Intracellular correlates of acquisition and long-term memory of classical conditioning in Purkinje cell dendrites in slices of rabbit cerebellar lobule HVI

Journal of Neuroscience

Volumn 18, Issue 14, 1998, Pages 5498-5507

  Schreurs, Bernard G ^a   Gusev, Pavel A ^a   Tomsic, Daniel ^a   Alkon, Daniel L ^a   Shi, Ting ^a  

^a NATIONAL INSTITUTE OF NEUROLOGICAL DISORDERS AND STROKE   (United States)

Author keywords

Cerebellum; Classical conditioning; Dendritic recording; Eyelid; Long term depression; Nictitating membrane; Purkinje cell; Rabbit; Slice

Indexed keywords

POTASSIUM CHANNEL;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONDITIONING; CONTROLLED STUDY; DENDRITE; EYELID; LONG TERM MEMORY; MALE; MOTONEURON; NERVE CELL EXCITABILITY; NICTITATING MEMBRANE; NONHUMAN; PRIORITY JOURNAL; PURKINJE CELL; PURKINJE FIBER MEMBRANE POTENTIAL; RABBIT; RED NUCLEUS;

EID: 0032527880     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.18-14-05498.1998     Document Type: Article

References (73)

1. Alkon DL (1984) Calcium-mediated reduction of ionic currents: a biophysical memory trace. Science 226:1037-1045.
2. Alkon DL (1989) Memory storage and neural systems. Sci Am 261:42-50.
3. Alkon DL, Lederhendler I, Shoukimas JJ (1982) Primary changes of membrane currents during retention of associative learning. Science 215:693-695.
4. Anderson CW, Keifer J (1997) The cerebellum and red nucleus are not required for in vitro classical conditioning of the turtle abducens nerve response. J Neurosci 17:9736-9745.
5. Andreasen NC, O'Leary DS, Arndt S, Cizadlo T, Hurtig R, Rezai K, Watkins GL, Boles Ponto LL, Hichiwa RD (1995) Short-term and long-term verbal memory: a positron emission tomography study. Proc Natl Acad Sci USA 92:5111-5115.
6. Berthier NE, Moore JW (1986) Cerebellar Purkinje cell activity related to the classically conditioned nictitating membrane response. Exp Brain Res 63:341-350.
7. Bloedel JR, Bracha V (1995) On the cerebellum, cutaneomuscular reflexes, movement control and the elusive engrams of memory. Behav Brain Res 68:1-44.
8. Chan-Palay V (1977) Cerebellar dentate nucleus. Berlin: Springer.
9. Chen C, Thompson RF (1995) Temporal specificity of long-term depression in parallel-Purkinje cell synapses in rat cerebellar slice. Learn Mem 2:185-198.
10. Collin C, Devan WA, Dahl D, Lee CJ, Axelrod J, Alkon DL (1995) Long-term synaptic transformation of hippocampal CA1 gamma-aminobutyric acid synapses and the effect of anandamide. Proc Natl Acad Sci USA 92:10167-10171.
11. Coulter DA, LoTurco J, Kubato M, Disterhoft JF, Alkon DL (1989) Classical conditioning alters the amplitude and time course of the calcium-dependent after hyperpolarization in rabbit hippocampal pyramidal cells. J Neurophysiol 61:971-981.
12. Cowan TM, Siegel RW (1986) Drosophila mutations that alter ionic conduction disrupts acquisition and retention of a conditioned odor avoidance response. J Neurogenet 3:187-201.
13. De Zeeuw CI, Berrebi AS (1995) Postsynaptic targets of Purkinje cell terminals in the cerebellar and vestibular nuclei of the rat. Eur J Neurosci 7:2322-2333.
14. Eccles JC, Ito M, Szentagothai J (1967) The cerebellum as a neuronal machine. Berlin: Springer.
15. Fiez JA (1996) Cerebellar contribution to cognition. Neuron 16:3-15.
16. Gormezano I (1966) Classical conditioning. In: Experimental methods and instrumentation in psychology (Sidowski JB, ed), pp 385-420. New York: McGraw-Hill.
17. Gormezano I, Schneiderman N, Deaux E, Fuentes I (1962) Nictitating membrane: classical conditioning and extinction in the albino rabbit. Science 138:33-34.
18. Gormezano I, Kehoe EJ, Marshall BS (1983) Twenty years of classical conditioning research with the rabbit. Prog Psychobiol Physiol Psychol 10:197-275.
19. Gould TJ, Steinmetz JE (1994) Multiple-unit activity from rabbit cerebellar cortex and interpositus nucleus during classical discrimination/ reversal eyelid conditioning. Brain Res 652:98-106.
20. 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.
21. Gruart A, Yeo CH (1995) Cerebellar cortex and eyeblink conditioning-bilateral regulation of conditioned responses. Exp Brain Res 104:431-438.
22. Hesslow G (1994a) Correspondence between climbing fibre input and motor output in eyeblink-related areas in cat cerebellar cortex. J Physiol (Lond) 476:229-244.
23. Hesslow G (1994b) Inhibition of classically conditioned eyeblink responses by stimulation of the cerbellar cortex in the decerebrate cat. J Physiol (Lond) 476:245-256.
24. Hesslow G, Ivarsson M (1994) Suppression of cerebellar Purkinje cells during conditioned responses in ferrets. NeuroReport 4:1127-1130.
25. Hounsgaard J, Midtgaard J (1988) Intrinsic determinants of firing pattern in Purkinje cells of the turtle cerebellum in vitro. J Physiol (Lond) 402:731-749.
26. Ito M (1989) Long-term depression. Annu Rev Neurosci 12:85-102.
27. Ivarsson M, Svensson P, Hesslow G (1997) Bilateral disruption of conditioned responses after unilateral blockade of cerebellar output in the decerrebrate ferret. J Physiol (Lond) 502:189-201.
28. Katz DB, Steinmetz JE (1997) Single-unit evidence for eye-blink conditioning in cerebellar cortex is altered, but not eliminated, by interpositus nucleus lesions. Learn Mem 3:88-104.
29. Kleim JA, Vij K, Ballard DH, Greenough WTJ (1997) Learning-dependent synaptic modifications in the cerebellar cortex of the adult rat persist for at least four weeks. J Neurosci 17:717-721.
30. LaLonde R (1994) Cerebellar contributions to instrumental learning. Neurosci Biobehav Rev 18:161-170.
31. Lavond DG, Steinmetz JE (1989) Acquisition of classical conditioning without cerebellar cortex. Behav Brain Res 33:113-164.
32. Lavond DG, Steinmetz JE, Yokaitis M H, Thompson RF (1987) Reacquisition of classical conditioning after removal of cerebellar cortex. Exp Brain Res 67:569-593.
33. Leiner HC, Leiner AL, Dow RS (1986) Does the cerebellum contribute to mental skills? Behav Neurosci 100:443-454.
34. Leiner HC, Leiner AL, Dow RS (1989) Reappraising the cerebellum: what does the hindbrain contribute to the forebrain? Behav Neurosci 103:998-1008.
35. Llinas RR, Sugimori M (1980) Electrophysiological properties of in vitro Purkinje cell dendrites in mammalian cerebellar slices. J Physiol (Lond) 305:197-213.
36. Llinas RR, Welsh JP (1993) On the cerebellum and motor learning. Curr Opin Neurobiol 3:958-965.
37. Linden DJ, Connor JA (1992) Participation of postsynaptic PKC in cerebellar long-term depression in culture, Science 254:1656-1659.
38. Logan CG, Grafton ST (1995) Functional anatomy of human eyeblink conditioning determined with regional cerebral glucose metabolism and positron-emission tomography. Proc Natl Acad Sci USA 92:7500-7504.
39. Matzel LD, Collin C, Alkon DL (1992) Biophysical and behavioral correlates of memory storage, degradation, and reactivation. Behav Neurosci 106:954-963.
40. McCormick DA, Thompson RF (1984) Cerebellum: essential involvement in the classically conditioned eyelid response. Science 223:296-299.
41. Meiri N, Ghelardini C, Tesco G, Galeotti N, Dahl D, Tomsic D, Cavallaro S, Quattrone A, Capaccioli S, Bartolini A, Alkon DL (1997) Reversible antisense inhibition of Shaker-like Kv1.1 potassium channel expression impairs associative memory in mouse and rat. Proc Natl Acad Sci USA 94:4430-4434.
42. Midtgaard J (1994) Processing of information from different sources: spatial synaptic integration in the dendrites of vertebrate CNS neurons. Trends Neurosci 17:166-173.
43. Midtgaard J (1995) Spatial synaptic integration in Purkinje cell dendrites. J Physiol (Paris) 89:23-32.
44. 2+ influx in turtle Purkinje cell dendriios in vitro: role of a transient outward current. J Neurophysiol 70:2455-2469.
45. Molchan SE, Sunderland T, McIntosh AR, Herscovitch P, Schreurs BG (1994) A functional anatomical study of associative learning in humans. Proc Natl Acad Sci USA 91:8122-8126.
46. Moyer Jr JR, Thompson LT, Distcrhoft JF (1996) Trace eyeblink conditioning increases CA1 excitability in a transient and learning-specific manner. J Neurosci 16:5536-5546.
47. Perrett SP, Ruiz BP, Mauk MD (1993) Cerebellar cortex lesions disrupt learning-dependent timing of conditioned eyelid responses. J Neurosci 13:1708-1718.
48. Pongs O (1993) Receptor sites for open channel blockers of shaker voltage-gated potassium channels: molecular approaches. J Recept Res 13:503-512.
49. Rudy B (1988) Diversity and ubiquity of K channels. Neuroscicnce 25:729-749.
50. Sanchez-Andres JV, Alkon DL (1991) Voltage-clamp analysis of the effect of classical conditioning on the hippocampus. J Neurophysiol 65:796-807.
51. Scharenberg AM, Olds JL, Schreurs BG, Craig AM, Alkon DL (1991) Protein kinase C redistribution within CA3 stratum oriens during acquisition of NM conditioning in the rabbit. Proc Natl Acad Sci USA 88:6637-6641.
52. Schreurs BG (1989) Classical conditioning of model systems: a behavioral review. Psychobiology 17:145-155.
53. Schreurs BG (1993) Long-term memory and extinction of the classically conditioned rabbit nictitatine membrane response. Learn Motiv 24:293-302.
54. Schreurs BG, Alkon DL (1990) US-US conditioning of the rabbit's nictitating membrane response: emergence of a conditioned response without alpha conditioning. Psychobiology 18:312-320.
55. Schreurs BG, Alkon DL (1992) Memory storage mechanisms, conservation across species. In: Neuroscience year: supplement 2 to the encyclopedia of neuroscience (Adelman G, Smith BH, eds), pp 99-101. Boston: Birkhauser.
56. Schreurs BG, Alkon DL (1993) Rabbit cerebellar slice analysis of longterm depression and its role in classical conditioning. Brain Res 631:235-240.
57. Schreurs BG, Sanchez-Andres JV, Alkon DL (1991) Learning-specific differences in Purkinje-cell dendrites of lobule H V I (lobulus simplex): intracellular recording in a rabbit cerebellar slice. Brain Res 548:18-22.
58. Schreurs BG, Sanchez-Andres JV, Alkon DL (1992) GABA-induced responses in Purkinje-cell dendrites of the rabbit cerebellar slice. Brain Res 597:79-87.
59. Schreurs BG, Oh MM, Alkon DL (1996) Pairing-specific long-term depression of Purkinje cell excitatory postsynaptic potentials results from a classical conditioning procedure in the rabbit cerebellar slice. J Neurophysiol 75:1051-1060.
60. Schreurs BG, Tomsic D, Gusev PA, Alkon DL (1997a) Dendritic excitability microzones and occluded long-term depression after classical conditioning of the rabbit's nictitating membrane response. J Neurophysiol 77:86-92.
61. Schreurs BG, McIntosh AR, Bahro M, Herscovitch P, Sunderland T, Molchan SE (1997b) Lateralization and behavioral correlation of changes in regional cerebral blood flow with classical conditioning of the human eyeblink response. J Neurophysiol 77:2153-2163.
62. Storm J (1990) Potassium currents in hippocampal pyramidal cells. Prog Brain Res 83:161-187.
63. Supple Jr WF, Kapp BS (1993) The anterior cerebellar vermis: essential involvement in classically conditioned bradycardia in the rabbit. J Neurosci 13:3705-3711.
64. Teune TM, Van Der Burg J, De Zeeuw CI, Voogd J, Ruigrok TJH (1998) Single Purkinje cell can innervate multiple classes of projection neurons in cerebellar nuclei of the rat: a light microscopic and ultrastructural triple-tracer study in the rat. J Comp Neurol 392:164-178.
65. Thompson LT, Moyer Jr JR, Disterhoft JE (1996) Transient changes in excitability of rabbit CA3 neurons with a time course appropriate to support memory consolidation. J Neurophysiol 76:1836-1849.
66. Thompson RF (1986) The neurobiology of learning and memory. Science 233:941-947.
67. Thompson RF (1990) Neural mechanisms of classical conditioning in mammals. Philos Trans R Soc Lond B Biol Sci 329:161-170.
68. Thompson RF, Krupa DJ (1994) Organization of memory traces in the mammalian brain. Annu Rev Neurosci 17:519-549.
69. Welsh JP, Harvey JA (1989) Cerebellar lesions and the nictitating membrane reflex: performance deficits of the conditioned and unconditioned response. J Neurosci 9:299-311.
70. Woody CD, Gruen E, Birt D (1991) Changes in membrane currents during Pavlovian conditioning of single cortical neurons. Brain Res 539:76-84.
71. Yeo CH, Hardiman MJ, 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.
72. Yeo CH, Hardiman MJ, Glickstein M (1985b) Classical conditioning of the nictitating membrane response of the rabbit. II. Lesions of the cerebellar cortex. Exp Brain Res 60:99-113.
73. Yeo CH, Hardiman MJ, Glickstein M (1985c) Classical conditioning of the nictitating membrane response of the rabbit. III. Connections of cerebellar lobule HVI. Exp Brain Res 60:114-126.