Temporal patterns of inputs to cerebellum necessary and sufficient for trace eyelid conditioning

Journal of Neurophysiology

Volumn 104, Issue 2, 2010, Pages 627-640

  Kalmbach, Brian E ^a,b   Ohyama, Tatsuya ^a   Mauk, Michael D ^a  

^a UNIVERSITY OF TEXAS AT AUSTIN   (United States)

^b UNIVERSITY OF TEXAS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ARTICLE; BRAIN DEPTH STIMULATION; CEREBELLUM; CEREBELLUM NUCLEUS; COMPUTER SIMULATION; ELECTROENCEPHALOGRAM; FOREBRAIN; MALE; NERVE CELL PLASTICITY; NONHUMAN; PREFRONTAL CORTEX; PRIORITY JOURNAL; PURKINJE CELL; STIMULUS RESPONSE;

ACOUSTIC STIMULATION; ANIMALS; CEREBELLUM; COMPUTER SIMULATION; CONDITIONING, CLASSICAL; CONDITIONING, EYELID; ELECTRIC STIMULATION; GABA ANTAGONISTS; MALE; MODELS, BIOLOGICAL; NERVE FIBERS; NEURAL PATHWAYS; NEURONAL PLASTICITY; PYRIDAZINES; RABBITS; REACTION TIME;

EID: 77955967031     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00169.2010     Document Type: Article

References (68)

1. Aitkin LM, Boyd J. Acoustic input to the lateral pontine nuclei. Hear Res 1: 67-77, 1978. (Pubitemid 9170343)
2. Bao S, Chen L, Kim JJ, Thompson RF. Cerebellar cortical inhibition and classical eyeblink conditioning. Proc Natl Acad Sci USA 99: 1592-1597, 2002.
3. Blum S, Hebert AE, Dash PK. A role for the prefrontal cortex in recall of recent and remote memories. Neuroreport 17: 341-344, 2006. (Pubitemid 43298030)
4. Boyd J, Aitkin LM. Responses of single units in the pontine nuclei of the cat to acoustic stimulation. Neurosci Lett 3: 259-263, 1976.
5. Bracha V, Zbarska S, Parker K, Carrel A, Zenitsky G, Bloedel JR. The cerebellum and eye-blink conditioning: learning versus network performance hypotheses. Neuroscience 162: 787-796, 2009.
6. Buchanan SL, Thompson RH, Maxwell BL, Powell DA. Efferent connections of the medial prefrontal cortex in the rabbit. Exp Brain Res 100: 469-483, 1994.
7. Clark RE, Manns JR, Squire LR. Classical conditioning, awareness, and brain systems. Trends Cogn Sci 6: 524-531, 2002.
8. Coesmans M, Weber JT, De Zeeuw CI, Hansel C. Bidirectional parallel fiber plasticity in the cerebellum under climbing fiber control. Neuron 44: 691-700, 2004. (Pubitemid 39531232)
9. Flores LC, Disterhoft JF. Caudate nucleus is critically involved in trace eyeblink conditioning. J Neurosci 29: 14511-14520, 2009.
10. Freeman JH Jr, Muckler AS. Developmental changes in eyeblink conditioning and neuronal activity in the pontine nuclei. Learn Mem 10: 337-345, 2003.
11. Galvez R, Weible AP, Disterhoft JF. Cortical barrel lesions impair whisker-CS trace eyeblink conditioning. Learn Mem 14: 94-100, 2007.
12. Garcia KS, Mauk MD. Pharmacological analysis of cerebellar contributions to the timing and expression of conditioned eyelid responses. Neuropharmacology 37: 471-480, 1998.
13. Garcia KS, Steele PM, Mauk MD. Cerebellar cortex lesions prevent acquisition of conditioned eyelid responses. J Neurosci 19: 10940-10947, 1999.
14. Goldman-Rakic PS. Cellular basis of working memory. Neuron 14: 477-485, 1995.
15. Goldman-Rakic PS. Regional and cellular fractionation of working memory. Proc Natl Acad Sci USA 93: 13473-13480, 1996.
16. Hesslow G. Correspondence between climbing fibre input and motor output in eyeblink-related areas in cat cerebellar cortex. J Physiol 476: 229-244, 1994. (Pubitemid 24129806)
17. Ito M. The Cerebellum and Neural Control. New York: Raven Press, 1984, p. 300-302.
18. 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.
19. Kalmbach BE, Davis T, Ohyama T, Riusech F, Nores WL, Mauk MD. Cerebellar cortex contributions to the expression and timing of conditioned eyelid responses. J Neurophysiol 103: 2039-2049, 2010.
20. Kalmbach BE, Ohyama T, Kreider JC, Riusech F, Mauk MD. Interactions between prefrontal cortex and cerebellum revealed by trace eyelid conditioning. Learn Mem 16: 86-95, 2009.
21. Kehoe EJ, Napier RM. In the blink of an eye: real-time stimulus factors in delay and trace conditioning of the rabbit's nictitating membrane response. Q J Exp Psychol B 43: 257-277, 1991.
22. Kehoe EJ, Weideman G. Within-stimulus competition in trace conditioning of the rabbit's nictitating membrane response. Psychobiology 27: 72-84, 1999.
23. Kim JJ, Clark RE, Thompson RF. Hippocampectomy impairs the memory of recently, but not remotely, acquired trace eyeblink conditioned responses. Behav Neurosci 109: 195-203, 1995.
24. Kishimoto Y, Kawahara S, Fujimichi R, Mori H, Mishina M, Kirino Y. Impairment of eyeblink conditioning in GluRdelta2-mutant mice depends on the temporal overlap between conditioned and unconditioned stimuli. Eur J Neurosci 14: 1515-1521, 2001a.
25. Kishimoto Y, Kawahara S, Suzuki M, Mori H, Mishina M, Kirino Y. Classical eyeblink conditioning in glutamate receptor subunit delta 2 mutant mice is impaired in the delay paradigm but not in the trace paradigm. Eur J Neurosci 13: 1249-1253, 2001b.
26. Koekkoek SK, Hulscher HC, Dortland BR, Hensbroek RA, Elgersma Y, Ruigrok TJ, De Zeeuw CI. Cerebellar LTD and learning-dependent timing of conditioned eyelid responses. Science 301: 1736-1739, 2003.
27. Koekkoek SK, Yamaguchi K, Milojkovic BA, Dortland BR, Ruigrok TJ, Maex R, De Graaf W, Smit AE, VanderWerf F, Bakker CE, Willemsen R, Ikeda T, Kakizawa S, Onodera K, Nelson DL, Mientjes E, Joosten M, De Schutter E, Oostra BA, Ito M, De Zeeuw CI. Deletion of FMR1 in Purkinje cells enhances parallel fiber LTD, enlarges spines, and attenuates cerebellar eyelid conditioning in Fragile X syndrome. Neuron 47: 339-352, 2005.
28. Kronforst-Collins MA, Disterhoft JF. Lesions of the caudal area of rabbit medial prefrontal cortex impair trace eyeblink conditioning. Neurobiol Learn Mem 69: 147-162, 1998.
29. Lev-Ram V, Mehta SB, Kleinfeld D, Tsien RY. Reversing cerebellar long-term depression. Proc Natl Acad Sci USA 100: 15989-15993, 2003.
30. Lev-Ram V, Wong ST, Storm DR, Tsien RY. A new form of cerebellar long-term potentiation is postsynaptic and depends on nitric oxide but not cAMP. Proc Natl Acad Sci USA 99: 8389-8393, 2002.
31. Mauk MD, Ohyama T. Extinction as new learning versus unlearning: considerations from a computer simulation of the cerebellum. Learn Mem 11: 566-571, 2004. (Pubitemid 39299706)
32. Mauk MD, Thompson RF. Retention of classically conditioned eyelid responses following acute decerebration. Brain Res 403: 89-95, 1987.
33. McLaughlin J, Skaggs H, Churchwell J, Powell DA. Medial prefrontal cortex and pavlovian conditioning: trace versus delay conditioning. Behav Neurosci 116: 37-47, 2002.
34. Medina JF, Garcia KS, Mauk MD. A mechanism for savings in the cerebellum. J Neurosci 21: 4081-4089, 2001.
35. Medina JF, Garcia KS, Nores WL, Taylor NM, Mauk MD. Timing mechanisms in the cerebellum: testing predictions of a large-scale computer simulation. J Neurosci 20: 5516-5525, 2000.
36. Medina JF, Mauk MD. Simulations of cerebellar motor learning: computational analysis of plasticity at the mossy fiber to deep nucleus synapse. J Neurosci 19: 7140-7151, 1999.
37. Medina JF, Mauk MD. Computer simulation of cerebellar information processing. Nat Neurosci 3: 1205-1211, 2000.
38. Medina JF, Nores WL, Mauk MD. Inhibition of climbing fibres is a signal for the extinction of conditioned eyelid responses. Nature 416: 330-333, 2002. (Pubitemid 34260248)
39. Middleton FA, Strick PL. Basal ganglia and cerebellar loops: motor and cognitive circuits. Brain Res Brain Res Rev 31: 236-250, 2000.
40. Moyer JR Jr, Deyo RA, Disterhoft JF. Hippocampectomy disrupts trace eye-blink conditioning in rabbits. Behav Neurosci 104: 243-252, 1990.
41. Ohyama T, Nores WL, Mauk MD. Stimulus generalization of conditioned eyelid responses produced without cerebellar cortex: implications for plasticity in the cerebellar nuclei. Learn Mem 10: 346-354, 2003.
42. Ohyama T, Nores WL, Medina JF, Riusech FA, Mauk MD. Learning-induced plasticity in deep cerebellar nucleus. J Neurosci 26: 12656-12663, 2006.
43. Oswald B, Knuckley B, Mahan K, Sanders C, Powell DA. Prefrontal control of trace versus delay eyeblink conditioning: role of the unconditioned stimulus in rabbits (Oryctolagus cuniculus). Behav Neurosci 120: 1033-1042, 2006. (Pubitemid 44584014)
44. Oswald BB, Maddox SA, Powell DA. Prefrontal control of trace eyeblink conditioning in rabbits: role in retrieval of the CR? Behav Neurosci 122: 841-848, 2008.
45. Pasternak T, Greenlee MW. Working memory in primate sensory systems. Nat Rev Neurosci 6: 97-107, 2005.
46. Pavlov IP. Conditioned Reflexes; An Investigation of the Physiological Activity of the Cerebral Cortex. London: Oxford UP, 1927.
47. Perrett SP, Ruiz BP, Mauk MD. Cerebellar cortex lesions disrupt learning-dependent timing of conditioned eyelid responses. J Neurosci 13: 1708-1718, 1993.
48. Powell DA, Skaggs H, Churchwell J, McLaughlin J. Posttraining lesions of the medial prefrontal cortex impair performance of Pavlovian eyeblink conditioning but have no effect on concomitant heart rate changes in rabbits (Oryctolagus cuniculus). Behav Neurosci 115: 1029-1038, 2001.
49. Pugh JR, Raman IM. Potentiation of mossy fiber EPSCs in the cerebellar nuclei by NMDA receptor activation followed by postinhibitory rebound current. Neuron 51: 113-123, 2006.
50. Pugh JR, Raman IM. Mechanisms of potentiation of mossy fiber EPSCs in the cerebellar nuclei by coincident synaptic excitation and inhibition. J Neurosci 28: 10549-10560, 2008.
51. Quinn JJ, Ma QD, Tinsley MR, Koch C, Fanselow MS. Inverse temporal contributions of the dorsal hippocampus and medial prefrontal cortex to the expression of long-term fear memories. Learn Mem 15: 368-372, 2008. (Pubitemid 351629601)
52. Raymond JL, Lisberger SG. Neural learning rules for the vestibulo-ocular reflex. J Neurosci 18: 9112-9129, 1998.
53. Raymond JL, Lisberger SG, Mauk MD. The cerebellum: a neuronal learning machine? Science 272: 1126-1131, 1996.
54. Safo P, Regehr WG. Timing dependence of the induction of cerebellar LTD. Neuropharmacology 54: 213-218, 2008. (Pubitemid 350299402)
55. Schmahmann JD, Pandya DN. Prefrontal cortex projections to the basilar pons in rhesus monkey: implications for the cerebellar contribution to higher function. Neurosci Lett 199: 175-178, 1995.
56. Sears LL, Steinmetz JE. Dorsal accessory inferior olive activity diminishes during acquisition of the rabbit classically conditioned eyelid response. Brain Res 545: 114-122, 1991.
57. Siegel JJ, Kalmbach BE, Chitwood RA, Dembrow N, Johnston D, Mauk MD. Prefrontal cortex and lateral pontine neurons display tone-evoked persistent activity during trace eyelid conditioning. Soc Neurosci Abstr 384.9, 2009.
58. Solomon PR, Vander Schaaf ER, Thompson RF, Weisz DJ. Hippocampus and trace conditioning of the rabbit's classically conditioned nictitating membrane response. Behav Neurosci 100: 729-744, 1986.
59. Steinmetz JE, Logan CG, Rosen DJ, Thompson JK, Lavond DG, Thompson RF. Initial localization of the acoustic conditioned stimulus projection system to the cerebellum essential for classical eyelid conditioning. Proc Natl Acad Sci USA 84: 3531-3535, 1987.
60. Takehara K, Kawahara S, Kirino Y. Time-dependent reorganization of the brain components underlying memory retention in trace eyeblink conditioning. J Neurosci 23: 9897-9905, 2003.
61. Takehara-Nishiuchi K, McNaughton BL. Spontaneous changes of neocortical code for associative memory during consolidation. Science 322: 960-963, 2008.
62. Thompson RF, Steinmetz JE. The role of the cerebellum in classical conditioning of discrete behavioral responses. Neuroscience 162: 732-755, 2009.
63. Weible AP, McEchron MD, Disterhoft JF. Cortical involvement in acquisition and extinction of trace eyeblink conditioning. Behav Neurosci 114: 1058-1067, 2000.
64. Weible AP, Weiss C, Disterhoft JF. Connections of the caudal anterior cingulate cortex in rabbit: neural circuitry participating in the acquisition of trace eyeblink conditioning. Neuroscience 145: 288-302, 2007. (Pubitemid 46227723)
65. Weiss C, Disterhoft JF. Eyeblink conditioning, motor control, and the analysis of limbic-cerebellar interactions. Behav Brain Sci 19: 479-480, 1996.
66. Woodruff-Pak DS, Disterhoft JF. Where is the trace in trace conditioning? Trends Neurosci 31: 105-112, 2008.
67. Woodruff-Pak DS, Green JT, Levin SI, Meisler MH. Inactivation of sodium channel Scn8A (Na-sub(v)1.6) in Purkinje neurons impairs learning in Morris water maze and delay but not trace eyeblink classical conditioning. Behav Neurosci 120: 229-240, 2006.
68. Woodruff-Pak DS, Lavond DG, Thompson RF. Trace conditioning: abolished by cerebellar nuclear lesions but not lateral cerebellar cortex aspirations. Brain Res 348: 249-260, 1985.