Sensitivity to theta-burst timing permits LTP in dorsal striatal adult brain slice

Journal of Neurophysiology

Volumn 110, Issue 9, 2013, Pages 2027-2036

  Hawes, Sarah L ^a   Gillani, Fawad ^a   Evans, Rebekah C ^a   Benkert, Elizabeth A ^a   Blackwell, Kim T ^a  

^a GEORGE MASON UNIVERSITY   (United States)

Author keywords

Learning; LTP; Plasticity; Striatum; Theta

Indexed keywords

CYCLIC AMP DEPENDENT PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; PROTEIN KINASE C;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN SLICE; CEREBROSPINAL FLUID; CONTROLLED STUDY; CORPUS STRIATUM; ENZYME ACTIVITY; HABIT; HIPPOCAMPUS THETA RHYTHM; HYPOTHESIS; LEARNING; LONG TERM DEPRESSION; LONG TERM POTENTIATION; MEMORY CONSOLIDATION; MOUSE; NONHUMAN; PLASTICITY; PRIORITY JOURNAL; SKILL; THALAMUS DORSOMEDIAL NUCLEUS;

LEARNING; LTP; PLASTICITY; STRIATUM; THETA;

ANIMALS; CEREBRAL CORTEX; CORPUS STRIATUM; EXCITATORY AMINO ACID ANTAGONISTS; GTP-BINDING PROTEIN ALPHA SUBUNITS, GQ-G11; GTP-BINDING PROTEIN ALPHA SUBUNITS, GS; LONG-TERM POTENTIATION; MALE; MICE; MICE, INBRED C57BL; PROTEIN KINASE INHIBITORS; THETA RHYTHM;

EID: 84886994787     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00115.2013     Document Type: Article

References (89)

1. Abraham WC, Huggett A. Induction and reversal of long-term potentiation by repeated high-frequency stimulation in rat hippocampal slices. Hippocampus 7: 137-145, 1997.
2. Adams JP, Roberson ED, English JD, Selcher JC, Sweatt JD. MAPK regulation of gene expression in the central nervous system. Acta Neurobiol Exp (Warsz) 60: 377-394, 2000.
3. Adermark L, Lovinger DM. Frequency-dependent inversion of net striatal output by endocannabinoid-dependent plasticity at different synaptic inputs. J Neurosci 29: 1375-1380, 2009.
4. Ahn SM, Choe ES. Alterations in GluR2 AMPA receptor phosphorylation at serine 880 following group I metabotropic glutamate receptor stimulation in the rat dorsal striatum. J Neurosci Res 88: 992-999, 2010.
5. Akopian G, Musleh W, Smith R, Walsh JP. Functional state of corticos-triatal synapses determines their expression of short- and long-term plasticity. Synapse 38: 271-280, 2000.
6. Akopian G, Walsh JP. Pre- and postsynaptic contributions to age-related alterations in corticostriatal synaptic plasticity. Synapse 60: 223-238, 2006.
7. Aosaki T, Graybiel AM, Kimura M. Effect of the nigrostriatal dopamine system on acquired neural reponses in the striatum of behaving monkeys. Science 265: 412-415, 1994.
8. Arbuthnott GW, Ingham CA, Wickens JR. Dopamine and synaptic plasticity in the neostriatum. J Anat 196: 587-596, 2000.
9. Asrar S, Zhou Z, Ren W, Jia Z. Ca(2+) permeable AMPA receptor induced long-term potentiation requires PI3/MAP kinases but not Ca/CaM-depen-dent kinase II. PLos One 4: e4339, 2009.
10. Barnes TD, Kubota Y, Hu D, Jin DZ, Graybiel AM. Activity of striatal neurons reflects dynamic encoding and recoding of procedural memories. Nature 437: 1158-1161, 2005.
11. Buzsaki G. Theta rhythm of navigation: link between path integration and landmark navigation, episodic and semantic memory. Hippocampus 15: 827-840, 2005.
12. Calabresi P, Centonze D, Gubellini P, Bernardi G. Activation of M1-like muscarinic receptors is required for the induction of corticostriatal LTP. Neuropharmacology 38: 323-326, 1999.
13. Calabresi P, Centonze D, Gubellini P, Pisani A, Bernardi G. Endogenous ACh enhances striatal NMDA-responses via M1-like muscarinic receptors and PKC activation. Eur J Neurosci 10: 2887-2895, 1998.
14. Calabresi P, Gubellini P, Centonze D, Picconi B, Bernardi G, Chergui K, Svenningsson P, Fienberg AA, Greengard P. Dopamine and cAMP-regulated phosphoprotein 32 kDa controls both striatal long-term depression and long-term potentiation, opposing forms of synaptic plasticity. J Neurosci 20: 8443-8451, 2000.
15. Calabresi P, Maj R, Mercuri NB, Bernardi G. Coactivation of D1 and D2 dopamine receptors is required for long-term synaptic depression in the striatum. Neurosci Lett 142: 95-99, 1992a.
16. Calabresi P, Pisani A, Mercuri NB, Bernardi G. Long-term potentiation in the striatum is unmasked by removing the voltage-dependent magnesium block of NMDA receptor channels. Eur J Neurosci 4: 929-935, 1992b.
17. Chapman DE, Keefe KA, Wilcox KS. Evidence for functionally distinct synaptic NMDA receptors in ventromedial versus dorsolateral striatum. J Neurophysiol 89: 69-80, 2003.
18. Charpier S, Mahon S, Deniau JM. In vivo induction of striatal long-term potentiation by low-frequency stimulation of the cerebral cortex. Neurosci-ence 91: 1209-1222, 1999.
19. Choi S, Lovinger DM. Decreased probability of neurotransmitter release underlies striatal long-term depression and postnatal development of corti-costriatal synapses. Proc Natl Acad Sci USA 94: 2665-2670, 1997.
20. DeCoteau WE, Thorn C, Gibson DJ, Courtemanche R, Mitra P, Kubota Y, Graybiel AM. Oscillations of local field potentials in the rat dorsal striatum during spontaneous and instructed behaviors. J Neurophysiol 97: 3800-3805, 2007.
21. Diez-Guerra FJ. Neurogranin, a link between calcium/calmodulin and protein kinase C signaling in synaptic plasticity. IUBMB Life 62: 597-606, 2010.
22. Doucet G, Descarries L, Garcia S. Quantification of the dopamine innerva-tion in adult rat neostriatum. Neuroscience 19: 427-445, 1986.
23. Dudman JT, Eaton ME, Rajadhyaksha A, Macias W, Taher M, Barczak A, Kameyama K, Huganir R, Konradi C. Dopamine D1 receptors mediate CREB phosphorylation via phosphorylation of the NMDA receptor at Ser897-NR1. J Neurochem 87: 922-934, 2003.
24. Fellous JM, Rudolph M, Destexhe A, Sejnowski TJ. Synaptic background noise controls the input/output characteristics of single cells in an in vitro model of in vivo activity. Neuroscience 122: 811-829, 2003.
25. Fino E, Deniau JM, Venance L. Cell-specific spike-timing-dependent plasticity in GABAergic and cholinergic interneurons in corticostriatal rat brain slices. J Physiol 586: 265-282, 2008.
26. Fino E, Glowinski J, Venance L. Bidirectional activity-dependent plasticity at corticostriatal synapses. J Neurosci 25: 11279-11287, 2005.
27. Fino E, Paille V, Cui Y, Morera-Herreras T, Deniau JM, Venance L. Distinct coincidence detectors govern the corticostriatal spike timing-dependent plasticity. J Physiol 588: 3045-3062, 2010.
28. Graybiel AM. Building action repertoires: memory and learning functions of the basal ganglia. Curr Opin Neurobiol 5: 733-741, 1995.
29. Guan X, Wang L, Chen CL, Guan Y, Li S. Roles of two subtypes of corticotrophin-releasing factor receptor in the corticostriatal long-term po-tentiation under cocaine withdrawal condition. J Neurochem 115: 795-803, 2010.
30. Gubellini P, Centonze D, Tropepi D, Bernardi G, Calabresi P. Induction of corticostriatal LTP by 3-nitropropionic acid requires the activation of mGluR1/PKC pathway. Neuropharmacology 46: 761-769, 2004.
31. Gubellini P, Saulle E, Centonze D, Costa C, Tropepi D, Bernardi G, Conquet F, Calabresi P. Corticostriatal LTP requires combined mGluR1 and mGluR5 activation. Neuropharmacology 44: 8-16, 2003.
32. Hawes SL, Gillani F, Blackwell KT. Striatal LTP mechanisms and connection to learning. Program No. 790.16. In: 2012 Neuroscience Meeting Planner. New Orleans, LA: Society for Neuroscience, 2012.
33. Hilario MR, Clouse E, Yin HH, Costa RM. Endocannabinoid signaling is critical for habit formation. Front Integr Neurosci 1: 6, 2007.
34. Hopf FW, Seif T, Mohamedi ML, Chen BT, Bonci A. The small-conductance calcium-activated potassium channel is a key modulator of firing and long-term depression in the dorsal striatum. Eur J Neurosci 31: 1946-1959, 2010.
35. 3H]dopamine release in striatum in response to cortical stimulation in a corticostriatal slice preparation. J Neurosci Methods 126: 57-67.
36. Kerr JN, Plenz D. Dendritic calcium encodes striatal neuron output during up-states. J Neurosci 22: 1499-1512, 2002.
37. Kerr JN, Wickens JR. Dopamine D-1/D-5 receptor activation is required for long-term potentiation in the rat neostriatum in vitro. J Neurophysiol 85: 117-124, 2001.
38. Koralek AC, Jin X, Long JD, Costa RM, Carmena JM. Corticostriatal plasticity is necessary for learning intentional neuroprosthetic skills. Nature 483: 331-335, 2012.
39. Kreitzer AC, Malenka RC. Dopamine modulation of state-dependent endo-cannabinoid release and long-term depression in the striatum. J Neurosci 25: 10537-10545, 2005.
40. Kreitzer AC, Malenka RC. Striatal plasticity and basal ganglia circuit function. Neuron 60: 543-554, 2008.
41. Larson J, Lynch G. Induction of synaptic potentiation in hippocampus by patterned stimulation involves two events. Science 232: 985-990, 1986.
42. Larson J, Wong D, Lynch G. Patterned stimulation at the theta frequency is optimal for the induction of hippocampal long-term potentiation. Brain Res 368: 347-350, 1986.
43. Lerner TN, Kreitzer AC. Neuromodulatory control of striatal plasticity and behavior. Curr Opin Neurobiol 21: 322-327, 2011.
44. Lerner TN, Kreitzer AC. RGS4 is required for dopaminergic control of striatal ltd and susceptibility to Parkinsonian motor deficits. Neuron 73: 347-359, 2012.
45. Lovinger DM, Tyler E, Fidler S, Merritt A. Properties of a presynaptic metabotropic glutamate receptor in rat neostriatal slices. J Neurophysiol 69: 1236-1244, 1993a.
46. Lovinger DM, Tyler EC, Merritt A. Short- and long-term synaptic depression in rat neostriatum. J Neurophysiol 70: 1937-1949, 1993b.
47. Malenka RC, Kocsis JD. Presynaptic actions of carbachol and adenosine on corticostriatal synaptic transmission studied in vitro. J Neurosci 8: 3750-3756, 1988.
48. Mao L, Yang L, Tang Q, Samdani S, Zhang G, Wang JQ. The scaffold protein Homer1b/c links metabotropic glutamate receptor 5 to extracellular signal-regulated protein kinase cascades in neurons. J Neurosci 25: 2741-2752, 2005.
49. Mazzucchelli C, Vantaggiato C, Ciamei A, Fasano S, Pakhotin P, Krezel W, Welzl H, Wolfer DP, Pages G, Valverde O, Marowsky A, Porrazzo A, Orban PC, Maldonado R, Ehrengruber MU, Cestari V, Lipp HP, Chapman PF, Pouyssegur J, Brambilla R. Knockout of ERK1 MAP kinase enhances synaptic plasticity in the striatum and facilitates striatal-mediated learning and memory. Neuron 34: 807-820, 2002.
50. Miller BR, Walker AG, Shah AS, Barton SJ, Rebec GV. Dysregulated information processing by medium spiny neurons in striatum of freely behaving mouse models of Huntington's disease. J Neurophysiol 100: 2205-2216, 2008.
51. Nie T, McDonough CB, Huang T, Nguyen PV, Abel T. Genetic disruption of protein kinase A anchoring reveals a role for compartmentalized kinase signaling in theta-burst long-term potentiation and spatial memory. J Neurosci 27: 10278-10288, 2007.
52. Packard MG, Teather LA. Double dissociation of hippocampal and dorsal-striatal memory systems by posttraining intracerebral injections of 2-amino-5-phosphonopentanoic acid. Behav Neurosci 111: 543-551, 1997.
53. Paille V, Fino E, Du K, Morera-Herreras T, Perez S, Kotaleski JH, Venance L. GABAergic circuits control spike-timing-dependent plasticity. J Neurosci 33: 9353-9363, 2013.
54. Partridge JG, Tang KC, Lovinger DM. Regional and postnatal heterogeneity of activity-dependent long-term changes in synaptic efficacy in the dorsal striatum. J Neurophysiol 84: 1422-1429, 2000.
55. Pascoli V, Besnard A, Herve D, Pages C, Heck N, Girault JA, Caboche J, Vanhoutte P. Cyclic adenosine monophosphate-independent tyrosine phosphorylation of NR2B mediates cocaine-induced extracellular signal-regulated kinase activation. Biol Psychiatry 69: 218-227, 2011.
56. Pauli WM, Clark AD, Guenther HJ, O'Reilly RC, Rudy JW. Inhibiting PKMzeta reveals dorsal lateral and dorsal medial striatum store the different memories needed to support adaptive behavior. Learn Mem 19: 307-314, 2012.
57. Pawlak V, Kerr JN. Dopamine receptor activation is required for corticostriatal spike-timing-dependent plasticity. J Neurosci 28: 2435-2446, 2008.
58. 2+/calmodulin-depen-dent protein kinase II at the PSD. J Neurosci 23: 11270-11278, 2003.
59. Reynolds JN, Hyland BI, Wickens JR. A cellular mechanism of reward-related learning. Nature 413: 67-70, 2001.
60. Reynolds JN, Wickens JR. Dopamine-dependent plasticity of corticostriatal synapses. Neural Netw 15: 507-521, 2002.
61. Rivera A, Alberti I, Martin AB, Narvaez JA, de la Calle A, Moratalla R. Molecular phenotype of rat striatal neurons expressing the dopamine D5 receptor subtype. Eur J Neurosci 16: 2049-2058, 2002.
62. Ronesi J, Lovinger DM. Induction of striatal long-term synaptic depression by moderate frequency activation of cortical afferents in rat. J Physiol 562: 245-256, 2004.
63. Schulz JM, Pitcher TL, Savanthrapadian S, Wickens JR, Oswald MJ, Reynolds JN. Enhanced high-frequency membrane potential fluctuations control spike output in striatal fast-spiking interneurones in vivo. J Physiol 589: 4365-4381, 2011.
64. Shen H, Moussawi K, Zhou W, Toda S, Kalivas PW. Heroin relapse requires long-term potentiation-like plasticity mediated by NMDA2b-con-taining receptors. Proc Natl Acad Sci USA 108: 19407-19412, 2011.
65. Shen W, Flajolet M, Greengard P, Surmeier DJ. Dichotomous dopaminergic control of striatal synaptic plasticity. Science 321: 848-851, 2008.
66. Shiflett MW, Balleine BW. Molecular substrates of action control in corticostriatal circuits. Prog Neurobiol 95: 1-13, 2011.
67. Shindou T, Ochi-Shindou M, Wickens JR. A Ca(2+) threshold for induction of spike-timing-dependent depression in the mouse striatum. J Neurosci 31: 13015-13022, 2011.
68. Smith R, Musleh W, Akopian G, Buckwalter G, Walsh JP. Regional differences in the expression of corticostriatal synaptic plasticity. Neurosci-ence 106: 95-101, 2001.
69. Spencer JP, Murphy KP. Bi-directional changes in synaptic plasticity induced at corticostriatal synapses in vitro. Exp Brain Res 135: 497-503, 2000.
70. Spencer JP, Murphy KP. Activation of cyclic AMP-dependent protein kinase is required for long-term enhancement at corticostriatal synapses in rats. Neurosci Lett 329: 217-221, 2002.
71. Stern EA, Kincaid AE, Wilson CJ. Spontaneous subthreshold membrane potential fluctuations and action potential variability of rat corticostriatal and striatal neurons in vivo. J Neurophysiol 77: 1697-1715, 1997.
72. Surmeier DJ, Song WJ, Yan Z. Coordinated expression of dopamine receptors in neostriatal medium spiny neurons. J Neurosci 16: 6579-6591, 1996.
73. Takagi M, Yamamoto C. Suppressing action of cholinergic agents on synaptic transmissions in the corpus striatum of rats. Exp Neurol 62: 433-443, 1978.
74. Threlfell S, Lalic T, Platt NJ, Jennings KA, Deisseroth K, Cragg SJ. Striatal dopamine release is triggered by synchronized activity in cholinergic interneurons. Neuron 75: 58-64, 2012.
75. Tort AB, Kramer MA, Thorn C, Gibson DJ, Kubota Y, Graybiel AM, Kopell NJ. Dynamic cross-frequency couplings of local field potential oscillations in rat striatum and hippocampus during performance of a T-maze task. Proc Natl Acad Sci USA 105: 20517-20522, 2008.
76. Tseng KY, Snyder-Keller A, O'Donnell P. Dopaminergic modulation of striatal plateau depolarizations in corticostriatal organotypic cocultures. Psychopharmacology (Berl) 191: 627-640, 2007.
77. Valjent E, Caboche J, Vanhoutte P. Mitogen-activated protein kinase/ extracellular signal-regulated kinase induced gene regulation in brain: a molecular substrate for learning and memory? Mol Neurobiol 23: 83-99, 2001.
78. Valjent E, Corbille AG, Bertran-Gonzalez J, Herve D, Girault JA. Inhibition of ERK pathway or protein synthesis during reexposure to drugs of abuse erases previously learned place preference. Proc Natl Acad Sci USA 103: 2932-2937, 2006.
79. Walsh JP. Depression of excitatory synaptic input in rat striatal neurons. Brain Res 608: 123-128, 1993.
80. Wang Z, Kai L, Day M, Ronesi J, Yin HH, Ding J, Tkatch T, Lovinger DM, Surmeier DJ. Dopaminergic control of corticostriatal long-term synaptic depression in medium spiny neurons is mediated by cholinergic interneurons. Neuron 50: 443-452, 2006.
81. Wickens JR, Budd CS, Hyland BI, Arbuthnott GW. Striatal contributions to reward and decision making: making sense of regional variations in a reiterated processing matrix. Ann N Y Acad Sci 1104: 192-212, 2007.
82. Wilson CJ, Groves PM. Spontaneous firing patterns of identified spiny neurons in the rat neostriatum. Brain Res 220: 67-80, 1981.
83. Xia JX, Li J, Zhou R, Zhang XH, Ge YB, Ru YX. Alterations of rat corticostriatal synaptic plasticity after chronic ethanol exposure and withdrawal. Alcohol Clin Exp Res 30: 819-824, 2006.
84. Yin HH, Knowlton BJ. The role of the basal ganglia in habit formation. Nat Rev Neurosci 7: 464-476, 2006.
85. Yin HH, Knowlton BJ, Balleine BW. Inactivation of dorsolateral striatum enhances sensitivity to changes in the action-outcome contingency in instrumental conditioning. Behav Brain Res 166: 189-196, 2006.
86. Yin HH, Lovinger DM. Frequency-specific and D2 receptor-mediated inhibition of glutamate release by retrograde endocannabinoid signaling. Proc Natl Acad Sci USA 103: 8251-8256, 2006.
87. Yin HH, Mulcare SP, Hilario MR, Clouse E, Holloway T, Davis MI, Hansson AC, Lovinger DM, Costa RM. Dynamic reorganization of striatal circuits during the acquisition and consolidation of a skill. Nat Neurosci 12: 333-341, 2009.
88. Yin HH, Ostlund SB, Knowlton BJ, Balleine BW. The role of the dorso-medial striatum in instrumental conditioning. Eur J Neurosci 22: 513-523, 2005.
89. Zhang H, Lin SC, Nicolelis MA. Spatiotemporal coupling between hippocampal acetylcholine release and theta oscillations in vivo. J Neurosci 30: 13431-13440, 2010.