Classical conditioning of motor responses: What is the learning mechanism?

Neural Networks

Volumn 47, Issue , 2013, Pages 81-87

  Hesslow, Germund ^a   Jirenhed, Dan Anders ^a   Rasmussen, Anders ^a   Johansson, Fredrik ^a  

^a LUND UNIVERSITY   (Sweden)

Author keywords

Cerebellum; Conditioning; Learning; Purkinje cells; Temporal; Timing

Indexed keywords

CEREBELLUM; LEARNING; PURKINJE CELLS; TEMPORAL; TIMING;

BRAIN; CELLS; DIGITAL STORAGE; NATURAL GAS CONDITIONING; NEURONS;

PHYSIOLOGICAL MODELS;

METABOTROPIC RECEPTOR;

ARTICLE; CEREBELLUM; CONDITIONED REFLEX; EXCITATORY POSTSYNAPTIC POTENTIAL; EYELID REFLEX; GRANULE CELL; INHIBITORY POSTSYNAPTIC POTENTIAL; LEARNING; LONG TERM DEPRESSION; MOTOR ACTIVITY; NONHUMAN; PRIORITY JOURNAL; PURKINJE CELL; SPIKE;

CEREBELLUM; CONDITIONING; LEARNING; PURKINJE CELLS; TEMPORAL; TIMING;

ANIMALS; CONDITIONING, CLASSICAL; HUMANS; LONG-TERM SYNAPTIC DEPRESSION; MODELS, NEUROLOGICAL; MOTOR ACTIVITY; PURKINJE CELLS; TIME FACTORS;

EID: 84884141397     PISSN: 08936080     EISSN: 18792782     Source Type: Journal    
DOI: 10.1016/j.neunet.2013.03.013     Document Type: Article

References (54)

1. Aiba A., et al. Deficient cerebellar long-term depression and impaired motor learning in mGluR1 mutant mice. Cell 1994, 79:377-388.
2. Albus J. A theory of cerebellar function. Mathematical Biosciences 1971, 10:25-61.
3. Attwell P.J.E., Cooke S.F., Yeo C.H. Cerebellar function in consolidation of a motor memory. Neuron 2002, 34:1011-1020.
4. Berthier N.E., Moore J.W. Cerebellar Purkinje cell activity related to the classically conditioned nictitating membrane response. Experimental Brain Research 1986, 63:341-350.
5. Cerminara N.L., Rawson J.A. Evidence that climbing fibers control an intrinsic spike generator in cerebellar Purkinje cells. Journal of Neuroscience 2004, 24:4510-4517.
6. Chen C., Thompson R.F. Temporal specificity of long-term depression in parallel fiber-Purkinje synapses in rat cerebellar slice. Learning and Memory 1995, 2:185-198.
7. Chettih S.N., McDougle S.D., Ruffolo L.I., Medina J.F. Adaptive timing of motor output in the mouse: the role of movement oscillations in eyelid conditioning. Frontiers in Integrative Neuroscience 2011, 5:1-11.
8. Christian K.M., Thompson R.F. Neural substrates of eyeblink conditioning: acquisition and retention. Learning & Memory 2003, 10:427-455.
9. de Schutter E. Cerebellar long-term depression might normalize excitation of Purkinje cells: a hypothesis. Trends in Neurosciences 1995, 18:291-295.
10. Eccles J.C., Ito M., Szentagothai J. The cerebellum as a neuronal machine 1967, Springer-Verlag, Berlin, Heidelberg, New York.
11. Ekerot C.F., Kano M. Stimulation parameters influencing climbing fibre induced long-term depression of parallel fibre synapses. Neuroscience Research 1989, 6:264-268.
12. Fiala J.C., Grossberg S., Bullock D. Metabotropic glutamate receptor activation in cerebellar Purkinje cells as substrate for adaptive timing of the classically conditioned eye-blink response. Journal of Neuroscience 1996, 16:3760-3774.
13. Gao Z., van Beugen B.J., de Zeeuw C.I. Distributed synergistic plasticity and cerebellar learning. Nature Reviews Neuroscience 2012, 3:619-635.
14. Gormezano I., Moore J.W. Classical conditioning. Learning: processes 1969, Macmillan, New York. M.H. Marx (Ed.).
15. Green J.T., Steinmetz J.E. Purkinje cell activity in the cerebellar anterior lobe after rabbit eyeblink conditioning. Learning & Memory 2005, 12:260-269.
16. Hansel C., Linden D.J., D'Angelo E. Beyond parallel fiber LTD: the diversity of synaptic and non-synaptic plasticity in the cerebellum. Nature Neuroscience 2001, 4:467-475.
17. Harvey R.J., Napper R.M.A. Quantitative studies on the mammalian cerebellum. Progress in Neurobiology 1991, 36:437-463.
18. Hauge S.A., Tracy J.A., Baudry M., Thompson R.F. Selective changes in AMPA receptors in rabbit cerebellum following classical conditioning of the eyelid-nictitating membrane response. Brain Research 1998, 803:9-18.
19. Hesslow G. Correspondence between climbing fibre input and motor output in eyeblink-related areas in cat cerebellar cortex. Journal of Physiology (London) 1994, 476:229-244.
20. Hesslow G. Inhibition of classically conditioned eyeblink responses by stimulation of the cerebellar cortex in the decerebrate cat. Journal of Physiology (London) 1994, 476:245-256.
21. Hesslow G., Ivarsson M. Suppression of cerebellar Purkinje cells during conditioned responses in ferrets. Neuroreport 1994, 5:649-652.
22. Hesslow G., Ivarsson M. Inhibition of the inferior olive during conditioned responses in the decerebrate ferret. Experimental Brain Research 1996, 110:36-46.
23. Hesslow G., Yeo C.H. The functional anatomy of Skeletal conditioning. A neuroscientist's guide to classical conditioning 2002, 86-146. Springer-Verlag, New York. J.W. Moore (Ed.).
24. Ito M. Cerebellar long-term depression: characterization, signal transduction, and functional roles. Physiological Reviews 2001, 81:1143-1195.
25. 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. Neuroscience Letters 1982, 33:253-258.
26. Jirenhed D.A., Bengtsson F., Hesslow G. Acquisition, extinction, and reacquisition of a cerebellar cortical memory trace. Journal of Neuroscience 2007, 27:2493-2502.
27. Jirenhed D.A., Hesslow G. Learning stimulus intervals-adaptive timing of conditioned Purkinje cell responses. The Cerebellum 2011, 10:523-535.
28. Jirenhed D.A., Hesslow G. Time course of classically conditioned Purkinje cell response is determined by initial part of conditioned stimulus. Journal of Neuroscience 2011, 31:9070-9074.
29. Jörntell H., Ekerot C.-F. Reciprocal bidirectional plasticity of parallel fiber receptive fields in cerebellar Purkinje cells and their afferent interneurons. Neuron 2002, 34:797-806.
30. Jörntell H., Ekerot C.F. Properties of somatosensory synaptic integration in cerebellar granule cells in vivo. Journal of Neuroscience 2006, 26:11786-11797.
31. Karachot L., Kado R.T., Ito M. Stimulus parameters for induction of long-term depression in vitro rat Purkinje cells. Neuroscience Research 1995, 21:161-168.
32. Kehoe E.J., Macrae M. Fundamental behavioral methods and findings in classical conditioning. A neuroscientist's guide to classical conditioning 2002, 171-231. Springer-Verlag, New York. J.W. Moore (Ed.).
33. Kellett D.O., Fukunaga I., Chen-Kubota E., Dean P., Yeo C.H. Memory consolidation in the cerebellar cortex. PLoS One 2010, 5:e11737.
34. 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. European Journal of Neuroscience 2001, 13:1249-1253.
35. Koekkoek S.K.E., et al. Cerebellar LTD and learning-dependent timing of conditioned eyelid responses. Science 2003, 301:1736-1739.
36. Konnerth A., Llano I., Armstrong C.M. Synaptic currents in cerebellar Purkinje cells. Proceedings of the National Academy of Sciences of the United States of America 1990, 87:2662.
37. Kotani S., Kawahara S., Kirino Y. Purkinje cell activity during classical eyeblink conditioning in decerebrate guinea pigs. Brain Research 2006, 1068:70-81.
38. Linden D.J. The return of the spike: postsynaptic action potentials and the induction of LTP and LTD. Neuron 1999, 22:661-666.
39. Marr D. A theory of cerebellar cortex. Journal of Physiology (London) 1969, 202:437-470.
40. Mauk M.D., Buonomano D.V. The neural basis of temporal processing. Annual Review of Neuroscience 2004, 27:307-340.
41. McCormick D.A., Clark G.A., Lavond D.G., Thompson R.F. Initial localization of the memory trace for a basic form of learning. Proceedings of the National Academy of Sciences of the United States of America 1982, 79:2731-2735.
42. Medina J.F., Mauk M.D. Computer simulation of cerebellar information processing. Nature Neuroscience 2000, 3:1205-1211.
43. Millenson J.R., Kehoe E.J., Gormezano I. Classical conditioning of the rabbit's nictitating membrane response under fixed and mixed CS-US intervals. Learning and Motivation 1977, 8:351-366.
44. Nordholm A.F., Lavond D.G., Thompson R.F. Are eyeblink responses to tone in the decerebrate, decerebellate rabbit conditioned responses?. Behavioural Brain Research 1991, 44:27-34.
45. Safo P., Regehr W.G. Timing dependence of the induction of cerebellar LTD. Neuropharmacology 2008, 54:213-218.
46. Schonewille M., et al. Reevaluating the role of LTD in cerebellar motor learning. Neuron 2011, 70:43-50.
47. Steuber V., Willshaw D. A biophysical model of synaptic delay learning and temporal pattern recognition in a cerebellar Purkinje cell. Journal of Computational Neuroscience 2004, 17:149-164.
48. Svensson P., Jirenhed D.A., Bengtsson F., Hesslow G. Effect of conditioned stimulus parameters on timing of conditioned Purkinje cell responses. Journal of Neurophysiology 2010, 103:1329-1336.
49. Wang S.S., Denk W., Häusser M. Coincidence detection in single dendritic spines mediated by calcium release. Nature Neuroscience 2000, 3:1266-1273.
50. Welsh J.P., et al. Normal motor learning during pharmacological prevention of Purkinje cell long-term depression. Proceedings of the National Academy of Sciences of the United States of America 2005, 102:17166-17171.
51. Wetmore D.Z. Computational, electrophysiological, and behavioral studies of cerebellum-dependent memory encoding and retrieval 2009, Stanford University, Stanford.
52. Yamazaki T., Tanaka S. Computational models of timing mechanisms in the cerebellar granular layer. The Cerebellum 2009, 8:423-432.
53. Yeo C.H., Hardiman M.J., Glickstein M. Discrete lesions of the cerebellar cortex abolish the classically conditioned nictitating membrane response of the rabbit. Behavioural Brain Research 1984, 13:261-266.
54. Yeo C.H., Hardiman M.J., Glickstein M. Classical conditioning of the nictitating membrane response of the rabbit. III. Connections of cerebellar lobule HVI. Experimental Brain Research 1985, 60:114-126.