Prolonging the postcomplex spike pause speeds eyeblink conditioning

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

Volumn 109, Issue 41, 2012, Pages 16726-16730

  Maiz, Jaione ^a   Karakossian, Movses H ^a   Pakaprot, Narawut ^b,c   Robleto, Karla ^b   Thompson, Richard F ^b   Otis, Thomas S ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^c MAHIDOL UNIVERSITY   (Thailand)

Author keywords

1 EBIO; Associative learning; Pavlovian; Rebound; ZD 7288

Indexed keywords

CALCIUM ACTIVATED POTASSIUM CHANNEL; PICROTOXIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CEREBELLUM NUCLEUS; CONDITIONING; CONTROLLED STUDY; EXPERIMENTAL RABBIT; EYELID REFLEX; LEARNING; NERVE CELL MEMBRANE POTENTIAL; NERVE CELL PLASTICITY; NERVE FIBER; NEUROPHYSIOLOGY; NONHUMAN; POSTCOMPLEX SPIKE; PRIORITY JOURNAL; PURKINJE FIBER; SIGNAL DETECTION; SPIKE; TEACHING;

ANALYSIS OF VARIANCE; ANIMALS; BENZIMIDAZOLES; BLINKING; CALCIUM CHANNEL AGONISTS; CARDIOVASCULAR AGENTS; CEREBELLAR NUCLEI; CEREBELLUM; CONDITIONING, EYELID; ELECTRIC STIMULATION; EXCITATORY AMINO ACID ANTAGONISTS; EXCITATORY POSTSYNAPTIC POTENTIALS; GABA ANTAGONISTS; LEARNING; MICE; NERVE FIBERS; PICROTOXIN; PURKINJE CELLS; PYRIMIDINES; QUINOXALINES; RATS; RATS, SPRAGUE-DAWLEY; TIME FACTORS;

EID: 84867375358     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1214274109     Document Type: Article

References (50)

1. Christian KM, Thompson RF (2003) Neural substrates of eyeblink conditioning: Acquisition and retention. Learn Mem 10:427-455. (Pubitemid 37499774)
2. Miles FA, Lisberger SG (1981) Plasticity in the vestibulo-ocular reflex: A new hypothesis. Annu Rev Neurosci 4:273-299.
3. Raymond JL, Lisberger SG, Mauk MD (1996) The cerebellum: a neuronal learning machine? Science 272:1126-1131. (Pubitemid 26169466)
4. Thompson RF (1986) The neurobiology of learning and memory. Science 233:941-947.
5. Kassardjian CD, et al. (2005) The site of a motor memory shifts with consolidation. J Neurosci 25:7979-7985. (Pubitemid 41254400)
6. Demer JL, Robinson DA (1982) Effects of reversible lesions and stimulation of olivocerebellar system on vestibuloocular reflex plasticity. J Neurophysiol 47:1084-1107. (Pubitemid 12086674)
7. Shutoh F, Ohki M, Kitazawa H, Itohara S, Nagao S (2006) Memory trace of motor learning shifts transsynaptically from cerebellar cortex to nuclei for consolidation. Neuroscience 139:767-777.
8. Christian KM, Thompson RF (2005) Long-term storage of an associative memory trace in the cerebellum. Behav Neurosci 119:526-537. (Pubitemid 40547958)
9. Clark RE, Zhang AA, Lavond DG (1992) Reversible lesions of the cerebellar interpositus nucleus during acquisition and retention of a classically conditioned behavior. Behav Neurosci 106:879-888. (Pubitemid 23034856)
10. Krupa DJ, Thompson JK, Thompson RF (1993) Localization of a memory trace in the mammalian brain. Science 260:989-991. (Pubitemid 23209974)
11. McCormick DA, Thompson RF (1984) Cerebellum: Essential involvement in the classically conditioned eyelid response. Science 223:296-299. (Pubitemid 14215791)
12. Yeo CH, Hardiman MJ, Glickstein M (1985) Classical conditioning of the nictitating membrane response of the rabbit. I. Lesions of the cerebellar nuclei. Exp Brain Res 60: 87-98. (Pubitemid 16252110)
13. Medina JF, Garcia KS, Mauk MD (2001) A mechanism for savings in the cerebellum. J Neurosci 21:4081-4089. (Pubitemid 32466500)
14. Bao S, Chen L, Kim JJ, Thompson RF (2002) Cerebellar cortical inhibition and classical eyeblink conditioning. Proc Natl Acad Sci USA 99:1592-1597. (Pubitemid 34136537)
15. Chen L, Bao S, Lockard JM, Kim JK, Thompson RF (1996) Impaired classical eyeblink conditioning in cerebellar-lesioned and Purkinje cell degeneration (pcd) mutant mice. J Neurosci 16:2829-2838. (Pubitemid 26122695)
16. Garcia KS, Mauk MD (1998) Pharmacological analysis of cerebellar contributions to the timing and expression of conditioned eyelid responses. Neuropharmacology 37: 471-480. (Pubitemid 28306936)
17. Lavond DG, Steinmetz JE (1989) Acquisition of classical conditioning without cerebellar cortex. Behav Brain Res 33:113-164. (Pubitemid 19141064)
18. Perrett SP, Ruiz BP, Mauk MD (1993) Cerebellar cortex lesions disrupt learning-dependent timing of conditioned eyelid responses. J Neurosci 13:1708-1718. (Pubitemid 23095412)
19. Albus JS (1971) A theory of cerebellar function. Math Biosci 10:25-61.
20. Ito M (1972) Neural design of the cerebellar motor control system. Brain Res 40:81- 84.
21. Marr D (1969) A theory of cerebellar cortex. J Physiol 202:437-470.
22. Thompson RF (1989) Role of inferior olive in classical conditioning. The Olivocerebellar System in Motor Control, ed Strata P (Springer, New York), pp 466.
23. Gilbert PF, Thach WT (1977) Purkinje cell activity during motor learning. Brain Res 128:309-328. (Pubitemid 8119303)
24. Jirenhed DA, Bengtsson F, Hesslow G (2007) Acquisition, extinction, and reacquisition of a cerebellar cortical memory trace. J Neurosci 27:2493-2502. (Pubitemid 46393596)
25. Medina JF, Lisberger SG (2008) Links from complex spikes to local plasticity and motor learning in the cerebellum of awake-behaving monkeys. Nat Neurosci 11:1185-1192.
26. Simpson JI, Alley KE (1974) Visual climbing fiber input to rabbit vestibulo-cerebellum: a source of direction-specific information. Brain Res 82:302-308.
27. Mauk MD, Steinmetz JE, Thompson RF (1986) Classical conditioning using stimulation of the inferior olive as the unconditioned stimulus. Proc Natl Acad Sci USA 83: 5349-5353.
28. Welsh JP, Harvey JA (1998) Acute inactivation of the inferior olive blocks associative learning. Eur J Neurosci 10:3321-3332. (Pubitemid 29074123)
29. McCormick DA, Steinmetz JE, Thompson RF (1985) Lesions of the inferior olivary complex cause extinction of the classically conditioned eyeblink response. Brain Res 359:120-130. (Pubitemid 16185323)
30. Thompson RF, Thompson JK, Kim JJ, Krupa DJ, Shinkman PG (1998) The nature of reinforcement in cerebellar learning. Neurobiol Learn Mem 70:150-176. (Pubitemid 28455589)
31. Häusser M, Clark BA (1997) Tonic synaptic inhibition modulates neuronal output pattern and spatiotemporal synaptic integration. Neuron 19:665-678. (Pubitemid 27430752)
32. Raman IM, Sprunger LK, Meisler MH, Bean BP (1997) Altered subthreshold sodium currents and disrupted firing patterns in Purkinje neurons of Scn8a mutant mice. Neuron 19:881-891. (Pubitemid 27471392)
33. Swensen AM, Bean BP (2003) Ionic mechanisms of burst firing in dissociated Purkinje neurons. J Neurosci 23:9650-9663. (Pubitemid 37352065)
34. Linden DJ, Connor JA (1995) Long-term synaptic depression. Annu Rev Neurosci 18: 319-357.
35. Pedarzani P, et al. (2001) Control of electrical activity in central neurons by modulating the gating of small conductance Ca2+-activated K+ channels. J Biol Chem 276: 9762-9769.
36. 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. (Pubitemid 43290969)
37. 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. (Pubitemid 36418594)
38. Nolan MF, et al. (2003) The hyperpolarization-activated HCN1 channel is important for motor learning and neuronal integration by cerebellar Purkinje cells. Cell 115: 551-564. (Pubitemid 37506044)
39. Ito M (1982) Cerebellar control of the vestibulo-ocular reflex - around the flocculus hypothesis. Annu Rev Neurosci 5:275-296.
40. Lang EJ, Sugihara I, Welsh JP, Llinás R (1999) Patterns of spontaneous purkinje cell complex spike activity in the awake rat. J Neurosci 19:2728-2739. (Pubitemid 29162420)
41. Mukamel EA, Nimmerjahn A, Schnitzer MJ (2009) Automated analysis of cellular signals from large-scale calcium imaging data. Neuron 63:747-760.
42. Ozden I, Sullivan MR, Lee HM, Wang SS (2009) Reliable coding emerges from coactivation of climbing fibers in microbands of cerebellar Purkinje neurons. J Neurosci 29:10463-10473.
43. Welsh JP, Lang EJ, Suglhara I, Llinás R (1995) Dynamic organization of motor control within the olivocerebellar system. Nature 374:453-457.
44. Ghosh KK, et al. (2011) Miniaturized integration of a fluorescence microscope. Nat Methods 8:871-878.
45. Person AL, Raman IM (2012) Purkinje neuron synchrony elicits time-locked spiking in the cerebellar nuclei. Nature 481:502-505.
46. Sugihara I, et al. (2009) Projection of reconstructed single Purkinje cell axons in relation to the cortical and nuclear aldolase C compartments of the rat cerebellum. J Comp Neurol 512:282-304.
47. Pugh JR, Raman IM (2006) Potentiation of mossy fiber EPSCs in the cerebellar nuclei by NMDA receptor activation followed by postinhibitory rebound current. Neuron 51: 113-123. (Pubitemid 43963335)
48. Hansel C, Linden DJ, D'Angelo E (2001) Beyond parallel fiber LTD: The diversity of synaptic and non-synaptic plasticity in the cerebellum. Nat Neurosci 4:467-475. (Pubitemid 32397183)
49. Pakaprot N, Karakossian M, Robleto K, Thompson R, Otis T (2007) The mechanism and role of cerebellar HCCs on the acquisition of standard-delay eyeblink conditioning memory. Online Soc Neurosci Mtg Planner 409:20.
50. Mittmann W, Koch U, Häusser M (2005) Feed-forward inhibition shapes the spike output of cerebellar Purkinje cells. J Physiol 563:369-378. (Pubitemid 40360898)