Bidirectional plasticity in striatonigral synapses: A switch to balance direct and indirect basal ganglia pathways

Learning and Memory

Volumn 18, Issue 12, 2011, Pages 764-773

  Aceves, Jose J ^a   Rueda Orozco, Pavel E ^a   Hernandez Martinez, Ricardo ^a   Galarraga, Elvira ^a   Bargas, Jose ^a  

^a INSTITUTO DE FISIOLOGÍA CELULAR   (Mexico)

Author keywords

[No Author keywords available]

Indexed keywords

CANNABINOID 1 RECEPTOR; DOPAMINE 1 RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BASAL GANGLION; CONTROLLED STUDY; DEPOLARIZATION; DOPAMINERGIC TRANSMISSION; ELECTROPHYSIOLOGY; LONG TERM DEPRESSION; MALE; MOTOR SYSTEM; NERVE CELL; NIGRONEOSTRIATAL SYSTEM; NONHUMAN; PLASTICITY; POST TETANIC POTENTIATION; PRIORITY JOURNAL; RAT; SUBTHALAMIC NUCLEUS; SYNAPSE;

6-CYANO-7-NITROQUINOXALINE-2,3-DIONE; ANIMALS; ANIMALS, NEWBORN; BASAL GANGLIA; BENZAZEPINES; BENZOXAZINES; BIOPHYSICS; CANNABINOIDS; CHELATING AGENTS; CORPUS STRIATUM; DOPAMINE AGONISTS; DRUG INTERACTIONS; EGTAZIC ACID; ELECTRIC STIMULATION; EXCITATORY AMINO ACID ANTAGONISTS; LONG-TERM SYNAPTIC DEPRESSION; MALE; MORPHOLINES; NAPHTHALENES; NEURAL PATHWAYS; PIPERIDINES; PYRAZOLES; RATS; SUBSTANTIA NIGRA; SYNAPSES; SYNAPTIC TRANSMISSION; TIME FACTORS; VALINE;

EID: 81755181063     PISSN: 10720502     EISSN: 15495485     Source Type: Journal    
DOI: 10.1101/lm.023432.111     Document Type: Article

References (86)

1. Aceves JJ, Rueda-Orozco PE, Hernández R, Plata V, Ibañez-Sandoval O, Galarraga E, Bargas J. 2011. Dopaminergic presynaptic modulation of nigral afferents: Its role in the generation of recurrent bursting in substantia nigra pars reticulata neurons. Front Syst Neurosci 5: 6. doi: 10.3389/fnsys.2011.00013.
2. Adermark L, Talani G, Lovinger DM. 2009. Endocannabinoid-dependent plasticity at GABAergic and glutamatergic synapses in the striatum is regulated by synaptic activity. Eur J Neurosci 29: 32-41.
3. Albin RL, Young AB, Penney JB. 1989. The functional anatomy of basal ganglia disorders. Trends Neurosci 12: 366-375. (Pubitemid 19238787)
4. Alexander GE, Crutcher MD. 1990. Functional architecture of basal ganglia circuits: Neural substrates of parallel processing. Trends Neurosci 13: 266-271. (Pubitemid 20193456)
5. Alexander GE, DeLong MR, Strick PL. 1986. Parallel organization of functionally segregated circuits linking basal ganglia and cortex. Annu Rev Neurosci 9: 357-381. (Pubitemid 16055790)
6. Barbour B, Brunel N, Hakim V, Nadal JP. 2007. What can we learn from synaptic weight distributions? Trends Neurosci 30: 622-629. (Pubitemid 350101853)
7. Bateup HS, Santini E, Shen W, Birnbaum S, Valjent E, Surmeier DJ, Fisone G, Nestler EJ, Greengard P. 2010. Distinct subclasses of medium spiny neurons differentially regulate striatal motor behaviors. Proc Natl Acad Sci 107: 14845-14850.
8. Beurrier C, Ben-Ari Y, Hammond C. 2006. Preservation of the direct and indirect pathways in an in vitro preparation of the mouse basal ganglia. Neurosci 140: 77-86.
9. Bevan MD, Bolam JP, Crossman AR. 1994. Convergent synaptic input from the neostriatum and the subthalamus onto identified nigrothalamic neurons in the rat. Eur J Neurosci 6: 320-334. (Pubitemid 24077145)
10. Calabresi P, Picconi B, Tozzi A, Di Filippo M. 2007. Dopamine-mediated regulation of corticostriatal synaptic plasticity. Trends Neurosci 30: 211-219. (Pubitemid 46654232)
11. Cameron DL, Williams JT. 1993. Dopamine D1 receptors facilitate transmitter release. Nature 366: 344-347. (Pubitemid 23349361)
12. Carrillo-Reid L, Tecuapetla F, Tapia D, Hernandez-Cruz A, Galarraga E, Drucker-Colin R, Bargas J. 2008. Encoding network states by striatal cell assemblies. J Neurophysiol 99: 1435-1450. (Pubitemid 351413721)
13. Castillo PE, Chiu CQ, Carroll RC. 2011. Long-term plasticity at inhibitory synapses. Curr Opin Neurobiol 21: 328-338.
14. Chase TN. 1998. The significance of continuous dopaminergic stimulation in the treatment of Parkinson's disease. Drugs 55: 1-9. (Pubitemid 28051032)
15. Cheramy A, Leviel V, Glowinski J. 1981. Dendritic release of dopamine in the substantia nigra. Nature 289: 537-542. (Pubitemid 11143145)
16. Chevaleyre V, Castillo PE. 2003. Heterosynaptic LTD of hippocampal GABAergic synapses: A novel role of endocannabinoids in regulating excitability. Neuron 38: 461-472. (Pubitemid 36579147)
17. Chevaleyre V, Takahashi KA, Castillo PE. 2006. Endocannabinoidmediated synaptic plasticity in the CNS. Annu Rev Neurosci 29: 37-76.
18. Chuhma N, Tanaka KF, Hen R, Rayport S. 2011. Functional connectome of the striatal medium-spiny neuron. J Neurosci 31: 1183-1192.
19. Connelly WM, Schulz JM, Lees G, Reynolds JN. 2010. Differential short-term plasticity at convergent inhibitory synapses to the substantia nigra pars reticulata. J Neurosci 30: 14854-14861.
20. Cools AR. 1984. Basal ganglia and Parkinson's disease: Neurobiological and pharmacological aspects in animals and man. Clin Neurol Neurosurg 86: 178-195. (Pubitemid 14030885)
21. DeLong MR, Wichmann T. 2007. Circuits and circuit disorders of the basal ganglia. Arch Neurol 64: 20-24. (Pubitemid 46072419)
22. Deniau JM, Mailly P, Maurice N, Charpier S. 2007. The pars reticulata of the substantia nigra: A window to basal ganglia output. Prog Brain Res 160: 151-172. (Pubitemid 46702290)
23. Di Filippo M, Picconi B, Tantucci M, Ghiglieri V, Bagetta V, Sgobio C, Tozzi A, Parnetti L, Calabresi P. 2009. Short-term and long-term plasticity at corticostriatal synapses: Implications for learning and memory. Behav Brain Res 199: 108-118.
24. Egertova M, Elphick MR. 2000. Localisation of cannabinoid receptors in the rat brain using antibodies to the intracellular C-terminal tail of CB. J Comp Neurol 422: 159-171. (Pubitemid 30390161)
25. Florán B, Aceves J, Sierra A, Martinez-Fong D. 1990. Activation of D1 dopamine receptors stimulates the release of GABA in the basal ganglia of the rat. Neurosci Lett 116: 136-140. (Pubitemid 20237149)
26. Gerdeman GL, Lovinger DM. 2003. Emerging roles for endocannabinoids in longterm synaptic plasticity. Br J Pharmacol 140: 781-789. (Pubitemid 37464059)
27. Gerdeman GL, Ronesi J, Lovinger DM. 2002. Postsynaptic endocannabinoid release is critical to long-term depression in the striatum. Nat Neurosci 5: 446-451. (Pubitemid 34454250)
28. Giuffrida A, Parsons LH, Kerr TM, Rodriguez de Fonseca F, Navarro M, Piomelli D. 1999. Dopamine activation of endogenous cannabinoid signaling in dorsal striatum. Nat Neurosci 2: 358-363. (Pubitemid 30491279)
29. Graybiel AM. 2004. Network-level neuroplasticity in cortico-basal ganglia pathways. Parkinsonism Relat Disord 10: 293-296. (Pubitemid 38757810)
30. Graybiel AM. 2008. Habits, rituals, and the evaluative brain. Annu Rev Neurosci 31: 359-387.
31. Grillner S, Hellgren J, Menard A, Saitoh K, Wikstrom MA. 2005. Mechanisms for selection of basic motor programs-roles for the striatum and pallidum. Trends Neurosci 28: 364-370. (Pubitemid 40853859)
32. Guzmán JN, Hernández A, Galarraga E, Tapia D, Laville A, Vergara R, Aceves J, Bargas J. 2003. Dopaminergic modulation of axon collaterals interconnecting spiny neurons of the rat striatum. J Neurosci 23: 8931-8940. (Pubitemid 37210906)
33. Hashimotodani Y, Ohno-Shosaku T, Tsubokawa H, Ogata H, Emoto K, Maejima T, Araishi K, Shin HS, Kano M. 2005. Phospholipase Cb serves as a coincidence detector through its Ca2+ dependency for triggering retrograde endocannabinoid signal. Neuron 45: 257-268. (Pubitemid 40128119)
34. 2+-assisted receptor-driven endocannabinoid release:Mechanisms that associate presynaptic and postsynaptic activities. Curr Opin Neurobiol 17: 360-365.
35. Hebb DO. 1949. The organization of behavior; a neuropsychological theory. Wiley, New York.
36. Ibañez-Sandoval O, Hernández A, Florán B, Galarraga E, Tapia D, Valdiosera R, Erlij D, Aceves J, Bargas J. 2006. Control of the subthalamic innervation of substantia nigra pars reticulata by D1 and D2 dopamine receptors. J Neurophysiol 95: 1800-1811.
37. Ibañez-Sandoval O, Carrillo-Reid L, Galarraga E, Tapia D, Mendoza E, Gomora JC, Aceves J, Bargas J. 2007. Bursting in substantia nigra pars reticulata neurons in vitro: Possible relevance for Parkinson disease. J Neurophysiol 98: 2311-2323. (Pubitemid 47591662)
38. Iribe Y, Moore K, Pang KC, Tepper JM. 1999. Subthalamic stimulation-induced synaptic responses in substantia nigra pars compacta dopaminergic neurons in vitro. J Neurophysiol 82: 925-933. (Pubitemid 29387864)
39. Kravitz AV, Freeze BS, Kay K, Thwin MT, Deisseroth K, Kreitzer AC. 2010. Regulation of parkinsonian motor behaviours by optogenetic control of basal ganglia circuitry. Nature 466: 622-626.
40. Kreitzer AC, Malenka RC. 2005. Dopamine modulation of state-dependent endocannabinoid release and long-term depression in the striatum. J Neurosci 25: 10537-10545. (Pubitemid 41628455)
41. Kreitzer AC, Malenka RC. 2007. Endocannabinoid-mediated rescue of striatal LTD and motor deficits in Parkinson's disease models. Nature 445: 643-647. (Pubitemid 46232883)
42. Kreitzer AC, Malenka RC. 2008. Striatal plasticity and basal ganglia circuit function. Neuron 60: 543-554.
43. Lovinger DM. 2010. Neurotransmitter roles in synaptic modulation, plasticity and learning in the dorsal striatum. Neuropharmacol 58: 951-961.
44. Malenka RC, Bear MF. 2004. LTP and LTD: an embarrassment of riches. Neuron 30: 5-21. (Pubitemid 39348827)
45. Manon MM. 1987. Digital design. Prentice-Hall, Inc., Upper Saddle River, NJ.
46. Massey PV, Bashir ZI. 2007. Long-term depression: Multiple forms and implications for brain function. Trends Neurosci 30: 176-184.
47. Mátyás F, Yanovsky Y, Mackie K, Kelsch W, Misgeld U, Freund TF. 2006. Subcellular localization of type 1 cannabinoid receptors in the rat basal ganglia. Neuroscience 137: 337-361. (Pubitemid 43031500)
48. Maurice N, Deniau JM, Glowinski J, Thierry AM. 1999. Relationships between the prefrontal cortex and the basal ganglia in the rat: Physiology of the cortico-nigral circuits. J Neurosci 19: 4674-4681. (Pubitemid 29241115)
49. Mendoza E, Galarraga E, Tapia D, Laville A, Hernández-Echeagaray E, Bargas J. 2006. Differential induction of long term synaptic plasticity in inhibitory synapses of the hippocampus. Synapse 60: 533-542. (Pubitemid 44537086)
50. Misgeld U. 2004. Innervation of the substantia nigra. Cell Tissue Res 318: 107-114. (Pubitemid 39362631)
51. Misgeld U, Drew G, Yanovsky Y. 2007. Presynaptic modulation of GABA release in the basal ganglia. Prog Brain Res 160: 245-259. (Pubitemid 46702295)
52. Mizuno T, Schmauss C, Rayport S. 2007. Distinct roles of presynaptic dopamine receptors in the differential modulation of the intrinsic synapses of medium-spiny neurons in the nucleus accumbens. BMC Neurosci 8: 8. doi: 10.1186/1471-2202-8-8.
53. Mulkey RM, Endo S, Shenolikar S, Malenka RC. 1994. Involvement of a calcineurin/inhibitor-1 phosphatase cascade in hippocampal long-term depression. Nature 369: 486-488.
54. Nakanishi H, Kita H, Kitai ST. 1987. Intracellular study of rat substantia nigra pars reticulata neurons in an in vitro slice preparation: Electrical membrane properties and response characteristics to subthalamic stimulation. Brain Res 437: 45-55. (Pubitemid 18029687)
55. Ohno-Shosaku T, Hashimotodani Y, Ano M, Takeda S, Tsubokawa H, Kano M. 2007. Endocannabinoid signalling triggered by NMDA receptor-mediated calcium entry into rat hippocampal neurons. J Physiol 584: 407-418. (Pubitemid 47578328)
56. Olanow CW, Obeso JA, Stocchi F. 2006. Continuous dopamine-receptor treatment of Parkinson's disease: Scientific rationale and clinical implications. Lancet Neurol 5: 677-687. (Pubitemid 44081890)
57. Radnikow G, Misgeld U. 1998. Dopamine D1 receptors facilitate GABAA synaptic currents in the rat substantia nigra pars reticulata. J Neurosci 18: 2009-2016. (Pubitemid 28141408)
58. Reynolds JN, Hyland BI, Wickens JR. 2001. A cellular mechanism of reward-related learning. Nature 413: 67-70. (Pubitemid 32843488)
59. Robbe D, Kopf M, Remaury A, Bockaert J, Manzoni OJ. 2002. Endogenous cannabinoids mediate long-term synaptic depression in the nucleus accumbens. Proc Natl Acad Sci 99: 8384-8388. (Pubitemid 34651061)
60. Robbe D, Montgomery SM, Thome A, Rueda-Orozco PE, McNaughton BL, Buzsaki G. 2006. Cannabinoids reveal importance of spike timing coordination in hippocampal function. Nat Neurosci 9: 1526-1533. (Pubitemid 44862661)
61. Robledo P, Feger J. 1990. Excitatory influence of rat subthalamic nucleus to substantia nigra pars reticulata and the pallidal complex: Electrophysiological data. Brain Res 518: 47-54. (Pubitemid 20197029)
62. Rommelfanger KS, Wichmann T. 2010. Extrastriatal dopaminergic circuits of the basal ganglia. Front Neuroanat 4: 139. doi: 10.3389/fnana.2010.00139.
63. Romo-Parra H, Misgeld U, Yanovsky Y. 2009. Regular firing of a single output neuron reduces its own inhibition through endocannabinoids in substantia nigra pars reticulata of juvenile mice. Neurosci 160: 596-605.
64. Rueda-Orozco PE, Mendoza E, Hernandez R, Aceves JJ, Ibanez-Sandoval O, Galarraga E, Bargas J. 2009. Diversity in long-term synaptic plasticity at inhibitory synapses of striatal spiny neurons. Learn Mem 16: 474-478.
65. Safo PK, Regehr WG. 2005. Endocannabinoids control the induction of cerebellar LTD. Neuron 48: 647-659. (Pubitemid 41654685)
66. Sarvestani IK, Lindahl M, Hellgren-Kotaleski J, Ekeberg O. 2011. The arbitration-extension hypothesis: A hierarchical interpretation of the functional organization of the Basal Ganglia. Front Syst Neurosci 5: 13. doi: 10.3389/dnaya.2011.00013.
67. Sergeeva OA, Doreulee N, Chepkova AN, Kazmierczak T, Haas HL. 2007. Long-term depression of cortico-striatal synaptic transmission by DHPG depends on endocannabinoid release and nitric oxide synthesis. Eur J Neurosci 26: 1889-1894. (Pubitemid 47493199)
68. Shen W, Flajolet M, Greengard P, Surmeier DJ. 2008. Dichotomous dopaminergic control of striatal synaptic plasticity. Science 321: 848-851.
69. Sjöström PJ, Rancz EA, Roth A, Häusser M. 2008. Dendritic excitability and synaptic plasticity. Physiol Rev 88: 769-840. (Pubitemid 351520092)
70. Smith Y, Bevan MD, Shink E, Bolam JP. 1998. Microcircuitry of the direct and indirect pathways of the basal ganglia. Neurosci 86: 353-387. (Pubitemid 28293917)
71. Surmeier DJ, Plotkin J, Shen W. 2009. Dopamine and synaptic plasticity in dorsal striatal circuits controlling action selection. Curr Op Neurobiol 19: 621-628.
72. Surmeier DJ, Carrillo-Reid L, Bargas J. 2011. Dopaminergic modulation of striatal neurons, circuits, and assemblies. Neuroscience. doi: 10.1016/j.neuroscience. 2011.08.051.
73. Szabadits E, Cserép C, Szonyi A, Fukazawa Y, Shigemoto R, Watanabe M, Itohara S, Freund TF, Nyiri G. 2011. NMDA receptors in hippocampal GABAergic synapses and their role in nitric oxide signaling. J Neurosci 31: 5893-5904.
74. Szabo B, Wallmichrath I, Mathonia P, Pfreundtner C. 2000. Cannabinoids inhibit excitatory neurotransmission in the substantia nigra pars reticulata. Neurosci 97: 89-97. (Pubitemid 30195879)
75. Takakusaki K, Habaguchi T, Ohtinata-Sugimoto J, Saitoh K, Sakamoto T. 2003. Basal ganglia efferents to the brainstem centers controlling postural muscle tone and locomotion: A new concept for understanding motor disorders in basal ganglia dysfunction. Neurosci 119: 293-308. (Pubitemid 36577431)
76. Takakusaki K, Oohinata-Sugimoto J, Saitoh K, Habaguchi T. 2004. Role of basal ganglia-brainstem systems in the control of postural muscle tone and locomotion. Prog Brain Res 143: 231-237. (Pubitemid 37442998)
77. Tecuapetla F, Carrillo-Reid L, Bargas J, Galarraga E. 2007. Dopaminergic modulation of short-term synaptic plasticity at striatal inhibitory synapses. Proc Natl Acad Sci 104: 10258-10263. (Pubitemid 47175296)
78. Tepper JM, Tecuapetla F, Koós T, Ibáñez-Sandoval O. 2010. Heterogeneity and diversity of striatal GABAergic interneurons. Front Neuroanat 4: 150. doi: 10.3389/fnana.2010.00150.
79. Tsou K, Brown S, Sanudo-Pena MC, Mackie K, Walker JM. 1998. Immunohistochemical distribution of cannabinoid CB1 receptors in the rat central nervous system. Neurosci 83: 393-411. (Pubitemid 28062631)
80. Wallmichrath I, Szabo B. 2002. Cannabinoids inhibit striatonigral GABAergic neurotransmission in the mouse. Neurosci 113: 671-682. (Pubitemid 34874691)
81. Wichmann T, DeLong MR. 2003. Functional neuroanatomy of the basal ganglia in Parkinson's disease. Adv Neurol 91: 9-18.
82. Wickens JR. 2009. Synaptic plasticity in the basal ganglia. Behav Brain Res 199: 119-128.
83. Xue JG, Masuoka T, Gong XD, Chen KS, Yanagawa Y, Law SK, Konishi S. 2011. NMDA receptor activation enhances inhibitory GABAergic transmission onto hippocampal pyramidal neurons via presynaptic and postsynaptic mechanisms. J Neurophysiol 105: 2897-2906.
84. Yanovsky Y, Mades S, Misgeld U. 2003. Retrograde signaling changes the venue of postsynaptic inhibition in rat substantia nigra. Neurosci 122: 317-328. (Pubitemid 37410163)
85. Yin HH, Knowlton BJ. 2006. The role of the basal ganglia in habit formation. Nat Rev Neurosci 7: 464-476. (Pubitemid 44012286)
86. Zhou FW, Jin Y, Matta SG, Xu M, Zhou FM. 2009. An ultra-short dopamine pathway regulates basal ganglia output. J Neurosci 29: 10424-10435.