A history of spike-timing-dependent plasticity

Frontiers in Synaptic Neuroscience

Volumn , Issue AUG, 2011, Pages 1-24

  Markram, Henry ^a   Gerstner, Wulfram ^a   Sjöström, Per Jesper ^b,c  

^a EPFL   (Switzerland)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

^c RESEARCH INSTITUTE OF THE MCGILL UNIVERSITY HEALTH CENTRE   (Canada)

Author keywords

Bidirectional plasticity; History; Learning; Long term depression; Long term plasticity; Memory; Spike timing dependent plasticity; Synaptic plasticity

Indexed keywords

N METHYL DEXTRO ASPARTIC ACID RECEPTOR;

BRAIN ELECTROPHYSIOLOGY; DENDRITE; HISTORY; HUMAN; INTERNEURON; LEARNING; LONG TERM POTENTIATION; MATHEMATICAL ANALYSIS; MATHEMATICAL MODEL; NERVE CELL EXCITABILITY; NERVE CELL NETWORK; NERVE CELL PLASTICITY; NERVE ROOT; NEUROMODULATION; NEUROTRANSMISSION; NONHUMAN; REVIEW; SENSORY NERVE; SIGNAL TRANSDUCTION; SPIKE TIMING DEPENDENT PLASTICITY; SPIKE WAVE; THEORETICAL MODEL; VISUAL CORTEX;

EID: 84862171078     PISSN: None     EISSN: 16633563     Source Type: Journal    
DOI: 10.3389/fnsyn.2011.00004     Document Type: Review

References (261)

1. Abbott, L. F., and Blum, K. I. (1996). Functional significance of long-term potentiation for sequence learning and prediction. Cereb. Cortex 6, 406-416.
2. Abbott, L. F., and Nelson, S. B. (2000). Synaptic plasticity: taming the beast. Nat. Neurosci. 3(Suppl.), 1178-1183.
3. Abbott, L. F., Varela, J. A., Sen, K., and Nelson, S. B. (1997). Synaptic depression and cortical gain control. Science 275, 220-224.
4. Abeles, M. (1991). Corticonics: Neural Circuits of the Cerebral Cortex. Cambridge: Cambridge University Press.
5. Abraham, W. C., and Bear, M. F. (1996). Metaplasticity: the plasticity of synaptic plasticity. Trends Neurosci. 19, 126-130.
6. Adrian, E. D., and Matthews, R. (1928). The action of light on the eye: part III. The interaction of retinal neurones. J. Physiol. 65, 273-298.
7. Albus, J. S. (1971). A theory of cerebellar function. Math. Biosci. 10, 25-61.
8. Aleman, A., and Torres-Aleman, I. (2009). Circulating insulin-like growth factor I and cognitive function: neuromodulation throughout the lifespan. Prog. Neurobiol. 89, 256-265.
9. Allen, C. B., Celikel, T., and Feldman, D. E. (2003). Long-term depression induced by sensory deprivation during cortical map plasticity in vivo. Nat. Neurosci. 6, 291-299.
10. Amit, D. J., and Tsodyks, M. V. (1991). Quantitative study of attractor neural network retrieving at low spike rates: I. Substrate-spikes, rates and neuronal gain. Network 2, 259.
11. Anderson, J. A. (1972). A simple neural network generating an interactive memory. Math. Biosci. 14, 197-220.
12. Artola, A., Brocher, S., and Singer, W. (1990). Different voltage-dependent thresholds for inducing long-term depression and long-term potentiation in slices of rat visual cortex. Nature 347, 69-72.
13. Bain, A. (1855). The Senses and the Intellect, 1st Edn. London: John W. Parker and Son.
14. Bain, A. (1873). Mind and Body. The Theories of Their Relation. New York: D. Appleton & Company.
15. Baranyi, A., and Feher, O. (1978). Conditioned changes of synaptic transmission in the motor cortex of the cat. Exp. Brain Res. 33, 283-298.
16. Baranyi, A., and Feher, O. (1981). Intracellular studies on cortical synaptic plasticity. Conditioning effect of antidromic activation on test-EPSPs. Exp. Brain Res. 41, 124-134.
17. Barrionuevo, G., Schottler, F., and Lynch, G. (1980). The effects of repetitive low frequency stimulation on control and "potentiated" synaptic responses in the hippocampus. Life Sci. 27, 2385-2391.
18. Bear, M. F. (1999). Homosynaptic long-term depression: a mechanism for memory? Proc. Natl. Acad. Sci. U.S.A. 96, 9457-9458.
19. Bear, M. F., and Singer, W. (1986). Modulation of visual cortical plasticity by acetylcholine and noradrenaline. Nature 320, 172-176.
20. Bell, C. C. (1981). An efference copy which is modified by reafferent input. Science 214, 450-453.
21. Bell, C. C., Han, V. Z., Sugawara, Y., and Grant, K. (1997). Synaptic plasticity in a cerebellum-like structure depends on temporal order. Nature 387, 278-281.
22. Bennett, M. R. (2000). The concept of transmitter receptors: 100 years on. Neuropharmacology 39, 523-546.
23. Berlucchi, G., and Buchtel, H.A. (2009). Neuronal plasticity: historical roots and evolution of meaning. Exp. Brain Res. 192, 307-319.
24. Bernstein, J. (1868). Ueber den zeitlichen Verlauf der negative Schwankung des Nervenstroms. Pflugers Arch. 1, 173-207.
25. Bernstein, J. (1902). Untersuchungen zur Thermodynamik der bioelek-trischen Strome. Pflugers Arch. ges. Physiol. 92, 521-562.
26. Bi, G.Q., and Poo, M. M.(1998). Synaptic modifications in cultured hippocampal neurons: dependence on spike timing, synaptic strength, and postsynaptic cell type. J. Neurosci. 18, 10464-10472.
27. Bienenstock, E. L., Cooper, L. N., and Munro, P. W. (1982). Theory for the development of neuron selectivity: orientation specificity and binocular interaction in visual cortex. J. Neurosci. 2, 32-48.
28. Bliss, T. V., and Lømo, T. (1970). Plasticity in a monosynaptic cortical pathway. J. Physiol. (Lond.) 207, 61P.
29. Bliss, T. V., and Lømo, T. (1973). Long-lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path. J. Physiol. 232, 331-356.
30. Blum, K. I., and Abbott, L. F. (1996). A model of spatial map formation in the hippocampus of the rat. Neural. Comput. 8, 85-93.
31. Braitenberg, V. (1984). Rules and Regularities. In Vehicles, Experiments in Synthetic Psychology. Cambridge, MA: The MIT Press, 55-61.
32. Bramham, C. R., and Srebro, B. (1987). Induction of long-term depression and potentiation by low- and high-frequency stimulation in the dentate area of the anesthetized rat: magnitude, time course and EEG. Brain Res. 405, 100-107.
33. Brindley, G. S. (1964). The use made by the cerebellum of the information that it receives from sense organs. I.B.R.O. Bull. 3, 80.
34. Brown, S. P., and Hestrin, S. (2009a). Cell-type identity: a key to unlocking the function of neocortical circuits. Curr. Opin. Neurobiol. 19, 415-421.
35. Brown, S. P., and Hestrin, S. (2009b). Intracortical circuits of pyramidal neurons reflect their long-range axonal targets. Nature 457, 1133-1136.
36. Buchanan, K. A., and Mellor, J. R. (2007). The development of synaptic plasticity induction rules and the requirement for postsynaptic spikes in rat hippocampal CA1 pyramidal neurones. J. Physiol. (Lond.) 585, 429-445.
37. Buchanan, K. A., and Mellor, J. R. (2010). The activity requirements for spike timing-dependent plasticity in the hippocampus. Front. Synaptic Neurosci. 2:11. doi: 10.3389/fnsyn.2010.00011
38. Bullmore, E., and Sporns, O. (2009). Complex brain networks: graph theoretical analysis of structural and functional systems. Nat. Rev. Neurosci. 10, 186-198.
39. Butts, D. A., Kanold, P. O., and Shatz, C.J. (2007). A burst-based "Hebbian" learning rule at retinogeniculate synapses links retinal waves to activity-dependent refinement. PLoS Biol. 5, e61. doi: 10.1371/journal.pbio.0050061
40. Byrne, J. H. (2008). Learning and Memory: A Comprehensive Reference. London: Academic Press.
41. Caporale, N., and Dan, Y. (2008). Spike timing-dependent plasticity: a Hebbian learning rule. Annu. Rev. Neurosci. 31, 25-46.
42. Carla Shatz, J. (1992). The developing brain. Sci. Am. 267, 60-67.
43. Carvalho, T. P., and Buonomano, D. (2011). A novel learning rule for long-term plasticity of short-term synaptic plasticity enhances temporal processing. Front. Integr. Neurosci. 5:20. doi: 10.3389/fnint.2011.00020
44. Cassenaer, S., and Laurent, G. (2007). Hebbian STDP in mushroom bodies facilitates the synchronous flow of olfactory information in locusts. Nature 448, 709-713.
45. Celikel, T., Szostak, V. A., and Feldman, D. E. (2004). Modulation of spike timing by sensory deprivation during induction of cortical map plasticity. Nat. Neurosci. 7, 534-541.
46. Clopath, C., Busing, L., Vasilaki, E., and Gerstner, W. (2010). Connectivity reflects coding: a model of voltage-based STDP with homeostasis. Nat. Neurosci. 13, 344-352.
47. Clopath, C., and Gerstner, W. (2010). Voltage and spike timing interact in STDP - a unified model. Front. Synaptic Neurosci. 2: 25. doi: 10.3389/fnsyn.2010.00025
48. Collingridge, G. L., Kehl, S. J., and McLennan, H. (1983). Excitatory amino acids in synaptic transmission in the Schaffer collateral-commissural pathway of the rat hippocampus. J. Physiol. (Lond.) 334, 33-46.
49. Cooper, L. N. (1973). "A possible organization of learning and memory," in Proceedings of the Nobel Symposium on Collective Properties of Physical Systems, eds B. Lundqvist, S. Lundqvist, and V. Runnstrom-Reio (Aspen Garden: Nobel), 252-264.
50. Cooper, L. N. (2010). STDP: spiking, timing, rates and beyond. Front. Synaptic Neurosci. 2:11. doi: 10.3389/fnsyn.2010.00014
51. Debanne, D., Gahwiler, B. H., and Thompson, S. M. (1994). Asynchronous pre- and postsynaptic activity induces associative long-term depression in area CA1 of the rat hippocampus in vitro. Proc. Natl. Acad. Sci U.S.A. 91, 1148-1152.
52. Debanne, D., Gähwiler, B. H., and Thompson, S. M. (1998). Long-term synaptic plasticity between pairs of individual CA3 pyramidal cells in rat hippocampal slice cultures. J. Physiol. 507, 237-247.
53. Debanne, D., Shulz, D. E., and Fregnac, Y. (1995). Temporal constraints in associative synaptic plasticity in hippocampus and neocortex. Can. J. Physiol. Pharmacol. 73, 1295-1311.
54. DeCamp, J. E. (1915). A Study of retroactive inhibition. Psychol. Monogr. 19.
55. Del Castillo, J., and Katz, B. (1954). Statistical factors involved in neuromuscular facilitation and depression. J. Physiol. (Lond.) 124, 574-585.
56. Douglas, R. M., and Goddard, G. V. (1975). Long-term potentiation of the perforant path-granule cell synapse in the rat hippocampus. Brain Res. 86, 205-215.
57. du Bois Reymond, E. (1848). Unter-suchungen über thierische Elektrizitkät. Berlin: Reimer.
58. Dudai, Y. (1989). The Neurobiology of Memory. Oxford: Oxford University Press.
59. Dudek, S. M., and Bear, M. F. (1992). Homosynaptic long-term depression in area CA1 of hippocampus and effects of N-methyl-D-aspartate receptor blockade. Proc. Natl. Acad. Sci. U.S.A. 89, 4363-4367.
60. Dunwiddie, T., and Lynch, G. (1978). Long-term potentiation and depression of synaptic responses in the rat hippocampus: localization and frequency dependency. J. Physiol. (Lond.) 276, 353-367.
61. Eccles, J. C. (1946). Synaptic potentials of motor neurones. J. Neurophysiol. 9, 89-120.
62. Eccles, J. C. (1960). The Properties of the Dendrites, Structure and Function of the Cerebral Cortex. New York: American Elsevier.
63. Eccles, J. C. (1961). The mechanism of synaptic transmission. Ergeb. Physiol. 51, 299-430.
64. Eccles, J. C. (1964). The Physiology of Synapses. New York: Academic Press.
65. Eccles, J. C., Katz, B., and Kuffler, S. W. (1941). Nature of the "endplate potential" in curarized muscle. J. Neurophysiol. 4, 362-387.
66. Eccles, J. C., and Sherrington, C. (1931). Studies on the Flexor Reflex. IV. After-Discharge. Proc. R. Soc. Lond. B Biol. Sci. 107, 586-596.
67. Ekerot, C. F., and Kano, M. (1985). Long-term depression of parallel fibre synapses following stimulation of climbing fibres. Brain Res. 342, 357-360.
68. Engert, F., and Bonhoeffer, T. (1999). Dendritic spine changes associated with hippocampal long-term synaptic plasticity. Nature 399, 66-70.
69. Feldman, D. E. (2000). Timing-based LTP and LTD at vertical inputs to layer II/III pyramidal cells in rat barrel cortex. Neuron 27, 45-56.
70. Feng, T. P. (1941). Studies on the neuromuscular junction. XXVI. The changes of the end-plate potential during and after prolonged stimulation. Chin. J. Physiol. 16, 301-372.
71. Fregnac, Y. (2002). "Hebbian synapses," in The Handbook of Brain Theory and Neural Networks,ed. M.A. Arbib (Cambridge, MA: The MIT Press), 515-521.
72. Frégnac, Y., Shulz, D., Thorpe, S., and Bienenstock, E. (1988). A cellular analogue of visual cortical plasticity. Nature 333, 367-370.
73. Froemke, R. C., and Dan, Y. (2002). Spike-timing-dependent synaptic modification induced by natural spike trains. Nature 416, 433-438.
74. Froemke, R. C., Debanne, D., and Bi, G.-Q. (2010a). Temporal modulation of spike-timing-dependent plasticity. Front. Synaptic Neurosci. 2:19. doi: 10.3389/fnsyn.2010.00019
75. Froemke, R. C., Letzkus, J. J., Kampa, B. M., Hang, G. B., and Stuart, G. J. (2010b). Dendritic synapse location and neocortical spike-timing-dependent plasticity. Front. Synaptic Neurosci. 2:29. doi: 10.3389/fnsyn.2010.00029
76. Froemke, R. C., Poo, M., and Dan, Y. (2005). Spike-timing-dependent plasticity depends on dendritic location. Nature 434, 221-225.
77. Froemke, R. C., Tsay, I. A., Raad, M., Long, J. D., and Dan, Y. (2006). Contribution of individual spikes in burst-induced long-term synaptic modification. J. Neurophysiol. 95, 1620-1629.
78. Fusi, S. (2002). Hebbian spike-driven synaptic plasticity for learning patterns of mean firing rates. Biol. Cybern. 87, 459-470.
79. Gasser, H. S., and Newcomer, H. S. (1921). Physiological action currents in the phrenic nerve. An application of the thermionic vacuum tube to nerve physiology. Am. J. Physiol. 57, 1-26.
80. Gelinas, J. N., and Nguyen, P. V. (2007). Neuromodulation of hip-pocampal synaptic plasticity, learning and memory by noradrenaline. Cent. Nerv. Syst. Agents Med. Chem. 7, 17-33.
81. Gerard, R. W. (1949). Physiology and psychiatry. Am. J. Psychiatry 106, 161-173.
82. Gerstner, W., Kempter, R., van Hem-men, J. L., and Wagner, H. (1996). A neuronal learning rule for sub-millisecond temporal coding. Nature 383, 76-81.
83. Gerstner, W., Ritz, R., and van Hemmen, J. L. (1993). Why spikes? Hebbian learning and retrieval of time-resolved excitation patterns. Biol. Cybern. 69, 503-515.
84. Gerstner, W., and van Hemmen, J. L. (1992). Universality in neural networks: the importance of the "mean firing rate." Biol. Cybern. 67, 195-205.
85. Gilson, M., Burkitt, A., and Van Hemmen, L. J. (2010). STDP in recurrent neuronal networks. Front. Comput. Neurosci. 4:23. doi: 10.3389/fncom.2010.00023
86. Golding, N. L., Staff, N. P., and Spruston, N. (2002). Dendritic spikes as a mechanism for cooperative long-term potentiation. Nature 418, 326-331.
87. Gotch, F., and Horsley, V. (1891). Croonian lecture: on the mammalian nervous system; its functions and their localisation determined by an electrical method. Philos. Trans. R. Soc. Lond., B, Biol. Sci. 182, 267-526.
88. Grossberg, S. (1969). On the production and release of chemical transmitters and related topics in cellular control. J. Theor. Biol. 22, 325-364.
89. Gustafsson, B., and Wigström, H. (1986). Hippocampal long-lasting potentiation produced by pairing single volleys and brief conditioning tetani evoked in separate afferents. J. Neurosci. 6, 1575-1582.
90. Gustafsson, B., Wigström, H., Abraham, W. C., and Huang, Y. Y. (1987). Long-term potentiation in the hippocampus using depolarizing current pulses as the conditioning stimulus to single volley synaptic potentials. J. Neurosci. 7, 774-780.
91. Han, V. Z., Grant, K., and Bell, C. C. (2000). Reversible associative depression and nonassociative potentiation at a parallel fiber synapse. Neuron 27, 611-622.
92. Hardie, J., and Spruston, N. (2009). Synaptic depolarization is more effective than back-propagating action potentials during induction of associative long-term potentiation in hippocampal pyramidal neurons. J. Neurosci. 29, 3233-3241.
93. Harris, E. W., Ganong, A. H., and Cotman, C. W. (1984). Long-term potentiation in the hippocampus involves activation of N-methyl-D-aspartate receptors. Brain Res. 323, 132-137.
94. Hartley, D. (1749). Observations on Man, His Frame, His Duty, and His Expectations. London: Cambridge University Press.
95. Hasselmo, M. E. (1995). Neuromodulation and cortical function: modeling the physiological basis of behavior. Behav. Brain Res. 67, 1-27.
96. Hasselmo, M. E., and Sarter, M. (2011). Modes and models of fore-brain cholinergic neuromodulation of cognition. Neuropsychopharmacology 36, 52-73.
97. Hebb, D. O. (1949). The Organisation of Behavior. New York: Wiley.
98. Hebb, D. O. (1972). A Textbook of Psychology. Montréal: W. B. Saunders Co.
99. Herz, A. V. M., Sulzer, B., Kühnvan, R., and van Hemmen, J. L. (1988). The Hebb rule: representation of static and dynamic objects in neural nets. Europhys. Lett. 7, 663-669.
100. Holmgren, C. D., and Zilberter, Y. (2001). Coincident spiking activity induces long-term changes in inhibition of neocortical pyramidal cells. J. Neurosci. 21, 8270-8277.
101. Hopfield, J. J. (1982). Neural networks and physical systems with emergent collective computational abilities. Proc. Natl. Acad. Sci. U.S.A. 79, 2554-2558.
102. Hubel, D. H., and Wiesel, T. N. (1965). Binocular interaction in striate cortex of kittens reared with artificial squint. J. Neurophysiol. 28, 1041-1059.
103. Ito, M. (1989). Long-term depression. Annu. Rev. Neurosci. 12, 85-102.
104. Ito, M., Sakurai, M., and Tongroach, P. (1982). Climbing fibre induced depression of both mossy fibre responsiveness and glutamate sensitivity of cerebellar Purkinje cells. J. Physiol. (Lond.) 324, 113-134.
105. Izhikevich, E. M., and Desai, N. S. (2003). Relating STDP to BCM. Neural. Comput. 15, 1511-1523.
106. Jacob, V., Brasier, D. J., Erchova, I., Feldman, D., and Shulz, D. E. (2007). Spike timing-dependent synaptic depression in the in vivo barrel cortex of the rat. J. Neurosci. 27, 1271-1284.
107. James, W. (1890). The Principles of Psychology. New York: Henry Holt and Company.
108. Kampa, B. M., Letzkus, J. J., and Stuart, G. J. (2006). Cortical feedforward networks for binding different streams of sensory information. Nat. Neurosci. 9, 1472-1473.
109. Kandel, E. R. (2001). The molecular biology of memory storage: a dialog between genes and synapses. Biosci. Rep. 21, 565-611.
110. Kandel, E. R. (2006). In Search of Memory: The Emergence of a New Science of Mind, 1st Edn. New York: W. W. Norton & Company.
111. Kandel, E. R., and Tauc, L. (1964). Mechanism of prolonged heterosynaptic facilitation. Nature 202, 145-147.
112. Kelso, S. R., Ganong, A. H., and Brown, T. H. (1986). Hebbian synapses in hippocampus. Proc. Natl. Acad. Sci. U.S.A. 83, 5326-5330.
113. Kempter, R., Gerstner, W., and van Hemmen, J. L. (1999a). Hebbian learning and spiking neurons. Phys. Rev. E 59, 4498-4514.
114. Kempter, R., Gerstner, W., and van Hemmen, J. L. (1999b). "Spike-based compared to rate-based Hebbian learning," in Advances in neural information processing systems, eds M.S. Kearns, S.A. Solla, and D.A. Cohn (Cambridge, MA: MIT Press), 125-131.
115. Kempter, R., Gerstner, W., and van Hemmen, J. L. (2001). Intrinsic stabilization of output rates by spike-based Hebbian learning. Neural Comput. 13, 2709-2741.
116. Kerr, D. S., and Abraham, W. C. (1993). Comparison of associative and non-associative conditioning procedures in the induction of LTD in CA1 of the hippocampus. Synapse 14, 305-313.
117. Kilgard, M. P., and Merzenich, M. M. (1998). Cortical map reorganization enabled by nucleus basalis activity. Science 279, 1714-1718.
118. Kleinfeld, D., and Sompolinsky, H. (1988). Associative neural network model for the generation of temporal patterns. Theory and application to central pattern generators. Biophys. J. 54, 1039-1051.
119. Ko, H., Hofer, S. B., Pichler, B., Buchanan, K. A., Sjöström, P. J., and Mrsic-Flogel, T. D. (2011). Functional specificity of local synaptic connections in neocortical networks. Nature 473, 87-91.
120. Kohonen, T. (1972). Correlation matrix memories. IEEE Trans. Comput. C-21, 353-359.
121. Konorski, J. (1948). Conditioned Reflexes and Neuron Organization. Cambridge: Cambridge University Press.
122. Kullmann, D. M., and Lamsa, K. P. (2007). Long-term synaptic plasticity in hippocampal interneurons. Nat. Rev. Neurosci. 8, 687-699.
123. Kwon, H. B., and Sabatini, B. L. (2011). Glutamate induces de novo growth of functional spines in developing cortex. Nature 474, 100-104.
124. Lamprecht, R., and LeDoux, J. (2004). Structural plasticity and memory. Nat. Rev. Neurosci. 5, 45-54.
125. Lamsa, K. P., Kullmann, D. M., and Woodin, M. A. (2010). Spike-timing dependent plasticity in inhibitory circuits. Front. Synaptic Neurosci. 2:8. doi: 10.3389/fnsyn.2010.00008
126. Larrabee, M. G., and Bronk, D. W. (1947). Prolonged facilitation of synaptic excitation in sympathetic ganglia. J. Neurophysiol. 10, 139-154.
127. Lashley, K. S. (1929). Brain Mechanisms and Intelligence. A Quantitative Study of Injuries to the Brain. Chicago: University of Chicago Press.
128. Le Be, J. V., and Markram, H. (2006). Spontaneous and evoked synaptic rewiring in the neonatal neocortex. Proc. Natl. Acad. Sci. U.S.A. 103, 13214-13219.
129. Le Be, J. V., Silberberg, G., Wang, Y., and Markram, H. (2007). Morphological, electrophysiological, and synaptic properties of corticocallosal pyramidal cells in the neonatal rat neocortex. Cereb. Cortex 17, 2204-2213.
130. Letzkus, J. J., Kampa, B. M., and Stuart, G. J. (2006). Learning rules for spike timing-dependent plasticity depend on dendritic synapse location. J. Neurosci. 26, 10420-10429.
131. Levy, W. B., and Steward, O. (1979). Synapses as associative memory elements in the hippocampal formation. Brain Res. 175, 233-245.
132. Levy, W. B., and Steward, O. (1983). Temporal contiguity requirements for long-term associative potentiation/depression in the hippocampus. Neuroscience 8, 791-797.
133. Li, S.-C., Brehmer, Y., Shing, Y. L., Werkle-Bergner, M., and Lindenberger, U. (2006). Neuromodulation of associative and organizational plasticity across the life span: empirical evidence and neurocomputational modeling. Neurosci. Biobehav. Rev. 30, 775-790.
134. Libet, B.,and Gerard, R. W. (1939). Control of the potential rhythm of the isolated frog brain. J. Neurophysiol. 2, 153-169.
135. Lisman, J., and Spruston, N. (2005). Postsynaptic depolarization requirements for LTP and LTD: a critique of spike timing-dependent plasticity. Nat. Neurosci. 8, 839-841.
136. Lisman, J., and Spruston, N. (2010). Questions about STDP as a general model of synaptic plasticity. Front. Synaptic Neurosci. 2:140. doi: 10.3389/fnsyn.2010.00140
137. Lloyd, D. P. (1949). Post-tetanic potentiation of response in monosynaptic reflex pathways of the spinal cord. J. Gen. Physiol. 33, 147-170.
138. Locke, J. (1689). An Essay Concerning Human Understanding, 38th Edn. London: William Tegg.
139. Lømo, T. (1964). Frequency potentiation of excitatory synaptic activity in the dentate area of the hippocampal formation. Acta Physiol. Scand. 68, 128.
140. Lorente de Nó, R. (1934). Studies on the structure of the cerebral cortex. II. Continuation of the study of the ammonic system. J. Psychol. Neurol. 46, 113-177.
141. Lugaro, E. (1898). Le resistenze nell'evoluzione della vita. Rivista moderna di cultura 1, 29-60.
142. Lugaro, E. (1906). I problemi odierni della psichiatria. Milano: Sandron.
143. Lugaro, E. (1909). Modern Problems in Psychiatry. (Translated by D. Orr and R. G. Rows). Manchester: The University Press.
144. Lynch, G. S., Dunwiddie, T., and Gribkoff, V. (1977). Heterosynaptic depression: a postsynaptic correlate of long-term potentiation. Nature 266, 737-739.
145. Magee, J. C., and Johnston, D. (1997). A synaptically controlled, associative signal for Hebbian plasticity in hippocampal neurons. Science 275, 209-213.
146. Malenka, R. C. (2003). The long-term potential of LTP. Nat. Rev. 4, 923-926.
147. Malenka, R. C., and Bear, M. F. (2004). LTP and LTD: an embarrassment of riches. Neuron 44, 5-21.
148. Malenka, R. C., and Nicoll, R. A. (1999). Long-term potentiation - a decade of progress? Science 285, 1870-1874.
149. Malinow, R. (1991). Transmission between pairs of hippocampal slice neurons: quantal levels, oscillations, and LTP. Science 252, 722-724.
150. Maren, S. (2005). Synaptic mechanisms of associative memory in the amygdala. Neuron 47, 783-786.
151. Maren, S., and Fanselow, M. S. (1996). The amygdala and fear conditioning: has the nut been cracked? Neuron 16, 237-240.
152. Markram, H., Gupta, A., Uziel, A., Wang, Y., and Tsodyks, M. (1998). Information processing with frequency-dependent synaptic connections. Neurobiol. Learn. Mem. 70, 101-112.
153. Markram, H., Helm, P. J., and Sakmann, B. (1995). Dendritic calcium transients evoked by single back-propagating action potentials in rat neocortical pyramidal neurons. J. Physiol. (Lond.) 485, 1-20.
154. Markram, H., Lubke, J., Frotscher, M., Roth, A., and 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.
155. Markram, H., Lübke, J., Frotscher, M., and Sakmann, B. (1997b). Regulation of synaptic efficacy by coincidence of postsynaptic APs and EPSPs. Science 275, 213-215.
156. Markram, H., and Sakmann, B. (1994). Calcium transients in dendrites of neocortical neurons evoked by single subthreshold excitatory postsynaptic potentials via low-voltage-activated calcium channels. Proc. Natl. Acad. Sci. U.S.A. 91, 5207-5211.
157. Markram, H., and Sakmann, B. (1995). Action potentials propogating back into dendrites triggers changes in efficacy of single-axon synapses between layer V pyramidal cells. Soc. Neurosci. Abstr. 21, 2007.
158. Markram, H., and Segal, M. (1990). Acetylcholine potentiates responses to N-methyl-d-aspartate in the rat hippocampus. Neurosci. Lett. 113, 62-65.
159. Markram, H., and Tsodyks, M. (1996a). Redistribution of synaptic efficacy between neocortical pyramidal neurons. Nature 382, 807-810.
160. Markram, H., and Tsodyks, M. (1996b). Redistribution of synaptic efficacy: a mechanism to generat infinite synaptic input diversity from a homogeneous population of neurons without changing absolute synaptic efficacies. J. Physiol. Paris 90, 229-232.
161. Marr, D. (1969). A theory of cerebellar cortex. J. Physiol. (Lond.) 202, 437-470.
162. Marr, D. (1971). Simple memory: a theory for archicortex. Philos. Trans. R. Soc. Lond., B, Biol. Sci. 262, 23-81.
163. Matteucci, C. (1838). Sur le courant électrique ou propre de la grénouille. Bibl. Univ. Genève 15, 157-168.
164. McCullogh, W. S., and Pitts, W. H. (1943). A logical calculus of the ideas immanent in nervous activity. Bull. Math. Biophys. 5, 115-113.
165. McNaughton, B. L. (2003). Long-term potentiation, cooperativity and Hebb's cell assemblies: a personal history. Philos. Trans. R. Soc. Lond., B, Biol. Sci. 358, 629-634.
166. McNaughton, B. L., Douglas, R. M., and Goddard, G. V. (1978). Synaptic enhancement in fascia dentata: cooperativity among coactive afferents. Brain Res. 157, 277-293.
167. Meliza, C. D., and Dan, Y. (2006). Receptive-field modification in rat visual cortex induced by paired visual stimulation and single-cell spiking. Neuron 49, 183-189.
168. Mihalas, S. (2011). Calcium messenger heterogeneity: a possible signal for spike-timing-dependent plasticity. Front. Comput. Neurosci. 4:158. doi: 10.3389/fncom.2010.00158
169. Mulkey, R. M., and Malenka, R. C. (1992). Mechanisms underlying induction of homosynaptic long-term depression in area CA1 of the hippocampus. Neuron 9, 967-975.
170. Müller-Dahlhaus, F., Ziemann, U., and Classen, J. (2010). Plasticity resembling spike-timing dependent synaptic plasticity: the evidence in human cortex. Front. Synaptic Neurosci. 2:34. doi: 10.3389/fnsyn.2010.00034
171. Nelson, S. B., Sjöström, P. J., and Turrigiano, G. G. (2002). Rate and timing in cortical synaptic plasticity. Philos. Trans. R. Soc. Lond., B, Biol. Sci. 357, 1851-1857.
172. Paulsen, O., Li, Y. G., Hvalby, O., Anderson, P., and Bliss, T. V. (1993). Failure to induce long-term depression by an anti-correlation procedure in area CA1 of the rat hippocampal slice. Eur. J. Neurosci. 5, 1241-1246.
173. Pavlov, I. P. (1897). The Work of the Digestive Glands English Translation by W. H. Thompson, London, 1902. (London: Griffin).
174. Pawlak, V., and Kerr, J. N. (2008). Dopamine receptor activation is required for corticostriatal spike-timing-dependent plasticity. J. Neurosci. 28, 2435-2446.
175. Pawlak, V., Wickens, J. R., Kirkwood, A., and Kerr, J. N. D. (2010). Timing is not everything: neuromodulation opens the STDP gate. Front. Synaptic Neurosci. 2, 146. doi: 10.3389/fnsyn.2010.00146
176. Penfield, W., and Boldrey, E. (1937). Somatic motor and sensory representation in the cerebral cortex of man as studied by electrical stimulation. Brain Res. 60, 389-443.
177. Perin, R., Berger, T. K., and Markram, H. (2011). A synaptic organizing principle for cortical neuronal groups. Proc. Natl. Acad. Sci. U.S.A. 108, 5419-5424.
178. Perrett, S. P., Dudek, S. M., Eagleman, D., Montague, P. R., and Friedlander, M. J. (2001). LTD induction in adult visual cortex: role of stimulus timing and inhibition. J. Neurosci. 21, 2308-2319.
179. Quiroga, R. Q., Reddy, L., Kreiman, G., Koch, C., and Fried, I. (2005). Invariant visual representation by single neurons in the human brain. Nature 435, 1102-1107.
180. Rackham, O., Tsaneva-Atanasova, K., Ganesh, A., and Mellor, J. (2010). A Ca2+-based computational model for NDMA receptor-dependent synaptic plasticity at individual post-synaptic spines in the hippocampus. Front. Synaptic Neurosci. 2, 31. doi: 10.3389/fnsyn.2010.00031
181. Ralf Gerard, W. (1930). Delayed action potentials in nerve. Am. J. Physiol. 93, 337-341.
182. Rall, W. (1955). A statistical theory of monosynaptic input-output relations. J. Cell. Physiol. 46, 373-411.
183. Rall, W. (1957). Membrane time constant of motoneurons. Science 126, 454.
184. Rall, W. (1959). Branching dendritic trees and motoneuron membrane resistivity. Exp. Neurol. 1, 491-527.
185. Rall, W. (1960). Membrane potential transients and membrane time constant of motoneurons. Exp. Neurol. 2, 503-532.
186. Rall, W. (1962). Electrophysiology of a dendritic neuron model. Biophys. J. 2, 145-167.
187. Rall, W., and Rinzel, J. (1971). Dendritic spine function and synaptic attenuation calculations. Prog. Abstr. Soc. Neurosci. First Ann. Mtg. 64.
188. Ramón y Cajal, S. (1894). The Croonian Lecture: La Fine Structure Des Centres Nerveux. Proc. R. Soc. Lond., B, Biol. Sci. 4, 444-468.
189. Ramón y Cajal, S. (1911). Histologie du Système Nerveux de l'Homme et des Vertebrés, Vol. 2. Paris: Malone.
190. Remy, S., and Spruston, N. (2007). Dendritic Spikes induce single-burst long-term potentiation. Proc. Natl. Acad. Sci. U.S.A. 104, 17192-17197.
191. Rescorla, R. A., and Wagner, A. R. (1972). "A theory of Pavlovian conditioning: variations in the effectiveness of reinforcement and nonrein-forcement," in Classical Conditioning II: Current Research and Theory, eds A. H. Black and W. F. Prokasy (New York: Appleton Century Crofts), 64-99.
192. Ribot, T. (1870). La Psychologie Anglaise Contemporaine. Paris: Librairie philosophique de Ladrange.
193. Roberts, P. D., and Bell, C. C. (2000). Computational consequences of temporally asymmetric learning rules: II. Sensory image cancellation. J. Comput. Neurosci. 9, 67-83.
194. Rochester, N., Holland, J., Haibt, L., and Duda, W. (1956). Tests on a cell assembly theory of the action of the brain, using a large digital computer. IRE Trans. Inf. Theory 2, 80-93.
195. Rodrigues, S. M., Schafe, G. E., and LeDoux, J. E. (2004). Molecular mechanisms underlying emotional learning and memory in the lateral amygdala. Neuron 44, 75-91.
196. Rosenblatt, F. (1958). The perceptron: a probabilistic model for information storage and organization in the brain. Psychol. Rev. 65, 386-408.
197. Sances, A., Myklebust, J., Larson, S. J., and Cusick, J. F. (1980). The evoked potential and early studies of bioelectricity. J. Clin. Eng. 5.
198. Sara, S. J. (2009). The locus coeruleus and noradrenergic modulation of cognition. Nat. Rev. 10, 211-223.
199. Schuett, S., Bonhoeffer, T., and Hubener, M. (2001). Pairing-induced changes of orientation maps in cat visual cortex. Neuron 32, 325-337.
200. Schuetze, S. M. (1983). The discovery of the action potential. Trends Neurosci. 6, 164-168.
201. Sejnowski, T. J. (1977a). Statistical constraints on synaptic plasticity. J. Theor. Biol. 69, 385-389.
202. Sejnowski, T. J. (1977b). Storing covariance with nonlinearly interacting neurons. J. Math. Biol. 4, 303-321.
203. Senn, W., Markram, H.,and Tsodyks, M. (2001). An algorithm for modifying neurotransmitter release probability based on pre- and postsynaptic spike timing. Neural. Comput. 13, 35-67.
204. Seol, G. H., Ziburkus, J., Huang, S., Song, L., Kim, I. T., Takamiya, K., Huganir, R. L., Lee, H. K., and Kirk-wood, A. (2007). Neuromodulators control the polarity of spike-timing-dependent synaptic plasticity. Neuron 55, 919-929.
205. Sherrington, C. S. (1897). "The central nervous system," in A Textbook of Physiology, 7th Edn, ed. M. Foster (London: Macmillan), 3, 929.
206. Sherrington, C. S. (1909). On plastic tonus and proprioceptive reflexes. Q. J. Exp. Physiol. 2, 109-156.
207. Shouval, H. Z., Bear, M. F., and Cooper, L. N. (2002). A unified model of NMDA receptor-dependent bidirectional synaptic plasticity. Proc. Natl. Acad. Sci. U.S.A. 99, 10831-10836.
208. Shulz, D. E., and Jacob, V. (2010). Spike timing dependent plasticity in the intact brain: counteracting spurious spike coincidences. Front. Synaptic Neurosci. 2, 137. doi: 10.3389/fnsyn.2010.00137
209. Sjöström, P. J., and Häusser, M. (2006). A cooperative switch determines the sign of synaptic plasticity in distal dendrites of neocortical pyramidal neurons. Neuron 51, 227-238.
210. Sjöström, P. J., Rancz, E. A., Roth, A., and Hausser, M. (2008). Dendritic excitability and synaptic plasticity. Physiol. Rev. 88, 769-840.
211. Sjöström, P. J., Turrigiano, G. G., and Nelson, S. B. (2001). Rate, timing, and cooperativity jointly determine cortical synaptic plasticity. Neuron 32, 1149-1164.
212. Sjöström, P. J., Turrigiano, G. G., and Nelson, S. B. (2003). Neocortical LTD via coincident activation of presynaptic NMDA and cannabinoid receptors. Neuron 39, 641-654.
213. Sjöström, P. J., Turrigiano, G. G., and Nelson, S. B. (2004). Endocannabinoid-dependent neocortical layer-5 LTD in the absence of postsynaptic spiking. J. Neurophysiol. 92, 3338-3343.
214. Skinner, B. F. (1938). The Behavior or Organisms: An Experimental Analysis. New York: Appleton-Century-Crofts.
215. Slater, N. T., Stelzer, A., and Galvan, M. (1985). Kindling-like stimulus patterns induce epileptiform discharges in the guinea pig in vitro hippocampus. Neurosci. Lett. 60, 25-31.
216. Sompolinsky, H., and Kanter, I. I. (1986). Temporal association in asymmetric neural networks. Phys. Rev. Lett. 57, 2861-2864.
217. Song, S., and Abbott, L. F. (2001). Cortical development and remapping through spike timing-dependent plasticity. Neuron 32, 339-350.
218. Song, S., Miller, K. D., and Abbott, L. F. (2000). Competitive Hebbian learning through spike-timing-dependent synaptic plasticity. Nat. Neurosci. 3, 919-926.
219. Song, S., Sjöström, P. J., Reigl, M., Nelson, S., and Chklovskii, D. B. (2005). Highly nonrandom features of synaptic connectivity in local cortical circuits. PLoS Biol. 3, e68. doi: 10.1371/journal.pbio.0030068
220. Stanton, P. K., and Sejnowski, T. J. (1989). Associative long-term depression in the hippocampus induced by hebbian covariance. Nature 339, 215-218.
221. Stefan, K., Kunesch, E., Cohen, L. G., Benecke, R., and Classen, J. (2000). Induction of plasticity in the human motor cortex by paired associative stimulation. Brain 123, 572-584.
222. Steinbuch, K., Jaenicke, W., and Reiner, H. (1965). Learning Matrix. C.I.P. Office. Available at: http://brevets-patents.ic.gc.ca/opic-cipo/cpd/eng/patent/717227/summary.html
223. Stent, G. S. (1973). A physiological mechanism for Hebb's postulate of learning. Proc. Natl. Acad. Sci. U.S.A. 70, 997-1001.
224. Stepanyants, A., Tamas, G., and Chklovskii, D. B. (2004). Class-specific features of neuronal wiring. Neuron 43, 251-259.
225. Stevens, C. F. (1998). A million dollar question: does LTP=memory? Neuron 20, 1-2.
226. Stuart, G. J., and Sakmann, B. (1994). Active propagation of somatic action potentials into neocortical pyramidal cell dendrites. Nature 367, 69-72.
227. Tanimoto, H., Heisenberg, M., and Gerber, B. (2004). Experimental psychology: event timing turns punishment to reward. Nature 430, 983.
228. Tanzi, E. (1893). I fatti e le induzioni dell'odierna istologia del sistema nervoso. Riv Sper Fren Med Leg 19, 419-472.
229. Toda, M., and Abi-Dargham, A. (2007). Dopamine hypothesis of schizophrenia: making sense of it all. Curr. Psychiatry Rep. 9, 329-336.
230. Toyoizumi, T., Pfister, J.-P., Aihara, K., and Gerstner, W. (2005). Generalized Bienenstock-Cooper-Munro rule for spiking neurons that maximizes information transmission. Proc. Natl. Acad. Sci. U.S.A. 102, 5239-5244.
231. Toyoizumi, T., Pfister, J.-P., Aihara, K., and Gerstner, W. (2007a). Optimality model of unsupervised spike-timing-dependent plasticity: synaptic memory and weight distribution. Neural. Comput. 19, 639-671.
232. Toyoizumi, T., Pfister, J. P., Aihara, K., and Gerstner, W. (2007b). Optimality model of unsupervised spike-timing-dependent plasticity: synaptic memory and weight distribution. Neural. Comput. 19, 639-671.
233. Traynor, B. J., and Singleton, A. B. (2010). Nature versus nurture: death of a dogma, and the road ahead. Neuron 68, 196-200.
234. Tsodyks, M. (2002). Spike-timing-dependent synaptic plasticity - the long road towards understanding neuronal mechanisms of learning and memory. Trends Neurosci. 25, 599-600.
235. Tsodyks, M., Pawelzik, K., and Markram, H. (1998). Neural networks with dynamic synapses. Neural. Comput. 10, 821-835.
236. Tsodyks, M. V., and 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.
237. Turrigiano, G., Abbott, L. F., and Marder, E. (1994). Activity-dependent changes in the intrinsic properties of cultured neurons. Science 264, 974-977.
238. Turrigiano, G. G., Leslie, K. R., Desai, N. S., Rutherford, L. C., and Nelson, S. B. (1998). Activity-dependent scaling of quantal amplitude in neocortical neurons. Nature 391, 892-896.
239. Turrigiano, G. G., and Nelson, S. B. (2000). Hebb and homeostasis in neuronal plasticity. Curr. Opin. Neurobiol. 10, 358-364.
240. Turrigiano, G. G., and Nelson, S. B. (2004). Homeostatic plasticity in the developing nervous system. Nat. Rev. Neurosci. 5, 97-107.
241. van Rossum, M. C. W., Bi, G. Q., and Turrigiano, G. G. (2000). Stable Hebbian learning from spike timing-dependent plasticity. J. Neurosci. 20, 8812-8821.
242. Varela, J. A., Sen, K., Gibson, J., Fost, J., Abbott, L. F., and Nelson, S. B. (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.
243. von der Malsburg, C. (1973). Self-organization of orientation sensitive cells in the striate cortex. Kybernetik. 14, 85-100.
244. von Waldeyer-Hartz, H. (1891). Ueber einige neuere Forschungen im Gebiete der Anatomie des Centralnerven-systems. Dtsch. Med. Wochenschr. 17, 1352-1356.
245. Wang, H. X., Gerkin, R. C., Nauen, D. W., and Bi, G. Q. (2005). Coactivation and timing-dependent integration of synaptic potentiation and depression. Nat. Neurosci. 8, 187-193.
246. Watson, J. B., and Rayner, R. (1920). Conditioned emotional reactions. J. Exp. Psychol. 3, 1-14.
247. Watt, A. J., and Desai, N. S. (2010). Homeostatic plasticity and STDP: keeping a neuron's cool in a fluctuating world. Front. Synaptic Neurosci. 2:5. doi: 10.3389/fnsyn.2010.00005
248. Wiesel, T. N., and Hubel, D. H. (1965). Comparison of the effects of unilateral and bilateral eye closure on cortical unit responses in kittens. J. Neurophysiol. 28, 1029-1040.
249. Wigström, H., and Gustafsson, B. (1984). A possible correlate of the postsynaptic condition for long-lasting potentiation in the guinea pig hippocampus in vitro. Neurosci. Lett. 44, 327-332.
250. Wigström, H., Gustafsson, B., and Huang, Y. Y. (1985). A synaptic potential following single volleys in the hippocampal CA1 region possibly involved in the induction of long-lasting potentiation. Acta Physiol. Scand. 124, 475-478.
251. Willshaw, D. J., Buneman, O. P., and Longuet-Higgins, H. C. (1969). Non-holographic associative memory. Nature 222, 960-962.
252. Willwacher, G. (1976). Fiihigkeiten eines assoziativen Speichersystems im. Vergleich zu Gehirnfunktionen. Biol. Cybernetics 24, 181-198.
253. Wittenberg, G. M., and Wang, S. S.-H. (2006). Malleability of spike-timing-dependent plasticity at the CA3-CA1 synapse. J. Neurosci. 26, 6610-6617.
254. Yao, H., and Dan, Y. (2001). Stimulus timing-dependent plasticity in cortical processing of orientation. Neuron 32, 315-323.
255. Yao, H., Shen, Y., and Dan, Y. (2004). Intracortical mechanism of stimulus-timing-dependent plasticity in visual cortical orientation tuning. Proc. Natl. Acad. Sci. U.S.A. 101, 5081-5086.
256. Yoshimura, Y., and Callaway, E. M. (2005). Fine-scale specificity of cortical networks depends on inhibitory cell type and connectivity. Nat. Neurosci. 8, 1552-1559.
257. Yoshimura, Y., Dantzker, J. L., and Dan, Y. (2005). Excitatory cortical neurons form fine-scale functional networks. Nature 433, 868-873.
258. Yu, Y. C., Bultje, R. S., Wang, X., and Shi, S. H. (2009). Specific synapses develop preferentially among sister excitatory neurons in the neocortex. Nature 458, 501-504.
259. Zhang, J. C., Lau, P. M., and Bi, G. Q. (2009). Gain in sensitivity and loss in temporal contrast of STDP by dopaminergic modulation at hippocampal synapses. Proc. Natl. Acad. Sci. U.S.A. 106, 13028-13033.
260. Zhang, L. I., Tao, H. W., Holt, C. E., Harris, W. A., and Poo, M. (1998). A critical window for cooperation and competition among developing retinotectal synapses. Nature 395, 37-44.
261. Zielinski, K. (2006). Jerzy Konorski on brain associations. Acta Neurobiol. Exp. (Wars) 66, 75-84; discussion 85-90, 95-77.