Inhibiting the Expression of a Classically Conditioned Behavior Prevents Its Extinction

Journal of Neuroscience

Volumn 23, Issue 33, 2003, Pages 10577-10584

  Krupa, David J ^a,b   Thompson, Richard F ^a  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^b DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Classical conditioning; Extinction; Eye blink; Learning; Memory; Motor nuclei

Indexed keywords

MUSCIMOL; SODIUM CHLORIDE;

ABDUCENS NERVE; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONDITIONING; CONTROLLED STUDY; EYELID REFLEX; FACIAL NERVE NUCLEUS; MEMORY; MOTONEURON NUCLEUS; NERVE CELL; NEUROANATOMY; NONHUMAN; PRIORITY JOURNAL; RABBIT; REINFORCEMENT; STIMULUS RESPONSE; TASK PERFORMANCE;

EID: 0344874564     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.23-33-10577.2003     Document Type: Article

References (58)

1. Akase E, Alkon DL, Disterhoft JF (1989) Hippocampal lesions impair memory of short delay conditioned eye blink in rabbits. Behav Neurosci 103:935-943.
2. Bailey DJ, Kim JJ, Sun W, Thompson RF, Helmstetter FJ (1999) Acquisition of fear conditioning in rats requires the synthesis of mRNA in the amygdala. Behav Neurosci 113:276-282.
3. Bao S, Chen L, Kim JJ, Thompson RF (2002) Cerebellar cortical inhibition and classical eyeblink conditioning. Proc Natl Acad Sci USA 99:1592-1597.
4. Berger TW, Alger BE, Thompson RF (1976) Neuronal substrate of classical conditioning in the hippocampus. Science 192:483-485.
5. Berthier NE, Moore JW (1990) Activity of deep cerebellar nuclear cells during classical conditioning of nictitating membrane extension in rabbits. Exp Brain Res 83:44-54.
6. Bouton ME (1984) Differential control by context in the inflation and rein-statement paradigms. J Exp Psychol Anim Behav Process 10:56-74.
7. Bouton ME, Swartzentruber D (1991) Sources of relapse after extinction in Pavlovian and instrumental learning. Clin Psychol Rev 11:123-140.
8. Christian KM, Thompson RF (2003) Neural substrates of eyeblink conditioning: acquisition and retention. Learn Mem, in press.
9. Clark RE, Lavond DG (1993) Reversible lesions of the red nucleus during acquisition and retention of a classically conditioned behavior in rabbits. Behav Neurosci 107:264-270.
10. 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.
11. Disterhoft JF, Coulter DA, Alkon DL (1986) Conditioning-specific membrane changes of rabbit hippocampal neurons measured in vitro. Proc Natl Acad Sci USA 83:2733-2737.
12. Falls WA (1998) Extinction: a review of theory and evidence suggesting that memories are not erased with non-reinforcement. In: Learning and behavior therapy (O'Donohue W, ed), pp 205-229. Boston: Allyn & Bacon.
13. Garcia KS, Steele PM, Mauk MD (1999) Cerebellar cortex lesions prevent acquisition of conditioned eyelid responses. J Neurosci 19:10940-10947.
14. Gould TJ, Steinmetz JE (1996) Changes in rabbit cerebellar cortical and interpositus nucleus activity during acquisition, extinction, and backward classical eyelid conditioning. Neurobiol Learn Mem 65:17-34.
15. Hardiman MJ, Ramnani N, Yeo CH (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.
16. Herry C, Garcia R (2002) Prefrontal cortex long-term potentiation, but not long-term depression, is associated with the maintenance of extinction of learned fear in mice. J Neurosci 22:577-583.
17. Hesslow G, Ivarsson M (1996) Inhibition of the inferior olive during conditioned responses in the decerebrate ferret. Exp Brain Res 110:36-46.
18. Holland PC, Rescorla RA (1975) The effect of two ways of devaluing the unconditioned stimulus after first- and second-order appetitive conditioning. J Exp Psychol Anim Behav Process 1:355-363.
19. Kim JJ, Krupa DJ, Thompson RF (1998) Inhibitory cerebello-olivary projections and blocking effect in classical conditioning. Science 279:570-573.
20. Krupa DJ, Thompson RF (1993) Effects of reversible lesions on extinction of the rabbits classically conditioned eyeblink response. Soc Neurosci Abstr 19:999.
21. Krupa DJ, Thompson RF (1995) Inactivation of the superior cerebellar peduncle blocks expression but not acquisition of the rabbit's classically conditioned eye-blink response. Proc Natl Acad Sci USA 92:5097-5101.
22. Krupa DJ, Thompson RF (1997) Reversible inactivation of the cerebellar interpositus nucleus completely prevents acquisition of the classically conditioned eye-blink response. Learn Mem 3:545-556.
23. Krupa DJ, Thompson JK, Thompson RF (1993) Localization of a memory trace in the mammalian brain. Science 260:989-991.
24. Krupa DJ, Weng J, Thompson RF (1996) Inactivation of brainstem motor nuclei blocks expression but not acquisition of the rabbit's classically conditioned eyeblink response. Behav Neurosci 110:219-227.
25. Lattal KM, Abel T (2001) Different requirements for protein synthesis in acquisition and extinction of spatial preferences and context-evoked fear. J Neurosci 21:5773-5780.
26. Macrae M, Kehoe EJ (1999) Savings after extinction in conditioning of the rabbit's nictitating membrane response. Psychobiology 27:85-94.
27. Mamounas LA, Thompson RF, Madden JT (1987) Cerebellar GABAergic processes: evidence for critical involvement in a form of simple associative learning in the rabbit. Proc Natl Acad Sci USA 84:2101-2105.
28. McBride RL, Klemm WR (1968) Stereotaxic atlas of the rabbit brain, based on the rapid method of photograpy of frozen, unstained sections. Commun Behav Biol 2:175-215.
29. McCormick DA, Thompson RF (1984) Neuronal responses of the rabbit cerebellum during acquisition and performance of a classically conditioned nictitating membrane-eyelid response. J Neurosci 4:2811-2822.
30. 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.
31. Medina JF, Garcia KS, Mauk MD (2001) A mechanism for savings in the cerebellum. J Neurosci 21:4081-4089.
32. Medina JF, Nores WL, Mauk MD (2002) Inhibition of climbing fibres is a signal for the extinction of conditioned eyelid responses. Nature 416:330-333.
33. Napier RM, Macrae M, Kehoe EJ (1992) Rapid reacquisition in conditioning of the rabbit's nictitating membrane response. J Exp Psychol Anim Behav Process 18:182-192.
34. Nelson BJ, Adams JC, Barmack NH, Mugnaini E (1989) Comparative study of glutamate decarboxylase immunoreactive boutons in the mammalian inferior olive. J Comp Neurol 286:514-539.
35. Nordholm AF, Thompson JK, Dersarkissian C, Thompson RF (1993) Lidocaine infusion in a critical region of cerebellum completely prevents learning of the conditioned eyeblink response. Behav Neurosci 107:882-886.
36. Nores WL, Medina JF, Steele PM, Mauk MD (2000) Relative contributions of cerebellar cortex and cerebellar nucleus to eyelid conditioning. In: Eyeblink classical conditioning: animal models (Woodruff-Pak DS, Steinmetz JE, eds). Boston: Kluwer Academic.
37. Pavlov IP (1927) Conditioned reflexes: an investigation of the physiological activity of the cerebral cortex. London: Oxford UP.
38. Perrett SP, Mauk MD (1995) Extinction of conditioned eyelid responses requires the anterior lobe of cerebellar cortex. J Neurosci 15:2074-2080.
39. Quirk GJ, Russo GK, Barron JL, Lebron K (2000) The role of ventromedial prefrontal cortex in the recovery of extinguished fear. J Neurosci 20:6225-6231.
40. Ramnani N, Yeo CH (1996) Reversible inactivations of the cerebellum prevent the extinction of conditioned nictitating membrane responses in rabbits. J Physiol (Lond) 495:159-168.
41. Rescorla RA (1993) Inhibitory associations between S and R in extinction. Anim Learn Behav 21:327-336.
42. Rescorla RA (1995) Full preservation of a response-outcome association through training with a second outcome. Q J Exp Psychol B 48:252-261.
43. Rescorla RA (1997) Response-inhibition in extinction. Q J Exp Psychol B 50:238-252.
44. Rescorla RA, Heth CD (1975) Reinstatement of fear to an extinguished conditioned stimulus. J Exp Psychol Anim Behav Process 1:88-96.
45. Rescorla RA, Skucy JC (1969) Effect of response-independent reinforcers during extinction. J Comp Physiol Psychol 67:381-389.
46. Rescorla RA, Wagner AR (1972) A theory of Pavlovian conditioning: variations in the effectiveness of reinforcement and nonreinforcement. In: Classical conditioning: II. Current research and theory (Black A, Prokasy WF, eds), pp 64-99. New York: Appleton-Century-Crofts.
47. Scavio MJ, Thompson RF (1979) Extinction and reacquisition performance alternations of the conditioned nictitating membrane response. Bull Psychon Soc 13:57-60.
48. Sears LL, Steinmetz JE (1991) Dorsal accessory inferior olive activity diminishes during acquisition of the rabbit classically conditioned eyelid response. Brain Res 545:114-122.
49. Steinmetz JE (1990) Neural activity in the cerebellar interpositus nucleus during classical NM conditioning with a pontine stimulation CS. Psychol Sci 1:378-382.
50. Steinmetz JE (2000) Brain substrates of classical eyeblink conditioning: a highly localized but also distributed system. Behav Brain Res 110:13-24.
51. Thompson RF (1986) The neurobiology of learning and memory. Science 233:941-947.
52. Thompson RF, Krupa DJ (1994) Organization of memory traces in the mammalian brain. Annu Rev Neurosci 17:519-549.
53. Voneida TJ, Christie D, Bogdanski R, 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.
54. Wagner AR (1971) Elementary associations. In: Essays in neo-behaviourism: a memorial volume to Kenneth W. Spence (Kendler HH, Spence JT, eds), pp 187-213. New York: Appleton-Century-Crofts.
55. Weiss C, Logan CG, Thompson RF (1991) Effects of cerebellar cortical lesions on extinction and reacquisition of NM conditioning in rabbits. Soc Neurosci Abstr 17:869.
56. Woodruff-Pak DS, Steinmetz JE (2000) Eyeblink classical conditioning: animal models. Boston, MA: Kluwer Academic.
57. Woody CD (1982) Memory, learning, and higher function. New York: Springer.
58. Yeo CH, Hesslow G (1998) Cerebellum and conditioned reflexes. Trends Cogn Sci 2:322-330.