Exposure to an enriched environment accelerates recovery from cerebellar lesion

Cerebellum

Volumn 10, Issue 1, 2011, Pages 104-119

  Foti, Francesca ^a,b   Laricchiuta, Daniela ^a,b   Cutuli, Debora ^a,b   De Bartolo, Paola ^a,b   Gelfo, Francesca ^a   Angelucci, Francesco ^a   Petrosini, Laura ^a,b  

^a IRCCS FONDAZIONE SANTA LUCIA   (Italy)

^b SAPIENZA UNIVERSITY OF ROME   (Italy)

Author keywords

Cerebellar compensation; Hemicerebellectomy; Postural and locomotor behavior; Spatial tests

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BODY POSTURE; CEREBELLECTOMY; CEREBELLUM INJURY; COGNITION; CONTROLLED STUDY; DEGENERATIVE DISEASE; ENVIRONMENTAL ENRICHMENT; ENVIRONMENTAL EXPOSURE; ENVIRONMENTAL FACTOR; LOCOMOTION; MALE; MENTAL PERFORMANCE; MOTOR PERFORMANCE; NONHUMAN; PHYSICAL ACTIVITY; PRIORITY JOURNAL; RAT; SYMPTOM;

ANIMALS; BEHAVIOR, ANIMAL; CEREBELLUM; CHOICE BEHAVIOR; COGNITION; ENVIRONMENT; HOUSING, ANIMAL; LOCOMOTION; MALE; MAZE LEARNING; MOTOR ACTIVITY; MOTOR SKILLS; POSTURE; PSYCHOMOTOR PERFORMANCE; RATS; RATS, WISTAR;

EID: 79952705766     PISSN: 14734222     EISSN: 14734230     Source Type: Journal    
DOI: 10.1007/s12311-010-0236-z     Document Type: Article

References (77)

1. Borenstein AR, Copenhaver CI, Mortimer JA. Early-life risk factors for Alzheimer disease. Alzheimer Dis Assoc Disord. 2006;20:63-72. (Pubitemid 44356897)
2. McDowell I, Xi G, Lindsay J, Tierney M. Mapping the connections between education and dementia. J Clin Exp Neuropsychol. 2007;29:127-41.
3. Green CS, Bavelier D. Exercising your brain: a review of human brain plasticity and training-induced learning. Psychol Aging. 2008;23:692-701.
4. Buckner RL. Memory and executive function in aging and AD: multiple factors that cause decline and reserve factors that compensate. Neuron. 2004;44:195-208. (Pubitemid 39348840)
5. Arendash GW, Garcia MF, Costa DA, Cracchiolo JR, Wefes IM, Potter H. Environmental enrichment improves cognition in aged Alzheimer's transgenic mice despite stable beta-amyloid deposition. NeuroReport. 2004;15:1751-4. (Pubitemid 39062588)
6. Artola A, von Frijtag JC, Fermont PC, Gispen WH, Schrama LH, Kamal A, et al. Long-lasting modulation of the induction of LTD and LTP in rat hippocampal CA1 by behavioural stress and environmental enrichment. Eur J Neurosci. 2006;23:261-72.
7. Ngandu T, von Strauss E, Helkala EL, Winblad B, Nissinen A, Tuomilehto J, et al. Education and dementia: what lies behind the association? Neurology. 2007;69:1442-50.
8. Normann C, Berger M. Neuroenhancement: status quo and perspectives. Eur Arch Psychiatry Clin Neurosci. 2008;258:110-4.
9. Nithianantharajah J, Hannan AJ. The neurobiology of brain and cognitive reserve: mental and physical activity as modulators of brain disorders. Prog Neurobiol. 2009;89:369-82.
10. Jankowsky JL, Melnikova T, Fadale DJ, Xu GM, Slunt HH, Gonzales V, et al. Environmental enrichment mitigates cognitive deficits in a mouse model of Alzheimer's disease. J Neurosci. 2005;25:5217-24. (Pubitemid 40726973)
11. Berardi N, Braschi C, Capsoni S, Cattaneo A, Maffei L. Environmental enrichment delays the onset of memory deficits and reduces neuropathological hallmarks in a mouse model of Alzheimer-like neurodegeneration. J Alzheimers Dis. 2007;11:359-70. (Pubitemid 47094033)
12. Mandolesi L, De Bartolo P, Foti F, Gelfo F, Federico F, Leggio MG, et al. Environmental enrichment provides a cognitive reserve to be spent in the case of brain lesion. J Alzheimers Dis. 2008;15:11-28.
13. Petrosini L, De Bartolo P, Foti F, Gelfo F, Cutuli D, Leggio MG, et al. On whether the environmental enrichment may provide cognitive and brain reserves. Brain Res Rev. 2009;61:221-39.
14. Luciani L. Il cervelletto: nuovi studi di fisiologia normale e patologica. Firenze: Le Monnier; 1891.
15. Holmes G. The cerebellum of man. Brain. 1939;62:1-30.
16. Schmahmann JD, Sherman JC. The cerebellar cognitive affective syndrome. Brain. 1998;121:561-79. (Pubitemid 28162120)
17. Schmahmann JD. Disorders of the cerebellum: ataxia, dysmetria of thought, and the cerebellar cognitive affective syndrome. J Neuropsychiatry Clin Neurosci. 2004;16:367-78. (Pubitemid 39244566)
18. Schmahmann JD, Caplan D. Cognition, emotion and the cerebellum. Brain. 2006;129:290-2.
19. Thach WT. Context-response linkage. Int Rev Neurobiol. 1997;41:599-611. (Pubitemid 127826246)
20. Thach WT. A role for the cerebellum in learning movement coordination. Neurobiol Learn Mem. 1998;70:177-88. (Pubitemid 28455590)
21. Thach WT. On the mechanism of cerebellar contributions to cognition. Cerebellum. 2007;6:163-7. (Pubitemid 47360076)
22. Drepper J, Timmann D, Kolb FP, Diener HC. Non-motor associative learning in patients with isolated degenerative cerebellar disease. Brain. 1999;122:87-97. (Pubitemid 29046275)
23. Ito M. Historical review of the significance of the cerebellum and the role of Purkinje cells in motor learning. Ann NY Acad Sci. 2002;978:273-88. (Pubitemid 36127117)
24. Molinari M, Petrosini L, Misciagna S, Leggio MG. Visuospatial abilities in cerebellar disorders. J Neurol Neurosurg Psychiatry. 2004;75:235-40. (Pubitemid 38183530)
25. Golla H, Thier P, Haarmeier T. Disturbed overt but normal covert shifts of attention in adult cerebellar patients. Brain. 2005;128:1525-35. (Pubitemid 41373672)
26. Ziemus B, Baumann O, Luerding R, Schlosser R, Schuierer G, Bogdahn U, et al. Impaired working-memory after cerebellar infarcts paralleled by changes in BOLD signal of a corticocerebellar circuit. Neuropsychologia. 2007;45:2016-24. (Pubitemid 46654116)
27. Amrani K, Dykes RW, Lamarre Y. Bilateral contributions to motor recovery in the monkey following lesions of the deep cerebellar nuclei. Brain Res. 1996;740:275-84. (Pubitemid 26411310)
28. Armano S, Rossi P, Taglietti V, D'Angelo E. Long-term potentiation of intrinsic excitability at the mossy fiber-granule cell synapse of rat cerebellum. J Neurosci. 2000;20:5208-16. (Pubitemid 30457717)
29. Casado M, Isope P, Ascher P. Involvement of presynaptic Nmethyl-D-aspartate receptors in cerebellar long-term depression. Neuron. 2002;33:123-30. (Pubitemid 34088184)
30. Federico F, Leggio MG, Mandolesi L, Petrosini L. The NMDA receptor antagonist CGS 19755 disrupts recovery following cerebellar lesions. Restor Neurol Neurosci. 2006a;24:1-7.
31. Centonze D, Rossi S, De Bartolo P, De Chiara V, Foti F, Musella A, et al. Adaptations of glutamatergic synapses in the striatum contribute to recovery from cerebellar damage. Eur J Neurosci. 2008;27:2188-96. (Pubitemid 351521497)
32. Morris RG, Garrud P, Rawlins JN, O'Keefe J. Place navigation impaired in rats with hippocampal lesions. Nature. 1982;297:681-3. (Pubitemid 12096189)
33. Petrosini L, Molinari M, Dell'Anna ME. Cerebellar contribution to spatial event processing: Morris water maze and T-maze. Eur J Neurosci. 1996;8:1882-96. (Pubitemid 26302283)
34. Federico F, Leggio MG, Neri P, Mandolesi L, Petrosini L. NMDA receptor activity in learning spatial procedural strategies II. The influence of cerebellar lesions. Brain Res Bull. 2006b;70:356-67.
35. Mandolesi L, Leggio MG, Graziano A, Neri P, Petrosini L. Cerebellar contribution to spatial event processing: involvement in procedural and working memory components. Eur J Neurosci. 2001;14:2011-22. (Pubitemid 35463688)
36. Paxinos G, Watson C. The rat brain in stereotaxic coordinates. 4th ed. San Diego: Academic; 1998.
37. Milgram NW, Siwak-Tapp CT, Arahujo J, Head E. Neuroprotective effects of cognitive enrichment. Ageing Res Rev. 2006;5:354-69. (Pubitemid 44374431)
38. Bennett EL. krech D, Rosenzweig MR. Reliability and regional specificity of cerebral effects of environmental complexity and training. J Comp Physiol Psychol. 1964;57:440-1.
39. van Praag H, Kempermann G, Gage FH. Neural consequences of environmental enrichment. Nat Rev Neurosci. 2000;1:191-8.
40. Greenough WT, Volkmar FR, Juraska J. Effects of rearing complexity on dendritic branching in frontolateral and temporal cortex of the rat. Exp Neurol. 1973;41:371-8.
41. van Dellen A, Cordery PM, Spires TL, Blakemore C, Hannan AJ. Wheel running from a juvenile age delays onset of specific motor deficits but does not alter protein aggregate density in a mouse model of Huntington's disease. BMC Neurosci. 2008;9:34.
42. Hicks RR, Zhang L, Atkinson A, Stevenon M, Veneracion M, Seroogy KB. Environmental enrichment attenuates cognitive deficits but does not alter neurotrophin gene expression in the hippocampus following lateral fluid percussion brain injury. Neuroscience. 2002;112:631-7. (Pubitemid 34634156)
43. Kempermann G, Kuhn HG, Gage FH. More hippocampal neurons in adult mice living in an enriched environment. Nature. 1997;386:493-5. (Pubitemid 27164074)
44. Kempermann G. The neurogenic reserve hypothesis: what is adult hippocampal neurogenesis good for? Trends Neurosci. 2008;31:163-9.
45. Kondo M, Gray LJ, Pelka GJ, Christodoulou J, Tam PP, Hannan AJ. Environmental enrichment ameliorates a motor coordination deficit in a mouse model of Rett syndrome - Mecp2 gene dosage effects and BDNF expression. Eur J Neurosci. 2008;27:3342-50. (Pubitemid 351847324)
46. Nag N, Moriuchi JM, Peitzman CG, Ward BC, Kolodny NH, Berger-Sweeney JE. Environmental enrichment alters locomotor behaviour and ventricular volume in Mecp2 1lox mice. Behav Brain Res. 2009;196:44-8.
47. van Dellen A, Blakemore C, Deacon R, York D, Hannan AJ. Delaying the onset of Huntington's in mice. Nature. 2000;404:721-2. (Pubitemid 30212388)
48. Spires TL, Grote HE, Varshney NK, Cordery PM, van Dellen A, Blakemore C, et al. Environmental enrichment rescues protein deficits in a mouse model of Huntington's disease, indicating a possible disease mechanism. J Neurosci. 2004;24:2270-6. (Pubitemid 38314558)
49. Lazic SE, Grote HE, Blakemore C, Hannan AJ, van Dellen A, Phillips W, et al. Neurogenesis in the R6/1 transgenic mouse model of Huntington's disease: effects of environmental enrichment. Eur J Neurosci. 2006;23:1829-38.
50. De Bartolo P, Leggio MG, Mandolesi L, Foti F, Gelfo F, Ferlazzo F, et al. Environmental enrichment mitigates the effects of basal forebrain lesions on cognitive flexibility. Neuroscience. 2008;154:444-53.
51. Richards M, Hardy R, Wadsworth ME. Does active leisure protect cognition? Evidence from a national birth cohort. Soc Sci Med. 2003;56:785-92.
52. Richards M, Deary IJ. A life course approach to cognitive reserve: a model for cognitive aging and development? Ann Neurol. 2005;58:617-22.
53. Leggio MG, Neri P, Graziano A, Mandolesi L, Molinari M, Petrosini L. Cerebellar contribution to spatial event processing: characterization of procedural learning. Exp Brain Res. 1999;127:1-11. (Pubitemid 29290552)
54. Rondi-Reig L, Le Marec N, Caston J, Mariani J. The role of climbing and parallel fibers inputs to cerebellar cortex in navigation. Behav Brain Res. 2002;132:11-8. (Pubitemid 34195454)
55. Gasbarri A, Pompili A, Pacitti C, Cicirata F. Comparative effects of lesions to the ponto-cerebellar and olivo-cerebellar pathways on motor and spatial learning in the rat. Neuroscience. 2003;116:1131-40. (Pubitemid 36262971)
56. Colombel C, Lalonde R, Caston J. The effects of unilateral removal of the cerebellar hemispheres on spatial learning and memory in rats. Brain Res. 2004;1004:108-15. (Pubitemid 38368066)
57. Leggio MG, Mandolesi L, Federico F, Spirito F, Ricci B, Gelfo F, et al. Environmental enrichment promotes improved spatial abilities and enhanced dendritic growth in the rat. Behav Brain Res. 2005;163:78-90. (Pubitemid 40991723)
58. Bambico FR, Cassano T, Dominguez-Lopez S, Katz N, Walker CD, Piomelli D, et al. Genetic deletion of fatty acid amide hydrolase alters emotional behavior and serotonergic transmission in the dorsal raphe, prefrontal cortex, and hippocampus. Neuropsychopharmacology. 2010;35:2083-100.
59. Long LE, Chesworth R, Arnold JC, Karl T. A follow-up study: acute behavioural effects of Delta(9)-THC in female heterozygous neuregulin 1 transmembrane domain mutant mice. Psychopharmacology. 2010;211:277-89.
60. Harris AP, D'Eath RB, Healy SD. Environmental enrichment enhances spatial cognition in rats by reducing thigmotaxis (wall hugging) during testing. Anim Behav. 2009;77:1459-64.
61. Mandolesi L, Leggio MG, Spirito F, Petrosini L. Cerebellar contribution to spatial event processing: do spatial procedures contribute to formation of spatial declarative knowledge? Eur J Neurosci. 2003;18:2618-26.
62. Middleton FA, Strick PL. Cerebellar projections to the prefrontal cortex of the primate. J Neurosci. 2001;21:700-12. (Pubitemid 32107458)
63. Ito M. Cerebellar circuitry as a neuronal machine. Prog Neurobiol. 2006;78:272-303. (Pubitemid 43850094)
64. Ito M. Control of mental activities by internal models in the cerebellum. Nat Rev Neurosci. 2008;9:304-13. (Pubitemid 351430830)
65. Diamond A. Close interrelation of motor development and cognitive development and of the cerebellum and prefrontal cortex. Child Dev. 2000;71:44-56.
66. Hyder F, Phelps EA, Wiggins CJ, Labar KS, Blamire AM, Shulman RG. "Willed action": a functional MRI study of the human prefrontal cortex during a sensorimotor task. Proc Natl Acad Sci USA. 1997;94:6989-94.
67. Spence SA, Hirsch SR, Brooks DJ, Grasby PM. Prefrontal cortex activity in people with schizophrenia and control subjects. Evidence from positron emission tomography for remission of 'hypofrontality' with recovery from acute schizophrenia. Br J Psychiatry. 1998;172:316-23.
68. Pochon JB, Levy R, Poline JB, Crozier S, Lehericy S, Pillon B, et al. The role of dorsolateral prefrontal cortex in the preparation of forthcoming actions: an fMRI study. Cereb Cortex. 2001;11:260-6. (Pubitemid 32199646)
69. Foti F, Mandolesi L, Cutuli D, Laricchiuta D, De Bartolo P, Gelfo F, et al. Cerebellar damage loosens the strategic use of the spatial structure of the search space. Cerebellum. 2010;9:29-41.
70. De Bartolo P, Mandolesi L, Federico F, Foti F, Cutuli D, Gelfo F, et al. Cerebellar involvement in cognitive flexibility. Neurobiol Learn Mem. 2009;92:310-7.
71. Mandolesi L, Foti F, Cutuli D, Laricchiuta D, Gelfo F, De Bartolo P, et al. Features of sequential learning in hemicerebellectomized rats. J Neurosci Res. 2010;88:478-86.
72. Pham TM, Ickes B, Albeck D, Soderstrom S, Granholm AC, Mohammed AH. Changes in brain nerve growth factor levels and nerve growth factor receptors in rats exposed to environmental enrichment for one year. Neuroscience. 1999;94:279-86. (Pubitemid 29457618)
73. Young D, Lawlor PA, Leone P, Dragunow M, During MJ. Environmental enrichment inhibits spontaneous apoptosis, prevents seizures and is neuroprotective. Nat Med. 1999;5:448-53. (Pubitemid 29180587)
74. Zajac MS, Pang TY, Wong N, Weinrich B, Leang LS, Craig JM, et al. Wheel running and environmental enrichment differentially modify exon-specific BDNF expression in the hippocampus of wild-type and pre-motor symptomatic male and female Huntington's disease mice. Hippocampus. 2010;20:621-36.
75. Ickes BR, Pham TM, Sanders LA, Albeck DS, Mohammed AH, Granholm AC. Long-term environmental enrichment leads to regional increases in neurotrophin levels in rat brain. Exp Neurol. 2000;64:45-52. (Pubitemid 30490721)
76. Angelucci F, De Bartolo P, Gelfo F, Foti F, Cutuli D, Bossu P, et al. Increased concentrations of nerve growth factor and brainderived neurotrophic factor in the rat cerebellum after exposure to environmental enrichment. Cerebellum. 2009;8:499-506.
77. Gelfo F, Cutuli D, Foti F, Laricchiuta D, De Bartolo P, Caltagirone C, et al. Enriched environment improves motor function and increases neurotrophins in hemicerebellar lesioned rats. Neurorehabil Neural Repair. 2010. doi:10.1177/1545968310380926