scholar 

  51. Llano, I., Marty, A., Armstrong, C. M. & Konnerth, A. Synaptic- and agonist-induced excitatory currents of Purkinje cells in rat cerebellar slices. J. Physiol. (Lond.) 434, 183–213 (1991).

    Article  CAS  Google Scholar 

  52. Farrant, M. & Cull-Candy, S. G. Excitatory amino acid receptor-channels in purkinje cells in thin cerebellar slices. Proc. R. Soc. Lond. B 244, 179–184 (1991).

    Article  CAS  Google Scholar 

  53. Hashimoto, K. & Kano, M. Presynaptic origin of paired-pulse depression at climbing fiber-Purkinje cell synapses in the rat cerebellum. J. Physiol. (Lond.) 506, 391–405 (1998).

    Article  CAS  Google Scholar 

  54. Dittman, J. S. & Regehr, W. G. Calcium dependence and recovery kinetics of presynaptic depression at the climbing fiber to Purkinje cell synapse. J. Neurosci. 18, 6147–6162 (1998).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Dzubay, J. A. & Jahr, C. E. The concentration of synaptically released glutamate outside of the climbing fiber-Purkinje cell synaptic cleft. J. Neurosci. 19, 5265–5274 (1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Hausser, M. & Roth, A. Dendritic and somatic glutamate receptor channels in rat cerebellar Purkinje cells. J. Physiol. (Lond.) 501, 77–95 (1997).

    Article  Google Scholar 

  57. Xu-Friedman, M. A., Harris, K. M. & Regehr, W. G. Three-dimensional comparison of ultrastructural characteristics at depressing and facilitating synapses onto cerebellar Purkinje cells. J. Neurosci. 21, 6666–6672 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Chaudhry, F. A. et al. Glutamate transporters in glial plasma membranes: highly differentiated localizations revealed by quantitative ultrastructural immunocytochemistry. Neuron 15, 711–720 (1995).

    Article  CAS  PubMed  Google Scholar 

  59. Rothstein, J. D. et al. Localization of neuronal and glial glutamate transporters. Neuron 13, 713–725 (1994).

    Article  CAS  PubMed  Google Scholar 

  60. Stevens, C. F. & Wesseling, J. F. Activity-dependent modulation of the rate at which synaptic vesicles become available to undergo exocytosis. Neuron 21, 415–424 (1998).

    Article  CAS  PubMed  Google Scholar 

  61. Wang, L. -Y. & Kaczmarek, L. K. High-frequency firing helps replenish the readily releasable pool of synaptic vesicles. Nature 394, 384–388 (1998).

    Article  CAS  PubMed  Google Scholar 

  62. Sakaba, T. & Neher, E. Calmodulin mediates rapid recruitment of fast-releasing synaptic vesicles at a calyx-type synapse. Neuron 32, 1119–1131 (2001). Previous studies had shown that elevations of presynaptic calcium accelerated recovery from depression. This study shows that this effect is mediated by calmodulin at the calyx of Held.

    Article  CAS  PubMed  Google Scholar 

  63. Lu, S. M., Guido, W. & Sherman, S. M. Effects of membrane voltage on receptive field properties of lateral geniculate neurons in the cat: contributions of the low-threshold Ca2+ conductance. J. Neurophysiol. 68, 2185–2198 (1992).

    Article  CAS  PubMed  Google Scholar 

  64. McCormick, D. A. Cellular mechanisms underlying cholinergic and noradrenergic modulation of neuronal firing mode in the cat and guinea pig dorsal lateral geniculate nucleus. J. Neurosci. 12, 278–289 (1992).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Steriade, M., Jones, E. G. & McCormick, D. A. Thalamus (Elsevier Science, Oxford, 1997).

    Google Scholar 

  66. Sherman, S. M. Dual response modes in lateral geniculate neurons: mechanisms and functions. Vis. Neurosci. 13, 205–213 (1996).

    Article  CAS  PubMed  Google Scholar 

  67. Sherman, S. M. Tonic and burst firing: dual modes of thalamocortical relay. Trends Neurosci. 24, 122–126 (2001).

    Article  CAS  PubMed  Google Scholar 

  68. Lu, S. M., Guido, W. & Sherman, S. M. The brain-stem parabrachial region controls mode of response to visual stimulation of neurons in the cat's lateral geniculate nucleus. Vis. Neurosci. 10, 631–642 (1993).

    Article  CAS  PubMed  Google Scholar 

  69. Guido, W. & Weyand, T. Burst responses in thalamic relay cells of the awake behaving cat. J. Neurophysiol. 74, 1782–1786 (1995).

    Article  CAS  PubMed  Google Scholar 

  70. Weyand, T. G., Boudreaux, M. & Guido, W. Burst and tonic response modes in thalamic neurons during sleep and wakefulness. J. Neurophysiol. 85, 1107–1118 (2001).

    Article  CAS  PubMed  Google Scholar 

  71. Ramcharan, E. J., Gnadt, J. W. & Sherman, S. M. Burst and tonic firing in thalamic cells of unanesthetized, behaving monkeys. Vis. Neurosci. 17, 55–62 (2000).

    Article  CAS  PubMed  Google Scholar 

  72. Cleland, B. G. & Lee, B. B. A comparison of visual responses of cat lateral geniculate nucleus neurones with those of ganglion cells afferent to them. J. Physiol. (Lond.) 369, 249–268 (1985).

    Article  CAS  Google Scholar 

  73. Usrey, W. M. Spike timing and visual processing in the retinogeniculocortical pathway. Phil. Trans. R. Soc. Lond. B 357, 1729–1737 (2002).

    Article  Google Scholar 

  74. Swadlow, H. A. & Gusev, A. G. The impact of 'bursting' thalamic impulses at a neocortical synapse. Nature Neurosci. 4, 402–408 (2001).

    Article  CAS  PubMed  Google Scholar 

  75. Mastronarde, D. N. Two classes of single-input X-cells in cat lateral geniculate nucleus. II. Retinal inputs and the generation of receptive-field properties. J. Neurophysiol. 57, 381–413 (1987).

    Article  CAS  PubMed  Google Scholar 

  76. Usrey, W. M., Reppas, J. B. & Reid, R. C. Paired-spike interactions and synaptic efficacy of retinal inputs to the thalamus. Nature 395, 384–387 (1998). Paired RGC and thalamocortical neuron recordings in vivo showed the dependence of postsynaptic spikes on the timing of RGC spikes. This study also established that presynaptic spike timing influenced the synchronous firing of thalamocortical neurons.

    Article  CAS  PubMed  Google Scholar 

  77. Rowe, M. H. & Fischer, Q. Dynamic properties of retino-geniculate synapses in the cat. Vis. Neurosci. 18, 219–231 (2001).

    Article  CAS  PubMed  Google Scholar 

  78. Rodieck, R. W. & Stone, J. Response of cat retinal ganglion cells to moving visual patterns. J. Neurophysiol. 28, 819–832 (1965).

    Article  CAS  PubMed  Google Scholar 

  79. Kara, P., Reinagel, P. & Reid, R. C. Low response variability in simultaneously recorded retinal, thalamic, and cortical neurons. Neuron 27, 635–646 (2000).

    Article  CAS  PubMed  Google Scholar 

  80. Meister, M. & Berry, M. J. 2nd. The neural code of the retina. Neuron 22, 435–450 (1999).

    Article  CAS  PubMed  Google Scholar 

  81. Kuffler, S. W. Discharge patterns and functional organization of mammalian retina. J. Neurophysiol. 16, 37–68 (1953).

    Article  CAS  PubMed  Google Scholar 

  82. Barlow, H. B. Summation and inhibition in the frog's retina. J. Physiol. (Lond.) 119, 69–88 (1953).

    Article  CAS  Google Scholar 

  83. Turner, J. P., Leresche, N., Guyon, A., Soltesz, I. & Crunelli, V. Sensory input and burst firing output of rat and cat thalamocortical cells: the role of NMDA and non-NMDA receptors. J. Physiol. (Lond.) 480, 281–295 (1994).

    Article  CAS  Google Scholar 

  84. Funke, K., Eysel, U. T. & FitzGibbon, T. Retinogeniculate transmission by NMDA and non-NMDA receptors in the cat. Brain Res. 547, 229–238 (1991).

    Article  CAS  PubMed  Google Scholar 

  85. Sillito, A. M., Murphy, P. C., Salt, T. E. & Moody, C. I. Dependence of retinogeniculate transmission in cat on NMDA receptors. J. Neurophysiol. 63, 347–355 (1990).

    Article  CAS  PubMed  Google Scholar 

  86. Kwon, Y. H., Esguerra, M. & Sur, M. NMDA and non-NMDA receptors mediate visual responses of neurons in the cat's lateral geniculate nucleus. J. Neurophysiol. 66, 414–428 (1991).

    Article  CAS  PubMed  Google Scholar 

  87. Hohnke, C. D., Oray, S. & Sur, M. Activity-dependent patterning of retinogeniculate axons proceeds with a constant contribution from AMPA and NMDA receptors. J. Neurosci. 20, 8051–8060 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Zorumski, C. F. & Thio, L. L. Properties of vertebrate glutamate receptors: calcium mobilization and desensitization. Prog. Neurobiol. 39, 295–336 (1992).

    Article  CAS  PubMed  Google Scholar 

  89. Mayer, M. L. & Westbrook, G. L. The physiology of excitatory amino acids in the vertebrate central nervous system. Prog. Neurobiol. 28, 197–276 (1987).

    Article  CAS  PubMed  Google Scholar 

  90. Monaghan, D. T., Bridges, R. J. & Cotman, C. W. The excitatory amino acid receptors: their classes, pharmacology, and distinct properties in the function of the central nervous system. Annu. Rev. Pharmacol. Toxicol. 29, 365–402 (1989).

    Article  CAS  PubMed  Google Scholar 

  91. Harata, N., Katayama, J. & Akaike, N. Excitatory amino acid responses in relay neurons of the rat lateral geniculate nucleus. Neuroscience 89, 109–125 (1999).

    Article  CAS  PubMed  Google Scholar 

  92. Esguerra, M., Kwon, Y. H. & Sur, M. Retinogeniculate EPSPs recorded intracellularly in the ferret lateral geniculate nucleus in vitro: role of NMDA receptors. Vis. Neurosci. 8, 545–555 (1992).

    Article  CAS  PubMed  Google Scholar 

  93. Ramoa, A. S. & McCormick, D. A. Enhanced activation of NMDA receptor responses at the immature retinogeniculate synapse. J. Neurosci. 14, 2098–2105 (1994).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  94. Mayer, M. L. & Westbrook, G. L. Permeation and block of N-methyl-D-aspartic acid receptor channels by divalent cations in mouse cultured central neurones. J. Physiol. (Lond.) 394, 501–527 (1987).

    Article  CAS  Google Scholar 

  95. Blitz, D. M. & Regehr, W. G. Retinogeniculate synaptic properties controlling spike number and timing in relay neurons. J. Neurophysiol. 90, 2438–2450 (2003). This follow up to reference 9 used current- and dynamic-clamp recordings to study the effects of single RGC inputs on the firing of thalamocortical neurons in brain slice. The AMPA component of the EPSC elicited precisely timed spikes whereas the NMDA component allowed a single presynaptic spike to evoke brief bursts of postsynaptic spikes.

    Article  PubMed  Google Scholar 

  96. Jonas, P. & Spruston, N. Mechanisms shaping glutamate-mediated excitatory postsynaptic currents in the CNS. Curr. Opin. Neurobiol. 4, 366–372 (1994).

    Article  CAS  PubMed  Google Scholar 

  97. Sprengel, R. & Seeburg, P. H. The unique properties of glutamate receptor channels. FEBS Lett. 325, 90–94 (1993).

    Article  CAS  PubMed  Google Scholar 

  98. Collingridge, G. L. & Bliss, T. V. Memories of NMDA receptors and LTP. Trends Neurosci. 18, 54–56 (1995).

    Article  CAS  PubMed  Google Scholar 

  99. Collingridge, G. L. & Bliss, T. V. NMDA receptors: their role in long-term potentiation. Trends Neurosci. 10, 288–293 (1987).

    Article  CAS  Google Scholar 

  100. Bear, M. F. Progress in understanding NMDA-receptor-dependent synaptic plasticity in the visual cortex. J. Physiol. (Paris) 90, 223–227 (1996).

    Article  CAS  Google Scholar 

  101. Armstrong-James, M., Welker, E. & Callahan, C. A. The contribution of NMDA and non-NMDA receptors to fast and slow transmission of sensory information in the rat SI barrel cortex. J. Neurosci. 13, 2149–2160 (1993).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  102. Binns, K. E. & Salt, T. E. Excitatory amino acid receptors participate in synaptic transmission of visual responses in the superficial layers of the cat superior colliculus. Eur. J. Neurosci. 6, 161–169 (1994).

    Article  CAS  PubMed  Google Scholar 

  103. Daw, N. W., Stein, P. S. G. & Fox, K. The role of NMDA receptors in information processing. Annu. Rev. Neurosci. 16, 207–222 (1993).

    Article  CAS  PubMed  Google Scholar 

  104. Scharfman, H. E., Lu, S. M., Guido, W., Adams, P. R. & Sherman, S. M. N-methyl-D-aspartate receptors contribute to excitatory postsynaptic potentials of cat lateral geniculate neurons recorded in thalamic slices. Proc. Natl Acad. Sci. USA 87, 4548–4552 (1990).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  105. Sillito, A. M., Murphy, P. C. & Salt, T. E. The contribution of the non-N-methyl-D-aspartate group of excitatory amino acid receptors to retinogeniculate transmission in the cat. Neuroscience 34, 273–280 (1990).

    Article  CAS  PubMed  Google Scholar 

  106. Famiglietti, E. V. Jr & Peters, A. The synaptic glomerulus and the intrinsic neuron in the dorsal lateral geniculate nucleus of the cat. J. Comp. Neurol. 144, 285–334 (1972).

    Article  PubMed  Google Scholar 

  107. Prinz, A. A., Abbott, L. F. & Marder, E. The dynamic clamp comes of age. Trends Neurosci. 27, 218–224 (2004).

    Article  CAS  PubMed  Google Scholar 

  108. Reinagel, P. & Reid, R. C. Precise firing events are conserved across neurons. J. Neurosci. 22, 6837–6841 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  109. McCormick, D. A. & Feeser, H. R. Functional implications of burst firing and single spike activity in lateral geniculate relay neurons. Neuroscience 39, 103–113 (1990).

    Article  CAS  PubMed  Google Scholar 

  110. Usrey, W. M., Alonso, J. M. & Reid, R. C. Synaptic interactions between thalamic inputs to simple cells in cat visual cortex. J. Neurosci. 20, 5461–5467 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  111. Usrey, W. M. The role of spike timing for thalamocortical processing. Curr. Opin. Neurobiol. 12, 411–417 (2002).

    Article  CAS  PubMed  Google Scholar 

  112. Kara, P. & Reid, R. C. Efficacy of retinal spikes in driving cortical responses. J. Neurosci. 23, 8547–8557 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  113. Nadim, F., Manor, Y., Kopell, N. & Marder, E. Synaptic depression creates a switch that controls the frequency of an oscillatory circuit. Proc. Natl Acad. Sci. USA 96, 8206–8211 (1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  114. Fortune, E. S. & Rose, G. J. Roles for short-term synaptic plasticity in behavior. J. Physiol. (Paris) 96, 539–545 (2002).

    Article  Google Scholar 

  115. Chung, S., Li, X. & Nelson, S. B. Short-term depression at thalamocortical synapses contributes to rapid adaptation of cortical sensory responses in vivo. Neuron 34, 437–446 (2002). Whole-cell patch-clamp recordings in vivo provided a convincing demonstration that short-term depression of thalamocortical synapses contributes to the adaptation of cortical neurons in response to whisker deflections.

    Article  CAS  PubMed  Google Scholar 

  116. Taschenberger, H. & von Gersdorff, H. Fine-tuning an auditory synapse for speed and fidelity: developmental changes in presynaptic waveform, EPSC kinetics, and synaptic plasticity. J. Neurosci. 20, 9162–9173 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  117. Axmacher, N. & Miles, R. Intrinsic cellular currents and the temporal precision of EPSP-action potential coupling in CA1 pyramidal cells. J. Physiol. (Lond.) 555, 713–725 (2004).

    Article  CAS  Google Scholar 

  118. Fricker, D. & Miles, R. EPSP amplification and the precision of spike timing in hippocampal neurons. Neuron 28, 559–569 (2000).

    Article  CAS  PubMed  Google Scholar 

  119. Magee, J. C. Dendritic integration of excitatory synaptic input. Nature Rev. Neurosci. 1, 181–190 (2000).

    Article  CAS  Google Scholar 

  120. Magee, J. C. & Johnston, D. Synaptic activation of voltage-gated channels in the dendrites of hippocampal pyramidal neurons. Science 268, 301–304 (1995).

    Article  CAS  PubMed  Google Scholar 

  121. Williams, S. R. & Stuart, G. J. Role of dendritic synapse location in the control of action potential output. Trends Neurosci. 26, 147–154 (2003).

    Article  CAS  PubMed  Google Scholar 

  122. Takagi, H. Roles of ion channels in EPSP integration at neuronal dendrites. Neurosci. Res. 37, 167–171 (2000).

    Article  CAS  PubMed  Google Scholar 

  123. Magee, J. C. Dendritic hyperpolarization-activated currents modify the integrative properties of hippocampal CA1 pyramidal neurons. J. Neurosci. 18, 7613–7624 (1998).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  124. Williams, S. R. & Stuart, G. J. Voltage- and site-dependent control of the somatic impact of dendritic IPSPs. J. Neurosci. 23, 7358–7367 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  125. Hanson, J. E., Smith, Y. & Jaeger, D. Sodium channels and dendritic spike initiation at excitatory synapses in globus pallidus neurons. J. Neurosci. 24, 329–340 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  126. Golding, N. L. & Spruston, N. Dendritic sodium spikes are variable triggers of axonal action potentials in hippocampal CA1 pyramidal neurons. Neuron 21, 1189–1200 (1998).

    Article  CAS  PubMed  Google Scholar 

  127. Fuentealba, P., Crochet, S., Timofeev, I. & Steriade, M. Synaptic interactions between thalamic and cortical inputs onto cortical neurons in vivo. J. Neurophysiol. 91, 1990–1998 (2004).

    Article  PubMed  Google Scholar 

  128. Carter, A. G. & Regehr, W. G. Quantal events shape cerebellar interneuron firing. Nature Neurosci. 5, 1309–1318 (2002).

    Article  CAS  PubMed  Google Scholar 

  129. Kreitzer, A. C., Gee, K. R., Archer, E. A. & Regehr, W. G. Monitoring presynaptic calcium dynamics in projection fibers by in vivo loading of a novel calcium indicator. Neuron 27, 25–32 (2000).

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

D.M.B. and K.A.F. contributed equally in the preparation of this review.

Author information

Authors and Affiliations

  1. Department of Neurobiology, Harvard Medical School, 220 Longwood Avenue, Boston, 02115, Massachusetts, USA

    Dawn M. Blitz, Kelly A. Foster & Wade G. Regehr

Authors
  1. Dawn M. Blitz
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Kelly A. Foster
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Wade G. Regehr
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Wade G. Regehr.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Related links

Related links

FURTHER INFORMATION

Encyclopedia of Life Sciences

Synaptic Plasticity: Short Term

AMPA Receptors

Long-term Depression and Depotentiation

Regehr's laboratory homepage

Glossary

READILY RELEASABLE POOL

A pool of synaptic vesicles that is available for rapid fusion with the presynaptic membrane on arrival of a nerve impulse. The vesicles are docked to the membrane and have been biochemically primed for release.

PAIRED-PULSE DEPRESSION

A decrease in the amplitude of the second of two closely timed excitatory postsynaptic currents. It can result presynaptically from a decrease in the amount of neurotransmitter released or postsynaptically as a result of desensitization.

BERGMANN GLIA

Astrocytes that are located in the cerebellum with their cell bodies close to a Purkinje cell. They extend radial fibres along the dendritic tree of the Purkinje cell and ensheath synapses made by the climbing fibre and parallel fibres.

DYNAMIC-CLAMP

A technique to introduce artificial synaptic or voltage-gated conductance into a neuron. The time course, voltage dependence and reversal potential are measured under voltage-clamp conditions and are used to determine the appropriate current to be injected to mimic the synaptic conductance by the dynamic-clamp technique, in current-clamp recording mode.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Blitz, D., Foster, K. & Regehr, W. Short-term synaptic plasticity: a comparison of two synapses. Nat Rev Neurosci 5, 630–640 (2004). https://doi.org/10.1038/nrn1475

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1038/nrn1475

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing