Developmental changes in eyeblink conditioning and neuronal activity in the pontine nuclei

Learning and Memory

Volumn 10, Issue 5, 2003, Pages 337-345

  Freeman Jr , John H ^a   Muckler, Adam S ^a  

^a E11 SSH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CLIMBING FIBER; CONDITIONING; CONTROLLED STUDY; ELECTROPHYSIOLOGY; EYELID REFLEX; FACILITATION; NERVE GROWTH; NERVE POTENTIAL; NEUROPHYSIOLOGY; NONHUMAN; PONS ANGLE; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; RAT; STIMULUS RESPONSE; TRAINING;

ACTION POTENTIALS; ANIMALS; BLINKING; CONDITIONING, EYELID; ELECTROPHYSIOLOGY; NEURONS; PONS; RATS; RATS, LONG-EVANS;

EID: 0142026344     PISSN: 10720502     EISSN: None     Source Type: Journal    
DOI: 10.1101/lm.63703     Document Type: Article

References (78)

1. Aitkin, L.M. and Boyd, J. 1978. Acoustic input to the lateral pontine nuclei. Hear. Res. 1: 67-77.
2. Andersson, G., Garwicz, M., and Hesslow, G. 1988. Evidence for a GABA-mediated cerebellar inhibition of the inferior olive in the cat. Exp. Brain Res. 72: 450-456.
3. Attwell, P.J., Rahman, S.; and Yeo C.H. 2001. Acquisition of eyeblink conditioning is critically dependent on normal function in cerebellar cortical lobule HVI. J. Neurosci. 21: 5715-5722.
4. Attwell, P.J., Cooke, S.F., and Yeo, C.H. 2002. Cerebellar function in consolidation of a motor memory. Neuron 34: 1011-1020.
5. Bao S., Chen, L., and Thompson, R.F. 2000. Learning- and cerebellum-dependent neuronal activity in the lateral pontine nucleus. Behav. Neurosci. 114: 254-261.
6. Bao, S., Chen, L., Kim, J.J., and Thompson, R.F. 2002. Cerebellar cortical inhibition and classical eyeblink conditioning. Proc. Natl. Acad. Sci. 99: 1592-1597.
7. Berthier, N.E. and Moore, J.W. 1986. Cerebellar Purkinje cell activity related to the classically conditioned nictitating membrane response. Exp. Brain Res. 63: 341-350.
8. -. 1990. Activity of deep cerebellar nuclear cells during classical conditioning of nictitating membrane extension in rabbits. Exp. Brain Res. 83: 44-54.
9. Cartford, M.C., Gohl, E.B., Singson, M., and Lavond, D.G. 1997. The effects of reversible inactivation of the red nucleus on learning-related and auditory-evoked unit activity in the pontine nuclei of classically conditioned rabbits. Learn. Mem. 3: 519-531.
10. Chapman, P.F., Steinmetz, J.E., Sears, L.L., and Thompson, R.F. 1990. Effects of lidocaine injection in the interpositus nucleus and red nucleus on conditioned behavioral and neuronal responses. Brain Res. 537: 149-156.
11. Clark, G.A., McCormick, D.A., Lavond, D.G., and Thompson, R.F. 1984. Effects of lesions of cerebellar nuclei on conditioned behavioral and hippocampal neuronal responses. Brain Res. 291: 125-136.
12. Clark, R.E., Zhang, A.A., and Lavond, D.G. 1992. Reversible lesions of the cerebellar interpositus nucleus during acquisition and retention of a classically conditioned behavior. Behav. Neurosci. 106: 879-888.
13. Clark, R.E., Gohl, E.B., and Lavond, D.G. 1997. The learning-related activity that develops in the pontine nuclei during classical eye-blink conditioning is dependent on the interpositus nucleus. Learn. Mem. 3: 532-544.
14. de Zeeuw, C.I., van Alphen, A.M., Hawkins, R.K., and Ruigrok, T.J. 1997. Climbing fiber collaterals contact neurons in the cerebellar nuclei that provide a GABAergic feedback to the inferior olive. Neuroscience 80: 981-986.
15. Freeman Jr., J.H. and Nicholson, D.A. 1999. Neuronal activity in the cerebellar interpositus and lateral pontine nuclei during inhibitory classical conditioning of the eyeblink response. Brain Res. 833: 225-233.
16. -. 2000. Developmental changes in eye-blink conditioning and neuronal activity in the cerebellar interpositus nucleus. J. Neurosci. 20: 813-819.
17. -. 2001. Ontogenetic changes in the neural mechanisms of eyeblink conditioning. Integrative Physiol. Behav. Sci. 36: 15-35.
18. Garcia, K.S. and Mauk, M.D. 1998. Pharmacological analysis of cerebellar contributions to the timing and expression of conditioned eyelid responses. Neuropharmacology 37: 471-480.
19. Garcia, K.S., Steele, P.M., and Mauk, M.D. 1999. Cerebellar cortex lesions prevent acquisition of conditioned eyelid responses. J. Neurosci. 19: 10940-10947.
20. Gormezano, I., Kehoe, E.J., and Marshall, B.S. 1983. Twenty years of classical conditioning research with the rabbit. Prog. Psychobiol. Physiol. Psych. 10: 197-275.
21. Gould, T.J. and Steinmetz, J.E. 1994. Multiple-unit activity from rabbit cerebellar cortex and interpositus nucleus during classical discrimination/reversal eyelid conditioning. Brain Res. 652: 98-106.
22. Gould, T.J., Sears, L.L., and Steinmetz, J.E. 1993. Possible CS and US pathways for rabbit classical eyelid conditioning: Electrophysiological evidence for projections from the pontine nuclei and inferior olive to cerebellar cortex and nuclei. Behav. Neur. Biol. 60: 172-185.
23. Hardiman, M.J., Ramnani, N., and Yeo, C.H. 1996. Reversible inactivations of the cerebellum with muscimol prevent the acquisition and extinction of conditioned nictitating membrane responses in the rabbit. Exp. Brain Res. 110: 235-247.
24. Harvey, J.A., Land, T., and McMaster, S.E. 1984. Anatomical study of the rabbit's corneal-VIth nerve reflex: Connections between cornea, trigeminal sensory complex, and the abducens and accessory abducens nuclei. Brain Res. 301: 307-321.
25. Hesslow, G. and Ivarsson, M. 1994. Suppression of cerebellar Purkinje cells during conditioned responses in ferrets. NeuroReport 5: 649-652.
26. -. 1996. Inhibition of the inferior olive during conditioned responses in the decerebrate ferret. Exp. Brain Res. 110: 36-46.
27. Katz, D.B. and Steinmetz, J.E. 1997. Single-unit evidence for eye-blink conditioning in cerebellar cortex is altered, but not eliminated, by interpositus nucleus lesions. Learn. Mem. 4: 88-104.
28. Kim, J.J., Krupa, D.J., and Thompson, R.F. 1998. Inhibitory cerebello-olivary projections and blocking effect in classical conditioning. Science 279: 570-573.
29. Kitai, S.T., McCrea, R.A., Preston, R.J., and Bishop, G.A. 1977. Electrophysiological and horseradish peroxidase studies of precerebellar afferents to the nucleus interpositus anterior. I. Climbing fiber system. Brain Res. 122: 197-214.
30. Krupa, D.J. and Thompson, R.F. 1997. Reversible inactivation of the cerebellar interpositus nucleus completely prevents acquisition of the classically conditioned eye-blink response. Learn. Mem. 3: 545-556.
31. Krupa, D.J., Thompson, J.K., and Thompson, R.F. 1993. Localization of a memory trace in the mammalian brain. Science 260: 989-991.
32. Kubota, Y., Wolske, M., Poremba, A., Kang, E., and Gabriel, M. 1996. Stimulus-related and movement-related single-unit activity in rabbit cingulate cortex and limbic thalamus during performance of discriminative avoidance behavior. Brain Res. 721: 22-38.
33. Lang, E.J., Sugihara, I., and Llinas, R. 1996. GABAergic modulation of complex spike activity by the cerebellar nucleoolivary pathway in rat. J. Neurophys. 76: 255-275.
34. Lavond, D.G. and Steinmetz, J.E. 1989. Acquisition of classical conditioning without cerebellar cortex. Behav. Brain Res. 33: 113-164.
35. Lavond, D.G., Hembree, T.L., and Thompson, R.F. 1985. Effect of kainic acid lesions of the cerebellar interpositus nucleus on eyelid conditioning. Brain Res. 326: 179-182.
36. Lavond, D.G., Steinmetz, J.E., Yokaitis, M.H., and Thompson, R.F. 1987. Reacquisition of classical conditioning after removal of cerebellar cortex. Exp. Brain Res. 67: 569-593.
37. Mauk, M.D., Steinmetz, J.E., and Thompson, R.F. 1986. Classical conditioning using stimulation of the inferior olive as the unconditioned stimulus. Proc. Natl. Acad. Sci. 83: 5349-5353.
38. McCormick, D.A. and Thompson, R.F. 1984a. Cerebellum: Essential involvement in the classically conditioned eyelid response. Science 223: 296-299.
39. -. 1984b. Neuronal responses of the rabbit cerebellum during acquisition and performance of a classically conditioned nictitating membrane-eyelid response. J. Neurosci. 11: 2811-2822.
40. McCormick, D.A., Clark, G.A., Lavond, D.G., and Thompson, R.F. 1982. Initial localization of the memory trace for a basic form of learning. Proc. Natl. Acad. Sci. 79: 2731-2735.
41. McCormick, D.A., Lavond, D.G., and Thompson, R.F. 1983. Neuronal responses of the rabbit brainstem during performance of the classically conditioned nictitating membrane (NM)/eyelid response. Brain Res. 271: 73-88.
42. McCormick, D.A., Steinmetz, J.E., and Thompson, R.F. 1985. Lesions of the inferior olivary complex cause extinction of the classically conditioned eyeblink response. Brain Res. 359: 120-130.
43. McCrea, R.A., Bishop, G.A., and Kitai, S.T. 1977. Electrophysiological and horseradish peroxidase studies of precerebellar afferents to the nucleus interpositus anterior. II. Mossy fiber system. Brain Res. 122: 215-228.
44. Medina, J.F. and Mauk, M.D. 2000. Computer simulation of cerebellar information processing. Nat. Neurosci. 3: 1205-1211.
45. Medina, J.F., Garcia, K.S., Nores, W.L., Taylor, N.M., and Mauk, M.D. 2000. Timing mechanisms in the cerebellum: Testing predictions of a large-scale computer simulation. J. Neurosci. 20: 5516-5525.
46. Medina, J.F., Nores, W.L., and Mauk, M.D. 2002. Inhibition of climbing fibres is a signal for the extinction of conditioned eyelid responses. Nature 416: 330-333.
47. Mihailoff, G.A. 1993. Cerebellar nuclear projections from the basilar pontine nuclei and nucleus reticularis tegmenti pontis as demonstrated with PHA-L tracing in the rat. J. Comparative Neurol. 330: 130-146.
48. Nicholson, D.A. and Freeman Jr., J.H. 2000. Developmental changes in eye-blink conditioning and neuronal activity in the inferior olive. J. Neurosci. 20: 8218-8226.
49. -. 2002. Neuronal correlates of conditioned inhibition of the eyeblink response in the anterior interpositus nucleus. Behav. Neurosci. 116: 22-36.
50. -. 2003. Addition of inhibition in the olivocerebellar system and the ontogeny of a motor memory. Nat. Neurosci. 6: 532-537.
51. Parenti, R., Zappala, A., Serapide, M.F., Panto, M.R., and Cicirata, F. 2002. Projections of the basilar pontine nuclei and nucleus reticularis tegmenti pontis to the cerebellar nuclei of the rat. J. Comparative Neurol. 452: 115-127.
52. Perrett, S.P., Ruiz, B.P., and Mauk, M.D. 1993. Cerebellar cortex lesions disrupt learning-dependent timing of conditioned eyelid responses. J. Neurosci. 13: 1708-1718.
53. Schreurs, B.G. 1988. Stimulation of the spinal trigeminal nucleus supports classical conditioning of the rabbit's nictitating membrane response. Behav. Neurosci. 102: 163-172.
54. Sears, L.L. and Steinmetz, J.E. 1991. Dorsal accessory inferior olive activity diminishes during acquisition of the rabbit classically conditioned eyelid response. Brain Res. 545: 114-122.
55. Skelton, R.W. 1988. Bilateral cerebellar lesions disrupt conditioned eyelid responses in unrestrained rats. Behav. Neurosci. 102: 586-590.
56. Stanton, M.E. and Freeman Jr., J.H. 2000. Developmental studies of eyeblink conditioning in a rat model. In Eyeblink classical conditioning: Animal models (eds. D.S. Woodruff-Pak and J.E. Steinmetz), Vol. 2., pp. 105-134. Kluwer Academic Publishers, Amsterdam.
57. Stanton, M.E., Freeman Jr., J.H., and Skelton, R.W. 1992. Eyeblink conditioning in the developing rat. Behav. Neurosci. 106: 657-665.
58. Steinmetz, J.E. 1990. Neuronal activity in the rabbit interpositus nucleus during classical NM-conditioning with a pontine-nucleus-stimulation CS. Psych. Sci. 1: 378-382.
59. Steinmetz, J.E. and Sengelaub, D.R. 1992. Possible conditioned stimulus pathway for classical eyelid conditioning in rabbits. Behav. Neur. Biol. 57: 103-115.
60. Steinmetz, J.E., Lavond, D.G., and Thompson, R.F. 1985. Classical conditioning of the rabbit eyelid response with mossy fiber stimulation as the conditioned stimulus. Bull. Psychonomic Soc. 23: 245-248.
61. Steinmetz, J.E., Rosen, D.J., Chapman, P.F., Lavond, D.G., and Thompson, R.F. 1986. Classical conditioning of the rabbit eyelid response with a mossy fiber stimulation CS. I. Pontine nuclei and middle cerebellar peduncle stimulation. Behav. Neurosci. 100: 878-887.
62. Steinmetz, J.E., Logan, C.G., Rosen, D.J., Thompson, J.K., Lavond, D.G., and Thompson, R.F. 1987. Initial localization of the acoustic conditioned stimulus projection system to the cerebellum essential for classical eyelid conditioning. Proc. Natl. Acad. Sci. 84: 3531-3535.
63. Steinmetz, J.E., Lavond, D.G., and Thompson, R.F. 1989. Classical conditioning in rabbits using pontine nucleus stimulation as a conditioned stimulus and inferior olive stimulation as an unconditioned stimulus. Synapse 3: 225-233.
64. Steinmetz, J.E., Lavond, D.G., Ivkovich, D., Logan, C.G., and Thompson, R.F. 1992. Disruption of classical eyelid conditioning after cerebellar lesions: Damage to a memory trace system or simple performance deficit? J. Neurosci. 12: 4403-4426.
65. Sugihara, I., Wu, H.S., and Shinoda Y. 2001. The entire trajectories of single olivocerebellar axons in the cerebellar cortex and their contribution to cerebellar compartmentalization. J. Neurosci. 21: 7715-7723.
66. Thompson, R.F. 2000. Discovering the brain substrates of eyeblink classical conditioning. In Eyeblink classical conditioning: Animal models (eds. D.S. Woodruff-Pak and J.E. Steinmetz), Vol. 2., pp. 17-49. Kluwer Academic Publishers, Amsterdam.
67. Thompson, R.F. and Krupa, D.J. 1994. Organization of memory traces in the mammalian brain. Ann. Rev. Neurosci. 17: 519-549.
68. Thompson, R.F., Thompson, J.K., Kim, J.J., Krupa, D.J., and Shinkman, P.G. 1998. The nature of reinforcement in cerebellar learning. Neurobiol. Learn. Mem. 70: 150-176.
69. Tracy, J.A., Thompson, J.K., Krupa, D.J., and Thompson, R.F. 1998. Evidence of plasticity in the pontocerebellar conditioned stimulus pathway during classical conditioning of the eyeblink response in the rabbit. Behav. Neurosci. 112: 267-285.
70. van der Want, J.J.L., Wiklund, L., Guegan, M., Ruigrok, T., and Voogd, J. 1989. Anterograde tracing of the rat olivocerebellar system with Phaseolus vulgaris leucoagglutinin (PHA-L). Demonstration of climbing fiber collateral innervation of the cerebellar nuclei. J. Comparative Neurol. 288: 1-18.
71. van Ham, J.J. and Yeo, C.H. 1996. The central distribution of primary afferents from the external eyelids, conjunctiva, and cornea in the rabbit, studied using WGA-HRP and B-HRP as transganglionic tracers. Exp. Neurol. 142: 217-225.
72. Voneida, T.J., Christie, D., Bogdanski, R., and Chopko, B. 1990. Changes in instrumentally and classically conditioned limb-flexion responses following inferior olivary lesions and olivocerebellar tractotomy in the cat. J. Neurosci. 10: 3583-3593.
73. Welsh, J.P. and Harvey, J.A. 1998. Acute inactivation of the inferior olive blocks associative learning. Eur. J. Neurosci. 10: 3321-3332.
74. Yeo, C.H. and Hardiman, M.J. 1992. Cerebellar cortex and eyeblink conditioning: A reexamination. Exp. Brain Res. 88: 623-638.
75. Yeo, C.H. and Hesslow, G. 1998. Cerebellum and conditioned reflexes. Trends Cog. Sci. 2: 322-330.
76. Yeo, C.H., Hardiman, M.J., and Glickstein, M. 1985a. Classical conditioning of the nictitating membrane response of the rabbit. I. Lesions of the cerebellar nuclei. Exp. Brain Res. 60: 87-98.
77. -. 1985b. Classical conditioning of the nictitating membrane response of the rabbit. II. Lesions of the cerebellar cortex. Exp. Brain Res. 60: 99-113.
78. -. 1986. Classical conditioning of the nictitating membrane response of the rabbit. IV. Lesions of the inferior olive. Exp. Brain Res. 63: 81-92.