NMDA receptor activity in learning spatial procedural strategies. II. The influence of cerebellar lesions

Brain Research Bulletin

Volumn 70, Issue 4-6, 2006, Pages 356-367

  Federico, Francesca ^a,c   Leggio, Maria G ^a   Neri, Paola ^a   Mandolesi, Laura ^a,b   Petrosini, Laura ^a  

^a SAPIENZA UNIVERSITY OF ROME   (Italy)

^b UNIVERSITY OF NAPLES PARTHENOPE   (Italy)

^c UNIVERSITY OF SIENA   (Italy)

Author keywords

Cerebellum; Navigational strategies; Procedural learning; Rats; Spatial function

Indexed keywords

4 PHOSPHONOMETHYLPIPECOLIC ACID; N METHYL DEXTRO ASPARTIC ACID RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CEREBELLECTOMY; CEREBELLUM; CEREBELLUM INJURY; CONTROLLED STUDY; LEARNING; MALE; MAZE TEST; NONHUMAN; PRIORITY JOURNAL; RAT;

ANALYSIS OF VARIANCE; ANIMALS; BEHAVIOR, ANIMAL; CEREBELLAR DISEASES; EXCITATORY AMINO ACID ANTAGONISTS; LEARNING; MALE; MAZE LEARNING; PIPECOLIC ACIDS; RATS; RATS, WISTAR; RECEPTORS, N-METHYL-D-ASPARTATE; SPATIAL BEHAVIOR;

EID: 33749259104     PISSN: 03619230     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainresbull.2006.06.005     Document Type: Article

References (83)

1. Abrahams S., Morris R.G.M., Polkey C.E., Jarosz J.M., Cox T.C., Graves M., and Pickering A. Hippocampal involvement in spatial and working memory: a structural MRI analysis of patients with unilateral mesial temporal lobe sclerosis. Brain Cogn. 41 (1999) 39-65
2. Aggleton J.P., Kyd R.J., and Bilkey D.K. When is the perirhinal cortex necessary for the performance of spatial memory tasks?. Neurosci. Biobehav. Rev. 41 (2004) 611-624
3. Armano S., Rossi P., Taglietti V., and D' Angelo E. Long-term potentiation of intrinsic excitability at the mossy fiber-granule cell synapse of rat cerebellum. J. Neurosci. 20 (2000) 5208-5216
4. Artola A., and Singer W. Long-term potentiation and NMDA receptors in rat visual cortex. Nature 330 (1987) 649-652
5. Bannerman D.M., Good M.A., Butcher S.P., Ramsay M., and Morris R.G.M. Distinct components of spatial learning revealed by prior training and NMDA receptor blockade. Nature 378 (1995) 182-186
6. Belzung C., Chapillon P., and Lalonde R. The effects of the lurcher mutation on object localization, T-maze discrimination, and radial arm maze tasks. Behav. Gen. 31 (2001) 151-155
7. Bennett D.A., Bernard P.S., Amrick C.L., Wilson D.E., Liebman J.M., and Hutchison A.J. Behavioral pharmacological profile of CGS19755, a competitive antagonist at N-methyl-d-aspartate receptors. J. Pharmacol. Exp. Ther. 250 (1989) 454-460
8. Bohbot V.D., Iaria G., and Petrides M. Hippocampal function and spatial memory: evidence from functional neuroimaging in healthy participants and performance of patients with medial temporal lobe resections. Neuropsychology 18 (2004) 418-425
9. Burgess N., Maguire E.A., and O'Keefe J. The human hippocampus and spatial and episodic memory. Neuron 35 (2002) 625-641
10. Burguière E., Arleo A., reza Hojjati M., Elgersma Y., De Zeeuw C.I., Berthoz A., and Rondi-Reig L. Spatial navigation impairment in mice lacking cerebellar LTD: a motor adaption deficit?. Nat. Neurosci. 8 (2005) 1292-1294
11. Cain D.P. Testing the NMDA, Long-term potentiation and cholinergic hypotheses of spatial learning. Neurosci. Biobehav. Rev. 22 (1998) 181-193
12. Cain D.P., Saucier D., and Boon F. Testing hypotheses of spatial learning: the role of NMDA receptors and NMDA-mediated long-term potentiation. Behav. Brain Res. 84 (1997) 179-193
13. Cain D.P., Saucier D., Hall J., Hargreaves E.L., and Boon F. Detailed behavioral analysis of water maze acquisition under APV or CNQX: contribution of sensorimotor disturbances to drug-induced acquisition deficits. Behav. Neurosci. 110 (1996) 86-102
14. Casado M., Isope P., and Ascher P. Involvement of presynaptic N-methyl-D-aspartate receptors in cerebellar long-term depression. Neuron 33 (2002) 123-130
15. Caston J., Chianale C., Delhaye-Bouchaud N., and Mariani J. Role of the cerebellum in exploration behavior. Brain Res. 808 (1998) 232-237
16. Chen G., and Steinmetz J.E. Intra-cerebellar infusion of NMDA receptor antagonist AP5 disrupts classical eyeblink conditioning in rabbits. Brain Res. 887 (2000) 144-156
17. Colombel C., Lalonde R., and Caston J. The effects of unilateral removal of the cerebellar hemispheres on spatial learning and memory in rats. Brain Res. 1004 (2004) 108-115
18. Cull-Candy S.G., and Leskiewicz D.N. Role of distinct NMDA receptor subtypes at centarl synapses. Sci. STKE 255 (2004) re 16
19. D'Angelo E., Rossi P., Armano S., and Taglietti V. Evidence for NMDA and mGlu receptor-dependent long-term potentiation of mossy fibre-granule cell transmission in rat cerebellum. J. Neurophysiol. 81 (1999) 277-287
20. Daniel H., Levenes C., and Crepel F. Cellular mechanism of cerebellar LTD. Trends Neurosci. 21 (1998) 401-407
21. Davis S., Butcher S.P., and Morris R.G.M. The NMDA receptor antagonist d-2-amino-5-phosphonopentanoate d-AP5 impairs spatial learning and LTP in vivo at intracerebral concentrations comparable to those that block LTP in vitro. J. Neurosci. 12 (1992) 21-34
22. de Hoz L., Martin S.J., and Morris R.G.M. Forgetting, reminding, and remembering: the retrieval of lost spatial memory. PLoS Biol. 2 (2004) E225
23. Doyon J., Song A.W., Karni A., Lalonde F., Adams M.M., and Underleider L.G. Experience-dependent changes in cerebellar contributions to motor sequence learning. Proc. Nat. Acad. Sci. 99 (2002) 1017-1022
24. Federico F., Leggio M.G., Mandolesi L., and Petrosini L. Effect of NMDA receptor antagonist on behavioral recovery following cerebellar lesions. Restor. Neurol. Neurosci. 24 (2006) 1-7
25. Federico F., Neri P., Leggio M.G., Graziano A., Molinari M., and Petrosini L. Role of Cerebellar NMDA Receptors in Spatial Learning. third ed. (2002), FENS, Paris p. 84
26. Fenton A.A., and Bures J. Place navigation in rats with unilateral tetrodotoxin inactivation of the dorsal hippocampus: place but not procedural learning can be lateralized to one hippocampus. Behav. Neurosci. 107 (1993) 552-564
27. Gandhi C.C., Kelly R.M., Wiley R.G., and Walsh T.J. Impaired acquisition of a Morris water maze task following selective destruction of cerebellar Purkinje cells with OX7-saporin. Behav. Brain Res. 109 (2000) 37-47
28. Gaytan-Tocaven L., and Olvera-Cortes M.E. Bilateral lesion of the cerebellar-dentate nucleus impairs egocentric sequential learning but not egocentric navigation in the rat. Neurobiol. Learn. Mem. 82 (2004) 120-127
29. Graziano A., Leggio M.G., Mandolesi L., Neri P., Molinari M., and Petrosini L. Learning power of single behavioral units in acquisition of a complex spatial behavior: an observational learning study in cerebellar-lesioned rats. Behav. Neurosci. 116 (2002) 116-125
30. Graziano A., Petrosini L., and Bartoletti A. Automatic recognition of explorative strategies in the Morris water maze. J. Neurosci. Meth. 130 (2003) 33-44
31. Hansel C., Linden D.J., and D'Angelo E. Beyond parallel fiber LTD: the diversity of synaptic and non-synaptic plasticity in the cerebellum. Nat. Neurosci. 4 (2001) 467-475
32. Harris E.W., Gonang A.H., and Cotman C.W. Long-term potentiation in the hippocampus involves activation of N-methyl-d-aspartate. Brain Res. 323 (1984) 132-137
33. Hoh T., Beiko J., Boon F., Weiss S., and Cain D.P. Complex behavioral strategy and reversal learning in the water maze without NMDA receptor-dependent long-term potentiation. J. Neurosci. 19RC (1999) 21-25
34. Ito M. The molecular organization of cerebellar long-term depression. Nat. Rev. Neurosci. 3 (2002) 896-902
35. Joyal C.C., Strazielle C., and Lalonde R. Effects of dentate nucleus lesions on spatial and postural sensorimotor learning in rats. Behav. Brain Res. 122 (2001) 131-137
36. Jones S., and Gibb A.J. Functional NR2B- and NR2D-containing NMDA receptor channels in rat substantia nigra dopaminergic neurons. J. Physiol. 569 (2005) 209-221
37. Jueptner M., Frith C.D., Brooks D.J., Frackowiak R.S., and Passingham R.E. Anatomy of motor learning. II. Subcortical structures and learning by trial and error. J. Neurophysiol. 77 (1997) 1325-1337
38. Kase M., Miller D.C., and Noda H. Discharges of Purkinje cells and mossy fibres in the cerebellar vermis of the monkey during saccadic eye movements. J. Physiol 300 (2000) 539-555
39. Lalonde R., and Strazielle C. Motor coordination exploration and spatial learning in a natural mouse mutation nervous with Purkinje cell degeneration. Behav. Gen. 33 (2003) 59-66
40. Lalonde R. Exploration and spatial learning in staggerer mutant mice. J. Neurogen. 42 (1987) 85-91
41. M.G. Leggio, F. Federico, P. Neri, A. Graziano, L. Mandolesi, L. Petrosini, NMDA receptor activity in learning spatial procedural strategies. I. The influence of hippocampal lesions. Brain Res. Bull. (2006), doi:10.1016/j.brainresbull.2006.06.006.
42. Leggio M.G., Molinari M., Neri P., Graziano A., Mandolesi L., and Petrosini L. Representation of action in rats: the role of cerebellum in learning spatial performances by observation. Proc. Nat. Acad. Sci. U.S.A. 97 (2000) 2320-2325
43. Leggio M.G., Neri P., Graziano A., Mandolesi L., Molinari M., and Petrosini L. Cerebellar contribution to spatial event processing: characterization of procedural learning. Exp. Brain Res. 127 (1999) 1-11
44. Lehmann J., Hutchison A.J., McPherson S.E., Mondadori C.M., SchmutzSinton C.M., Tsai C., Murphy D.E., Steel D.J., Williams M., et al. CPP a selective and competitive N-methyl-aspartate-type excitatory amino acid receptor antagonist. J. Pharmacol. Exp. Ther. 240 (1988) 737-746
45. Lisberger S.G. Cerebellar LTD: a molecular mechanism of behavioral learning?. Cell 92 (1998) 701-704
46. Luciani L. Il cervelletto: Nuovi studi di fisiologia normale e patologica (1891), Le Monnier, Firenze
47. Mandolesi L., Leggio M.G., Graziano A., Neri P., and Petrosini L. Cerebellar contribution to spatial event processing: involvement in procedural and working memory components. Eur. J. Neurosci. 14 (2001) 1-13
48. Mandolesi L., Leggio M.G., Spirito F., and Petrosini L. Cerebellar contribution to spatial event processing: do spatial procedures contribute to formation of spatial declarative knowledge?. Eur. J. Neurosci. 18 (2003) 2618-2626
49. Micheau J., Riedel G., Roloff E., Inglis J., and Morris R.G.M. Reversible hippocampal inactivation partially dissociates how and where to search in the water maze. Behav. Neurosci. 118 (2004) 1022-1052
50. Molinari M., Grammaldo L.G., and Petrosini L. Cerebellar contribution to spatial event processing: right-left discrimination abilities in rats. Eur. J. Neurosci. 9 (1997) 1986-1992
51. Molinari M., Leggio M.G., Solida A., Ciorra R., Misciagna S., Silveri M.C., and Petrosini L. Cerebellum and procedural learning: evidence from focal cerebellar lesions. Brain 120 (1997) 1753-1762
52. Molinari M., Petrosini L., and Gremoli T. Hemicerebellectomy and motor behaviour in rats. II. Effects of cerebellar lesion performed at different developmental stages. Exp. Brain Res. 82 (1990) 483-492
53. Morishita W., and Sastry B.R. Postsynaptic mechanisms underlying long-term depression of GABAergic transmission in neurons of the deep cerebellar nuclei. J. Neurophysiol. 76 (1996) 59-68
54. Morris R.G.M., Garrud P., Rawlins J.N., and O'Keefe J. Place navigation impaired in rats with hippocampal lesions. Nature 297 (1982) 681-683
55. Morris R.G.M. Synaptic plasticity and learning: selective impairment of learning in rats and blockade of long-term potentiation in vivo by the N-methyl-d-aspartate receptor antagonist AP5. J. Neurosci. 9 (1989) 3040-3057
56. Morris R.G.M., Anderson E., Lynch G.S., and Baudry M. Selective impairment of learning and blockade of long-term potentiation by an N-methyl-d-aspartate receptor antagonist AP5. Nature 319 (1986) 774-776
57. Moser E.I., Krobbert K.A., Moser M.-B., and Morris R.G.M. Impaired spatial learning after saturation of long-term potentiation. Science 281 (1998) 2038-2042
58. Nieus T., Sola E., Mapelli J., Saftenku E., Rossi P., and D'Angelo E. LTP regulates burst initiation and frequency at mossy fiber-granule cell synapses of rat cerebellum: experimental observations and theoretical predictions. J. Neurophysiol. 95 (2006) 686-699
59. Noblett K.L., and Swain R.A. Pretraining enhances recovery from visuospatial deficit following cerebellar dentate nucleus lesion. Behav. Neurosci. 117 (2003) 785-798
60. O'Keefe J. Spatial memory within and without the hippocampal system. In: Seifert J.W. (Ed). Neurobiology of the Hippocampus (1983), Academic Press, London 375-403
61. O'Keefe J. A computational theory of the hippocampal cognitive map. In: Storm-Mathisen J., Zimmer J., and Ottersen O.P. (Eds). Understanding the Brain Through the Hippocampus. Progress in Brain Research vol. 83 (1990), Elsevier, Amsterdam 301-312
62. Ouardouz M., and Sastry B.R. Mechanisms underlying LTP of inhibitory synaptic transmission in the deep cerebellar nuclei. J. Neurophysiol. 84 (2000) 1414-1421
63. Packard M.G., and McGaugh J.L. Inactivation of hippocampus or caudate nucleus with lidocaine differentially affects expression of place and response learning. Neurobiol. Learn. Mem. 65 (1996) 65-72
64. Paxinos G., and Watson C. The Rat Brain in Sereotaxic Coordinates. fourth ed. (1998), Academic Press, San Diego
65. Pellerin P.-P., and Lamarre Y. Local field potential oscillations in primate cerebellar cortex during voluntary movement. J. Neurophysiol. 78 (1997) 3502-3507
66. Petrosini L., Molinari M., and Dell'Anna M.E. Cerebellar contribution to spatial event processing: Morris water maze and T-maze. Eur. J. Neurosci. 8 (1996) 1882-1896
67. Petrosini L., Molinari M., and Gremoli T. Hemicerebellectomy and motor behaviour in rats. I. Development of motor function after neonatal lesion. Exp. Brain Res. 82 (1990) 472-482
68. Petrosini L., Leggio M.G., and Molinari M. The cerebellum in the spatial problem solving: a co-star or a guest star?. Progr. Neurobiol. 56 (1998) 191-210
69. Pinto-Hamuy T., Montero V.M., and Torrealba F. Neurotoxic lesion of anteromedial/posterior parietal cortex disrupts spatial maze memory in blind rats. Behav. Brain Res. 153 (2004) 465-470
70. Redish A.D. Beyond the Cognitive Map: From Place Cells to Episodic Memory (1999), MIT Press, Cambridge MA
71. Robertson B.J., Boon F., Cain D.P., and Vanderwolf C.H. Behavioral effects of anti-muscarinic, antiserotonergic and anti-NMDA treatments: hippocampal and neocortical slow wave electrophysiology predict the effects on grooming in the rat. Behav. Brain Res. 838 (1999) 234-240
72. Rondi-Reig L., Le Marec N., Caston J., and Mariani J. The role of climbing and parallel fibers inputs to cerebellar cortex in navigation. Behav. Brain Res. 132 (2002) 11-18
73. Rossi P., Sola E., Taglietti V., Borchardt T., Steigerwald F., Utvik J.K., Ottersen O.P., Kohr G., and D'Angelo E. NMDA receptor 2 (NR2) C-terminal control of NR open probability regulates synaptic transmission and plasticity at a cerebellar synapse. J. Neurosci. 22 (2002) 9687-9697
74. Saucier D., and Cain D.P. Spatial learning without NMDA receptor-dependent long-term potentiation. Nature 378 (1995) 186-189
75. Save E., Paz-Villagran V., Alexinsky T., and Poucet B. Functional interaction between the associative parietal cortex and hippocampal place cell firing in the rat. Eur. J. Neurosci. 21 (2005) 522-530
76. Thach W.T. On the specific role of the cerebellum in motor learning and cognition: clues from PET activation and lesion studies in man. Behav. Brain Sci. 19 (1996) 411-431
77. Thompson C.L., Drewery D.L., Atkins H.D., Stephenson F.A., and Chazot P.L. Immunohistochemical localization of N-methyl-d-aspartate receptor NR1, NR2A, NR2B and NR2C/D subunits in the adult mammalian cerebellum. Neurosci. Lett. 283 (2000) 85-88
78. Torriero S., Oliveri M., Koch R., Caltagirone C., and Petrosini L. Interference of left and right cerebellar rTMS with procedural learning. J. Cogn. Neurosci. 16 (2004) 1605-1611
79. Yeshenko O., Guazzelli A., and Mizumori S.J. Context-dependent reorganization of spatial and movement representations by simultaneously recorded hippocampal and striatal neurons during performance of allocentric and egocentric tasks. Behav. Neurosci. 118 (2004) 751-769
80. Weitlauf C., Honse Y., Auberson Y.P., Mishina M., Lovinger D.M., and Winder D.G. Activation of NR2A-containing NMDA receptors is not obligatory for NMDA receptor-dependent long-term potentiation. J. Neurosci. 25 (2005) 8386-8390
81. Whishaw I.Q., Mittleman G., Bunch S.T., and Dunnett S.B. Impairments in the acquisition, retention and selection of spatial navigation strategies after medial caudate-putamen lesions in rats. Behav. Brain Res. 24 (1987) 125-138
82. Wolbers T., and Buchel C. Dissociable retrosplenial and hippocampal contributions to successful formation of survey representations. J. Neurosci. 25 (2005) 3333-3340
83. Wood E.R., and Dudchenko P.A. Aging, spatial behavior and the cognitive map. Nat. Neurosci. 6 (2003) 546-548