Modulation of synaptic transmission in neocortex by network activities

European Journal of Neuroscience

Volumn 21, Issue 4, 2005, Pages 1030-1044

  Crochet, Sylvain ^a   Chauvette, Sylvain ^a   Boucetta, Sofiane ^a   Timofeev, Igor ^a  

^a UNIVERSITÉ LAVAL   (Canada)

Author keywords

Calcium; Modulation of synaptic transmission; Neocortex; Oscillation; Synaptic failures

Indexed keywords

BARBITURIC ACID DERIVATIVE; KETAMINE; XYLAZINE;

AMPLITUDE MODULATION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; CALCIUM TRANSPORT; CAT; CONCENTRATION RESPONSE; CONTROLLED STUDY; DENDRITE; EXCITATORY POSTSYNAPTIC POTENTIAL; FILTRATION; FREQUENCY MODULATION; IN VIVO STUDY; MICRODIALYSIS; NEOCORTEX; NEUROMODULATION; NONHUMAN; PRESYNAPTIC NERVE; PRESYNAPTIC POTENTIAL; PRIORITY JOURNAL; PROBABILITY; QUANTITATIVE ANALYSIS; SAFETY; SHUNTING; STATISTICAL SIGNIFICANCE; SYNAPTIC TRANSMISSION; TREATMENT FAILURE;

ACTION POTENTIALS; ANIMALS; AXONS; CALCIUM; CATS; DOSE-RESPONSE RELATIONSHIP, DRUG; ELECTRIC STIMULATION; ELECTROENCEPHALOGRAPHY; EXCITATORY POSTSYNAPTIC POTENTIALS; MICRODIALYSIS; NEOCORTEX; NERVE NET; NEURONS; SYNAPTIC TRANSMISSION;

EID: 16244377735     PISSN: 0953816X     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2005.03932.x     Document Type: Article

References (80)

1. Abbott, L.F., Varela, J.A., Sen, K. & Nelson, S.B. (1997) Synaptic depression and cortical gain control. Science, 275, 220-224.
2. Allen, C. & Stevens, C.F. (1994) An evaluation of causes for unreliability of synaptic transmission. Proc. Natl Acad. Sci. USA, 91, 10380-10383.
3. Amitai, Y., Friedman, A., Connors, B.W. & Gutnick, M.J. (1993) Regenerative activity in apical dendrites of pyramidal cells in neocortex. Cereb. Cortex. 3, 26-38.
4. Auger, C., Kondo, S. & Marty, A. (1998) Multivesicular release at single functional synaptic sites in cerebellar stellate and basket cells. J. Neurosci., 18, 4532-4547.
5. Auger, C. & Marty, A. (2000) Quantal currents at single-site central synapses. J. Physiol. (Lond.), 526, 3-11.
6. Benardo, L.S., Masukawa, L.M. & Prince, D.A. (1982) Electrophysiology of isolated hippocampal pyramidal dendrites. J. Neurosci., 2, 1614-1622.
7. Berger, T. & Luscher, H.R. (2003) Timing and precision of spike initiation in layer V pyramidal cells of the rat somatosensory cortex. Cereb. Cortex, 13, 274-281.
8. Borg-Graham, L.J., Monier, C. & Fregnac, Y. (1998) Visual input evokes transient and strong shunting inhibition in visual cortical neurons. Nature, 393, 369-373.
9. Buhl, E.H., Tamãs, G., Szilãgyi, T., Stricker, C., Paulsen, O. & Somogyi, P. (1997) Effect, number and location of synapses made by single pyramidal cells onto aspiny interneurones of cat visual cortex. J. Physiol. (Lond.), 500, 689-713.
10. Conti, R. & Lisman, J. (2003) The high variance of AMPA receptor- and NMDA receptor-mediated responses at single hippocampal synapses: Evidence for multiquantal release. Proc. Natl Acad. Sci. USA, 100, 4885-4890.
11. Contreras, D., Timofeev, I. & Steriade, M. (1996) Mechanisms of long-lasting hyperpolarizations underlying slow sleep oscillations in cat corticothalamic networks. J. Physiol. (Lond.), 494, 251-264.
12. Cragg, B.G. (1967) The density of synapses and neurones in the motor and visual areas of the cerebral cortex. J. Anat, 101, 639-654.
13. Crochet, S., Fuentealba, P., Timofeev, I. & Steriade, M. (2004) Selective amplification of neocortical neuronal output by fast prepotentials in vivo. Cereb Cortex, 14, 1110-1121.
14. Crochet, S. & Sakai, K. (1999) Effects of microdialysis application of monoamines on the EEG and behavioural states in the cat mesopontine tegmentum. Eur J. Neurosci., 11, 3738-3752.
15. Debanne, D., Guerineau, N.C., Gahwiler, B.H. & Thompson, S.M. (1996) Paired-pulse facilitation and depression at unitary synapses in rat hippocampus: quantal fluctuation affects subsequent release. J. Physiol. (Lond.), 491, 163-176.
16. DeFelipe, J. & Farinas, I. (1992) The pyramidal neuron of the cerebral cortex: morphological and chemical characteristics of the synaptic inputs. Prog. Neurobiol., 39, 563-607.
17. Destexhe, A. & Paré, D. (1999) Impact of network activity on the integrative properties of neocortical pyramidal neurons in vivo. J. Neurophysiol., 81, 1531-1547.
18. Destexhe, A., Rudolph, M. & Pare, D. (2003) The high-conductance state of neocortical neurons in vivo. Nat. Rev. Neurosci., 4, 739-751.
19. Egelman, D.M. & Montague, P.R. (1998) Computational properties of peridendritic calcium fluctuations. J. Neurosci., 18, 8580-8589.
20. Feldmeyer, D., Egger, V., Lubke, J. & Sakmann, B. (1999) Reliable synaptic connections between pairs of excitatory layer 4 neurones within a single 'barrel' of developing rat somatosensory cortex. J. Physiol. (Lond.), 521, 169-190.
21. Finnerty, G.T., Roberts, L.S. & Connors, B.W. (1999) Sensory experience modifies the short-term dynamics of neocortical synapses. Nature, 400, 367-371.
22. Galarreta, M. & Hestrin, S. (1998) Frequency-dependent synaptic depression and the balance of excitation and inhibition in the neocortex. Nat. Neurosci., 1, 587-594.
23. Gil, Z., Connors, B.W. & Amitai, Y. (1997) Differential regulation of neocortical synapses by neuromodulators and activity. Neuron, 19, 679-686.
24. Gonzalez-Burgos, G. & Barrionuevo, G. (2001) Voltage-gated sodium channels shape subthreshold EPSPs in layer 5 pyramidal neurons from rat prefrontal cortex. J. Neurophysiol., 86, 1671-1684.
25. Gray, C.M. & McCormick, D.A. (1996) Chattering cells: superficial pyramidal neurons contributing to the generation of synchronous oscillations in the visual cortex. Science, 274, 109-113.
26. Gruner, J.E., Hirsch, J.C. & Sotelo, C. (1974) Ultrastructural features of the isolated suprasylvian gyrus in the cat. J. Comp. Neurol, 154, 1-27.
27. Hanse, E. & Gustafsson, B. (2001) Quantal variability at glutamatergic synapses in area CA1 of the rat neonatal hippocampus. J. Physiol (Lond.), 531, 467-480.
28. Harris, K.M. & Sultan, P. (1995) Variation in the number, location and size of synaptic vesicles provides an anatomical basis for the nonuniform probability of release at hippocampal CA1 synapses. Neuropharmacology, 34, 1387-1395.
29. Hassler, R. & Muhs-Clement, K. (1964) Architektonischer Aufbau des Sensomotorischen und Parietalen Cortex der Katze. J. Hirnforschung, 6, 377-422.
30. Heinemann, U., Lux, H.D. & Gutnick, M.J. (1977) Extracellular free calcium and potassium during paroxsmal activity in the cerebral cortex of the cat. Exp. Brain Res., 27, 237-243.
31. Hempel, C.M., Hartman, K.H., Wang, X.J., Turrigiano, G.G. & Nelson, S.B. (2000) Multiple forms of short-term plasticity at excitatory synapses in rat medial prefrontal cortex. J. Neurophysiol., 83, 3031-3041.
32. Hirsch, J.A., Alonso, J.M., Reid, R.C. & Martinez, L.M. (1998) Synaptic integration in striate cortical simple cells. J. Neurosci., 18, 9517-9528.
33. Hubel, D.H. (1959) Single unit activity in striate cortex of unrestrained cats. J. Physiol. (Lond.), 147, 226-238.
34. Isaac, J.T., Luthi, A., Palmer, M.J., Anderson, W.W., Benke, T.A. & Collingridge, G.L. (1998) An investigation of the expression mechanism of LTP of AMPA receptor-mediated synaptic transmission at hippocampal CA1 synapses using failures analysis and dendritic recordings. Neuropharmacology, 37, 1399-1410.
35. Juhasz, G., Tarcali, J., Pungor, K. & Pungor, E. (1989) Electrochemical calibration of in vivo brain dialysis samplers. J. Neurosci. Meth., 29, 131-137.
36. Katz, B. & Miledi, R. (1968) The role of calcium in neuromuscular facilitation. J. Physiol (Lond.), 195, 481-492.
37. Krimer, L.S. & Goldman-Rakic, P.S. (2001) Prefrontal microcircuits: membrane properties and excitatory input of local, medium, and wide arbor interneurons, J. Neurosci., 21, 3788-3796.
38. Magee, J.C. & Johnston, D. (1995) Synaptic activation of voltage-gated channels in the dendrites of hippocampal pyramidal neurons. Science, 268, 301-304.
39. Markram, H., Lubke, J., Frotscher, M., Roth, A. & Sakmann, B. (1997a) Physiology and anatomy of synaptic connections between thick tufted pyramidal neurones in the developing rat neocortex. J. Physiol. (Lond.), 500, 409-440.
40. Markram, H., Lubke, J., Frotscher, M. & Sakmann, B. (1997b) Regulation of synaptic efficacy by coincidence of postsynaptic APs and EPSPs. Science, 275, 213-215.
41. Markiam, H., Wang, Y. & Tsodyks, M. (1998) Differential signaling via the same axon of neocortical pyramidal neurons. Proc. Natl. Acad. Sci. USA, 95, 5323-5328.
42. Massimini, M. & Amzica, F. (2001) Extracellular calcium fluctuations and intracellular potentials in the cortex during the slow sleep oscillation. J. Neurophysiol., 85, 1346-1350.
43. McCormick, D.A., Connors, B.W., Lighthall, J.W. & Prince, D.A. (1985) Comparative electrophysiology of pyramidal and sparsely spiny stellate neurons of the neocortex. J. Neurophysiol., 54, 782-806.
44. Oertner, T.G., Sabatini, B.L., Nimchinsky, E.A. & Svoboda, K. (2002) Facilitation at single synapses probed with optical quantal analysis. Nat. Neurosci., 5, 657-664.
45. Paré, D., Shink, E., Gaudreau, H., Destexhe, A. & Lang, E.J. (1998) Impact of spontaneous synaptic activity on the resting properties of cat neocortical pyramidal neurons in vivo. J. Neurophysiol., 79, 1450-1460.
46. Petersen, C. C. & Sakmann, B. (2000) The excitatory neuronal network of rat layer 4 barrel cortex. J. Neurosci., 20, 7579-7586.
47. Quan, N. & Blatteis, C.M. (1989) Microdialysis: a system for localized drug delivery into the brain. Brain Res. Bull., 22, 621-625.
48. Raastad, M. & Shepherd, G.M. (2003) Single-axon action potentials in the rat hippocampal cortex. J. Physiol. (Lond.), 548, 745-752.
49. Redman, S. (1990) Quantal analysis of synaptic potentials in neurons of the central nervous system. Physiol. Rev., 70, 165-198.
50. Rhodes, P.A. & Llinas, R.R. (2001) Apical tuft input efficacy in layer 5 pyramidal cells from rat visual cortex. J. Physiol. (Lond.), 536, 167-187.
51. Rudolph, M. & Destexhe, A. (2003) A fast-conducting, stochastic integrative mode for neocortical neurons in vivo. J. Neurosci., 23, 2466-2476.
52. Rusakov, D.A. & Fine, A. (2003) Extracellular Ca2+ depletion contributes to fast activity-dependent modulation of synaptic transmission in the brain. Neuron, 37, 287-297.
53. Schikorski, T. & Stevens, C.F. (1997) Quantitative ultrastructural analysis of hippocampal excitatory synapses. J. Neurosci., 17, 5858-5867.
54. Schikorski, T. & Stevens. C.F. (1999) Quantitative fine-structural analysis of olfactory cortical synapses. Proc. Natl. Acad. Sci. USA, 96, 4107-4112.
55. Schwindt, P.C. & Crill, W.E. (1995) Amplification of synaptic current by persistent sodium conductance in apical dendrite of neocortical neurons. J. Neurophysiol., 74, 2220-2224.
56. Silver, R.A., Lubke, J., Sakmann, B. & Feldmeyer, D. (2003) High-probability uniquantal transmission at excitatory synapses in barrel cortex. Science, 302, 1981-1984.
57. Spencer, W.A. & Kandel, E.R. (1961) Electrophysiology of hippocampal neurons IV. fast prepotentials. J. Neurophysiol., 24, 272-285.
58. Steriade, M. (2001) The Intact and Sliced Brain. MIT Press, Cambridge, MA, USA.
59. Steriade, M., Nuñez, A. & Amzica, F. (1993) A novel slow (< 1 Hz) oscillation of neocortical neurons in vivo: depolarizing and hyperpolarizing components. J. Neurosci., 13, 3252-3265.
60. Steriade, M., Timofeev, I., Dürmüller, N. & Grenier, F. (1998) Dynamic properties of corticothalamic neurons and local cortical interneurons generating fast rhythmic (30-40 Hz) spike bursts. J. Neurophysiol., 79, 483-490.
61. Steriade, M., Timofeev, I. & Grenier, F. (2001) Natural waking and sleep states: a view from inside neocortical neurons. J. Neurophysiol., 85, 1969-1985.
62. Stevens, C.F. & Wang, Y. (1995) Facilitation and depression at single central synapses. Neuron, 14, 795-802.
63. Stuart, G.J. & Hausser, M. (2001) Dendritic coincidence detection of EPSPs and action potentials. Nat. Neurosci., 4, 63-71.
64. Stuart, G. & Sakmann, B. (1995) Amplification of EPSPs by axosomatic sodium channels in neocortical pyramidal neurons. Neuron, 15, 1065-1076.
65. Szentagothai, J. (1965) The use of degeneration methods in the investigation of short neuronal connections. In Singer, M. & Schadé, P. (eds) Degeneration Patterns in the Nervous System, Progress in Brain Research. Elsevier, Amsterdam, pp. 1-32.
66. Thomson, A.M. (1997) Activity-dependent properties of synaptic transmission at two classes of connections made by rat neocortical pyramidal axons in vitro. J. Physiol (Lond.), 502, 131-147.
67. Thomson, A.M. & Deuchars, J. (1997) Synaptic interactions in neocortical local circuits: dual intracellular recordings in vitro. Cereb. Cortex, 7, 510-522.
68. Thomson, A.M., Deuchars, J. & West, D.C. (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.
69. Thomson, A.M., Girdlestone, D. & West, D.C. (1988) Voltage-dependent currents prolong single-axon postsynaptic potentials in layer III pyramidal neurons in rat neocortical slices. J. Neurophysiol., 60, 1896-1907.
70. Thomson, A.M., West, D.C. & Deuchars, J. (1995) Properties of single axon excitatory postsynaptic potentials elicited in spiny intemeurons by action potentials in pyramidal neurons in slices of rat neocortex. Neuroscience, 69, 727-738.
71. Timofeev, I., Grenier, F., Bazhenov, M., Sejnowski, T.J. & Steriade, M. (2000) Origin of slow cortical oscillations in deafferented cortical slabs. Cereb. Cortex, 10, 1185-1199.
72. Tong, G. & Jahr, C.E. (1994) Multivesicular release from excitatory synapses of cultured hippocampal neurons. Neuron, 12, 51-59.
73. Triller, A. & Korn, H. (1982) Transmission at a central inhibitory synapse. III. Ultrastructure of physiologically identified and stained terminals. J. Neurophysiol., 48, 708-736.
74. Tsodyks, M.V. & Markram, H. (1997) The neural code between neocortical pyramidal neurons depends on neurotransmitter release probability. Proc. Natl. Acad. Sci. USA, 94, 719-723.
75. Turner, R.W., Meyers, D.E., Richardson, T.L. & Barker, J.L. (1991) The site for initiation of action potential discharge over the somatodendritic axis of rat hippocampal CA1 pyramidal neurons. J. Neurosci., 11, 2270-2280.
76. Varela, J.A., Song, S., Turrigiano, G.G. & Nelson, S.B. (1999) Differential depression at excitatory and inhibitory synapses in visual cortex. J. Neurosci., 19, 4293-4304.
77. Wadiche, J.I. & Jahr, C.E. (2001) Multivesicular release at climbing fiber-Purkinje cell synapses. Neuron, 32, 301-313.
78. Wang, S.S., Denk, W. & Hausser, M. (2000) Coincidence detection in single dendritic spines mediated by calcium release. Nat. Neurosci., 3, 1266-1273.
79. Zador, A. (1998) Impact of synaptic unreliability on the information transmitted by spiking neurons. J. Neurophysiol., 79, 1219-1229.
80. Zucker, R.S. & Regehr, W.G. (2002) Short-term synaptic plasticity. Annu. Rev. Physiol., 64, 355-405.