Disruption of the olivo-cerebellar circuit by Purkinje neuron-specific ablation of BK channels

Proceedings of the National Academy of Sciences of the United States of America

Volumn 107, Issue 27, 2010, Pages 12323-12328

  Chena, Xiaowei ^a   Kovalchuka, Yury ^a   Adelsberger, Helmuth ^a   Henning, Horst A ^a   Sausbierb, Matthias ^b   Wietzorrek, Georg ^c   Ruth, Peter ^b   Yarom, Yosef ^d   Konnerth, Arthur ^a  

^a TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^b UNIVERSITY OF TÜBINGEN   (Germany)

^c INNSBRUCK MEDICAL UNIVERSITY   (Austria)

^d HEBREW UNIVERSITY OF JERUSALEM   (Israel)

Author keywords

Cerebellar ataxia; Climbing fiber; Complex spike; Two photon imaging

Indexed keywords

LARGE CONDUCTANCE CALCIUM ACTIVATED POTASSIUM CHANNEL;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ATAXIA; CEREBELLUM; CEREBELLUM CORTEX; CEREBELLUM NUCLEUS; CLIMBING FIBER; CONTROLLED STUDY; COORDINATION DISORDER; FEEDBACK SYSTEM; IMAGING; INFERIOR OLIVE; LOCOMOTION; MOTOR COORDINATION; MOUSE; NERVE PROJECTION; NONHUMAN; OLIVARY NUCLEUS; PATCH CLAMP; PRIORITY JOURNAL; PURKINJE CELL; SPIKE WAVE; SYNAPTIC TRANSMISSION; TREMOR;

ACTION POTENTIALS; ANIMALS; BRAIN; CEREBELLAR NUCLEI; CEREBELLUM; IMMUNOHISTOCHEMISTRY; LARGE-CONDUCTANCE CALCIUM-ACTIVATED POTASSIUM CHANNELS; MICE; MICE, KNOCKOUT; MOTOR ACTIVITY; MUSCIMOL; ORGANIC CHEMICALS; PATCH-CLAMP TECHNIQUES; PURKINJE CELLS; PYRIDAZINES;

MUS;

EID: 77955462982     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1001745107     Document Type: Article

References (43)

1. Faber ES, Sah P (2003) Calcium-activated potassium channels: multiple contributions to neuronal function. Neuroscientist 9:181-194.
2. + channel deficiency. Proc Natl Acad Sci USA 101:9474-9478.
3. + channels of the BK-type in the mouse brain. Histochem Cell Biol 125:725-741.
4. Womack MD, Hoang C, Khodakhah K (2009) Large conductance calcium-activated potassium channels affect both spontaneous firing and intracellular calcium concentration in cerebellar Purkinje neurons. Neuroscience 162:989-1000.
5. Womack MD, Khodakhah K (2003) Somatic and dendritic small-conductance calcium-activated potassium channels regulate the output of cerebellar Purkinje neurons. J Neurosci 23:2600-2607.
6. + channels in cerebellar Purkinje neurons. Eur J Neurosci 16:1214-1222.
7. + channels to rat Purkinje neuron function. J Physiol 548:53-69.
8. + currents recorded from the somatic and dendritic regions of cerebellar Purkinje neurons in culture. J Neurosci 11:1002-1015.
9. Knaus HG, et al. (1996) Distribution of high-conductance Ca(2+)-activated K+ channels in rat brain: Targeting to axons and nerve terminals. J Neurosci 16:955-963.
10. + (BK) channels regulate the spike configuration in the burst firing of cerebellar Purkinje neurons. Brain Res 1212:1-8.
11. Cheron G, et al. (2009) BK channels control cerebellar Purkinje and Golgi cell rhythmicity in vivo. PLoS ONE 4:e7991.
12. Orr HT (2004) Into the depths of ataxia. J Clin Invest 113:505-507.
13. Shakkottai VG, et al. (2004) Enhanced neuronal excitability in the absence of neurodegeneration induces cerebellar ataxia. J Clin Invest 113:582-590.
14. Llinás RR (2009) Inferior olive oscillation as the temporal basis for motricity and oscillatory reset as the basis for motor error correction. Neuroscience 162:797-804.
15. Jacobson GA, Rokni D, Yarom Y (2008) A model of the olivo-cerebellar system as a temporal pattern generator. Trends Neurosci 31:617-625.
16. Welsh JP, Lang EJ, Suglhara I, Llinás R (1995) Dynamic organization of motor control within the olivocerebellar system. Nature 374:453-457.
17. De Zeeuw CI, Berrebi AS (1995) Postsynaptic targets of Purkinje cell terminals in the cerebellar and vestibular nuclei of the rat. Eur J Neurosci 7:2322-2333.
18. De Zeeuw CI, Wylie DR, DiGiorgi PL, Simpson JI (1994) Projections of individual Purkinje cells of identified zones in the flocculus to the vestibular and cerebellar nuclei in the rabbit. J Comp Neurol 349:428-447.
19. Fredette BJ, Mugnaini E (1991) The GABAergic cerebello-olivary projection in the rat. Anat Embryol (Berl) 184:225-243.
20. Barski JJ, Dethleffsen K, Meyer M (2000) Cre recombinase expression in cerebellar Purkinje cells. Genesis 28:93-98.
21. Kitamura K, Judkewitz B, Kano M, Denk W, Häusser M (2008) Targeted patch-clamp recordings and single-cell electroporation of unlabeled neurons in vivo. Nat Methods 5:61-67.
22. Miall RC, Keating JG, Malkmus M, Thach WT (1998) Simple spike activity predicts occurrence of complex spikes in cerebellar Purkinje cells. Nat Neurosci 1:13-15.
23. Murphy JT, Sabah NH (1970) Spontaneous firing of cerebellar Purkinje cells in decerebrate and barbiturate anesthetized cats. Brain Res 17:515-519.
24. Häusser M, Clark BA (1997) Tonic synaptic inhibition modulates neuronal output pattern and spatiotemporal synaptic integration. Neuron 19:665-678.
25. Loewenstein Y, et al. (2005) Bistability of cerebellar Purkinje cells modulated by sensory stimulation. Nat Neurosci 8:202-211.
26. Eccles JC, Llinás R, Sasaki K (1966) The excitatory synaptic action of climbing fibres on the purinje cells of the cerebellum. J Physiol 182:268-296.
27. Miyakawa H, Lev-Ram V, Lasser-Ross N, Ross WN (1992) Calcium transients evoked by climbing fiber and parallel fiber synaptic inputs in guinea pig cerebellar Purkinje neurons. J Neurophysiol 68:1178-1189.
28. Maejima T, Hashimoto K, Yoshida T, Aiba A, Kano M (2001) Presynaptic inhibition caused by retrograde signal from metabotropic glutamate to cannabinoid receptors. Neuron 31:463-475.
29. Konnerth A, Llano I, Armstrong CM (1990) Synaptic currents in cerebellar Purkinje cells. Proc Natl Acad Sci USA 87:2662-2665.
30. Zagha E, Lang EJ, Rudy B (2008) Kv3.3 channels at the Purkinje cell soma are necessary for generation of the classical complex spike waveform. J Neurosci 28:1291-1300.
31. Llinás R, Volkind RA (1973) The olivo-cerebellar system: Functional properties as revealed by harmaline-induced tremor. Exp Brain Res 18:69-87.
32. Marshall SP, Lang EJ (2009) Local changes in the excitability of the cerebellar cortex produce spatially restricted changes in complex spike synchrony. J Neurosci 29:14352-14362.
33. Lang EJ, Sugihara I, Llinás R (1996) GABAergic modulation of complex spike activity by the cerebellar nucleoolivary pathway in rat. J Neurophysiol 76:255-275.
34. Barski JJ, et al. (2003) Calbindin in cerebellar Purkinje cells is a critical determinant of the precision of motor coordination. J Neurosci 23:3469-3477.
35. Levin SI, et al. (2006) Impaired motor function in mice with cell-specific knockout of sodium channel Scn8a (NaV1.6) in cerebellar purkinje neurons and granule cells. J Neurophysiol 96:785-793.
36. Kalume F, Yu FH, Westenbroek RE, Scheuer T, Catterall WA (2007) Reduced sodium current in Purkinje neurons from Nav1.1 mutant mice: implications for ataxia in severe myoclonic epilepsy in infancy. J Neurosci 27:11065-11074.
37. Walter JT, Alviña K, Womack MD, Chevez C, Khodakhah K (2006) Decreases in the precision of Purkinje cell pacemaking cause cerebellar dysfunction and ataxia. Nat Neurosci 9:389-397.
38. Hoebeek FE, et al. (2005) Increased noise level of purkinje cell activities minimizes impact of their modulation during sensorimotor control. Neuron 45:953-965.
39. Waters MF, et al. (2006) Mutations in voltage-gated potassium channel KCNC3 cause degenerative and developmental central nervous system phenotypes. Nat Genet 38:447-451.
40. McMahon A, et al. (2004) Allele-dependent changes of olivocerebellar circuit properties in the absence of the voltage-gated potassium channels Kv3.1 and Kv3.3. Eur J Neurosci 19:3317-3327.
41. Rochefort NL, et al. (2009) Sparsification of neuronal activity in the visual cortex at eye-opening. Proc Natl Acad Sci USA 106:15049-15054.
42. Stosiek C, Garaschuk O, Holthoff K, Konnerth A (2003) In vivo two-photon calcium imaging of neuronal networks. Proc Natl Acad Sci USA 100:7319-7324.
43. Takechi H, Eilers J, Konnerth A (1998) A new class of synaptic response involving calcium release in dendritic spines. Nature 396:757-760.