Selective participation of somatodendritic HCN channels in inhibitory but not excitatory synaptic integration in neurons of the subthalamic nucleus

Journal of Neuroscience

Volumn 30, Issue 47, 2010, Pages 16025-16040

  Atherton, Jeremy F ^a   Kitano, Katsunori ^b,c   Baufreton, Jerome ^d   Fan, Kai ^b   Wokosin, David ^a   Tkatch, Tatiana ^a,e   Shigemoto, Ryuichi ^f   Surmeier, D James ^a   Bevan, Mark D ^a,b  

^a NORTHWESTERN UNIVERSITY   (United States)

^b UNIVERSITY OF SHEFFIELD   (United Kingdom)

^c RITSUMEIKAN UNIVERSITY   (Japan)

^d UMR 5287   (France)

^e ISTITUTO ITALIANO DI TECNOLOGIA   (Italy)

^f GRADUATE UNIVERSITY FOR ADVANCED STUDIES   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; CALCIUM CHANNEL; CYCLIC NUCLEOTIDE GATED CHANNEL; CYCLIC NUCLEOTIDE GATED CHANNEL 2; CYCLIC NUCLEOTIDE GATED CHANNEL 3; GLUTAMIC ACID; MESSENGER RNA; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN NERVE CELL; CONTROLLED STUDY; ELECTRIC POTENTIAL; ELECTRON MICROSCOPY; HYPERPOLARIZATION; MALE; MICROSCOPY; NERVE CELL MEMBRANE; NERVOUS SYSTEM ELECTROPHYSIOLOGY; NEUROIMAGING; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RAT; SUBTHALAMIC NUCLEUS; SYNAPTIC TRANSMISSION;

ANIMALS; DENDRITES; EXCITATORY POSTSYNAPTIC POTENTIALS; ION CHANNELS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NEURAL INHIBITION; NEURONS; PYRIMIDINES; RATS; RATS, SPRAGUE-DAWLEY; RATS, WISTAR; SUBTHALAMIC NUCLEUS; SYNAPTIC TRANSMISSION;

EID: 78649432574     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3898-10.2010     Document Type: Article

References (74)

1. Afsharpour S (1985) Light microscopic analysis of Golgi-impregnated rat subthalamic neurons. J Comp Neurol 236:1-13.
2. h distribution in dendrites of mammalian neurons. J Neurosci 27:8643-8653.
3. Atherton JF, Wokosin DL, Ramanathan S, Bevan MD (2008) Autonomous initiation and propagation of action potentials in neurons of the subthalamic nucleus. J Physiol 586:5679-5700.
4. Baruscotti M, DiFrancesco D (2004) Pacemaker channels. Ann N Y Acad Sci 1015:111-121.
5. Baufreton J, Bevan MD (2008) D2-like dopamine receptor-mediated modulation of activity-dependent plasticity at GABAergic synapses in the subthalamic nucleus. J Physiol 586:2121-2142.
6. Baufreton J, Atherton JF, Surmeier DJ, Bevan MD (2005) Enhancement of excitatory synaptic integration by GABAergic inhibition in the subthalamic nucleus. J Neurosci 25:8505-8517.
7. Baufreton J, Kirkham E, Atherton JF, Menard A, Magill PJ, Bolam JP, Bevan MD (2009) Sparse but selective and potent synaptic transmission from the globus pallidus to the subthalamic nucleus. J Neurophysiol 102:532-545.
8. Baunez C, Nieoullon A, Amalric M (1995) 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 15:6531-6541.
9. Bennett BD, Callaway JC, Wilson CJ (2000) Intrinsic membrane properties underlying spontaneous tonic firing in neostriatal cholinergic interneurons. J Neurosci 20:8493-8503.
10. Bergman H, Wichmann T, Karmon B, DeLong MR (1994) The primate subthalamic nucleus. II. Neuronal activity in the MPTP model of parkinsonism. J Neurophysiol 72:507-520.
11. Beurrier C, Congar P, Bioulac B, Hammond C (1999) Subthalamic nucleus neurons switch from single-spike activity to burst-firing mode. J Neurosci 19:599-609.
12. Beurrier C, Bioulac B, Hammond C (2000) Slowly inactivating sodium current (INaP) underlies single-spike activity in rat subthalamic neurons. J Neurophysiol 83:1951-1957. (Pubitemid 30198651)
13. Bevan MD, Wilson CJ (1999) Mechanisms underlying spontaneous oscillation and rhythmic firing in rat subthalamic neurons. J Neurosci 19:7617-7628.
14. Bevan MD, Wilson CJ, Bolam JP, Magill PJ (2000) Equilibrium potential of GABA(A) current and implications for rebound burst firing in rat subthalamic neurons in vitro. J Neurophysiol 83:3169-3172.
15. Bevan MD, Magill PJ, Hallworth NE, Bolam JP, Wilson CJ (2002) Regulation of the timing and pattern of action potential generation in rat subthalamic neurons in vitro by GABA-A IPSPs. J Neurophysiol 87:1348-1362.
16. Bevan MD, Atherton JF, Baufreton J (2006) Cellular principles underlying normal and pathological activity in the subthalamic nucleus. Curr Opin Neurobiol 16:621-628.
17. Biel M, Wahl-Schott C, Michalakis S, Zong X (2009) Hyperpolarization- activated cation channels: from genes to function. Physiol Rev 89:847-885.
18. Boyes J, Bolam JP, Shigemoto R, Stanford IM (2007) Functional presynaptic HCN channels in the rat globus pallidus. Eur J Neurosci 25:2081-2092.
19. Brown P (2003) Oscillatory nature of human basal ganglia activity: relationship to the pathophysiology of Parkinson's disease. Mov Disord 18:357-363.
20. Bullis JB, Jones TD, Poolos NP (2007) Reversed somatodendritic I(h) gradient in a class of rat hippocampal neurons with pyramidal morphology. J Physiol 579:431-443.
21. Chan CS, Shigemoto R, Mercer JN, Surmeier DJ (2004) HCN2 and HCN1 channels govern the regularity of autonomous pacemaking and synaptic resetting in globus pallidus neurons. J Neurosci 24:9921-9932.
22. Chevaleyre V, Castillo PE (2002) Assessing the role of Ih channels in synaptic transmission and mossy fiber LTP. Proc Natl Acad Sci U S A 99:9538-9543.
23. Crossman AR (2000) Functional anatomy of movement disorders. J Anat 196:519-525.
24. Crossman AR, Sambrook MA, Jackson A (1984) Experimental hemichorea/hemiballismus in the monkey. Studies on the intracerebral site of action in a drug-induced dyskinesia. Brain 107:579-596.
25. DeLong MR (1990) Primate models of movement disorders of basal ganglia origin. Trends Neurosci 13:281-285.
26. Destexhe A, Mainen ZF, Sejnowski TJ (1998) Kinetic models of synaptic transmission. In: Methods in neural modeling (Koch C, Segev I, eds), pp 1-25. Cambridge, MA: MIT.
27. Do MT, Bean BP (2003) Subthreshold sodium currents and pacemaking of subthalamic neurons: modulation by slow inactivation. Neuron 39:109-120.
28. Twindow. J Neurosci 30:99-109.
29. Fan Y, Fricker D, Brager DH, Chen X, Lu HC, Chitwood RA, Johnston D (2005) Activity-dependent decrease of excitability in rat hippocampal neurons through increases in I(h). Nat Neurosci 8:1542-1551. (Pubitemid 41573669)
30. 2+ channel activity and regulates sperm function. Biochem Biophys Res Commun 311:187-192.
31. François C, Savy C, Jan C, Tande D, Hirsch EC, Yelnik J (2000) Dopaminergic innervation of the subthalamic nucleus in the normal state, in MPTP-treated monkeys, and in Parkinson's disease patients. J Comp Neurol 425:121-129.
32. Garden DL, Dodson PD, O'Donnell C, White MD, Nolan MF (2008) Tuning of synaptic integration in the medial entorhinal cortex to the organization of grid cell firing fields. Neuron 60:875-889.
33. Gillies A, Willshaw D (2006) Membrane channel interactions underlying rat subthalamic projection neuron rhythmic and bursting activity. J Neurophysiol 95:2352-2365.
34. Halliwell JV, Adams PR (1982) Voltage-clamp analysis of muscarinic excitation in hippocampal neurons. Brain Res 250:71-92.
35. B receptors. J Neurosci 25:6304-6315.
36. Hallworth NE, Wilson CJ, Bevan MD (2003) 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 in vitro. J Neurosci 23:7525-7542.
37. Holderith NB, Shigemoto R, Nusser Z (2003) Cell type-dependent expression of HCN1 in the main olfactory bulb. Eur J Neurosci 18:344-354.
38. Karachi C, Grabli D, Baup N, Mounayar S, Tandé D, François C, Hirsch EC (2009) Dysfunction of the subthalamic nucleus induces behavioral and movement disorders in monkeys. Mov Disord 24:1183-1192.
39. Kass JI, Mintz IM (2006) Silent plateau potentials, rhythmic bursts, and pacemaker firing: three patterns of activity that coexist in quadristable subthalamic neurons. Proc Natl Acad Sci U S A 103:183-188.
40. Kita H, Chang HT, Kitai ST (1983) The morphology of intracellularly labeled rat subthalamic neurons: a light microscopic analysis. J Comp Neurol 215:245-257.
41. Kole MH, Bräuer AU, Stuart GJ (2007) Inherited cortical HCN1 channel loss amplifies dendritic calcium electrogenesis and burst firing in a rat absence epilepsy model. J Physiol 578:507-525.
42. Levy R, Hutchison WD, Lozano AM, Dostrovsky JO (2002) Synchronized neuronal discharge in the basal ganglia of parkinsonian patients is limited to oscillatory activity. J Neurosci 22:2855-2861. (Pubitemid 37465834)
43. London M, Häusser M (2005) Dendritic computation. Annu Rev Neurosci 28:503-532.
44. Lörincz A, Notomi T, Tamás G, Shigemoto R, Nusser Z (2002) Polarized and compartment-dependent distribution of HCN1 in pyramidal cell dendrites. Nat Neurosci 5:1185-1193.
45. Ludwig A, Budde T, Stieber J, Moosmang S, Wahl C, Holthoff K, Langebartels A, Wotjak C, Munsch T, Zong X, Feil S, Feil R, Lancel M, Chien KR, Konnerth A, Pape HC, Biel M, Hofmann F (2003) Absence epilepsy and sinus dysrhythmia in mice lacking the pacemaker channel HCN2. EMBO J 22:216-224.
46. Ludwin SK (1979) The perineuronal satellite oligodendrocyte. A role in remyelination. Acta Neuropathol 47:49-53.
47. Lüthi A, McCormick DA (1998) Periodicity of thalamic synchronized oscillations: the role of Ca2+-mediated upregulation of Ih. Neuron 20:553-563.
48. Magee JC (1998) Dendritic hyperpolarization-activated currents modify the integrative properties of hippocampal CA1 pyramidal neurons. J Neurosci 18:7613-7624.
49. Magee JC (1999) Dendritic lh normalizes temporal summation in hippocampal CA1 neurons. Nat Neurosci 2:508-514.
50. Magill PJ, Bolam JP, Bevan MD (2001) Dopamine regulates the impact of the cerebral cortex on the subthalamic nucleus-globus pallidus network. Neuroscience 106:313-330.
51. Meurers BH, Dziewczapolski G, Bittner A, Shi T, Kamme F, Shults CW (2009) Dopamine depletion induced up-regulation of HCN3 enhances rebound excitability of basal ganglia output neurons. Neurobiol Dis 34:178-188.
52. Monteggia LM, Eisch AJ, Tang MD, Kaczmarek LK, Nestler EJ (2000) Cloning and localization of the hyperpolarization-activated cyclic nucleotide-gated channel family in rat brain. Brain Res Mol Brain Res 81:129-139.
53. Notomi T, Shigemoto R (2004) Immunohistochemical localization of Ih channel subunits, HCN1-4, in the rat brain. J Comp Neurol 471:241-276.
54. Otsuka T, Murakami F, Song WJ (2001) Excitatory postsynaptic potentials trigger a plateau potential in rat subthalamic neurons at hyperpolarized states. J Neurophysiol 86:1816-1825.
55. Otsuka T, Abe T, Tsukagawa T, Song WJ (2004) Conductance-based model of the voltage-dependent generation of a plateau potential in subthalamic neurons. J Neurophysiol 92:255-264.
56. Pape HC, McCormick DA (1989) Noradrenaline and serotonin selectively modulate thalamic burst firing by enhancing a hyperpolarization-activated cation current. Nature 340:715-718.
57. v2.2 channels. J Neurophysiol 99:442-459.
58. Raz A, Vaadia E, Bergman H (2000) Firing patterns and correlations of spontaneous discharge of pallidal neurons in the normal and the tremulous 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine vervet model of parkinsonism. J Neurosci 20:8559-8571.
59. Robinson RB, Siegelbaum SA (2003) Hyperpolarization-activated cation currents: from molecules to physiological function. Annu Rev Physiol 65:453-480.
60. Santoro B, Chen S, Lüthi A, Pavlidis P, Shumyatsky GP, Tibbs GR, Siegelbaum SA (2000) Molecular and functional heterogeneity of hyperpolarization-activated pacemaker channels in the mouse CNS. J Neurosci 20:5264-5275.
61. Shah MM, Anderson AE, Leung V, Lin X, Johnston D (2004) Seizure-induced plasticity of h channels in entorhinal cortical layer III pyramidal neurons. Neuron 44:495-508.
62. Shen KZ, Johnson SW (2005) Dopamine depletion alters responses to glutamate and GABA in the rat subthalamic nucleus. Neuroreport 16:171-174.
63. Shin M, Brager D, Jaramillo TC, Johnston D, Chetkovich DM (2008) Mislocalization of h channel subunits underlies h channelopathy in temporal lobe epilepsy. Neurobiol Dis 32:26-36.
64. Tachibana Y, Kita H, Chiken S, Takada M, Nambu A (2008) Motor cortical control of internal pallidal activity through glutamatergic and GABAergic inputs in awake monkeys. Eur J Neurosci 27:238-253.
65. + current amplitude are linearly related in basal ganglia and basal forebrain neurons. J Neurosci 20:579-588.
66. Tsay D, Dudman JT, Siegelbaum SA (2007) HCN1 channels constrain synaptically evoked Ca2+ spikes in distal dendrites of CA1 pyramidal neurons. Neuron 56:1076-1089.
67. Tsodyks MV, Markram H (1997) The neural code between neocortical pyramidal neurons depends on neurotransmitter release probability. Proc Natl Acad Sci U S A 94:719-723.
68. Urbain N, Gervasoni D, Soulière F, Lobo L, Rentéro N, Windels F, Astier B, Savasta M, Fort P, Renaud B, Luppi PH, Chouvet G (2000) Unrelated course of subthalamic nucleus and globus pallidus neuronal activities across vigilance states in the rat. Eur J Neurosci 12:3361-3374.
69. Wichmann T, DeLong MR (2003) Pathophysiology of Parkinson's disease: the MPTP primate model of the human disorder. Ann N Y Acad Sci 991:199-213.
70. Wichmann T, Bergman H, DeLong MR (1994) The primate subthalamic nucleus. III. Changes in motor behavior and neuronal activity in the internal pallidum induced by subthalamic inactivation in the MPTP model of parkinsonism. J Neurophysiol 72:521-530.
71. Williams SR, Mitchell SJ (2008) Direct measurement of somatic voltage clamp errors in central neurons. Nat Neurosci 11:790-798.
72. Williams SR, Stuart GJ (2000) Site independence of EPSP time course is mediated by dendritic I(h) in neocortical pyramidal neurons. J Neurophysiol 83:3177-3182.
73. Williams SR, Stuart GJ (2003) Voltage- and site-dependent control of the somatic impact of dendritic IPSPs. J Neurosci 23:7358-7367.
74. Williams SR, Christensen SR, Stuart GJ, Häusser M (2002) Membrane potential bistability is controlled by the hyperpolarization-activated current I(H) in rat cerebellar Purkinje neurons in vitro. J Physiol 539:469-483.