Non-Hebbian spike-timing dependent plasticity in cerebellar circuits

Frontiers in Neural Circuits

Volumn , Issue DEC, 2012, Pages

  Piochon, Claire ^a   Kruskal, Peter ^a   Maclean, Jason ^a   Hansel, Christian ^a  

^a UNIVERSITY OF CHICAGO   (United States)

Author keywords

Calcium; Climbing fiber; Dendrite; Long term depression; Long term potentiation; Parallel fiber; Purkinje cell; Pyramidal cell

Indexed keywords

ACTION POTENTIAL; BACK PROPAGATION; CALCIUM TRANSPORT; CEREBELLUM; DENDRITE; DEPOLARIZATION; EXCITATORY POSTSYNAPTIC POTENTIAL; LONG TERM DEPRESSION; LONG TERM POTENTIATION; NERVE CELL PLASTICITY; NONHUMAN; PURKINJE CELL; PYRAMIDAL NERVE CELL; REVIEW; SPIKE; SPIKE TIMING DEPENDENT PLASTICITY; SYNAPSE;

EID: 84872090689     PISSN: 16625110     EISSN: None     Source Type: Journal    
DOI: 10.3389/fncir.2012.00124     Document Type: Review

References (55)

1. Bear, M.F., Cooper, L.N., and Ebner, F.F. (1987). A physiological basis for a theory of synapse modification. Science 237, 42-48.
2. 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.
3. 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.
4. 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.
5. Bliss, T.V.P., and Lømo, T. (1973). Long-lasting potentiation of synaptic transmission in the dentate area of the anesthetized rabbit following stimulation of the perforant path. J. Physiol. 232, 331-356.
6. Chen, C., and Thompson, R.F. (1995). Temporal specificity of long-term depression in parallel fiber-Purkinje synapses in rat cerebellar slice. Learn. & Mem. 2, 185-198.
7. Coesmans, M., Weber, J.T., De Zeeuw, C.I., and Hansel, C. (2004). Bidirectional parallel fiber plasticity in the cerebellum under climbing fiber control. Neuron 44, 691-700.
8. Davie, J.T., Clark, B.A., and Häusser, M. (2008). The origin of the complex spike in cerebellar Purkinje cells. J. Neurosci. 28, 7599-7609.
9. 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. 507.1, 237-247.
10. De Ruiter, M.M., De Zeeuw, C.I., and Hansel, C. (2006). Voltage-gated sodium channels in cerebellar Purkinje cells of mormyrid fish. J. Neurophysiol. 96, 378-390.
11. Ekerot, C.F., and Kano, M. (1989). Stimulation parameters influencing climbing fibre induced long-term depression of parallel fibre synapses. Neurosci. Res. 6, 264-268.
12. Engelmann, J., van den Burg, E., Bacelo, J., de Ruiter, M., Kuwana, S., Sugawara, Y., and Grant, K. (2008). Dendritic backpropagation and synaptic plasticity in the mormyrid electrosensory lobe. J. Physiol. (Paris) 102, 233-245.
13. Golding, N.L., Staff, N.P., and Spruston, N. (2002). Dendritic spikes as a mechanism for cooperative long-term potentiation. Nature 418, 326-331.
14. Gomez, L., Kanneworff, M., Budelli, R., and Grant, K. (2005). Dendritic spike back propagation in the electrosensory lobe of Gnathonemus petersii. J. Exp. Biol. 208, 141-155.
15. Graupner, M., and Brunel, N. (2007). STDP in a bistable synapse model based on CaMKII and associated signaling pathways. PLoS Comp. Biol. 3, 2299-2323.
16. 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.
17. Han, V. Z., Zhang, Y., Bell, C.C., and Hansel, C. (2007). Synaptic plasticity and calcium signaling in Purkinje cells of the central cerebellar lobes of mormyrid fish. J. Neurosci. 27, 13499-13512.
18. Hansel, C., Artola, A., and Singer, W. (1997). Relation between dendritic Ca2+ levels and the polarity of synaptic long-term modifications in rat visual cortex neurons. Eur. J. Neurosci. 9, 2309-2322.
19. Hardie, J., and Spruston, N. (2009). Synaptic depolarization is more effective than backpropagating action potentials during induction of associative long-term potentiation in hippocampal pyramidal neurons. J. Neurosci. 29, 3233-3241.
20. Häusser, M., and Clark, B.A. (1997). Tonic synaptic inhibition modulates neuronal output pattern and spatiotemporal synaptic integration. Neuron 19, 665-678.
21. Hebb, D.O. (1949). The Organization of Behavior (New York: Wiley).
22. Hubel, D.H., and Wiesel, T.N. (1965). Binocular interaction in striate cortex of kittens reared with artificial squint. J. Neurophysiol. 28, 1041-1059.
23. 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. 324: 113-134.
24. Kitamura, K., and Häusser, M. (2011). Dendritic calcium signaling triggered by spontaneous and sensory-evoked climbing fiber input to cerebellar Purkinje cells in vivo. J. Neurosci. 31, 10847-10858.
25. Koester, H.J., and Sakmann, B. (1998). Calcium dynamics in single spines during coincident pre- and postsynaptic activity depend on relative timing of back-propagating action potentials and subthreshold excitatory postsynaptic potentials. Proc. Natl. A cad. Sci. USA 95, 9596-9601.
26. König, P., Engel, A.K., and Singer, W. (1996). Integrator or coincidence detector? The role of the cortical neuron revisited. Trends Neurosci. 19, 130-137.
27. Lev-Ram, V., Wong, S.T., Storm, D.R., and Tsien, R.Y. (2002). A new form of cerebellar long-term potentiation is postsynaptic and depends on nitric oxide but not cAMP. Proc. Natl. A cad. Sci. USA 99, 8389-8393.
28. Linden, D.J. (1999). The return of the spike: postsynaptic action potentials and the induction of LTP and LTD. Neuron 22, 661-666.
29. Lisman, J., and Spruston, N. (2010). Questions about STDP as a general model of synaptic plasticity. Front. Synaptic Neurosci. 2, 140.
30. Magee, J.C., Johnston, D. (1997). A synaptically controlled, associative signal for Hebbian plasticity in hippocampal neurons. Science 275, 209-213.
31. Margrie, T.W., Brecht, M., and Sakmann, B. (2002). In vivo, low resistance, whole-cell recordings from neurons in the anaesthetized and awake mammalian brain. Pflugers Arch. 444, 491-498.
32. 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. 485.1, 1-20.
33. Markram, H., Lübke, J., Frotscher, M., and Sakmann, B. (1997). Regulation of synaptic efficacy by coincidence of postsynaptic APs and EPSPs. Science 275, 213-215.
34. Nevian, T., and Sakmann, B. (2006). Spine Ca2+ signaling in spike-timing-dependent plasticity. J. Neurosci. 26, 11001-11013.
35. Ohtsuki, G., Piochon, C., and Hansel, C. (2009). Climbing fiber signaling and cerebellar gain control. Front. Cell. Neurosci. 3, 4.
36. Ohtsuki, G., Piochon, C., Adelman, J.P., and Hansel, C. (2012). SK2 channel modulation contributes to compartment-specific dendritic plasticity in cerebellar Purkinje cells. Neuron 75, 108-120.
37. Piochon, C., Levenes, C., Ohtsuki, G., and Hansel, C. (2010). Purkinje cell NMDA receptors assume a key role in synaptic gain control in the mature cerebellum. J. Neurosci. 30, 15330-15335.
38. Raymond, J.L., and Lisberger, S.G. (1998). Neural learning rules for the vestibulo-ocular reflex. J. Neurosci. 18, 9112-9129.
39. Rumsey, C.C., and Abbott, L. F. (2006). Synaptic democracy in active dendrites. J. Neurophysiol. 96, 2307-2318.
40. Safo, P., and Regehr, W. G. (2008). Timing dependence of the induction of cerebellar LTD. Neuropharmacol. 54, 213-218.
41. Salin, P.A., Malenka, R.C., and Nicoll, R.A. (1996). Cyclic AMP mediates a presynaptic form of LTP at cerebellar parallel fiber synapses. Neuron 16, 797-803.
42. Schmolesky, M.T., Weber, J.T., De Zeeuw, C.I., and Hansel, C. (2002). The making of a complex spike: ionic composition and plasticity. Ann. N.Y. Acad. Sci. 978, 359-390.
43. Simpson, J.I., Wylie, D.R., and De Zeeuw, C.I. (1996). On climbing fiber signals and their consequence(s). Behav. Brain Sci. 19, 384-398.
44. Sjöström, P.J., Turrigiano, G.G., and Nelson, S.B. (2001). Rate, timing, and cooperativity jointly determine cortical synaptic plasticity. Neuron 32, 1149-1164.
45. 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.
46. Spruston, N., Schiller, Y., Stuart, G., and Sakmann, B. (1995). Activity-dependent action potential invasion and calcium influx into hippocampal CA1 dendrites. Science 268, 297-300.
47. Stent G.S. (1973). A physiological mechanism for Hebb's postulate of learning. Proc. Nat. A cad. Sci. USA 70, 997-1001.
48. Stuart, G., and Häusser, M. (1994). Initiation and spread of sodium action potentials in cerebellar Purkinje cells. Neuron 13, 703-712.
49. Stuart, G., and Sakmann, B. (1994). Active propagation of somatic action potentials into neocortical pyramidal cell dendrites. Nature 367, 69-72.
50. Thompson, R.F., and Krupa, D.J. (1994). Organization of memory traces in the mammalian brain. Annu. Rev. Neurosci. 17, 519-549.
51. Tzounopoulos, T., Kim, Y., Oertel, D., and Trussell, L.O. (2004). Cell-specific, spike timing-dependent plasticities in the dorsal cochlear nucleus. Nat. Neurosci. 7, 719-725.
52. Tzounopoulos, T., Rubio, M.E., Keen, J.E., and Trussell, L.O. (2007). Coactivation of pre- and postsynaptic signaling mechanisms determines cell-specific spike-timing dependent plasticity. Neuron 54, 291-301.
53. Wang, S.S.H., Denk, W., and Häusser, M. (2000). Coincidence detection in single den dritic spines mediated by calcium release. Nat. Neurosci. 3, 1266-1273.
54. 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.
55. Zilberter, M., Holmgren, C., Shemer, I., Silberberg, G., Grillner, S., Harkany, T., and Zilberter, Y. (2009). Input specificity and dependence of spike timing-dependent plasticity on preceding postsynaptic activity at unitary connections between neocortical layer 2/3 pyramidal cells. Cereb. Cortex 19, 2308-2320.