Dopamine regulates intrinsic excitability thereby gating successful induction of spike timing-dependent plasticity in CA1 of the hippocampus

Frontiers in Neuroscience

Volumn 7, Issue MAR, 2013, Pages

  Edelmann, Elke ^a   Lessmann, Volkmar ^a,b  

^a OTTO VON GUERICKE UNIVERSITY   (Germany)

^b Center for Behavioral Brain Sciences   (Germany)

Author keywords

Action potential; Dopamine; Hippocampal slice; Spike timing dependent plasticity; adrenergic signaling

Indexed keywords

DOPAMINE; ISOPRENALINE; NORADRENALIN;

HIPPOCAMPAL CA1 REGION; HIPPOCAMPAL CA3 REGION; HUMAN; NERVE CELL EXCITABILITY; NERVE CELL PLASTICITY; REFRACTORY PERIOD; REVIEW; SIGNAL TRANSDUCTION; SPIKE TIMING DEPENDENT PLASTICITY; SPIKE WAVE; SYNAPTIC POTENTIAL;

EID: 84890429152     PISSN: 16624548     EISSN: 1662453X     Source Type: Journal    
DOI: 10.3389/fnins.2013.00025     Document Type: Review

References (70)

1. Argilli, E., Sibley, D. R., Malenka, R. C., England, P. M., and Bonci, A. (2008). Mechanism and time course of cocaine-induced long-term potentiation in the ventral tegmental area. J. Neurosci. 28, 9092-9100.
2. Benardo, L. S., and Prince, D. A. (1982). Dopamine modulates a Ca2+-activated potassium conductance in mammalian hippocampal pyramidal cells. Nature 297, 76-79.
3. Bender, K. J., Ford, C. P., and Trussell, L. O. (2010). Dopaminergic modulation of axon initial segment calcium channels regulates action potential initiation. Neuron 68, 500-511.
4. 1 pyramidal cells in guinea pig. Exp. Brain Res. 83, 124-130.
5. 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.
6. Bi, G. Q., and Poo, M. M. (2001). Synaptic modification by correlated activity: Hebb's postulate revisited. Annu. Rev. Neurosci. 24, 139-166.
7. Bissiere, S., Humeau, Y., and Luthi, A. (2003). Dopamine gates LTP induction in lateral amygdala by suppressing feedforward inhibition. Nat. Neurosci. 6, 587-592.
8. Bliss, T. V., and Collingridge, G. L. (1993). A synaptic model of long-term potentiation in the hippocampus. Nature 361, 31-39.
9. Buchanan, K. A., and Mellor, J. R. (2010). The activity requirements for spike timing-dependent plasticity in the hippocampus. Front. Syn. Neurosci. 2:11. doi: 10.3389/fnsyn.2010.00011
10. 1 pyramidal neurons. J. Physiol. 586, 779-793.
11. Cantrell, A. R., Smith, R. D., Goldin, A. L., Scheuer, T., and Catterall, W. A. (1997). Dopaminergic modulation of sodium current in hippocampal neurons via cAMP-dependent phosphorylation of specific sites in the sodium channel alpha subunit. J. Neurosci. 17, 7330-7338.
12. Caporale, N., and Dan, Y. (2008). Spike timing-dependent plasticity: a Hebbian learning rule. Annu. Rev. Neurosci. 31, 25-46.
13. 95 on long-term potentiation and spike timing-dependent plasticity. J. Physiol. 586, 5885-5900.
14. Couey, J. J., Meredith, R. M., Spijker, S., Poorthuis, R. B., Smit, A. B., Brussaard, A. B., et al. (2007). Distributed network actions by nicotine increase the threshold for spike-timing-dependent plasticity in prefrontal cortex. Neuron 54, 73-87.
15. 1 of the rat hippocampus in vitro. Proc. Natl. Acad. Sci. U.S.A. 91, 1148-1152.
16. 1 cell pairs in vitro. Proc. Natl. Acad. Sci. U.S.A. 93, 11225-11230.
17. Duguid, I., and Sjostrom, P. J. (2006). Novel presynaptic mechanisms for coincidence detection in synaptic plasticity. Curr. Opin. Neurobiol. 16, 312-322.
18. 1 pyramidal neurons of acute rat hippocampal slices. Front. Syn. Neurosci. 3:6. doi: 10.3389/fnsyn.2011.00006
19. Feldman, D. (2012). The spike timing dependence of plasticity. Neuron 75, 556-571.
20. Gao, C., Sun, X., and Wolf, M. E. (2006). Activation of D1 dopamine receptors increases surface expression of AMPA receptors and facilitates their synaptic incorporation in cultured hippocampal neurons. J. Neurochem. 98, 1664-1677.
21. Gasbarri, A., Verney, C., Innocenzi, R., Campana, E., and Pacitti, C. (1994). Mesolimbic dopaminergic neurons innervating the hippocampal formation in the rat: a combined retrograde tracing and immunohistochemical study. Brain Res. 668, 71-79.
22. Gerkin, R. C., Lau, P. M., Nauen, D. W., Wang, Y. T., and Bi, G. Q. (2007). Modular competition driven by NMDA receptor subtypes in spike-timing-dependent plasticity. J. Neurophysiol. 97, 2851-2862.
23. 1 neurons in vitro. Brain Res. 292, 327-338.
24. Hamilton, T. J., Wheatley, B. M., Sinclair, D. B., Bachmann, M., Larkum, M. E., and Colmers, W. F. (2010). Dopamine modulates synaptic plasticity in dendrites of rat and human dentate granule cells. Proc. Natl. Acad. Sci. U.S.A. 107, 18185-18190.
25. 3 receptor activation. J. Pharmacol. Exp. Ther. 316, 113-120.
26. 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.
27. Harvey, C. D., and Svoboda, K. (2007). Locally dynamic synaptic learning rules in pyramidal neuron dendrites. Nature 450, 1195-1200.
28. Hoffman, D. A., and Johnston, D. (1999). Neuromodulation of dendritic action potentials. J. Neurophysiol. 81, 408-411.
29. Huang, S., Trevino, M., He, K., Ardiles, A., Pasquale, R., Guo, Y., et al. (2012). Pull-push neuromodulation of LTP and LTD enables bidirectional experience-induced synaptic scaling in visual cortex. Neuron 73, 497-510.
30. Ito, H. T., and Schuman, E. M. (2008). Frequency-dependent signal transmission and modulation by neuromodulators. Front. Neurosci. 2:138-144. doi: 10.3389/neuro.01.027.2008
31. Johnston, D., Hoffman, D. A., Colbert, C. M., and Magee, J. C. (1999). Regulation of back-propagating action potentials in hippocampal neurons. Curr. Opin. Neurobiol. 9, 288-292.
32. 5 receptors gate the acquisition of novel information through hippocampal long-term potentiation and long-term depression. J. Neurosci. 26, 7723-7729.
33. 5 dopamine receptors stimulate intracellular calcium release in primary cultures of neocortical and hippocampal neurons. J. Neurophysiol. 87, 2167-2175.
34. Li, C., Dabrowska, J., Hazra, R., and Rainnie, D. G. (2011). Synergistic activation of dopamine D1 and TrkB receptors mediate gain control of synaptic plasticity in the basolateral amygdala. PLoS ONE 6:e26065. doi: 10.1371/journal.pone.0026065
35. 1 by exposure to spatial novelty. Nat. Neurosci. 6, 526-531.
36. 1 synapses in rat hippocampal slices. J. Neurosci. 23, 4173-4181.
37. Lisman, J., Grace, A. A., and Duzel, E. (2011). A neoHebbian framework for episodic memory; role of dopamine-dependent late LTP. Trends Neurosci. 34, 536-547.
38. Lisman, J. E., and Grace, A. A. (2005). The hippocampal-VTA loop: controlling the entry of information into long-term memory. Neuron 46, 703-713.
39. Magee, J. C., and Johnston, D. (1997). A synaptically controlled, associative signal for Hebbian plasticity in hippocampal neurons. Science 275, 209-213.
40. 1 pyramidal cells. Brain Res. 379, 210-215.
41. Malenka, R. C., and Nicoll, R. A. (1999). Long-term potentiation: a decade of progress? Science 285, 1870-1874.
42. Markram, H., Gerstner, W., and Sjostrom, P. J. (2011). A history of spike-timing-dependent plasticity. Front. Syn. Neurosci. 3:4. doi: 10.3389/fnsyn.2011.00004
43. Markram, H., Gerstner, W., and Sjostrom, P. J. (2012). Spike-timing-dependent plasticity: a comprehensive overview. Front. Syn. Neurosci. 4:2. doi: 10.3389/fnsyn.2012.00002
44. Markram, H., Lubke, J., Frotscher, M., and Sakmann, B. (1997). Regulation of synaptic efficacy by coincidence of postsynaptic APs and EPSPs. Science 275, 213-215.
45. Meredith, R. M., Floyer-Lea, A. M., and Paulsen, O. (2003). Maturation of long-term potentiation induction rules in rodent hippocampus: role of GABAergic inhibition. J. Neurosci. 23, 11142-11146.
46. Neve, K. A., Seamans, J. K., and Trantham-Davidson, H. (2004). Dopamine receptor signaling. J. Recept. Signal Transduct. Res. 24, 165-205.
47. Nishiyama, M., Hong, K., Mikoshiba, K., Poo, M. M., and Kato, K. (2000). Calcium stores regulate the polarity and input specificity of synaptic modification. Nature 408, 584-588.
48. Pawlak, V., and Kerr, J. N. (2008). Dopamine receptor activation is required for corticostriatal spike-timing-dependent plasticity. J. Neurosci. 28, 2435-2446.
49. Pawlak, V., Wickens, J. R., Kirkwood, A., and Kerr, J. N. D. (2010). Timing is not everything: neuromodulation opens the STDP gate. Front. Syn. Neurosci. 2:146. doi: 10.3389/fnsyn.2010.00146
50. Pedarzani, P., and Storm, J. F. (1995). Dopamine modulates the slow Ca(2+)-activated K+ current IAHP via cyclic AMP-dependent protein kinase in hippocampal neurons. J. Neurophysiol. 74, 2749-2753.
51. Pike, F. G., Meredith, R. M., Olding, A. W., and Paulsen, O. (1999). Rapid report: postsynaptic bursting is essential for "Hebbian" induction of associative long-term potentiation at excitatory synapses in rat hippocampus. J. Physiol. 518(Pt 2), 571-576.
52. Pockett, S. (1985). Dopamine changes the shape of action potentials in hippocampal pyramidal cells. Brain Res. 342, 386-390.
53. Remy, S., and Spruston, N. (2007). Dendritic spikes induce single-burst long-term potentiation. Proc. Natl. Acad. Sci. U.S.A. 104, 17192-17197.
54. Rosenkranz, J. A., and Johnston, D. (2006). Dopaminergic regulation of neuronal excitability through modulation of Ih in layer V entorhinal cortex. J. Neurosci. 26, 3229-3244.
55. Rossato, J. I., Bevilaqua, L. R., Izquierdo, I., Medina, J. H., and Cammarota, M. (2009). Dopamine controls persistence of long-term memory storage. Science 325, 1017-1020.
56. Salgado, H., Kohr, G., and Trevino, M. (2012). Noradrenergic 'tone' determines dichotomous control of cortical spike-timing-dependent plasticity. Sci. Rep. 2:417. doi: 10.1038/srep00417
57. Sara, S. J. (2009). The locus coeruleus and noradrenergic modulation of cognition. Nat. Rev. Neurosci. 10, 211-223.
58. 1 synapses in rat hippocampus. J. Neurosci. 28, 5350-5358.
59. Seol, G. H., Ziburkus, J., Huang, S., Song, L., Kim, I. T., Takamiya, K., et al. (2007). Neuromodulators control the polarity of spike-timing-dependent synaptic plasticity. Neuron 55, 919-929.
60. Shen, W., Flajolet, M., Greengard, P., and Surmeier, D. J. (2008). Dichotomous dopaminergic control of striatal synaptic plasticity. Science 321, 848-851.
61. 1 network. Neuroscience 192, 91-101.
62. 5 receptor and beta-adrenergic receptor contributions to the persistence of long-term potentiation. Neuroscience 92, 485-497.
63. 1 region of the rat hippocampus via activation of the D3 dopamine receptor. Learn. Mem. 13, 161-167.
64. Tanaka, J., Horiike, Y., Matsuzaki, M., Miyazaki, T., Ellis-Davies, G. C., and Kasai, H. (2008). Protein synthesis and neurotrophin-dependent structural plasticity of single dendritic spines. Science 319, 1683-1687.
65. Whitlock, J. R., Heynen, A. J., Shuler, M. G., and Bear, M. F. (2006). Learning induces long-term potentiation in the hippocampus. Science 313, 1093-1097.
66. Williams, G. V., and Castner, S. A. (2006). Under the curve: critical issues for elucidating D1 receptor function in working memory. Neuroscience 139, 263-276.
67. 1 synapse. J. Neurosci. 26, 6610-6617.
68. Xu, T. X., and Yao, W. D. (2010). D1 and D2 dopamine receptors in separate circuits cooperate to drive associative long-term potentiation in the prefrontal cortex. Proc. Natl. Acad. Sci. U.S.A. 107, 16366-16371.
69. 1 synapses in hippocampal slices taken from 6-hydroxydopamine-treated rats: the role of endogenous norepinephrine. Eur. J. Neurosci. 16, 1117-1128.
70. 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.