HCN channelopathy in external globus pallidus neurons in models of Parkinson's disease

Nature Neuroscience

Volumn 14, Issue 1, 2011, Pages 85-94

  Chan, C Savio ^a   Glajch, Kelly E ^a   Gertler, Tracy S ^a   Guzman, Jaime N ^a   Mercer, Jeff N ^a,f   Lewis, Alan S ^a   Goldberg, Alan B ^a   Tkatch, Tatiana ^a,g   Shigemoto, Ryuichi ^b   Fleming, Sheila M ^c   Chetkovich, Dane M ^a   Osten, Pavel ^a,d   Kita, Hitoshi ^e   Surmeier, D James ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

^b NATIONAL INSTITUTE FOR PHYSIOLOGICAL SCIENCES   (Japan)

^c UNIVERSITY OF CINCINNATI   (United States)

^d Howard Hughes Medical Institute Cold Spring Harbor Laboratory Cold Spring Harbor   (United States)

^e UNIVERSITY OF TENNESSEE COLLEGE OF MEDICINE   (United States)

^f UNIVERSITY OF CALIFORNIA   (United States)

^g ISTITUTO ITALIANO DI TECNOLOGIA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC NUCLEOTIDE GATED CHANNEL; DOPAMINE; ION CHANNEL;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN NERVE CELL; CHANNELOPATHY; CONTROLLED STUDY; DOPAMINE DEFICIENT MOUSE; DOWN REGULATION; GLOBUS PALLIDUS; HYPERPOLARIZATION; MALE; MOTOR DYSFUNCTION; MOUSE; NONHUMAN; PACEMAKER NERVE CELL; PARKINSON DISEASE; PATHOPHYSIOLOGY; PRIORITY JOURNAL; RAT;

ANIMALS; CALCIUM; CHANNELOPATHIES; DEPENDOVIRUS; DISEASE MODELS, ANIMAL; DOPAMINE; DOWN-REGULATION; GENETIC VECTORS; GLOBUS PALLIDUS; ION CHANNELS; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICROINJECTIONS; NEURONS; OXIDOPAMINE; PARKINSON DISEASE; SUBSTANTIA NIGRA;

EID: 78650677330     PISSN: 10976256     EISSN: None     Source Type: Journal    
DOI: 10.1038/nn.2692     Document Type: Article

References (47)

1. DeLong, M.R. & Wichmann, T. Circuits and circuit disorders of the basal ganglia. Arch. Neurol. 64, 20-24 (2007). (Pubitemid 46072419)
2. Hammond, C., Bergman, H. & Brown, P. Pathological synchronization in Parkinson's disease: networks, models and treatments. Trends Neurosci. 30, 357-364 (2007).
3. Rivlin-Etzion, M. et al. Basal ganglia oscillations and pathophysiology of movement disorders. Curr. Opin. Neurobiol. 16, 629-637 (2006).
4. Graybiel, A.M. Habits, rituals, and the evaluative brain. Annu. Rev. Neurosci. 31, 359-387 (2008).
5. DeLong, M.R. Activity of pallidal neurons during movement. J. Neurophysiol. 34, 414-427 (1971).
6. Chan, C.S., Shigemoto, R., Mercer, J.N. & Surmeier, D.J. HCN2 and HCN1 channels govern the regularity of autonomous pacemaking and synaptic resetting in globus pallidus neurons. J. Neurosci. 24, 9921-9932 (2004).
7. Stanford, I.M. Independent neuronal oscillators of the rat globus pallidus. J. Neurophysiol. 89, 1713-1717 (2003).
8. Kita, H. & Kitai, S.T. Intracellular study of rat globus pallidus neurons: membrane properties and responses to neostriatal, subthalamic and nigral stimulation. Brain Res. 564, 296-305 (1991).
9. Nambu, A. & Llinas, R. Electrophysiology of globus pallidus neurons in vitro. J. Neurophysiol. 72, 1127-1139 (1994).
10. Bevan, M.D., Magill, P.J., Terman, D., Bolam, J.P. & Wilson, C.J. Move to the rhythm: oscillations in the subthalamic nucleus-external globus pallidus network. Trends Neurosci. 25, 525-531 (2002).
11. Obeso, J.A. et al. Pathophysiology of the basal ganglia in Parkinson's disease. Trends Neurosci. 23, S8-S19 (2000).
12. Walters, J.R., Ruskin, D.N., Allers, K.A. & Bergstrom, D.A. Pre-and postsynaptic aspects of dopamine-mediated transmission. Trends Neurosci. 23, S41-S47 (2000).
13. 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. 26, 3875-3884 (2006).
14. 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. 22, 2963-2976 (2002).
15. Gillies, A., Willshaw, D. & Li, Z. Subthalamic-pallidal interactions are critical in determining normal and abnormal functioning of the basal ganglia. Proc. R. Soc. Lond. B 269, 545-551 (2002).
16. Surmeier, D.J., Mercer, J.N. & Chan, C.S. Autonomous pacemakers in the basal ganglia: who needs excitatory synapses anyway? Curr. Opin. Neurobiol. 15, 312-318 (2005).
17. Mercer, J.N., Chan, C.S., Tkatch, T., Held, J. & Surmeier, D.J. Nav1.6 sodium channels are critical to pacemaking and fast spiking in globus pallidus neurons. J. Neurosci. 27, 13552-13566 (2007).
18. Zhang, W. & Linden, D.J. The other side of the engram: experience-driven changes in neuronal intrinsic excitability. Nat. Rev. Neurosci. 4, 885-900 (2003).
19. Turrigiano, G.G. & Nelson, S.B. Homeostatic plasticity in the developing nervous system. Nat. Rev. Neurosci. 5, 97-107 (2004).
20. Iancu, R., Mohapel, P., Brundin, P. & Paul, G. Behavioral characterization of a unilateral 6-OHDA-lesion model of Parkinson's disease in mice. Behav. Brain Res. 162, 1-10 (2005).
21. Schallert, T., Fleming, S.M., Leasure, J.L., Tillerson, J.L. & Bland, S.T. CNS plasticity and assessment of forelimb sensorimotor outcome in unilateral rat models of stroke, cortical ablation, parkinsonism and spinal cord injury. Neuropharmacology 39, 777-787 (2000).
22. Albin, R.L., Young, A.B. & Penney, J.B. The functional anatomy of basal ganglia disorders. Trends Neurosci. 12, 366-375 (1989).
23. Shin, R.M. et al. Dopamine D4 receptor-induced postsynaptic inhibition of GABAergic currents in mouse globus pallidus neurons. J. Neurosci. 23, 11662-11672 (2003).
24. Cooper, A.J. & Stanford, I.M. Dopamine D2 receptor mediated presynaptic inhibition of striatopallidal GABA(A) IPSCs in vitro. Neuropharmacology 41, 62-71 (2001).
25. Watanabe, K. Kita, T. & Kita, H. Presynaptic actions of D2-like receptors in the rat cortico-striato-globus pallidus disynaptic connection in vitro. J. Neurophysiol 101, 665-671 (2009).
26. Chan, C.S. et al. 'Rejuvenation' protects neurons in mouse models of Parkinson's disease. Nature 447, 1081-1086 (2007).
27. Biel, M., Wahl-Schott, C., Michalakis, S. & Zong, X. Hyperpolarization-activated cation channels: from genes to function. Physiol. Rev. 89, 847-885 (2009).
28. Lewis, A.S. et al. Alternatively spliced isoforms of TRIP8b differentially control h channel traffcking and function. J. Neurosci. 29, 6250-6265 (2009).
29. Santoro, B., Wainger, B.J. & Siegelbaum, S.A. Regulation of HCN channel surface expression by a novel C-terminal protein-protein interaction. J. Neurosci. 24, 10750-10762 (2004).
30. Notomi, T. & Shigemoto, R. Immunohistochemical localization of Ih channel subunits, HCN1-4, in the rat brain. J. Comp. Neurol. 471, 241-276 (2004).
31. Chung, W.K. et al. Absence epilepsy in apathetic, a spontaneous mutant mouse lacking the h channel subunit, HCN2. Neurobiol. Dis. 33, 499-508 (2009).
32. Nolan, M.F. et al. The hyperpolarization-activated HCN1 channel is important for motor learning and neuronal integration by cerebellar Purkinje cells. Cell 115, 551-564 (2003).
33. Galati, S. et al. The pharmacological blockade of medial forebrain bundle induces an acute pathological synchronization of the cortico-subthalamic nucleus-globus pallidus pathway. J. Physiol. (Lond.) 587, 4405-4423 (2009).
34. Heimer, G., Bar-Gad, I., Goldberg, J.A. & Bergman, H. Dopamine replacement therapy reverses abnormal synchronization of pallidal neurons in the 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine primate model of parkinsonism. J. Neurosci. 22, 7850-7855 (2002).
35. Walters, J.R., Hu, D., Itoga, C.A., Parr-Brownlie, L.C. & Bergstrom, D.A. Phase relationships support a role for coordinated activity in the indirect pathway in organizing slow oscillations in basal ganglia output after loss of dopamine. Neuroscience 144, 762-776 (2007).
36. Mallet, N. et al. Parkinsonian beta oscillations in the external globus pallidus and their relationship with subthalamic nucleus activity. J. Neurosci. 28, 14245-14258 (2008).
37. Shah, M.M., Anderson, A.E., Leung, V., Lin, X. & Johnston, D. Seizure-induced plasticity of h channels in entorhinal cortical layer III pyramidal neurons. Neuron 44, 495-508 (2004).
38. Strauss, U. et al. An impaired neocortical Ih is associated with enhanced excitability and absence epilepsy. Eur. J. Neurosci. 19, 3048-3058 (2004).
39. Kole, M.H., Brauer, A.U. & Stuart, G.J. Inherited cortical HCN1 channel loss amplifes dendritic calcium electrogenesis and burst fring in a rat absence epilepsy model. J. Physiol. (Lond.) 578, 507-525 (2007).
40. Destexhe, A. & Marder, E. Plasticity in single neuron and circuit computations. Nature 431, 789-795 (2004).
41. Zucker, R.S. Calcium-and activity-dependent synaptic plasticity. Curr. Opin. Neurobiol. 9, 305-313 (1999).
42. Xu, W. & Lipscombe, D. Neuronal Ca(V)1.3alpha(1) L-type channels activate at relatively hyperpolarized membrane potentials and are incompletely inhibited by dihydropyridines. J. Neurosci. 21, 5944-5951 (2001).
43. Robinson, R.B. & Siegelbaum, S.A. Hyperpolarization-activated cation currents: from molecules to physiological function. Annu. Rev. Physiol. 65, 453-480 (2003).
44. Hernández, A. et al. Control of the subthalamic innervation of the rat globus pallidus by D2/3 and D4 dopamine receptors. J. Neurophysiol. 96, 2877-2888 (2006).
45. 2+ infux by D2 dopamine and A2A adenosine receptors. Nat. Neurosci. 13, 958-966 (2010).
46. Fleming, S.M. et al. Early and progressive sensorimotor anomalies in mice overexpressing wild-type human α-synuclein. J. Neurosci. 24, 9434-9440 (2004).
47. Blume, S.R., Cass, D.K. & Tseng, K.Y. Stepping test in mice: a reliable approach in determining forelimb akinesia in MPTP-induced Parkinsonism. Exp. Neurol. 219, 208-211 (2009).