The linear computational algorithm of cerebellar Purkinje cells

Journal of Neuroscience

Volumn 26, Issue 50, 2006, Pages 12861-12872

  Walter, Joy T ^a   Khodakhah, Kamran ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

Activity; Cerebellum; Computational algorithm; Granule cell; Purkinje neurons; Synaptic communication

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL ACTIVATION; CELL ACTIVITY; CELL FUNCTION; CELL MEMBRANE POTENTIAL; CELL STIMULATION; CEREBELLUM CORTEX; CONTROLLED STUDY; GRANULE CELL; NONHUMAN; PRIORITY JOURNAL; PURKINJE CELL; RAT; SPIKE WAVE; SYNAPTIC POTENTIAL; SYNAPTIC TRANSMISSION;

ACTION POTENTIALS; ALGORITHMS; ANIMALS; CEREBELLUM; COMPUTATIONAL BIOLOGY; ELECTRIC STIMULATION; LINEAR MODELS; PURKINJE CELLS; RATS; RATS, WISTAR;

EID: 33845668474     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4507-05.2006     Document Type: Article

References (68)

1. Albus JS (1971) A theory of cerebellar function. Math Biosci 10:25-61.
2. Allen GI, Azzena GB, Ohno T (1974) Somatotopically organized inputs from fore- and hindlimb areas of sensorimotor cortex to cerebellar Purkyne cells. Exp Brain Res 20:255-272.
3. 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.
4. Benardo LS, Masukawa LM, Prince DA (1982) Electrophysiology of isolated hippocampal pyramidal dendrites. J Neurosci 2:1614-1622.
5. Bower JM, Woolston DC (1983) Congruence of spatial organization of tactile projections to granule cell and Purkinje cell layers of cerebellar hemispheres of the albino rat: vertical organization of cerebellar cortex. J Neurophysiol 49:745-766.
6. Brunel N, Hakim V, Isope P, Nadal JP, Barbour B (2004) Optimal information storage and the distribution of synaptic weights: perceptron versus Purkinje cell. Neuron 43:745-757.
7. 2+]i increases in the dendrites of cerebellar Purkinje neurons. J Neurosci 15:2777-2787.
8. Canepari M, Nelson L, Papageorgiou G, Corrie JE, Ogden D (2001) Photochemical and pharmacological evaluation of 7-nitroindolinyl- and 4-methoxy-7-nitroindolinyl-amino acids as novel, fast caged neurotransmitters. J Neurosci Methods 112:29-42.
9. Cash S, Yuste R (1999) Linear summation of excitatory inputs by CA1 pyramidal neurons. Neuron 22:383-394.
10. Chadderton P, Margrie TW, Hausser M (2004) Integration of quanta in cerebellar granule cells during sensory processing. Nature 428:856-860.
11. Davies CH, Pozza MF, Collingridge GL (1993) CGP 55845A: a potent antagonist of GABAB receptors in the CA1 region of rat hippocampus. Neuropharmacology 32:1071-1073.
12. Dickson CT, Mena AR, Alonso A (1997) Electroresponsiveness of medial entorhinal cortex layer III neurons in vitro. Neuroscience 81:937-950.
13. Eccles JC, Llinas R, Sasaki K (1966) The excitatory synaptic action of climbing fibres on the purinje cells of the cerebellum. J Physiol (Lond) 182:268-296.
14. Eccles JC, Sabah NH, Schmidt RF, Taborikova H (1972) Integration by Purkyne cells of mossy and climbing fiber inputs from cutaneous mechanoreceptors. Exp Brain Res 15:498-520.
15. Espinoza E, Smith AM (1990) Purkinje cell simple spike activity during grasping and lifting objects of different textures and weights. J Neurophysiol 64:698-714.
16. Gasparini S, Magee JC (2006) State-dependent dendritic computation in hippocampal CA1 pyramidal neurons. J Neurosci 26:2088-2100.
17. Golding NL, Spruston N (1998) Dendritic sodium spikes are variable triggers of axonal action potentials in hippocampal CA1 pyramidal neurons. Neuron 21:1189-1200.
18. Hausser M, Stuart G, Racca C, Sakmann B (1995) Axonal initiation and active dendritic propagation of action potentials in substantia nigra neurons. Neuron 15:637-647.
19. Hirata Y, Highstein SM (2001) Acute adaptation of the vestibuloocular reflex: signal processing by floccular and ventral parafloccular Purkinje cells. J Neurophysiol 85:2267-2288.
20. Hounsgaard J, Yamamoto C (1979) Dendritic spikes in Purkinje cells of the guinea pig cerebellum studied in vitro. Exp Brain Res 37:387-398.
21. Ito M (1984) The cerebellum and neural control. New York: Raven Press.
22. Ito M (1989) Long-term depression. Annu Rev Neurosci 12:85-102.
23. Ito M, Kano M (1982) Long-lasting depression of parallel fiber-Purkinje cell transmission induced by conjunctive stimulation of parallel fibers and climbing fibers in the cerebellar cortex. Neurosci Lett 33:253-258.
24. Jaeger D, Bower JM (1994) Prolonged responses in rat cerebellar Purkinje cells following activation of the granule cell layer: an intracellular in vitro and in vivo investigation. Exp Brain Res 100:200-214.
25. Johnston D, Magee JC, Colbert CM, Cristie BR (1996) Active properties of neuronal dendrites. Annu Rev Neurosci 19:165-186.
26. Khavandgar S, Walter JT, Sageser K, Khodakhah K (2005) Kv1 channels selectively prevent dendritic hyperexcitability in Purkinje cells. J Physiol (Lond) 569:545-557.
27. Kim HG, Connors BW (1993) Apical dendrites of the neocortex: correlation between sodium- and calcium-dependent spiking and pyramidal cell morphology. J Neurosci 13:5301-5311.
28. Lev-Ram V, Miyakawa H, Lasser-Ross N, Ross WN (1992) Calcium transients in cerebellar Purkinje neurons evoked by intracellular stimulation. J Neurophysiol 68:1167-1177.
29. Lisberger SG, Fuchs AF (1978) Role of primate flocculus during rapid behavioral modification of vestibuloocular reflex. I. Purkinje cell activity during visually guided horizontal smooth-pursuit eye movements and passive head rotation. J Neurophysiol 41:733-763.
30. Llinas R, Sugimori M (1980a) Electrophysiological properties of in vitro Purkinje cell somata in mammalian cerebellar slices. J Physiol (Lond) 305:171-195.
31. Llinas R, Sugimori M (1980b) Electrophysiological properties of in vitro Purkinje cell dendrites in mammalian cerebellar slices. J Physiol (Lond) 305:197-213.
32. Losonczy A, Magee JC (2006) Integrative properties of radial oblique dendrites in hippocampal CA1 pyramidal neurons. Neuron 50:291-307.
33. Marple-Horvat DE, Criado JM, Armstrong DM (1998) Neuronal activity in the lateral cerebellum of the cat related to visual stimuli at rest, visually guided step modification, and saccadic eye movements. J Physiol (Lond) 506:489-514.
34. Marr D (1969) A theory of cerebellar cortex. J Physiol (Lond) 202:437- 470.
35. Martina M, Vida I, Jonas P (2000) Distal initiation and active propagation of action potentials in interneuron dendrites. Science 287:295-300.
36. Martinez FE, Crill WE, Kennedy TT (1971) Electrogenesis of cerebellar Purkinje cell responses in cats. J Neurophysiol 34:348-356.
37. Mauk MD, Garcia KS, Medina JF, Steele PM (1998) Does cerebellar LTD mediate motor learning? Toward a resolution without a smoking gun. Neuron 20:359-362.
38. Miles FA, Fuller JH, Braitman DJ, Dow BM (1980) Long-term adaptive changes in primate vestibuloocular reflex. III. Electrophysiological observations in flocculus of normal monkeys. J Neurophysiol 43:1437-1476.
39. Mittmann W, Koch U, Hausser M (2005) Feed-forward inhibition shapes the spike output of cerebellar Purkinje cells. J Physiol (Lond) 563:369-378.
40. 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.
41. Napper RM, Harvey RJ (1988) Number of parallel fiber synapses on an individual Purkinje cell in the cerebellum of the rat. J Comp Neurol 274:168-177.
42. Nettleton JS, Spain WJ (2000) Linear to supralinear summation of AMPA-mediated EPSPs in neocortical pyramidal neurons. J Neurophysiol 83:3310-3322.
43. Oakley JC, Schwindt PC, Crill WE (2001) Dendritic calcium spikes in layer 5 pyramidal neurons amplify and limit transmission of ligand-gated dendritic current to soma. J Neurophysiol 86:514-527.
44. Ogawa T, Ito S, Kato H (1981) Membrane characteristics of visual cortical neurons in in vitro slices. Brain Res 226:315-319.
45. Palay SL, Chan-Palay V (1974) Cerebellar cortex. Berlin: Springer.
46. Ramon y Cajal S (1904) Textura del Sistema Nervioso del Hombre y los Vertebrados. Madrid: Moya.
47. Ramon y Cajal (1911) Histologie du systeme nerveux de l'homme et des vertebres. Paris: Maloine.
48. 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.
49. Regan LJ (1991) Voltage-dependent calcium currents in Purkinje cells from rat cerebellar vermis. J Neurosci 11:2259-2269.
50. Rowland NC, Jaeger D (2005) Coding of tactile response properties in the rat deep cerebellar nuclei. J Neurophysiol 94:1236-1251.
51. Sakurai M (1990) Calcium is an intracellular mediator of the climbing fiber in induction of cerebellar long-term depression. Proc Natl Acad Sci USA 87:3383-3385.
52. Schiller J, Schiller Y, Stuart G, Sakmann B (1997) Calcium action potentials restricted to distal apical dendrites of rat neocortical pyramidal neurons. J Physiol (Lond) 505:605-616.
53. Schiller J, Major G, Koester HJ, Schiller Y (2000) NMDA spikes in basal dendrites of cortical pyramidal neurons. Nature 404:285-289.
54. Spruston N, Schiller Y, Stuart G, Sakmann B (1995) Activity-dependent action potential invasion and calcium influx into hippocampal CA1 dendrites. Science 268:297-300.
55. Stafstrom CE, Schwindt PC, Crill WE (1984) Repetitive firing in layer V neurons from cat neocortex in vitro. J Neurophysiol 52:264-277.
56. Stone LS, Lisberger SG (1990) Visual responses of Purkinje cells in the cerebellar flocculus during smooth-pursuit eye movements in monkeys. I. Simple spikes. J Neurophysiol 63:1241-1261.
57. Stuart G, Schiller J, Sakmann B (1997) Action potential initiation and propagation in rat neocortical pyramidal neurons. J Physiol (Lond) 505:617-632.
58. Telgkamp P, Padgett DE, Ledoux VA, Woolley CS, Raman IM (2004) Maintenance of high-frequency transmission at purkinje to cerebellar nuclear synapses by spillover from boutons with multiple release sites. Neuron 41:113-126.
59. Thach Jr WT (1967) Somatosensory receptive fields of single units in cat cerebellar cortex. J Neurophysiol 30:675-696.
60. Thach WT (1968) Discharge of Purkinje and cerebellar nuclear neurons during rapidly alternating arm movements in the monkey. J Neurophysiol 31:785-797.
61. Thach WT (1970) Discharge of cerebellar neurons related to two maintained postures and two prompt movements. II. Purkinje cell output and input. J Neurophysiol 33:537-547.
62. Udo M, Matsukawa K, Kamei H, Minoda K, Oda Y (1981) Simple and complex spike activities of Purkinje cells during locomotion in the cerebellar vermal zones of decerebrate cats. Exp Brain Res 41:292-300.
63. 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.
64. Viana F, Bayliss DA, Berger AJ (1995) Repetitive firing properties of developing rat brainstem motoneurones. J Physiol (Lond) 486:745-761.
65. Walter JT, Alvina 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.
66. 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.
67. Yoon KW, Covey DF, Rothman SM (1993) Multiple mechanisms of picrotoxin block of GABA-induced currents in rat hippocampal neurons. J Physiol (Lond) 464:423-439.
68. Yuste R, Tank DW (1996) Dendritic integration in mammalian neurons, a century after Cajal. Neuron 16:701-716.