Distinct kinetics of synaptic structural plasticity, memory formation, and memory decay in massed and spaced learning

Proceedings of the National Academy of Sciences of the United States of America

Volumn 111, Issue 1, 2014, Pages

  Aziz, Wajeeha ^a,b   Wang, Wen ^a,c   Kesaf, Sebnem ^a,b,d   Mohamed, Alsayed Abdelhamid ^a,e   Fukazawa, Yugo ^a,b,f,g   Shigemoto, Ryuichi ^a,b,d  

^a NATIONAL INSTITUTE FOR PHYSIOLOGICAL SCIENCES   (Japan)

^b GRADUATE UNIVERSITY FOR ADVANCED STUDIES   (Japan)

^c FOURTH MILITARY MEDICAL UNIVERSITY   (China)

^d INSTITUTE OF SCIENCE AND TECHNOLOGY AUSTRIA   (Austria)

^e South Valley University   (Egypt)

^f JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^g NAGOYA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

AMPA receptor reduction; Cerebellar motor learning; Synapse shrinkage and elimination

Indexed keywords

AMPA RECEPTOR;

ADAPTATION; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL DENSITY; CELL SIZE; CELL STRUCTURE; CEREBELLUM CORTEX; CONTROLLED STUDY; DENDRITE; LEARNING; LONG TERM MEMORY; MALE; MEMORY; MEMORY CONSOLIDATION; MOUSE; NERVE CELL PLASTICITY; NONHUMAN; OCULOGRAPHY; OPTOKINETIC STIMULATION; PRIORITY JOURNAL; PURKINJE CELL; SACCADIC EYE MOVEMENT; SHORT TERM MEMORY; SPACED LEARNING; SPINE; SYNAPSE;

AMPA RECEPTOR REDUCTION; CEREBELLAR MOTOR LEARNING; SYNAPSE SHRINKAGE AND ELIMINATION;

ANIMALS; DENDRITIC SPINES; EYE MOVEMENTS; LEARNING; MALE; MEMORY, LONG-TERM; MICE; MICE, INBRED C57BL; NEURONAL PLASTICITY; PURKINJE CELLS; RECEPTORS, AMPA; SYNAPSES; TIME FACTORS;

EID: 84891941098     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1303317110     Document Type: Article

References (57)

1. McGaugh JL (2000) Memory-A century of consolidation. Science 287(5451): 248-251.
2. Kandel ER (2001) The molecular biology of memory storage: A dialogue between genes and synapses. Science 294(5544): 1030-1038.
3. Moga DE, Shapiro ML, Morrison JH (2006) Bidirectional redistribution of AMPA but not NMDA receptors after perforant path simulation in the adult rat hippocampus in vivo. Hippocampus 16(11): 990-1003.
4. Lee S-JR, Escobedo-Lozoya Y, Szatmari EM, Yasuda R (2009) Activation of CaMKII in single dendritic spines during long-term potentiation. Nature 458(7236): 299-304.
5. Lee HK, Kirkwood A (2011) AMPA receptor regulation during synaptic plasticity in hippocampus and neocortex. Semin Cell Dev Biol 22(5): 514-520.
6. Bailey CH, Kandel ER (1993) Structural changes accompanying memory storage. Annu Rev Physiol 55(1): 397-426.
7. Geinisman Y (2000) Structural synaptic modifications associated with hippocampal LTP and behavioral learning. Cereb Cortex 10(10): 952-962.
8. Gómez-Palacio-Schjetnan A, Escobar ML (2008) In vivo BDNF modulation of adult functional and morphological synaptic plasticity at hippocampal mossy fibers. Neurosci Lett 445(1): 62-67.
9. Ebbinghaus H (1885) A Contribution to Experimental Psychology (Teachers College, Columbia University Press, New York).
10. Spreng M, Rossier J, Schenk F (2002) Spaced training facilitates long-term retention of place navigation in adult but not in adolescent rats. Behav Brain Res 128(1): 103-108.
11. Commins S, Cunningham L, Harvey D, Walsh D (2003) Massed but not spaced training impairs spatial memory. Behav Brain Res 139(1-2): 215-223.
12. Okamoto T, Endo S, Shirao T, Nagao S (2011) Role of cerebellar cortical protein synthesis in transfer of memory trace of cerebellum-dependent motor learning. J Neurosci 31(24): 8958-8966.
13. Carew TJ, Pinsker HM, Kandel ER (1972) Long-term habituation of a defensive withdrawal reflex in aplysia. Science 175(4020): 451-454.
14. Naqib F, Sossin WS, Farah CA (2012) Molecular determinants of the spacing effect. Neural Plast 2012:581291.
15. Philips GT, Ye X, Kopec AM (2013) MAPK establishes a molecular context that defines effective training patterns for long-term memory formation. J Neurosci 33(17): 7565-7573.
16. Tully T, Preat T, Boynton SC, Del Vecchio M (1994) Genetic dissection of consolidated memory in Drosophila. Cell 79(1): 35-47.
17. Yin JCP, Del Vecchio M, Zhou H, Tully T (1995) CREB as a memory modulator: induced expression of a dCREB2 activator isoform enhances long-term memory in Drosophila. Cell 81(1): 107-115.
18. Sutton MA, Ide J, Masters SE, Carew TJ (2002) Interaction between amount and pattern of training in the induction of intermediate- and long-term memory for sensitization in aplysia. Learn Mem 9(1): 29-40.
19. Josselyn SA, et al. (2001) Long-term memory is facilitated by cAMP response elementbinding protein overexpression in the amygdala. J Neurosci 21(7): 2404-2412.
20. Wu G-Y, Deisseroth K, Tsien RW (2001) Spaced stimuli stabilize MAPK pathway activation and its effects on dendritic morphology. Nat Neurosci 4(2): 151-158.
21. Pagani MR, Oishi K, Gelb BD, Zhong Y (2009) The phosphatase SHP2 regulates the spacing effect for long-term memory induction. Cell 139(1): 186-198.
22. Hawkins RD, Kandel ER, Bailey CH (2006) Molecular mechanisms of memory storage in Aplysia. Biol Bull 210(3): 174-191.
23. Woo NH, Duffy SN, Abel T, Nguyen PV (2003) Temporal spacing of synaptic stimulation critically modulates the dependence of LTP on cyclic AMP-dependent protein kinase. Hippocampus 13(2): 293-300.
24. Kramár EA, et al. (2012) Synaptic evidence for the efficacy of spaced learning. Proc Natl Acad Sci USA 109(13): 5121-5126.
25. Nagao S (1988) Behavior of floccular Purkinje cells correlated with adaptation of horizontal optokinetic eye movement response in pigmented rabbits. Exp Brain Res 73(3): 489-497.
26. Raymond JL (1998) Learning in the oculomotor system: From molecules to behavior. Curr Opin Neurobiol 8(6): 770-776.
27. van Alphen AM, Stahl JS, De Zeeuw CI (2001) The dynamic characteristics of the mouse horizontal vestibulo-ocular and optokinetic response. Brain Res 890(2): 296-305.
28. Katoh A, Kitazawa H, Itohara S, Nagao S (1998) Dynamic characteristics and adaptability of mouse vestibulo-ocular and optokinetic response eye movements and the role of the flocculo-olivary system revealed by chemical lesions. Proc Natl Acad Sci USA 95(13): 7705-7710.
29. Shutoh F, et al. (2003) Role of protein kinase C family in the cerebellum-dependent adaptive learning of horizontal optokinetic response eye movements in mice. Eur J Neurosci 18(1): 134-142.
30. Wang, et al. (2013) Distinct cerebellar engrams in short-term and long-term motor learning. Proc Natl Acad USA 110:E188-E193.
31. SchonewilleM, et al. (2011) Reevaluating the role of LTD in cerebellar motor learning. Neuron 70(1): 43-50.
32. Gao Z, van Beugen BJ, De Zeeuw CI (2012) Distributed synergistic plasticity and cerebellar learning. Nat Rev Neurosci 13(9): 619-635.
33. Schonewille M, et al. (2010) Purkinje cell-specific knockout of the protein phosphatase PP2B impairs potentiation and cerebellar motor learning. Neuron 67(4): 618-628.
34. Schonewille M, et al. (2006) Zonal organization of the mouse flocculus: Physiology, input, and output. J Comp Neurol 497(4): 670-682.
35. Hintzman DL (1974) Theoretical Implications of the Spacing Effect (Lawrence Erlbaum Associates, Potomac, MD), pp 77-97.
36. Fishman EJK, Keller L, Atkinson RC (1968) Massed versus distributed practice in computerized spelling drills. J Educ Psychol 59(4): 290-296.
37. Domjan M (1980) Effects of the intertrial interval on taste-aversion learning in rats. Physiol Behav 25(1): 117-125.
38. Sunsay C, Bouton ME (2008) Analysis of a trial-spacing effect with relatively long intertrial intervals. Learn Behav 36(2): 104-115.
39. Shutoh F, Ohki M, Kitazawa H, Itohara S, Nagao S (2006) Memory trace of motor learning shifts transsynaptically from cerebellar cortex to nuclei for consolidation. Neuroscience 139(2): 767-777.
40. Scharf MT, et al. (2002) Protein synthesis is required for the enhancement of longterm potentiation and long-term memory by spaced training. J Neurophysiol 87(6): 2770-2777.
41. Houpt TA, Berlin R (1999) Rapid, labile, and protein synthesis- independent short-term memory in conditioned taste aversion. Learn Mem 6(1): 37-46.
42. Colbran RJ (2004) Protein phosphatases and calcium/calmodulin-dependent protein kinase II-dependent synaptic plasticity. J Neurosci 24(39): 8404-8409.
43. De Zeeuw CI, et al. (1998) Expression of a protein kinase C inhibitor in Purkinje cells blocks cerebellar LTD and adaptation of the vestibulo-ocular reflex. Neuron 20(3): 495-508.
44. Feil R, et al. (2003) Impairment of LTD and cerebellar learning by Purkinje cell-specific ablation of cGMP-dependent protein kinase I. J Cell Biol 163(2): 295-302.
45. van Woerden GM, et al. (2009) betaCaMKII controls the direction of plasticity at parallel fiber-Purkinje cell synapses. Nat Neurosci 12(7): 823-825.
46. Jörntell H, Hansel C (2006) Synaptic memories upside down: Bidirectional plasticity at cerebellar parallel fiber-Purkinje cell synapses. Neuron 52(2): 227-238.
47. Frankland PW, et al. (2004) Consolidation of CS and US representations in associative fear conditioning. Hippocampus 14(5): 557-569.
48. Pickens CL, Golden SA, Adams-Deutsch T, Nair SG, Shaham Y (2009) Long-lasting incubation of conditioned fear in rats. Biol Psychiatry 65(10): 881-886.
49. Cole CJ, et al. (2012) MEF2 negatively regulates learning-induced structural plasticity and memory formation. Nat Neurosci 15(9): 1255-1264.
50. Nagao S (1983) Effects of vestibulocerebellar lesions upon dynamic characteristics and adaptation of vestibulo-ocular and optokinetic responses in pigmented rabbits. Exp Brain Res 53(1): 36-46.
51. Sakatani T, Isa T (2004) PC-based high-speed video-oculography for measuring rapid eye movements in mice. Neurosci Res 49(1): 123-131.
52. Tarusawa E, et al. (2009) Input-specific intrasynaptic arrangements of ionotropic glutamate receptors and their impact on postsynaptic responses. J Neurosci 29(41): 12896-12908.
53. Masugi-Tokita M, et al. (2007) Number and density of AMPA receptors in individual synapses in the rat cerebellum as revealed by SDS-digested freeze-fracture replica labeling. J Neurosci 27(8): 2135-2144.
54. Harris KM, Stevens JK (1988) Dendritic spines of rat cerebellar Purkinje cells: Serial electron microscopy with reference to their biophysical characteristics. J Neurosci 8(12): 4455-4469.
55. Palay SL, Chan-Palay V (1974) Cerebellar Cortex: Cytology and Organization (Springer, Berlin).
56. Sterio DC (1984) The unbiased estimation of number and sizes of arbitrary particles using the disector. J Microsc 134(Pt 2): 127-136.
57. Lee KJ, Kim H, Kim TS, Park S-H, Rhyu IJ (2004) Morphological analysis of spine shapes of Purkinje cell dendrites in the rat cerebellum using high-voltage electron microscopy. Neurosci Lett 359(1-2): 21-24.