Purkinje-cell plasticity and cerebellar motor learning are graded by complex-spike duration

Nature

Volumn 510, Issue 7506, 2014, Pages 529-532

  Yang, Yan ^a   Lisberger, Stephen G ^a,b  

^a DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b DUKE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GENETIC ANALYSIS; LEARNING; NERVOUS SYSTEM; PHENOTYPIC PLASTICITY; PRIMATE;

ADULT; ANIMAL EXPERIMENT; ARTICLE; CEREBELLUM; CLIMBING FIBER; COMPLEX SPIKE; EYE TRACKING; LONG TERM DEPRESSION; MOTONEURON; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; PURKINJE CELL; SMOOTH PURSUIT EYE MOVEMENT; SPIKE WAVE; SYNAPSE;

ANIMALIA;

ACTION POTENTIALS; ANIMALS; AXONS; CALCIUM; LEARNING; LONG-TERM SYNAPTIC DEPRESSION; MACACA MULATTA; MALE; MOTOR SKILLS; NEURONAL PLASTICITY; OLIVARY NUCLEUS; PURKINJE CELLS;

EID: 84903527141     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature13282     Document Type: Article

References (30)

1. Marr, D. A theory of cerebellar cortex. J. Physiol. (Lond.) 202, 437-470 (1969).
2. Albus, J. S. A theory of cerebellar function. Math. Biosci. 10, 25-61 (1971).
3. Ito, M. Neural design of the cerebellar motor control system. Brain Res. 40, 81-84 (1972).
4. Gilbert, P. F. & Thach, W. T. Purkinje cell activity during motor learning. Brain Res. 128, 309-328 (1977).
5. Ito, M. & Kano, M. 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 (1982).
6. Najafi, F. & Medina, J. F. Beyond "all-or-nothing" climbing fibers: graded representation of teaching signals in Purkinje cells. Front. Neural Circ. 7 (2013).
7. Maruta, J., Hensbroek, R. A. & Simpson, J. I. Intraburst and interburst signaling by climbing fibers. J. Neurosci. 27, 11263-11270 (2007).
8. Mathy, A. et al. Encoding of oscillations by axonal bursts in inferior olive neurons. Neuron 62, 388-399 (2009).
9. Rasmussen, A. et al. Number of spikes in climbing fibers determines the direction of cerebellar learning. J. Neurosci. 33, 13436-13440 (2013).
10. Bazzigaluppi, P. et al. Olivary subthreshold oscillations and burst activity revisited. Front. Neural Circ. 6, 91 (2012).
11. Medina, J. F. & Lisberger, S. G. Links from complex spikes to local plasticity and motor learning in the cerebellum of awake-behaving monkeys. Nature Neurosci. 11, 1185-1192 (2008).
12. Yang, Y. & Lisberger, S. G. Learning on multiple timescales in smooth pursuit eye movements. J. Neurophysiol. 104, 2850-2862 (2010).
13. Zee, D. S., Yamazaki, A., Butler, P. H. & Gü cer, G. Effects of ablation of flocculus and paraflocculus of eye movements in primate. J. Neurophysiol. 46, 878-899 (1981).
14. Kahlon, M. & Lisberger, S. G. Changes in the responses of Purkinje cells in the floccular complex of monkeys after motor learning in smooth pursuit eye movements. J. Neurophysiol. 84, 2945-2960 (2000).
15. Highstein, S. M. Synaptic linkage in the vestibulo-ocular and cerebello-vestibular pathways to the VIth nucleus in the rabbit. Exp. Brain Res. 17, 301-314 (1973).
16. Yang, Y. & Lisberger, S. G. Interaction of plasticity and circuit organization during the acquisition of cerebellum-dependent motor learning. eLife 2, e01574 (2013).
17. Hartell, N. A. Strong activation of parallel fibers produces localized calcium transients and a form of LTD that spreads to distant synapses. Neuron 16, 601-610 (1996).
18. Wang, S. S.-H., Denk, W. & Hausser, M. Coincidence detection in single dendritic spines mediated by calcium release. Nature Neurosci. 3, 1266-1273 (2000).
19. Bengtsson, F. & Hesslow, G. Cerebellar control of the inferior olive. Cerebellum 5, 7-14 (2006).
20. Callaway, J. C., Lasser-Ross, N. & Ross, W. N. IPSPs strongly inhibit climbing fiberactivated [Ca21]i increases in the dendrites of cerebellar Purkinje neurons. J. Neurosci. 15, 2777-2787 (1995).
21. Kitamura, K. & Hausser, M. Dendritic calcium signaling triggered by spontaneous and sensory-evoked climbing fiber input to cerebellar Purkinje cells in vivo. J. Neurosci. 31, 10847-10858 (2011).
22. Medina, J. F. & Lisberger, S. G. Variation, signal, and noise in cerebellar sensorymotor processing forsmooth-pursuit eyemovements. J.Neurosci. 27, 6832-6842 (2007).
23. Najafi, F., Giavannucci, A., Wang, S. S.-H. & Medina, J. F. Sensory driven enhancement of calcium signals in individual Purkinje cell dendrites of awake mice. Cell Rep. 6, 792-798 (2014).
24. Mauk, M. D. & Donegan, N. H. A model of Pavlovian eyelid conditioning based on the synaptic organization of the cerebellum. Learn. Mem. 4, 130-158 (1997).
25. Kenyon, G. T., Medina, J. F. & Mauk, M. D. A mathematical model of the cerebellarolivary system I: self-regulating equilibrium of climbing fiber activity. J. Comput. Neurosci. 5, 17-33 (1998).
26. Miall, R. C., Keating, J. G., Malkmus, M. & Thach, W. T. Simple spike activity predicts occurrence of complex spikes in cerebellar Purkinje cells. Nature Neurosci. 1, 13-15 (1998).
27. Ohyama, T., Nores, W. L., Medina, J. F., Riusech, F. A. & Mauk, M. D. Learninginduced plasticity in deep cerebellar nucleus. J. Neurosci. 26, 12656-12663 (2006).
28. Gilbert, P. F. C. A theory of memory that explains the function and structure of the cerebellum. Brain Res. 70, 1-18 (1974).
29. Yang, Y.& Lisberger, S. G. (2014) Role of plasticity at different sites across the time course of cerebellar motor learning. J. Neurosci. (in the press).
30. Maiz, J. et al. Prolonging the postcomplex spike pause speeds eyeblink conditioning. Proc. Natl Acad. Sci. USA 109, 16726-16730 (2012).