New rules governing synaptic plasticity in core nucleus accumbens medium spiny neurons

European Journal of Neuroscience

Volumn 36, Issue 12, 2012, Pages 3615-3627

  Ji, Xincai ^a   Martin, Gilles E ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

Calcium stores; Dopamine; Endocannabinoids; Mouse; Spike timing dependent plasticity; Whole cell patch clamp recording

Indexed keywords

DOPAMINE RECEPTOR STIMULATING AGENT; N METHYL DEXTRO ASPARTIC ACID RECEPTOR;

ACTION POTENTIAL; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN NERVE CELL; BRAIN REGION; BRAIN TISSUE; CALCIUM SIGNALING; CALCIUM TRANSPORT; CONTROLLED STUDY; CORE NUCLEUS ACCUMBENS MEDIUM SPINY NEURON; ELECTROPHYSIOLOGY; EXCITATORY POSTSYNAPTIC POTENTIAL; LONG TERM DEPRESSION; LONG TERM POTENTIATION; MALE; MOUSE; NERVE CELL PLASTICITY; NONHUMAN; NUCLEUS ACCUMBENS; PRIORITY JOURNAL; SPIKE;

ACTION POTENTIALS; ANIMALS; CALCIUM; CALCIUM SIGNALING; DOPAMINE AGONISTS; EXCITATORY POSTSYNAPTIC POTENTIALS; LONG-TERM POTENTIATION; LONG-TERM SYNAPTIC DEPRESSION; MALE; MICE; MICE, INBRED C57BL; NEURONS; NUCLEUS ACCUMBENS; RECEPTORS, N-METHYL-D-ASPARTATE;

EID: 84871275347     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/ejn.12002     Document Type: Article

References (81)

1. Aizman, O., Brismar, H., Uhlen, P., Zettergren, E., Levey, A.I., Forssberg, H., Greengard, P. & Aperia, A. (2000) Anatomical and physiological evidence for D1 and D2 dopamine receptor colocalization in neostriatal neurons. Nat. Neurosci., 3, 226-230.
2. Akaike, A., Ohno, Y., Sasa, M. & Takaori, S. (1987) Excitatory and inhibitory effects of dopamine on neuronal activity of the caudate nucleus neurons in vitro. Brain Res., 418, 262-272.
3. Altier, N. & Stewart, J. (1999) The role of dopamine in the nucleus accumbens in analgesia. Life Sci., 65, 2269-2287.
4. Baldo, B.A. & Kelley, A.E. (2007) Discrete neurochemical coding of distinguishable motivational processes: insights from nucleus accumbens control of feeding. Psychopharmacology, 191, 439-459.
5. Behrens, R., Nolting, A., Reimann, F., Schwarz, M., Waldschutz, R. & Pongs, O. (2000) hKCNMB3 and hKCNMB4, cloning and characterization of two members of the large-conductance calcium-activated potassium channel beta subunit family. FEBS Lett., 474, 99-106.
6. Bell, C.C., Han, V.Z., Sugawara, Y. & Grant, K. (1997) Synaptic plasticity in a cerebellum-like structure depends on temporal order. Nature, 387, 278-281.
7. Bender, V.A., Bender, K.J., Brasier, D.J. & Feldman, D.E. (2006) Two coincidence detectors for spike timing-dependent plasticity in somatosensory cortex. J. Neurosci., 26, 4166-4177.
8. Bi, G.Q. & 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.
9. Bliss, T.V. & Collingridge, G.L. (1993) A synaptic model of memory: long-term potentiation in the hippocampus. Nature, 361, 31-39.
10. Bliss, T.V. & 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.
11. Calabresi, P., Mercuri, N., Stanzione, P., Stefani, A. & Bernardi, G. (1987) Intracellular studies on the dopamine-induced firing inhibition of neostriatal neurons in vitro: evidence for D1 receptor involvement. Neuroscience, 20, 757-771.
12. Caporale, N. & Dan, Y. (2008) Spike timing-dependent plasticity: a hebbian learning rule. Annu. Rev. Neurosci., 31, 25-46.
13. Carelli, R.M. & Ijames, S.G. (2000) Nucleus accumbens cell firing during maintenance, extinction, and reinstatement of cocaine self-administration behavior in rats. Brain Res., 866, 44-54.
14. 2+ channels in neurons. Eur. J. Neurosci., 10, 2322-2327.
15. Chen, B.T., Hopf, F.W. & Bonci, A. (2010) Synaptic plasticity in the mesolimbic system: therapeutic implications for substance abuse. Ann N.Y. Acad. Sci., 1187, 129-139.
16. Choi, S. & Lovinger, D.M. (1997) Decreased probability of neurotransmitter release underlies striatal long-term depression and postnatal development of corticostriatal synapses. Proc. Natl. Acad. Sci. USA, 94, 2665-2670.
17. Debanne, D., Gahwiler, B.H. & 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.
18. Emptage, N., Bliss, T.V. & Fine, A. (1999) Single synaptic events evoke NMDA receptor-mediated release of calcium from internal stores in hippocampal dendritic spines. Neuron, 22, 115-124.
19. Fino, E., Glowinski, J. & Venance, L. (2005) Bidirectional activity-dependent plasticity at corticostriatal synapses. J. Neurosci., 25, 11279-11287.
20. Fino, E., Deniau, J.M. & Venance, L. (2009) Brief subthreshold events can act as Hebbian signals for long-term plasticity. PLoS ONE, 4, e6557.
21. Fino, E., Paille, V., Cui, Y., Morera-Herreras, T., Deniau, J.M. & Venance, L. (2010) Distinct coincidence detectors govern the corticostriatal spike timing-dependent plasticity. J. Physiol., 588, 3045-3062.
22. Gerfen, C.R., Engber, T.M., Mahan, L.C., Susel, Z., Chase, T.N., Monsma, F.J.J. & Sibley, D.R. (1990) D1 and D2 dopamine receptor-regulated gene expression of striatonigral and striatopallidal neurons. Science, 250, 1429-1432.
23. Grueter, B.A., Brasnjo, G. & Malenka, R.C. (2010) Postsynaptic TRPV1 triggers cell type-specific long-term depression in the nucleus accumbens. Nat. Neurosci., 13, 1519-1525.
24. 2+signaling in cerebellar Purkinje neurons. J. Neurosci. Res., 88, 275-289.
25. 2+ conductance. J. Neurosci., 17, 3334-3342.
26. Hollander, J.A., Ijames, S.G., Roop, R.G. & Carelli, R.M. (2002) An examination of nucleus accumbens cell firing during extinction and reinstatement of water reinforcement behavior in rats. Brain Res., 929, 226-235.
27. Huang, Y.Y. & Kandel, E.R. (1998) Postsynaptic induction and PKA-dependent expression of LTP in the lateral amygdala. Neuron, 21, 169-178.
28. Humeau, Y., Shaban, H., Bissiere, S. & Luthi, A. (2003) Presynaptic induction of heterosynaptic associative plasticity in the mammalian brain. Nature, 426, 841-845.
29. Humeau, Y., Herry, C., Kemp, N., Shaban, H., Fourcaudot, E., Bissiere, S. & Luthi, A. (2005) Dendritic spine heterogeneity determines afferent-specific Hebbian plasticity in the amygdala. Neuron, 45, 119-131.
30. Hyman, S.E., Malenka, R.C. & Nestler, E.J. (2006) Neural mechanisms of addiction: the role of reward-related learning and memory. Annu. Rev. Neurosci., 29, 565-598.
31. Inoue, T., Kato, K., Kohda, K. & Mikoshiba, K. (1998) Type 1 inositol 1, 4, 5-trisphosphate receptor is required for induction of long-term depression in cerebellar Purkinje neurons. J. Neurosci., 18, 5366-5373.
32. Kauer, J.A. & Malenka, R.C. (2007) Synaptic plasticity and addiction. Nat. Rev. Neurosci., 8, 844-858.
33. Kombian, S.B. & Malenka, R.C. (1994) Simultaneous LTP of non-NMDA- and LTD of NMDA-receptor-mediated responses in the nucleus accumbens. Nature, 368, 242-246.
34. 2+) signals in spines of hippocampal neurons. J. Neurosci., 20, 1791-1799.
35. Krause, M., German, P.W., Taha, S.A. & Fields, H.L. (2010) A pause in nucleus accumbens neuron firing is required to initiate and maintain feeding. J. Neurosci., 30, 4746-4756.
36. Kreitzer, A.C. & Malenka, R.C. (2005) Dopamine modulation of state-dependent endocannabinoid release and long-term depression in the striatum. J. Neurosci., 25, 10537-10545.
37. Le Moine, C. & Bloch, B. (1996) Expression of the D3 dopamine receptor in peptidergic neurons of the nucleus accumbens: comparison with the D1 and D2 dopamine receptors. Neuroscience, 73, 131-143.
38. Lisman, J., Schulman, H. & Cline, H. (2002) The molecular basis of CaMKII function in synaptic and behavioural memory. Nat. Rev. Neurosci., 3, 175-190.
39. Lu, X.Y., Ghasemzadeh, M.B. & Kalivas, P.W. (1998) Expression of D1 receptor, D2 receptor, substance P and enkephalin messenger RNAs in the neurons projecting from the nucleus accumbens. Neuroscience, 82, 767-780.
40. Lynch, G., Kessler, M., Arai, A. & Larson, J. (1990) The nature and causes of hippocampal long-term potentiation. Prog. Brain Res., 83, 233-250.
41. Magee, J.C. & Johnston, D. (1997) A synaptically controlled, associative signal for Hebbian plasticity in hippocampal neurons. Science, 275, 209-213.
42. Mainen, Z.F., Malinow, R. & Svoboda, K. (1999) Synaptic calcium transients in single spines indicate that NMDA receptors are not saturated. Nature, 399, 151-155.
43. Marcantoni, A., Vandael, D.H., Mahapatra, S., Carabelli, V., Sinnegger-Brauns, M.J., Striessnig, J. & Carbone, E. (2010) Loss of Cav1.3 channels reveals the critical role of L-type and BK channel coupling in pacemaking mouse adrenal chromaffin cells. J. Neurosci., 30, 491-504.
44. Margrie, T.W., 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.
45. Markram, H., Lubke, J., Frotscher, M. & Sakmann, B. (1997) Regulation of synaptic efficacy by coincidence of postsynaptic APs and EPSPs. Science, 275, 213-215.
46. 2+ channels in hippocampal neurons. Nature, 395, 900-905.
47. Martin, G., Puig, S., Pietrzykowski, A., Zadek, P., Emery, P. & Treistman, S. (2004) Somatic localization of a specific large-conductance calcium-activated potassium channel subtype controls compartmentalized ethanol sensitivity in the nucleus accumbens. J. Neurosci., 24, 6563-6572.
48. Matthews, E.A., Weible, A.P., Shah, S. & Disterhoft, J.F. (2008) The BK-mediated fAHP is modulated by learning a hippocampus-dependent task. Proc. Natl. Acad. Sci. USA, 105, 15154-15159.
49. Meredith, G.E. & Totterdell, S. (1999) Microcircuits in nucleus accumbens' shell and core involved in cognition and reward. Psychobiology, 27, 165-186.
50. 2+)](i) oscillations in GH(3) rat anterior pituitary cells. Neuroendocrinology, 77, 162-176.
51. 2+ channels. J. Neurosci., 20, 8290-8297.
52. Pacheco-Cano, M.T., Bargas, J., Hernandez-Lopez, S., Tapia, D. & Galarraga, E. (1996) Inhibitory action of dopamine involves a subthreshold Cs(+)-sensitive conductance in neostriatal neurons. Exp. Brain Res., 110, 205-211.
53. Pennartz, C.M., Ameerun, R.F., Groenewegen, H.J. & Lopes da Silva, F.H. (1993) Synaptic plasticity in an in vitro slice preparation of the rat nucleus accumbens. Eur. J. Neurosci., 5, 107-117.
54. Poolos, N.P. & Johnston, D. (1999) Calcium-activated potassium conductances contribute to action potential repolarization at the soma but not the dendrites of hippocampal CA1 pyramidal neurons. J. Neurosci., 19, 5205-5212.
55. 2+ release in the ventral striatum. J. Neurophysiol., 104, 1673-1680.
56. Puig, M.V., Celada, P., Diaz-Mataix, L. & Artigas, F. (2003) In vivo modulation of the activity of pyramidal neurons in the rat medial prefrontal cortex by 5-HT2A receptors: relationship to thalamocortical afferents. Cereb. Cortex, 13, 870-882.
57. 2+ from separate presynaptic and postsynaptic intracellular stores. J. Neurosci., 16, 5951-5960.
58. Robbe, D., Alonso, G., Duchamp, F., Bockaert, J. & Manzoni, O.J. (2001) Localization and mechanisms of action of cannabinoid receptors at the glutamatergic synapses of the mouse nucleus accumbens. J. Neurosci., 21, 109-116.
59. Robbe, D., Bockaert, J. & Manzoni, O.J. (2002a) Metabotropic glutamate receptor 2/3-dependent long-term depression in the nucleus accumbens is blocked in morphine withdrawn mice. Eur. J. Neurosci., 16, 2231-2235.
60. Robbe, D., Kopf, M., Remaury, A., Bockaert, J. & Manzoni, O.J. (2002b) Endogenous cannabinoids mediate long-term synaptic depression in the nucleus accumbens. Proc. Natl. Acad. Sci. USA, 99, 8384-8388.
61. Robbe, D., Alonso, G. & Manzoni, O.J. (2003) Exogenous and endogenous cannabinoids control synaptic transmission in mice nucleus accumbens. Ann N.Y. Acad. Sci., 1003, 212-225.
62. Rosenkranz, J.A. & Grace, A.A. (1999) Modulation of basolateral amygdala neuronal firing and afferent drive by dopamine receptor activation in vivo. J. Neurosci., 19, 11027-11039.
63. Salamone, J.D., Correa, M., Mingote, S.M. & Weber, S.M. (2005) Beyond the reward hypothesis: alternative functions of nucleus accumbens dopamine. Curr. Opin. Pharmacol., 5, 34-41.
64. 2+ channel current and its dopaminergic D2 modulation in developing neostriatal neurons. J. Neurophysiol., 94, 3771-3787.
65. Schramm, N.L., Egli, R.E. & Winder, D.G. (2002) LTP in the mouse nucleus accumbens is developmentally regulated. Synapse, 45, 213-219.
66. Schwartz, J.C., Diaz, J., Bordet, R., Griffon, N., Perachon, S., Pilon, C., Ridray, S. & Sokoloff, P. (1998) Functional implications of multiple dopamine receptor subtypes: the D1/D3 receptor coexistence. Brain Res. Brain Res. Rev., 26, 236-242.
67. + channels in spike broadening during repetitive firing in rat hippocampal pyramidal cells. J. Physiol., 521, 135-146.
68. Shen, W., Flajolet, M., Greengard, P. & Surmeier, D.J. (2008) Dichotomous dopaminergic control of striatal synaptic plasticity. Science, 321, 848-851.
69. Sjostrom, P.J., Turrigiano, G.G. & Nelson, S.B. (2004) Endocannabinoid-dependent neocortical layer-5 LTD in the absence of postsynaptic spiking. J. Neurophysiol., 92, 3338-3343.
70. Sjostrom, P.J., Rancz, E.A., Roth, A. & Hausser, M. (2008) Dendritic excitability and synaptic plasticity. Physiol. Rev., 88, 769-840.
71. Spacek, J. & Harris, K.M. (1997) Three-dimensional organization of smooth endoplasmic reticulum in hippocampal CA1 dendrites and dendritic spines of the immature and mature rat. J. Neurosci., 17, 190-203.
72. + current in mouse neocortical pyramidal neurons. J. Neurosci., 23, 3639-3648.
73. Surmeier, D.J., Eberwine, J., Wilson, C.J., Cao, Y., Stefani, A. & Kitai, S.T. (1992) Dopamine receptor subtypes colocalize in rat striatonigral neurons. Proc. Natl. Acad. Sci. USA, 89, 10178-10182.
74. Surmeier, D.J., Bargas, J., Hemmings, H.C.J., Nairn, A.C. & Greengard, P. (1995) Modulation of calcium currents by a D1 dopaminergic protein kinase/phosphatase cascade in rat neostriatal neurons. Neuron, 14, 385-397.
75. Surmeier, D.J., Ding, J., Day, M., Wang, Z. & Shen, W. (2007) D1 and D2 dopamine-receptor modulation of striatal glutamatergic signaling in striatal medium spiny neurons. Trends Neurosci., 30, 228-235.
76. Thomas, M.J., Malenka, R.C. & Bonci, A. (2000) Modulation of long-term depression by dopamine in the mesolimbic system. J. Neurosci., 20, 5581-5586.
77. Van der Kloot, W. (1991) The regulation of quantal size. Prog. Neurobiol., 36, 93-130.
78. Wang, Y., Wu, J., Rowan, M.J. & Anwyl, R. (1996) Ryanodine produces a low frequency stimulation-induced NMDA receptor-independent long-term potentiation in the rat dentate gyrus in vitro. J. Physiol., 495, 755-767.
79. Yaka, R., Phamluong, K. & Ron, D. (2003) Scaffolding of Fyn kinase to the NMDA receptor determines brain region sensitivity to ethanol. J. Neurosci., 23, 3623-3632.
80. Zhou, L., Furuta, T. & Kaneko, T. (2003) Chemical organization of projection neurons in the rat accumbens nucleus and olfactory tubercle. Neuroscience, 120, 783-798.
81. Zhuo, M. & Hawkins, R.D. (1995) Long-term depression: a learning-related type of synaptic plasticity in the mammalian central nervous system. Rev. Neurosci., 6, 259-277.