Pathway-specific use-dependent dynamics of excitatory synaptic transmission in rat intracortical circuits

Journal of Physiology

Volumn 585, Issue 3, 2007, Pages 759-777

  Williams, Stephen R ^a   Atkinson, Susan E ^a  

^a MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; EPILEPTIC DISCHARGE; EVOKED RESPONSE; EXCITATORY POSTSYNAPTIC POTENTIAL; LONG TERM DEPRESSION; NEOCORTEX; NERVE CELL NETWORK; NONHUMAN; PRESYNAPTIC POTENTIAL; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT; SYNAPTIC EFFICACY; SYNAPTIC TRANSMISSION; ACTION POTENTIAL; ANALYSIS OF VARIANCE; ANIMAL TISSUE; DENDRITIC SPINE; EXCITATORY JUNCTION POTENTIAL; FLUORESCENCE MICROSCOPY; LONG TERM POTENTIATION; MOLECULAR DYNAMICS; MORPHOLOGY; NEUROMODULATION; SIGNAL TRANSDUCTION; SYNAPSE;

ANIMALS; CEREBRAL CORTEX; ELECTRIC STIMULATION; EXCITATORY POSTSYNAPTIC POTENTIALS; NERVE NET; PYRAMIDAL TRACTS; RATS; RATS, WISTAR; SIGNAL TRANSDUCTION; SYNAPTIC TRANSMISSION;

AMPA RECEPTOR;

EID: 37249044365     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2007.138453     Document Type: Article

References (86)

1. Abbott LF & Regehr WG (2004). Synaptic computation. Nature 431, 796-803.
2. Abbott LF, Varela JA, Sen K & Nelson SB (1997). Synaptic depression and cortical gain control. Science 275, 220-224.
3. Alle H & Geiger JR (2006). Combined analog and action potential coding in hippocampal mossy fibers. Science 311, 1290-1293.
4. Angulo MC, Staiger JF, Rossier J & Audinat E (1999). Developmental synaptic changes increase the range of integrative capabilities of an identified excitatory neocortical connection. J Neurosci 19, 1566-1576.
5. Arieli A, Sterkin A, Grinvald A & Aertsen A (1996). Dynamics of ongoing activity: Explanation of the large variability in evoked cortical responses. Science 273, 1868-1871.
6. Atluri PP & Regehr WG (1996). Determinants of the time course of facilitation at the granule cell to Purkinje cell synapse. J Neurosci 16, 5661-5671.
7. Atzori M, Lei S, Evans DI, Kanold PO, Phillips-Tansey E, McIntyre O & McBain CJ (2001). Differential synaptic processing separates stationary from transient inputs to the auditory cortex. Nat Neurosci 4, 1230-1237.
8. Banitt Y, Martin KA & Segev I (2005). Depressed responses of facilitatory synapses. J Neurophysiol 94, 865-870.
9. Blundon JA, Wright SN, Brodwick MS & Bittner GD (1993). Residual free calcium is not responsible for facilitation of neurotransmitter release. Proc Natl Acad Sci U S A 90, 9388-9392.
10. Bolshakov VY & Siegelbaum SA (1995). Regulation of hippocampal transmitter release during development and long-term potentiation. Science 269, 1730-1734.
11. Brecht M, Schneider M, Sakmann B & Margrie TW (2004). Whisker movements evoked by stimulation of single pyramidal cells in rat motor cortex. Nature 427, 704-710.
12. Buracas GT, Zador AM, Deweese MR & Albright TD (1998). Efficient discrimination of temporal patterns by motion-sensitive neurons in primate visual cortex. Neuron 20, 959-969.
13. Chen D & Fetz EE (2005). Characteristic membrane potential trajectories in primate sensorimotor cortex neurons recorded in vivo. J Neurophysiol 94, 2713-2725.
14. Connors BW (1984). Initiation of synchronized neuronal bursting in neocortex. Nature 310, 685-687.
15. Crochet S & Petersen CC (2006). Correlating whisker behavior with membrane potential in barrel cortex of awake mice. Nat Neurosci 9, 608-610.
16. Curtis DR & Eccles JC (1960). Synaptic action during and after repetitive stimulation. J Physiol 150, 374-398.
17. de Kock CP, Bruno RM, Spors H & Sakmann B (2007). Layer- and cell-type-specific suprathreshold stimulus representation in rat primary somatosensory cortex. J Physiol 581, 139-154.
18. + conductance in hippocampus. Nature 389, 286-289.
19. deCharms RC, Blake DT & Merzenich MM (1998). Optimizing sound features for cortical neurons. Science 280, 1439-1443.
20. deCharms RC & Zador A (2000). Neural representation and the cortical code. Annu Rev Neurosci 23, 613-647.
21. Delaney KR & Tank DW (1994). A quantitative measurement of the dependence of short-term synaptic enhancement on presynaptic residual calcium. J Neurosci 14, 5885-5902.
22. Dittman JS, Kreitzer AC & Regehr WG (2000). Interplay between facilitation, depression, and residual calcium at three presynaptic terminals. J Neurosci 20, 1374-1385.
23. Dobrunz LE & Stevens CF (1997). Heterogeneity of release probability, facilitation, and depletion at central synapses. Neuron 18, 995-1008.
24. Douglas RJ & Martin KA (2004). Neuronal circuits of the neocortex. Annu Rev Neurosci 27, 419-451.
25. Faber DS & Korn H (1991). Applicability of the coefficient of variation method for analyzing synaptic plasticity. Biophys J 60, 1288-1294.
26. Fernandez-Alfonso T & Ryan TA (2004). The kinetics of synaptic vesicle pool depletion at CNS synaptic terminals. Neuron 41, 943-953.
27. Fuhrmann G, Segev I, Markram H & Tsodyks M (2002). Coding of temporal information by activity-dependent synapses. J Neurophysiol 87, 140-148.
28. Galarreta M & Hestrin S (1998). Frequency-dependent synaptic depression and the balance of excitation and inhibition in the neocortex. Nat Neurosci 1, 587-594.
29. Gilbert CD (1983). Microcircuitry of the visual cortex. Annu Rev Neurosci 6, 217-247.
30. Habets RL & Borst JG (2005). Post-tetanic potentiation in the rat calyx of Held synapse. J Physiol 564, 173-187.
31. Harsch A & Robinson HP (2000). Postsynaptic variability of firing in rat cortical neurons: The roles of input synchronization and synaptic NMDA receptor conductance. J Neurosci 20, 6181-6192.
32. Hefft S, Kraushaar U, Geiger JRP & Jonas P (2002). Presynaptic short-term depression is maintained during regulation of transmitter release at a GABAergic synapse in rat hippocampus. J Physiol 539, 201-208.
33. Hubel DH (1959). Single unit activity in striate cortex of unrestrained cats. J Physiol 147, 226-238.
34. Hubel DH & Wiesel TN (1959). Receptive fields of single neurones in the cat's striate cortex. J Physiol 148, 574-591.
35. Ikegaya Y, Aaron G, Cossart R, Aronov D, Lampl I, Ferster D & Yuste R (2004). Synfire chains and cortical songs: Temporal modules of cortical activity. Science 304, 559-564.
36. Ishikawa T, Sahara Y & Takahashi T (2002). A single packet of transmitter does not saturate postsynaptic glutamate receptors. Neuron 34, 613-621.
37. 2+ and short-term synaptic plasticity. Nature 371, 603-606.
38. Katz B & Miledi R (1968). The role of calcium in neuromuscular facilitation. J Physiol 195, 481-492.
39. Klyachko VA & Stevens CF (2006). Temperature-dependent shift of balance among the components of short-term plasticity in hippocampal synapses. J Neurosci 26, 6945-6957.
40. Koester HJ & Johnston D (2005). Target cell-dependent normalization of transmitter release at neocortical synapses. Science 308, 863-866.
41. Krupa DJ, Wiest MC, Shuler MG, Laubach M & Nicolelis MA (2004). Layer-specific somatosensory cortical activation during active tactile discrimination. Science 304, 1989-1992.
42. Kushmerick C, Renden R & Von Gersdorff H (2006). Physiological temperatures reduce the rate of vesicle pool depletion and short-term depression via an acceleration of vesicle recruitment. J Neurosci 26, 1366-1377.
43. Luna R, Hernandez A, Brody CD & Romo R (2005). Neural codes for perceptual discrimination in primary somatosensory cortex. Nat Neurosci 8, 1210-1219.
44. Mainen ZF & Sejnowski TJ (1995). Reliability of spike timing in neocortical neurons. Science 268, 1503-1506.
45. Margrie TW, Brecht M & Sakmann B (2002). In vivo, low-resistance, whole-cell recordings from neurons in the anaesthetized and awake mammalian brain. Pflugers Arch 444, 491-498.
46. Markram H, Lubke 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.
47. Markram H & Tsodyks M (1996). Redistribution of synaptic efficacy between neocortical pyramidal neurons. Nature 382, 807-810.
48. Markram H, Wang Y & Tsodyks M (1998). Differential signaling via the same axon of neocortical pyramidal neurons. Proc Natl Acad Sci USA 95, 5323-5328.
49. 2+ buffers on synaptic facilitation. J Neurophysiol 96, 3389-3397.
50. Mitchell SJ & Silver RA (2000). GABA spillover from single inhibitory axons suppresses low-frequency excitatory transmission at the cerebellar glomerulus. J Neurosci 20, 8651-8658.
51. Park D & Dunlap K (1998). Dynamic regulation of calcium influx by G-proteins, action potential waveform, and neuronal firing frequency. J Neurosci 18, 6757-6766.
52. Porter R (1970). Early facilitation at corticomotoneuronal synapses. J Physiol 207, 733-745.
53. Porter R, Lewis MM & Horne M (1971). Analysis of patterns of natural activity of neurones in the precentral gyrus of conscious monkeys. Brain Res 34, 99-113.
54. Porter R & Muir RB (1971). The meaning for motoneurones of the temporal pattern of natural activity in pyramidal tract neurones of conscious monkeys. Brain Res 34, 127-142.
55. Pyott SJ & Rosenmund C (2002). The effects of temperature on vesicular supply and release in autaptic cultures of rat and mouse hippocampal neurons. J Physiol 539, 523-535.
56. Reyes A, Lujan R, Rosov A, Burnashev N, Somogyi P & Sakmann B (1999). Target-cell-specific facilitation and depression in neocortical circuits. Nat Neurosci 1, 279-285.
57. Reyes A & Sakmann B (1999). Developmental switch in the short-term modification of unitary EPSPs evoked in layer 2/3 and layer 5 pyramidal neurons of rat neocortex. J Neurosci 19, 3827-3835.
58. Rosenmund C & Stevens CF (1996). Definition of the readily releasable pool of vesicles at hippocampal synapses. Neuron 16, 1197-1207.
59. 2+ buffers in facilitating and depressing nerve terminals of pyramidal cells in layer 2/3 of the rat neocortex indicates a target cell-specific difference in presynaptic calcium dynamics. J Physiol 531, 807-826.
60. Sanchez-Vives MV & McCormick DA (2000). Cellular and network mechanisms of rhythmic recurrent activity in neocortex. Nat Neurosci 3, 1027-1034.
61. Shadlen MN & Newsome WT (1998). The variable discharge of cortical neurons: Implications for connectivity, computation, and information coding. J Neurosci 18, 3870-3896.
62. Shin J, Shen F & Huguenard JR (2005). Polyamines modulate AMPA receptor-dependent synaptic responses in immature layer V pyramidal neurons. J Neurophysiol 93, 2634-2643.
63. Shoham S, O'Connor DH & Segev R (2006). How silent is the brain: Is there a 'dark matter'problem in neuroscience? J Comp Physiol A Neuroethol Sens Neuro Behav Physiol 192, 777-784.
64. Shu Y, Hasenstaub A, Duque A, Yu Y & McCormick DA (2006). Modulation of intracortical synaptic potentials by presynaptic somatic membrane potential. Nature 441, 761-765.
65. Silver RA, Lubke J, Sakmann B & Feldmeyer D (2003). High-probability uniquantal transmission at excitatory synapses in barrel cortex. Science 302, 1981-1984.
66. Sjostrom PJ & Hausser M (2006). A cooperative switch determines the sign of synaptic plasticity in distal dendrites of neocortical pyramidal neurons. Neuron 51, 227-238.
67. Sjostrom PJ, Turrigiano GG & Nelson SB (2001). Rate, timing, and cooperativity jointly determine cortical synaptic plasticity. Neuron 32, 1149-1164.
68. Sjostrom PJ, Turrigiano GG & Nelson SB (2003). Neocortical LTD via coincident activation of presynaptic NMDA and cannabinoid receptors. Neuron 39, 641-654.
69. Steriade M, Timofeev I & Grenier F (2001). Natural waking and sleep states: A view from inside neocortical neurons. J Neurophysiol 85, 1969-1985.
70. 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.
71. 2+ at the frog neuromuscular junction. Neurosci Lett 99, 147-152.
72. 2+-dependent and -independent components of transmitter release at the frog neuromuscular junction. J Physiol 455, 271-289.
73. Thomson AM & Bannister AP (1998). Postsynaptic pyramidal target selection by descending layer III pyramidal axons: Dual intracellular recordings and biocytin filling in slices of rat neocortex. Neuroscience 84, 669-683.
74. 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.
75. Trussell LO, Zhang S & Raman IM (1993). Desensitization of AMPA receptors upon multiquantal neurotransmitter release. Neuron 10, 1185-1196.
76. 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.
77. Varela JA, Sen K, Gibson J, Fost J, Abbott LF & Nelson SB (1997). A quantitative description of short-term plasticity at excitatory synapses in layer 2/3 of rat primary visual cortex. J Neurosci 17, 7926-7940.
78. B receptor variants. Neuron 50, 589-601.
79. Williams SR (2004). Spatial compartmentalization and functional impact of conductance in pyramidal neurons. Nat Neurosci 7, 961-967.
80. Williams SR (2005). Encoding and decoding of dendritic excitation during active states in pyramidal neurons. J Neurosci 25, 5894-5902.
81. Williams SR & Stuart GJ (1999). Mechanisms and consequences of action potential burst firing in rat neocortical pyramidal neurons. J Physiol 521, 467-482.
82. Williams SR & Stuart GJ (2000). Backpropagation of physiological spike trains in neocortical pyramidal neurons: Implications for temporal coding in dendrites. J Neurosci 20, 8238-8246.
83. Williams SR & Stuart GJ (2002). Dependence of EPSP efficacy on synapse location in neocortical pyramidal neurons. Science 295, 1907-1910.
84. Wojtowicz JM & Atwood HL (1988). Presynaptic long-term facilitation at the crayfish neuromuscular junction: Voltage-dependent and ion-dependent phases. J Neurosci 8, 4667-4674.
85. Xu J & Wu LG (2005). The decrease in the presynaptic calcium current is a major cause of short-term depression at a calyx-type synapse. Neuron 46, 633-645.
86. Zucker RS & Regehr WG (2002). Short-term synaptic plasticity. Annu Rev Physiol 64, 355-405.