Heterosynaptic regulation of external globus pallidus inputs to the subthalamic nucleus by the motor cortex

Neuron

Volumn 85, Issue 2, 2015, Pages 364-376

  Chu, Hong Yuan ^a   Atherton, Jeremy F ^a   Wokosin, David ^a   Surmeier, D James ^a   Bevan, Mark D ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; CYCLIC GMP DEPENDENT PROTEIN KINASE; DOPAMINE; GUANYLATE CYCLASE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; 4 AMINOBUTYRIC ACID; 4 AMINOBUTYRIC ACID RECEPTOR; GLUTAMIC ACID;

ADULT; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DOPAMINE BRAIN LEVEL; ELECTROSTIMULATION; GABAERGIC TRANSMISSION; GLOBUS PALLIDUS; HETEROSYNAPTIC REGULATION; HOMEOSTASIS; LONG TERM POTENTIATION; MALE; MOTOR CORTEX; MOUSE; NERVE CELL PLASTICITY; NERVE STIMULATION; NEUROMODULATION; NONHUMAN; OPTOGENETICS; POSTSYNAPTIC MEMBRANE; SIGNAL TRANSDUCTION; SUBTHALAMIC NUCLEUS; SYNAPTIC INHIBITION; SYNAPTIC TRANSMISSION; ANIMAL; METABOLISM; NERVE TRACT; PARKINSONISM; PATHOPHYSIOLOGY; PHYSIOLOGY;

ANIMALS; DOPAMINE; GABAERGIC NEURONS; GAMMA-AMINOBUTYRIC ACID; GLOBUS PALLIDUS; GLUTAMIC ACID; LONG-TERM POTENTIATION; MICE; MOTOR CORTEX; NEURAL PATHWAYS; NEURONAL PLASTICITY; OPTOGENETICS; PARKINSONIAN DISORDERS; RECEPTORS, GABA-A; RECEPTORS, N-METHYL-D-ASPARTATE; SUBTHALAMIC NUCLEUS; SYNAPTIC TRANSMISSION;

EID: 84921424407     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2014.12.022     Document Type: Article

References (70)

1. Afsharpour S. Topographical projections of the cerebral cortex to the subthalamic nucleus. J.Comp. Neurol. 1985, 236:14-28.
2. Albin R.L., Young A.B., Penney J.B. The functional anatomy of basal ganglia disorders. Trends Neurosci. 1989, 12:366-375.
3. Atherton J.F., Kitano K., Baufreton J., Fan K., Wokosin D., Tkatch T., Shigemoto R., Surmeier D.J., Bevan M.D. Selective participation of somatodendritic HCN channels in inhibitory but not excitatory synaptic integration in neurons of the subthalamic nucleus. J.Neurosci. 2010, 30:16025-16040.
4. Baufreton J., Atherton J.F., Surmeier D.J., Bevan M.D. Enhancement of excitatory synaptic integration by GABAergic inhibition in the subthalamic nucleus. J.Neurosci. 2005, 25:8505-8517.
5. Baufreton J., Kirkham E., Atherton J.F., Menard A., Magill P.J., Bolam J.P., Bevan M.D. Sparse but selective and potent synaptic transmission from the globus pallidus to the subthalamic nucleus. J.Neurophysiol. 2009, 102:532-545.
6. Baunez C., Nieoullon A., Amalric M. In a rat model of parkinsonism, lesions of the subthalamic nucleus reverse increases of reaction time but induce a dramatic premature responding deficit. J.Neurosci. 1995, 15:6531-6541.
7. Bevan M.D., Bolam J.P. Cholinergic, GABAergic, and glutamate-enriched inputs from the mesopontine tegmentum to the subthalamic nucleus in the rat. J.Neurosci. 1995, 15:7105-7120.
8. Bevan M.D., Magill P.J., Hallworth N.E., Bolam J.P., Wilson C.J. Regulation of the timing and pattern of action potential generation in rat subthalamic neurons invitro by GABA-A IPSPs. J.Neurophysiol. 2002, 87:1348-1362.
9. Castillo P.E., Chiu C.Q., Carroll R.C. Long-term plasticity at inhibitory synapses. Curr. Opin. Neurobiol. 2011, 21:328-338.
10. Chan C.S., Glajch K.E., Gertler T.S., Guzman J.N., Mercer J.N., Lewis A.S., Goldberg A.B., Tkatch T., Shigemoto R., Fleming S.M., et al. HCN channelopathy in external globus pallidus neurons in models of Parkinson's disease. Nat. Neurosci. 2011, 14:85-92.
11. Chevalier G., Deniau J.M. Disinhibition as a basic process in the expression of striatal functions. Trends Neurosci. 1990, 13:277-280.
12. Clements J.D., Silver R.A. Unveiling synaptic plasticity: a new graphical and analytical approach. Trends Neurosci. 2000, 23:105-113.
13. Coizet V., Graham J.H., Moss J., Bolam J.P., Savasta M., McHaffie J.G., Redgrave P., Overton P.G. Short-latency visual input to the subthalamic nucleus is provided by the midbrain superior colliculus. J.Neurosci. 2009, 29:5701-5709.
14. Day M., Wang Z., Ding J., An X., Ingham C.A., Shering A.F., Wokosin D., Ilijic E., Sun Z., Sampson A.R., et al. Selective elimination of glutamatergic synapses on striatopallidal neurons in Parkinson disease models. Nat. Neurosci. 2006, 9:251-259.
15. Fan K.Y., Baufreton J., Surmeier D.J., Chan C.S., Bevan M.D. Proliferation of external globus pallidus-subthalamic nucleus synapses following degeneration of midbrain dopamine neurons. J.Neurosci. 2012, 32:13718-13728.
16. Fujimoto K., Kita H. Response characteristics of subthalamic neurons to the stimulation of the sensorimotor cortex in the rat. Brain Res. 1993, 609:185-192.
17. Galvan A., Wichmann T. Pathophysiology of parkinsonism. Clin. Neurophysiol. 2008, 119:1459-1474.
18. Gerfen C.R., Surmeier D.J. Modulation of striatal projection systems by dopamine. Annu. Rev. Neurosci. 2011, 34:441-466.
19. Gittis A.H., Hang G.B., LaDow E.S., Shoenfeld L.R., Atallah B.V., Finkbeiner S., Kreitzer A.C. Rapid target-specific remodeling of fast-spiking inhibitory circuits after loss of dopamine. Neuron 2011, 71:858-868.
20. Goldberg J.A., Boraud T., Maraton S., Haber S.N., Vaadia E., Bergman H. Enhanced synchrony among primary motor cortex neurons in the 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine primate model of Parkinson's disease. J.Neurosci. 2002, 22:4639-4653.
21. B receptors. J.Neurosci. 2005, 25:6304-6315.
22. Hallworth N.E., Wilson C.J., Bevan M.D. Apamin-sensitive small conductance calcium-activated potassium channels, through their selective coupling to voltage-gated calcium channels, are critical determinants of the precision, pace, and pattern of action potential generation in rat subthalamic nucleus neurons invitro. J.Neurosci. 2003, 23:7525-7542.
23. Hammond C., Bergman H., Brown P. Pathological synchronization in Parkinson's disease: networks, models and treatments. Trends Neurosci. 2007, 30:357-364.
24. Hikosaka O., Takikawa Y., Kawagoe R. Role of the basal ganglia in the control of purposive saccadic eye movements. Physiol. Rev. 2000, 80:953-978.
25. Holgado A.J., Terry J.R., Bogacz R. Conditions for the generation of beta oscillations in the subthalamic nucleus-globus pallidus network. J.Neurosci. 2010, 30:12340-12352.
26. Isomura Y., Harukuni R., Takekawa T., Aizawa H., Fukai T. Microcircuitry coordination of cortical motor information in self-initiation of voluntary movements. Nat. Neurosci. 2009, 12:1586-1593.
27. Jenkinson N., Brown P. New insights into the relationship between dopamine, beta oscillations and motor function. Trends Neurosci. 2011, 34:611-618.
28. Jonas P. Glutamate receptors in the central nervous system. Ann. N Y Acad. Sci. 1993, 707:126-135.
29. Kita T., Kita H. The subthalamic nucleus is one of multiple innervation sites for long-range corticofugal axons: a single-axon tracing study in the rat. J.Neurosci. 2012, 32:5990-5999.
30. Kravitz A.V., Freeze B.S., Parker P.R., Kay K., Thwin M.T., Deisseroth K., Kreitzer A.C. Regulation of parkinsonian motor behaviours by optogenetic control of basal ganglia circuitry. Nature 2010, 466:622-626.
31. Kurotani T., Yamada K., Yoshimura Y., Crair M.C., Komatsu Y. State-dependent bidirectional modification of somatic inhibition in neocortical pyramidal cells. Neuron 2008, 57:905-916.
32. Lange M.D., Doengi M., Lesting J., Pape H.C., Jüngling K. Heterosynaptic long-term potentiation at interneuron-principal neuron synapses in the amygdala requires nitric oxide signalling. J.Physiol. 2012, 590:131-143.
33. Lu W., Man H., Ju W., Trimble W.S., MacDonald J.F., Wang Y.T. Activation of synaptic NMDA receptors induces membrane insertion of new AMPA receptors and LTP in cultured hippocampal neurons. Neuron 2001, 29:243-254.
34. A receptor trafficking-mediated plasticity of inhibitory synapses. Neuron 2011, 70:385-409.
35. Magill P.J., Bolam J.P., Bevan M.D. Dopamine regulates the impact of the cerebral cortex on the subthalamic nucleus-globus pallidus network. Neuroscience 2001, 106:313-330.
36. Malenka R.C., Nicoll R.A. Long-term potentiation-a decade of progress?. Science 1999, 285:1870-1874.
37. Mallet N., Ballion B., Le Moine C., Gonon F. Cortical inputs and GABA interneurons imbalance projection neurons in the striatum of parkinsonian rats. J.Neurosci. 2006, 26:3875-3884.
38. Mallet N., Pogosyan A., Márton L.F., Bolam J.P., Brown P., Magill P.J. Parkinsonian beta oscillations in the external globus pallidus and their relationship with subthalamic nucleus activity. J.Neurosci. 2008, 28:14245-14258.
39. Mallet N., Pogosyan A., Sharott A., Csicsvari J., Bolam J.P., Brown P., Magill P.J. Disrupted dopamine transmission and the emergence of exaggerated beta oscillations in subthalamic nucleus and cerebral cortex. J.Neurosci. 2008, 28:4795-4806.
40. Mallet N., Micklem B.R., Henny P., Brown M.T., Williams C., Bolam J.P., Nakamura K.C., Magill P.J. Dichotomous organization of the external globus pallidus. Neuron 2012, 74:1075-1086.
41. Marsden K.C., Beattie J.B., Friedenthal J., Carroll R.C. NMDA receptor activation potentiates inhibitory transmission through GABA receptor-associated protein-dependent exocytosis of GABA(A) receptors. J.Neurosci. 2007, 27:14326-14337.
42. Maurice N., Deniau J.M., Glowinski J., Thierry A.M. Relationships between the prefrontal cortex and the basal ganglia in the rat: physiology of the corticosubthalamic circuits. J.Neurosci. 1998, 18:9539-9546.
43. Maurice N., Deniau J.M., Glowinski J., Thierry A.M. Relationships between the prefrontal cortex and the basal ganglia in the rat: physiology of the cortico-nigral circuits. J.Neurosci. 1999, 19:4674-4681.
44. Mink J.W., Thach W.T. Basal ganglia intrinsic circuits and their role in behavior. Curr. Opin. Neurobiol. 1993, 3:950-957.
45. Monakow K.H., Akert K., Künzle H. Projections of the precentral motor cortex and other cortical areas of the frontal lobe to the subthalamic nucleus in the monkey. Exp. Brain Res. 1978, 33:395-403.
46. Moran R.J., Mallet N., Litvak V., Dolan R.J., Magill P.J., Friston K.J., Brown P. Alterations in brain connectivity underlying beta oscillations in Parkinsonism. PLoS Comput. Biol. 2011, 7:e1002124.
47. Nambu A., Tokuno H., Takada M. Functional significance of the cortico-subthalamo-pallidal 'hyperdirect' pathway. Neurosci. Res. 2002, 43:111-117.
48. Nisbet A.P., Foster O.J., Kingsbury A., Lees A.J., Marsden C.D. Nitric oxide synthase mRNA expression in human subthalamic nucleus, striatum and globus pallidus: implications for basal ganglia function. Brain Res. Mol. Brain Res. 1994, 22:329-332.
49. Nugent F.S., Penick E.C., Kauer J.A. Opioids block long-term potentiation of inhibitory synapses. Nature 2007, 446:1086-1090.
50. Otsuka T., Murakami F., Song W.J. Excitatory postsynaptic potentials trigger a plateau potential in rat subthalamic neurons at hyperpolarized states. J.Neurophysiol. 2001, 86:1816-1825.
51. Ouardouz M., Sastry B.R. Mechanisms underlying LTP of inhibitory synaptic transmission in the deep cerebellar nuclei. J.Neurophysiol. 2000, 84:1414-1421.
52. A synaptic transmission. J.Physiol. 2003, 553:155-167.
53. Paz J.T., Deniau J.M., Charpier S. Rhythmic bursting in the cortico-subthalamo-pallidal network during spontaneous genetically determined spike and wave discharges. J.Neurosci. 2005, 25:2092-2101.
54. Peng Y.R., Zeng S.Y., Song H.L., Li M.Y., Yamada M.K., Yu X. Postsynaptic spiking homeostatically induces cell-autonomous regulation of inhibitory inputs via retrograde signaling. J.Neurosci. 2010, 30:16220-16231.
55. Pifarré P., García A., Mengod G. Species differences in the localization of soluble guanylyl cyclase subunits in monkey and rat brain. J.Comp. Neurol. 2007, 500:942-957.
56. Shen K.Z., Johnson S.W. Dopamine depletion alters responses to glutamate and GABA in the rat subthalamic nucleus. Neuroreport 2005, 16:171-174.
57. Shimamoto S.A., Ryapolova-Webb E.S., Ostrem J.L., Galifianakis N.B., Miller K.J., Starr P.A. Subthalamic nucleus neurons are synchronized to primary motor cortex local field potentials in Parkinson's disease. J.Neurosci. 2013, 33:7220-7233.
58. Smith K.R., Kittler J.T. The cell biology of synaptic inhibition in health and disease. Curr. Opin. Neurobiol. 2010, 20:550-556.
59. Smith Y., Bolam J.P., Von Krosigk M. Topographical and synaptic organization of the GABA-containing pallidosubthalamic projection in the rat. Eur. J. Neurosci. 1990, 2:500-511.
60. Smith Y., Bevan M.D., Shink E., Bolam J.P. Microcircuitry of the direct and indirect pathways of the basal ganglia. Neuroscience 1998, 86:353-387.
61. Tachibana Y., Kita H., Chiken S., Takada M., Nambu A. Motor cortical control of internal pallidal activity through glutamatergic and GABAergic inputs in awake monkeys. Eur. J. Neurosci. 2008, 27:238-253.
62. Tachibana Y., Iwamuro H., Kita H., Takada M., Nambu A. Subthalamo-pallidal interactions underlying parkinsonian neuronal oscillations in the primate basal ganglia. Eur. J. Neurosci. 2011, 34:1470-1484.
63. Tennant K.A., Adkins D.L., Donlan N.A., Asay A.L., Thomas N., Kleim J.A., Jones T.A. The organization of the forelimb representation of the C57BL/6 mouse motor cortex as defined by intracortical microstimulation and cytoarchitecture. Cereb. Cortex 2011, 21:865-876.
64. Terman D., Rubin J.E., Yew A.C., Wilson C.J. Activity patterns in a model for the subthalamopallidal network of the basal ganglia. J.Neurosci. 2002, 22:2963-2976.
65. Tsien J.Z., Chen D.F., Gerber D., Tom C., Mercer E.H., Anderson D.J., Mayford M., Kandel E.R., Tonegawa S. Subregion- and cell type-restricted gene knockout in mouse brain. Cell 1996, 87:1317-1326.
66. Turrigiano G. Too many cooks? Intrinsic and synaptic homeostatic mechanisms in cortical circuit refinement. Annu. Rev. Neurosci. 2011, 34:89-103.
67. A) receptors, gephyrin and homeostatic synaptic plasticity. J.Physiol. 2010, 588:101-106.
68. Vithlani M., Terunuma M., Moss S.J. The dynamic modulation of GABA(A) receptor trafficking and its role in regulating the plasticity of inhibitory synapses. Physiol. Rev. 2011, 91:1009-1022.
69. Wang L., Kitai S.T., Xiang Z. Activity-dependent bidirectional modification of inhibitory synaptic transmission in rat subthalamic neurons. J.Neurosci. 2006, 26:7321-7327.
70. West M.J. Stereological methods for estimating the total number of neurons and synapses: issues of precision and bias. Trends Neurosci. 1999, 22:51-61.