Dendritic spikes mediate negative synaptic gain control in cerebellar Purkinje cells

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

Volumn 107, Issue 51, 2010, Pages 22284-22289

  Rancz, Ede A ^a,b   Häusser, Michael ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

Author keywords

Cerebellum; Dendrite; Patch clamp; Synaptic integration

Indexed keywords

CALCIUM ACTIVATED POTASSIUM CHANNEL;

ACTION POTENTIAL; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DENDRITE; DENDRITIC SPIKE; NERVE FIBER; NONHUMAN; PRIORITY JOURNAL; PURKINJE CELL; RAT; SOMATIC CELL; SPIKE; SYNAPSE;

ACTION POTENTIALS; ANIMALS; AXONS; DENDRITES; POTASSIUM CHANNELS, CALCIUM-ACTIVATED; PURKINJE CELLS; RATS; RATS, SPRAGUE-DAWLEY; SYNAPSES;

EID: 78650647433     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1008605107     Document Type: Article

References (68)

1. Gasparini S, Magee JC (2006) State-dependent dendritic computation in hippocampal CA1 pyramidal neurons. J Neurosci 26:2088-2100.
2. Williams SR, Stuart GJ (2002) Dependence of EPSP efficacy on synapse location in neocortical pyramidal neurons. Science 295:1907-1910.
3. Larkum ME, Nevian T, Sandler M, Polsky A, Schiller J (2009) Synaptic integration in tuft dendrites of layer 5 pyramidal neurons: A new unifying principle. Science 325:756-760.
4. Murayama M, Larkum ME (2009) Enhanced dendritic activity in awake rats. Proc Natl Acad Sci USA 106:20482-20486.
5. Larkum ME, Zhu JJ, Sakmann B (1999) A new cellular mechanism for coupling inputs arriving at different cortical layers. Nature 398:338-341.
6. Williams SR (2004) Spatial compartmentalization and functional impact of conductance in pyramidal neurons. Nat Neurosci 7:961-967.
7. Ariav G, Polsky A, Schiller J (2003) Submillisecond precision of the input-output transformation function mediated by fast sodium dendritic spikes in basal dendrites of CA1 pyramidal neurons. J Neurosci 23:7750-7758.
8. Crochet S, Fuentealba P, Timofeev I, Steriade M (2004) Selective amplification of neocortical neuronal output by fast prepotentials in vivo. Cereb Cortex 14:1110-1121.
9. Larkum ME, Senn W, Lüscher HR (2004) Top-down dendritic input increases the gain of layer 5 pyramidal neurons. Cereb Cortex 14:1059-1070.
10. Reyes A (2001) Influence of dendritic conductances on the input-output properties of neurons. Annu Rev Neurosci 24:653-675.
11. Llinás R, Nicholson C, Freeman JA, Hillman DE (1968) Dendritic spikes and their inhibition in alligator Purkinje cells. Science 160:1132-1135.
12. Llinas R, Nicholson C (1971) Electrophysiological properties of dendrites and somata in alligator Purkinje cells. J Neurophysiol 34:532-551.
13. Rancz EA, Hausser M (2006) Dendritic calcium spikes are tunable triggers of cannabinoid release and short-term synaptic plasticity in cerebellar Purkinje neurons. J Neurosci 26:5428-5437.
14. Davie JT, Clark BA, Hausser M (2008) The origin of the complex spike in cerebellar Purkinje cells. J Neurosci 28:7599-7609.
15. Schultz SR, Kitamura K, Post-Uiterweer A, Krupic J, Hausser M (2009) Spatial pattern coding of sensory information by climbing fiber-evoked calcium signals in networks of neighboring cerebellar Purkinje cells. J Neurosci 29:8005-8015.
16. Llinas R, Hess R (1976) Tetrodotoxin-resistant dendritic spikes in avian Purkinje cells. Proc Natl Acad Sci USA 73:2520-2523.
17. Llinas R, Sugimori M (1980) Electrophysiological properties of in vitro Purkinje cell dendrites in mammalian cerebellar slices. J Physiol 305:197-213. (Pubitemid 10048156)
18. Usowicz MM, Sugimori M, Cherksey B, Llinas R (1992) P-type calcium channels in the somata and dendrites of adult cerebellar Purkinje cells. Neuron 9:1185-1199.
19. Stuart G, Hausser M (1994) Initiation and spread of sodium action potentials in cerebellar Purkinje cells. Neuron 13:703-712.
20. Hartell NA (1996) Strong activation of parallel fibers produces localized calcium transients and a form of LTD that spreads to distant synapses. Neuron 16:601-610.
21. Schreurs BG, Alkon DL (1993) Rabbit cerebellar slice analysis of long-term depression and its role in classical conditioning. Brain Res 631:235-240.
22. Wang SS, Denk W, Hausser M (2000) Coincidence detection in single dendritic spines mediated by calcium release. Nat Neurosci 3:1266-1273.
23. Shin JH, Kim YS, Linden DJ (2008) Dendritic glutamate release produces autocrine activation of mGluR1 in cerebellar Purkinje cells. Proc Natl Acad Sci USA 105:746-750.
24. Duguid IC, Pankratov Y, Moss GW, Smart TG (2007) Somatodendritic release of glutamate regulates synaptic inhibition in cerebellar Purkinje cells via autocrine mGluR1 activation. J Neurosci 27:12464-12474.
25. De Schutter E, Bower JM (1994) An active membrane model of the cerebellar Purkinje cell II. Simulation of synaptic responses. J Neurophysiol 71:401-419. (Pubitemid 24058865)
26. Armstrong DM, Rawson JA (1979) Activity patterns of cerebellar cortical neurones and climbing fibre afferents in the awake cat. J Physiol 289:425-448.
27. Lang EJ, Sugihara I, Welsh JP, Llinas R (1999) Patterns of spontaneous purkinje cell complex spike activity in the awake rat. J Neurosci 19:2728-2739.
28. Hausser M, Clark BA (1997) Tonic synaptic inhibition modulates neuronal output pattern and spatiotemporal synaptic integration. Neuron 19:665-678.
29. Mittmann W, Hausser M (2007) Linking synaptic plasticity and spike output atexcitatory and inhibitory synapses onto cerebellar Purkinje cells. J Neurosci 27:5559-5570.
30. Mittmann W, Koch U, Hausser M (2005) Feed-forward inhibition shapes the spike output of cerebellar Purkinje cells. J Physiol 563:369-378.
31. Chadderton P, Margrie TW, Hausser M (2004) Integration of quanta in cerebellar granule cells during sensory processing. Nature 428:856-860.
32. Rancz EA, et al. (2007) High-fidelity transmission of sensory information by single cerebellar mossy fibre boutons. Nature 450:1245-1248.
33. Walter JT, Khodakhah K (2006) The linear computational algorithm of cerebellar Purkinje cells. J Neurosci 26:12861-12872.
34. Dittman JS, Kreitzer AC, Regehr WG (2000) Interplay between facilitation, depression, and residual calcium at three presynaptic terminals. J Neurosci 20:1374-1385.
35. + channels in cerebellar Purkinje neurons. Eur J Neurosci 16:1214-1222.
36. + channels to rat Purkinje neuron function. J Physiol 548:53-69.
37. Knaus HG, et al. (1994) Tremorgenic indole alkaloids potently inhibit smooth muscle high-conductance calcium-activated potassium channels. Biochemistry 33:5819-5828.
38. Jaeger D, De Schutter E, Bower JM (1997) The role of synaptic and voltage-gated currents in the control of Purkinje cell spiking: a modeling study. J Neurosci 17:91-106.
39. De Schutter E (1998) Dendritic voltage and calcium-gated channels amplify the variability of postsynaptic responses in a Purkinje cell model. J Neurophysiol 80: 504-519.
40. Jaeger D, Bower JM (1999) Synaptic control of spiking in cerebellar Purkinje cells: dynamic current clamp based on model conductances. J Neurosci 19:6090-6101.
41. Khaliq ZM, Raman IM (2005) Axonal propagation of simple and complex spikes in cerebellar Purkinje neurons. J Neurosci 25:454-463.
42. Monsivais P, Clark BA, Roth A, Hausser M (2005) Determinants of action potential propagation in cerebellar Purkinje cell axons. J Neurosci 25:464-472. (Pubitemid 40105617)
43. Shin SL, et al. (2007) Regular patterns in cerebellar Purkinje cell simple spike trains. PLoS ONE 2:e485.
44. Riehle A, Grun S, Diesmann M, Aertsen A (1997) Spike synchronization and rate modulation differentially involved in motor cortical function. Science 278:1950-1953.
45. Latham A, Paul DH (1971) Spontaneous activity of cerebellar Purkinje cells and their responses to impulses in climbing fibres. J Physiol 213:135-156.
46. Thach WT (1968) Discharge of Purkinje and cerebellar nuclear neurons during rapidly alternating arm movements in the monkey. J Neurophysiol 31:785-797.
47. De Schutter E, Steuber V (2009) Patterns and pauses in Purkinje cell simple spike trains: experiments, modeling and theory. Neuroscience 162:816-826.
48. Steuber V, et al. (2007) Cerebellar LTD and pattern recognition by Purkinje cells. Neuron 54:121-136.
49. Raman IM, Bean BP (1999) Ionic currents underlying spontaneous action potentials in isolated cerebellar Purkinje neurons. J Neurosci 19:1663-1674.
50. + channels of the BK-type in the mouse brain. Histochem Cell Biol 125:725-741.
51. 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.
52. Khavandgar S, Walter JT, Sageser K, Khodakhah K (2005) Kv1 channels selectively prevent dendritic hyperexcitability in rat Purkinje cells. J Physiol 569:545-557.
53. Martina M, Yao GL, Bean BP (2003) Properties and functional role of voltage-dependent potassium channels in dendrites of rat cerebellar Purkinje neurons. J Neurosci 23:5698-5707.
54. + channels control Purkinje cell output to facilitate postsynaptic rebound discharge in deep cerebellar neurons. J Neurosci 25:1481-1492.
55. + channels enable burst output in rat cerebellar Purkinje cells. Eur J Neurosci 20:729-739.
56. Womack MD, Chevez C, Khodakhah K (2004) Calcium-activated potassium channels are selectively coupled to P/Q-type calcium channels in cerebellar Purkinje neurons. J Neurosci 24:8818-8822.
57. 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.
58. Llinás R, Sugimori M (1980) Electrophysiological properties of in vitro Purkinje cell somata in mammalian cerebellar slices. J Physiol 305:171-195. (Pubitemid 10048155)
59. Bekkers JM, Hausser M (2007) Targeted dendrotomy reveals active and passive contributions of the dendritic tree to synaptic integration and neuronal output. Proc Natl Acad Sci USA 104:11447-11452.
60. Epsztein J, Lee AK, Chorev E, Brecht M (2010) Impactof spikelets on hippocampal CA1 pyramidal cell activity during spatial exploration. Science 327:474-477.
61. Attwell D, Laughlin SB (2001) An energy budget for signaling in the grey matter of the brain. J Cereb Blood Flow Metab 21:1133-1145.
62. Alle H, Roth A, Geiger JR (2009) Energy-efficient action potentials in hippocampal mossy fibers. Science 325:1405-1408.
63. Pedroarena CM, Schwarz C (2003) Efficacy and short-term plasticity at GABAergic synapses between Purkinje and cerebellar nuclei neurons. J Neurophysiol 89:704-715.
64. Telgkamp P, Raman IM (2002) Depression of inhibitory synaptic transmission between Purkinje cells and neurons of the cerebellar nuclei. J Neurosci 22:8447-8457.
65. Gauck V, Jaeger D (2000) The control of rate and timing of spikes in the deep cerebellar nuclei by inhibition. J Neurosci 20:3006-3016.
66. Llinas R, Muhlethaler M (1988) Electrophysiology of guinea-pig cerebellar nuclear cells in the in vitro brain stem-cerebellar preparation. J Physiol 404:241-258.
67. Zhang W, Shin JH, Linden DJ (2004) Persistent changes in the intrinsic excitability of rat deep cerebellar nuclear neurones induced by EPSP or IPSP bursts. J Physiol 561:703-719.
68. Davie JT, et al. (2006) Dendritic patch-clamp recording. Nat Protoc 1:1235-1247.