Multiple mechanisms govern the dynamics of depression at neocortical synapses of young rats

Journal of Physiology

Volumn 557, Issue 2, 2004, Pages 415-438

  Fuhrmann, Galit ^a,b   Cowan, Anna ^c,d   Segev, Idan ^b   Tsodyks, Misha ^a   Stricker, Christian ^c,d,e  

^a WEIZMANN INSTITUTE OF SCIENCE   (Israel)

^b HEBREW UNIVERSITY OF JERUSALEM   (Israel)

^c Institute of Neuroinformatics Zurich   (Switzerland)

^d Biology and Environment   (Australia)

^e The Australian National University   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM ACTIVATED POTASSIUM CHANNEL; CALCIUM ION; NEUROTRANSMITTER; POTASSIUM ION;

ANIMAL CELL; ARTICLE; BRAIN SLICE; CONTROLLED STUDY; EXCITATORY POSTSYNAPTIC POTENTIAL; NERVE CELL EXCITABILITY; NERVE POTENTIAL; NEUROTRANSMISSION; NONHUMAN; POSTSYNAPTIC POTENTIAL; PRESYNAPTIC POTENTIAL; PRIORITY JOURNAL; RAT; SOMATOSENSORY CORTEX; SYNAPTIC POTENTIAL; SYNAPTIC TRANSMISSION; ANIMAL TISSUE; EVOKED CORTICAL RESPONSE; HOMEOSTASIS; NEOCORTICAL SYNAPSE; NERVE CELL MEMBRANE STEADY POTENTIAL; NERVE CELL NETWORK; NERVE CELL STIMULATION; NEUROTRANSMITTER RELEASE; PYRAMIDAL NERVE CELL; QUANTITATIVE ANALYSIS; SHORT-TERM SYNAPTIC DEPRESSION; SIMULATION; SYNAPSE; TEMPERATURE DEPENDENCE;

ANIMALS; CALCIUM; ELECTRIC STIMULATION; EXCITATORY POSTSYNAPTIC POTENTIALS; MODELS, NEUROLOGICAL; NEOCORTEX; NEURONS; PATCH-CLAMP TECHNIQUES; RATS; RATS, WISTAR; SYNAPSES; SYNAPTIC TRANSMISSION; TEMPERATURE;

EID: 3042595548     PISSN: 00223751     EISSN: None     Source Type: Journal    
DOI: 10.1113/jphysiol.2003.058107     Document Type: Article

References (64)

1. Abbott LF, Varela JA, Sen K & Nelson SB (1997). Synaptic depression and cortical gain control. Science 275, 220-224.
2. Bellingham MC & Walmsley B (1999). A novel presynaptic inhibitory mechanism underlies paired pulse depression at a fast central synapse. Neuron 23, 159-170.
3. Bielefeldt K & Jackson MB (1993). A calcium-activated potassium channel causes frequency-dependent action-potential failures in a mammalian nerve terminal. J Neurophysiol 70, 284-298.
4. Borst JGG & Sakmann B (1999). Depletion of calcium in the synaptic cleft of a calyx-type synapse in the rat brainstem. J Physiol 521, 123-133.
5. Brecht M & Sakmann B (2002). Dynamic representation of whisker deflection by postsynaptic potentials in morphologically reconstructed spiny stellate and pyramidal cells in the barrels and septa of layer 4 in rat somatosensory cortex. J Physiol 543, 49-70.
6. Brody DL & Yue DT (2000). Release-independent short-term synaptic depression in cultured hippocampal neurons. J Neurosci 20, 2480-2494.
7. Coulter DA, Huguenard JR & Prince DA (1989). Calcium currents in rat thalamocortical relay neurons: Kinetic properties of the transient, low-threshold current. J Physiol 414, 587-604.
8. Courtney KR (1978). Extended moment analysis for binomial parameters of transmitter release. J Theor Biol 73, 285-292.
9. Cox CL, Denk W, Tank DW & Svoboda K (2000). Action potentials reliably invade axonal arbors of rat neocortical neurons. Proc Natl Acad Sci U S A 97, 9724-9728.
10. + conductance in hippocampus. Nature 389, 286-289.
11. AHP in reticularis neurons. J Neurophysiol 79, 2911-2918.
12. Del Castillo J & Katz B (1954). Quantal components of the end-plate potential. J Physiol 124, 560-573.
13. Dittman JS, Kreitzer AC & Regehr WG (2000). Interplay between facilitation, depression, and residual calcium at three presynaptic terminals. J Neurosci 20, 1374-1385.
14. Dittman JS & Regehr WG (1998). Calcium dependence and recovery kinetics of presynaptic depression at the climbing fiber to Purkinje cell synapse. J Neurosci 18, 6147-6167.
15. Dobrunz LE, Huang EP & Stevens CF (1997). Very short-term plasticity in hippocampal synapses. Proc Natl Acad Sci U S A 94, 14843-14847.
16. Dreyer F, Walther C & Peper K (1976). Junctional and extrajunctional acetylcholine receptors in normal and denervated frog muscle fibres. Pflugers Arch 366, 1-9.
17. Forsythe ID, Tsujimoto T, Barnes-Davies M, Cuttle MF & Takahashi T (1998). Inactivation of presynaptic calcium current contributes to synaptic depression at a fast central synapse. Neuron 20, 797-807.
18. Fuhrmann G, Segev I, Markram H & Tsodyks MV (2002). Coding of temporal information by activity-dependent synapses. J Neurophysiol 87, 140-148.
19. Gover TD, Jiang X-Y & Abrams TW (2002). Persistent, exocytosis-independent silencing of release sites underlies homosynaptic depression at sensory synapses in Aplysia. J Neurosci 22, 1942-1955.
20. Granit R, Kernell D & Lamarre Y (1966). Algebraical summation in synaptic activation of motoneurones firing within the 'primary range' to injected current. J Physiol 187, 379-399.
21. Hardingham NR & Larkman AU (1998). The reliability of excitatory synaptic transmission in slices of rat visual cortex in vitro is temperature dependent. J Physiol 507, 249-256.
22. Hatt H & Smith DO (1976). Synaptic depression related to presynaptic axon conduction block. J Physiol 259, 367-393.
23. Hille B (2001). Ionic Channels of Excitable Membranes. Sinauer Assoc., Inc, Sunderland, MA, USA.
24. Huguenard JR, Coulter DA & Prince DA (1991). A fast transient potassium current in thalamic relay neurons: Kinetics of activation and inactivation. J Neurophysiol 66, 1304-1315.
25. Jack JJB, Redman SJ & Wong K (1981). The components of synaptic potentials evoked in cat spinal motoneurones by impulses in single group Ia afferents. J Physiol 321, 65-96.
26. Klein M (1994). Synaptic augmentation by 5-HT at rested Aplysia sensorimotor synapses: Independence of action potential prolongation. Neuron 13, 159-166.
27. Koester HJ & Sakmann B (2000). Calcium dynamics associated with action potentials in single nerve terminals of pyramidal cells in layer 2/3 of the young rat neocortex. J Physiol 529, 625-646.
28. Korn H & Faber DS (1991). Quantal analysis and synaptic efficacy in the CNS. Trends Neurosci 14, 439-445.
29. Korn H, Faber DS, Burnod Y & Triller A (1984). Regulation of efficacy at central synapses. J Neurosci 4, 125-130.
30. Kraushaar U & Jonas P (2000). Efficacy and stability of quantal GABA release at a hippocampal interneuron-principal neuron synapse. J Neurosci 20, 5594-5607.
31. Kuno M (1964). Quantal components of excitatory synaptic potentials in spinal motoneurones. J Physiol 175, 81-99.
32. Lüscher C, Streit J, Quadroni R & Lüscher H-R (1994). Action potential propagation through embryonic dorsal root ganglion cells in culture. I. Influence of the cell morphology and propagation properties. J Neurophysiol 72, 622-633.
33. Maass W & Zador AM (1999). Dynamic stochastic synapses as computational units. Neural Comput 11, 903-917.
34. Magleby KL (1987). Short-term changes in synaptic efficacy. In Synaptic Function, ed.Edelman GM, Gall WE & Cowan WM, pp. 21-56. John Wiley & Sons, New York.
35. Magleby KL & Zengel JE (1976). Augmentation: a process that acts to increase transmitter release at the frog neuromuscular junction. J Physiol 257, 449-470.
36. Markram H, Lübke J, Frotscher M, Roth A & Sakmann B (1997). Physiology and anatomy of synaptic connections between thick tufted pyramidal neurones in the developing rat neocortex. J Physiol 500, 409-440.
37. Matveev V & Wang X-J (2000). Implications of all-or none synaptic transmission and short-term depression beyond vesicle depletion: a computational study. J Neurosci 20, 1575-1588.
38. O'Donovan MJ & Rinzel J (1997). Synaptic depression: a dynamic regulator of synaptic communication with varied functional roles. Trends Neurosci 20, 431-433.
39. Ohana O & Sakmann B (1998). Transmitter release modulation in nerve terminals of rat neocortical pyramidal cells by intracellular calcium buffers. J Physiol 513, 135-148.
40. Quastel DMJ (1997). The binomial model in fluctuation analysis of quantal neurotransmitter release. Biophys J 72, 728-753.
41. Redman SJ (1990). Quantal analysis of synaptic potentials in neurons of the central nervous system. Physiol Rev 70, 165-198.
42. Reyes AD, Luján R, Rozov A, Burnashev N, Somogyi P & Sakmann B (1998). Target-cell-specific facilitation and depression in neocortical circuits. Nat Neurosci 1, 279-285.
43. 2+ buffers in facilitating and depressing nerve terminals of pyramidal cells in layer 2/3 ofthe rat neocortex indicates a target cell-specific difference in presynaptic calcium dynamics. J Physiol 531, 807-826.
44. Sakaba T & Neher E (2001). Calmodulin mediates rapid recruitment of fast-releasing synaptic vesicles at a calyx-type synapse. Neuron 32, 1119-1131.
45. B receptor activation at a glutamatergic synapse. Nature 424, 775-778.
46. Scheuss V, Schneggenburger R & Neher E (2002). Separation of presynaptic and postsynaptic contributions to depression by covariance analysis of successive EPSCs at the calyx of Held synapse. J Neurosci 22, 728-739.
47. Simkus CRL & Stricker C (2002). Analysis of mEPSCs recorded in layer II neurons of rat barrel cortex. J Physiol 545, 509-520.
48. Stevens CF & Wesseling JF (1998). Activity-dependent modulation of the rate at which synaptic vesicles become available to undergo exocytosis. Neuron 21, 415-424.
49. Stevens CF & Wesseling JF (1999). Augmentation is a potentiation of the exocytotic process. Neuron 22, 139-146.
50. Stricker C, Daley D & Redman SJ (1994). Statistical analysis of synaptic transmission: Model discrimination and confidence limits. Biophys J 67, 532-547.
51. Stricker C, Field AC & Redman SJ (1996). Statistical analysis of amplitude fluctuations in EPSCs evoked in rat CA1 pyramidal neurones in vitro. J Physiol 490, 419-441.
52. Stuart GJ & Sakmann B (1995). Amplification of EPSPs by axosomatic sodium channels in neocortical pyramdial neurons. Neuron 15, 1065-1076.
53. Swandulla D, Hans M, Zipser K & Augustine GJ (1991). Role of residual calcium in synaptic depression and posttetanic potentiation: Fast and slow calcium signaling in nerve terminals. Neuron 7, 915-926.
54. Tarczy-Hornoch K, Martin KAC, Jack JJB & Stratford KJ (1998). Synaptic interaction between smooth and spiny neurones in layer 4 of cat visual cortex in vitro. J Physiol 508, 351-363.
55. Thomson AM & Bannister AP (1999). Release-independent depression at pyramidal inputs onto specific cell targets: Dual recordings in slices of rat cortex. J Physiol 519, 57-70.
56. Thomson AM, Deuchars J & West DC (1993). Large, deep layer pyramid-pyramid single axon EPSPs in slices of rat motor cortex display paired pulse and frequency-dependent depression, mediated presynaptically and self-facilitation, mediated postsynaptically. J Neurophysiol 70, 2354-2369.
57. Tsodyks MV & Markram H (1997). The neural code between neocortical pyramidal neurons depends on neurotransmitter release probability. Proc Natl Acad Sci U S A 94, 719-723.
58. Waldeck RF, Pereda AE & Faber DS (2000). Properties and plasticity of paired-pulse depression at a central synapse. J Neurosci 20, 5312-5320.
59. Wang L-Y & Kaczmarek LK (1998). High-frequency firing helps replenish the readily releasable pool of synaptic vesicles. Nature 394, 384-388.
60. 2+-dependent vesicle pool dynamics and short term synaptic depression. Biophys J 77, 2418-2429.
61. Wilts CH (1960). Principles of Feedback Control. Addison-Wesley, Reading, MA, USA.
62. Zengel JE, Magleby KL, Horn JP, McAfee DA & Yarowsky PJ (1980). Facilitation, augmentation, and potentiation of synaptic transmission at the superior cervical ganglion of the rabbit. J General Physiol 76, 213-231.
63. Zucker RS (1973). Changes in the statistics of transmitter release during facilitation. J Physiol 229, 787-810.
64. Zucker RS & Regehr WG (2002). Short-term synaptic plasticity. Annu Rev Physiol 64, 355-405.