Before or after does it matter? Different protocols of environmental enrichment differently influence motor, synaptic and structural deficits of cerebellar origin

Neurobiology of Disease

Volumn 42, Issue 1, 2011, Pages 9-20

  Cutuli, Debora ^a,b   Rossi, Silvia ^a,c   Burello, Lorena ^a,b   Laricchiuta, Daniela ^a,b   De Chiara, Valentina ^a,c   Foti, Francesca ^a,b   De Bartolo, Paola ^a,b   Musella, Alessandra ^a,b   Gelfo, Francesca ^a,b   Centonze, Diego ^a,c   Petrosini, Laura ^a,b  

^a IRCCS FONDAZIONE SANTA LUCIA   (Italy)

^b SAPIENZA UNIVERSITY OF ROME   (Italy)

^c UNIVERSITY OF ROME TOR VERGATA   (Italy)

Author keywords

Cerebellar compensation; Functional recovery; Glutamate transmission; Postural and motor behavior; Rat; Striatal interneuronal morphology

Indexed keywords

GLUTAMIC ACID;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BODY POSTURE; CELL DENSITY; CELL STRUCTURE; CEREBELLECTOMY; CEREBELLUM DISEASE; CONTROLLED STUDY; CORPUS STRIATUM; DENDRITIC CELL; ENVIRONMENTAL ENRICHMENT; EXCITATORY POSTSYNAPTIC POTENTIAL; INTERNEURON; LOCOMOTION; MALE; MOTOR DYSFUNCTION; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; RAT; SYNAPSE;

ANIMALS; BRAIN INJURIES; CEREBELLAR DISEASES; DISEASE MODELS, ANIMAL; ENVIRONMENT; ENVIRONMENT, CONTROLLED; MALE; MOTOR ACTIVITY; RATS; RATS, WISTAR; SYNAPTIC TRANSMISSION;

EID: 79751525641     PISSN: 09699961     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.nbd.2010.12.007     Document Type: Article

References (77)

1. Amrani K., Dykes R.W., Lamarre Y. Bilateral contributions to motor recovery in the monkey following lesions of the deep cerebellar nuclei. Brain Res. 1996, 740:275-284.
2. Angelucci F., De Bartolo P., Gelfo F., Foti F., Cutuli D., Bossù P., Caltagirone C., Petrosini L. Increased concentrations of nerve growth factor and brain-derived neurotrophic factor in the rat cerebellum after exposure to environmental enrichment. Cerebellum 2009, 8:499-506.
3. Apps R., Garwicz M. Anatomical and physiological foundations of cerebellar information processing. Nat. Rev. Neurosci. 2005, 6:297-311.
4. Arendash G.W., Garcia M.F., Costa D.A., Cracchiolo J.R., Wefes I.M., Potter H. Environmental enrichment improves cognition in aged Alzheimer's transgenic mice despite stable beta-amyloid deposition. NeuroReport 2004, 15:1751-1754.
5. Bezard E., Dovero S., Belin D., Duconger S., Jackson-Lewis V., Przedborski S., Piazza P.V., Gross C.E., Jaber M. Enriched environment confers resistance to 1-methyl-4-phenyl-1, 2, 3, 6-tetrahydropyridine and cocaine: involvement of dopamine transporter and trophic factors. J. Neurosci. 2003, 23:10999-11007.
6. Blum D., Galas M.C., Pintor A., Brouillet E., Ledent C., Muller C.E., Bantubungi K., Galluzzo M., Gall D., Cuvelier L., Rolland A.S., Popoli P., Schiffmann S.N. A dual role of adenosine A2A receptors in 3-nitropropionic acid-induced striatal lesions: implications for the neuroprotective potential of A2A antagonists. J. Neurosci. 2003, 23:5361-5369.
7. Bracci E., Centonze D., Bernardi G., Calabresi P. Voltage-dependent membrane potential oscillations of rat striatal fast-spiking interneurons. J. Physiol. 2003, 15:121-130.
8. Calabresi P., Mercuri N.B., De Murtas M., Bernardi G. Endogenous GABA mediates presynaptic inhibition of spontaneous and evoked excitatory synaptic potentials in the rat neostriatum. Neurosci. Lett. 1990, 118:99-102.
9. Centonze D., Rossi S., Prosperetti C., Tscherter A., Bernardi G., Maccarrone M., Calabresi P. Abnormal sensitivity to cannabinoid receptor stimulation might contribute to altered gamma-aminobutyric acid transmission in the striatum of R6/2 Huntington's disease mice. Biol. Psychiatry 2005, 57:1583-1589.
10. Centonze D., Rossi S., De Bartolo P., De C.V., Foti F., Musella A., Mataluni G., Rossi S., Bernardi G., Koch G., Petrosini L. Adaptations of glutamatergic synapses in the striatum contribute to recovery from cerebellar damage. Eur. J. Neurosci. 2008, 27:2188-2196.
11. Cepeda C., Hurst R.S., Calvert C.R., Hernández-Echeagaray E., Nguyen O.K., Jocoy E., Christian L.J., Ariano M.A., Levine M.S. Transient and progressive electrophysiological alterations in the corticostriatal pathway in a mouse model of Huntington's disease. J. Neurosci. 2003, 23:961-969.
12. Chauvet C., Lardeux V., Goldberg S.R., Jaber M., Solinas M. Environmental enrichment reduces cocaine seeking and reinstatement induced by cues and stress but not by cocaine. Neuropsychopharmacology 2009, 34:2767-2778.
13. De Bartolo P., Leggio M.G., Mandolesi L., Foti F., Gelfo F., Ferlazzo F., Petrosini L. Environmental enrichment mitigates the effects of basal forebrain lesions on cognitive flexibility. Neuroscience 2008, 154:444-453.
14. De Chiara V., Errico F., Musella A., Rossi S., Mataluni G., Sacchetti L., Siracusano A., Castelli M., Cavasinni F., Bernardi G., Usiello A., Centonze D. Voluntary exercise and sucrose consumption enhance cannabinoid CB1 receptor sensitivity in the striatum. Neuropsychopharmacology 2010, 35:374-387.
15. Desmurget M., Gaveau V., Vindras P., Turner R.S., Broussolle E., Thobois S. On-line motor control in patients with Parkinson's disease. Brain 2004, 127:1755-1773.
16. Dhanushkodi A., Bindu B., Raju T.R., Kutty B.M. Exposure to enriched environment improves spatial learning performances and enhances cell density but not choline acetyltransferase activity in the hippocampus of ventral subicular-lesioned rats. Behav. Neurosci. 2007, 121:491-500.
17. Diamond M.C., Law F., Rhodes H., Lindner B., Rosenzweig M.R., Krech D., Bennett E.L. Increases in cortical depth and glia numbers in rats subjected to enriched environment. J. Comp. Neurol. 1966, 128:117-126.
18. Dowie M.J., Bradshaw H.B., Howard M.L., Nicholson L.F., Faull R.L., Hannan A.J., Glass M. Altered CB1 receptor and endocannabinoid levels precede motor symptom onset in a transgenic mouse model of Huntington's disease. Neuroscience 2009, 163:456-465.
19. Dube L., Smith A.D., Bolam J.P. Identification of synaptic terminals of thalamic or cortical origin in contact with distinct medium-size spiny neurons in the rat neostriatum. J. Comp. Neurol. 1988, 267:455-471.
20. Faherty C.J., Kerley D., Smeyne R.J. A Golgi-Cox morphological analysis of neuronal changes induced by environmental enrichment. Brain Res. Dev. Brain Res. 2003, 141:55-61.
21. Federico F., Leggio M.G., Mandolesi L., Petrosini L. The NMDA receptor antagonist CGS 19755 disrupts recovery following cerebellar lesions. Restor. Neurol. Neurosci. 2006, 24:1-7.
22. Foti F., Laricchiuta D., Cutuli D., De Bartolo P., Gelfo F., Angelucci F., Petrosini L. Exposure to an enriched environment accelerates recovery from cerebellar lesion. Cerebellum 2010, 10.1007/s12311-010-0236-z.
23. Gelfo F., De Bartolo P., Giovine A., Petrosini L., Leggio M.G. Layer and regional effects of environmental enrichment on the pyramidal neuron morphology of the rat. Neurobiol. Learn. Mem. 2009, 91:353-365.
24. Gelfo F., Cutuli D., Foti F., Laricchiuta D., De Bartolo P., Caltagirone C., Petrosini L., Angelucci F. Enriched environment improves motor function and increases neurotrophins in hemicerebellar lesioned rats. Neurorehabil. Neural. Repair. 2010, 10.1177/1545968310380926.
25. Glass M., van Dellen A., Blakemore C., Hannan A.J., Faull R.L. Delayed onset of Huntington's disease in mice in an enriched environment correlates with delayed loss of cannabinoid CB1 receptors. Neuroscience 2004, 123:207-212.
26. Goldberger M.E., Growdon J.H. Pattern of recovery following cerebellar deep nuclear lesions in monkeys. Exp. Neurol. 1973, 39:307-322.
27. Gramsbergen A. Neural compensation after early lesions: a clinical view of animal experiments. Neurosci. Biobehav. Rev. 2007, 31:1088-1094.
28. Graybiel A.M. The basal ganglia: learning new tricks and loving it. Curr. Opin. Neurobiol. 2005, 15:638-644.
29. Greenough W.T., Volkmar F.R., Juraska J.M. Effects of rearing complexity on dendritic branching in frontolateral and temporal cortex of the rat. Exp. Neurol. 1973, 41:371-378.
30. Hockly E., Cordery P.M., Woodman B., Mahal A., van Dellen A., Blakemore C., Lewis C.M., Hannan A.J., Bates G.P. Environmental enrichment slows disease progression in R61/2 Huntington's disease mice. Ann. Neurol. 2002, 51:235-242.
31. Hoshi E., Tremblay L., Feger J., Carras P.L., Strick P.L. The cerebellum communicates with the basal ganglia. Nat. Neurosci. 2005, 8:1491-1493.
32. Jankowsky J.L., Melnikova T., Fadale D.J., Xu G.M., Slunt H.H., Gonzales V., Younkin L.H., Younkin S.G., Borchelt D.R., Savonenko A.V. Environmental enrichment mitigates cognitive deficits in a mouse model of Alzheimer's disease. J. Neurosci. 2005, 25:5217-5224.
33. Kao M.H., Doupe A.J., Brainard M.S. Contributions of an avian basal ganglia-forebrain circuit to real-time modulation of song. Nature 2005, 433:638-643.
34. Kawaguchi Y., Wilson C.J., Augood S.J., Emson P.C. Striatal interneurones: chemical, physiological and morphological characterization. Trends Neurosci. 1995, 18:527-535.
35. Kincaid A.E., Zheng T., Wilson C.J. Connectivity and convergence of single corticostriatal axons. J. Neurosci. 1998, 18:4722-4731.
36. Kita H. Glutamatergic and GABAergic postsynaptic responses of striatal spiny neurons to intrastriatal and cortical stimulation recorded in slice preparations. Neuroscience 1996, 70:925-940.
37. Kolb B., Gibb R., Gorny G. Experience-dependent changes in dendritic arbor and spine density in neocortex vary qualitatively with age and sex. Neurobiol. Learn. Mem. 2003, 79:1-10.
38. Koòs T., Tepper J.M. Inhibitory control of neostriatal projection neurons by GABAergic interneurons. Nat. Neurosci. 1999, 2:467-472.
39. Krech D., Rosenzweig M.R., Bennett E.L. Effects of environmental complexity and training on brain chemistry. J. Comp. Physiol. Psychol. 1960, 53:509-519.
40. Krech D., Rosenzweig M.R., Bennett E.L. Relations between chemistry and problem-solving among rats raised in enriched and impoverished environments. J. Comp. Physiol. Psychol. 1962, 55:801-807.
41. Laviola G., Hannan A.J., Macri S., Solinas M., Jaber M. Effects of enriched environment on animal models of neurodegenerative diseases and psychiatric disorders. Neurobiol. Dis. 2008, 31:159-168.
42. Lazarov O., Robinson J., Tang Y.P., Hairston I.S., Korade-Mirnics Z., Lee V.M.Y., Hersh L.B., Sapolsky R.M., Mirnics K., Sisodia S.S. Environmental enrichment reduces A beta levels and amyloid deposition in transgenic mice. Cell 2005, 120:701-713.
43. Leggio M.G., Mandolesi L., Federico F., Spirito F., Ricci B., Gelfo F., Petrosini L. Environmental enrichment promotes improved spatial abilities and enhanced dendritic growth in the rat. Behav. Brain Res. 2005, 163:78-90.
44. Lei W., Jiao Y., Del Mar N., Reiner A. Evidence for differential cortical input to direct pathway versus indirect pathway striatal projection neurons in rats. J. Neurosci. 2004, 24:8289-8299.
45. Levi O., Jongen-Relo A.L., Feldon J., Roses A.D., Michaelson D.M. ApoE4 impairs hippocampal plasticity isoform-specifically and blocks the environmental stimulation of synaptogenesis and memory. Neurobiol. Dis. 2003, 13:273-282.
46. Mandolesi L., De Bartolo P., Foti F., Gelfo F., Federico F., Leggio M.G., Petrosini L. Environmental enrichment provides a cognitive reserve to be spent in the case of brain lesion. J. Alzheimers Dis. 2008, 15:11-28.
47. McOmish C.E., Burrows E., Howard M., Scarr E., Kim D., Shin H.S., Dean B., van den B.M., Hannan A.J. Phospholipase C-beta1 knockout mice exhibit endophenotypes modeling schizophrenia which are rescued by environmental enrichment and clozapine administration. Mol. Psychiatry 2008, 13:661-672.
48. Nichols J.A., Jakkamsetti V.P., Salgado H., Dinh L., Kilgard M.P., Atzori M. Environmental enrichment selectively increases glutamatergic responses in layer II/III of the auditory cortex of the rat. Neuroscience 2007, 145:832-840.
49. Nithianantharajah J., Hannan A.J. Enriched environments, experience-dependent plasticity and disorders of the nervous system. Nat. Rev. Neurosci. 2006, 7:697-709.
50. Nithianantharajah J., Levis H., Murphy M. Environmental enrichment results in cortical and subcortical changes in levels of synaptophysin and PSD-95 proteins. Neurobiol. Learn. Mem. 2004, 81:200-210.
51. Nudo R.J., Wise B.M., SiFuentes F., Milliken G.W. Neural substrates for the effects of rehabilitative training on motor recovery after ischemic infarct. Science 1996, 272:1791-1794.
52. Paban V., Jaffard M., Chambon C., Malafosse M., Alescio-Lautier B. Time course of behavioral changes following basal forebrain cholinergic damage in rats: environmental enrichment as a therapeutic intervention. Neuroscience 2005, 132:13-32.
53. Passineau M.J., Green E.J., Dietrich W.D. Therapeutic effects of environmental enrichment on cognitive function and tissue integrity following severe traumatic brain injury in rats. Exp. Neurol. 2001, 168:373-384.
54. Pong M., Horn K.M., Gibson A.R. Pathways for control of face and neck musculature by the basal ganglia and cerebellum. Brain Res. Rev. 2008, 58:249-264.
55. Restivo L., Ferrari F., Passino E., Sgobio C., Bock J., Oostra B.A., Bagni C., Ammassari-Teule M. Enriched environment promotes behavioral and morphological recovery in a mouse model for the fragile X syndrome. Proc. Natl Acad. Sci. USA 2005, 102:11557-11562.
56. Richards M., Deary I.J. A life course approach to cognitive reserve: a model for cognitive aging and development?. Ann. Neurol. 2005, 58:617-622.
57. Rosenzweig M.R., Bennett E.L. Psychobiology of plasticity: effects of training and experience on brain and behavior. Behav. Brain Res. 1996, 78:57-65.
58. Sadikot A.F., Parent A., Francois C. The center median and parafascicular thalamic nuclei project respectively to the sensorimotor and associative limbic striatal territories in the squirrel-monkey. Brain Res. 1990, 510:161-165.
59. Sadikot A.F., Parent A., Smith Y., Bolam J.P. Efferent connections of the centromedian and parafascicular thalamic nuclei in the squirrel monkey: a light and electron microscopic study of the thalamostriatal projection in relation to striatal heterogeneity. J. Comp. Neurol. 1992, 320:228-242.
60. Segovia G., Yague A.G., Garcia-Verdugo J.M., Mora F. Environmental enrichment promotes neurogenesis and changes the extracellular concentrations of glutamate and GABA in the hippocampus of aged rats. Brain Res. Bull. 2006, 70:8-14.
61. Segovia G., Del Arco A., de Blas M., Garrido P., Mora F. Effects of an enriched environment on the release of dopamine in the prefrontal cortex produced by stress and on working memory during aging in the awake rat. Behav. Brain Res. 2008, 187:304-311.
62. Segovia G., Del Arco A., Garrido P., de Blas M., Mora F. Environmental enrichment reduces the response to stress of the cholinergic system in the prefrontal cortex during aging. Neurochem. Int. 2008, 52:1198-1203.
63. Sidibe M., Smith Y. Thalamic inputs to striatal interneurons in monkeys: synaptic organization and co-localization of calcium binding proteins. Neuroscience 1999, 89:1189-1208.
64. Smith P.F., Darlington C.L. The NMDA antagonists MK801 and CPP disrupt compensation for unilateral labyrinthectomy in the guinea pig. Neurosi. Lett. 1988, 94:309-313.
65. Smith R.L., Mosko S., Lynch G. Role of various brain areas in recovery from partial cerebellar lesions in the adult rat. Behav. Biol. 1974, 12:165-176.
66. Solinas M., Chauvet C., Thiriet N., El Rawas R., Jaber M. Reversal of cocaine addiction by environmental enrichment. Proc. Natl Acad. Sci. USA 2008, 105:17145-17150.
67. Spires T.L., Grote H.E., Varshney N.K., Cordery P.M., van Dellen A., Blakemore C., Hannan A.J. Environmental enrichment rescues protein deficits in a mouse model of Huntington's disease, indicating a possible disease mechanism. J. Neurosci. 2004, 24:2270-2276.
68. Stern Y. Cognitive reserve. Neuropsychologia 2009, 47:2015-2028.
69. Tang K., Low M.J., Grandy D.K., Lovinger D.M. Dopamine-dependent synaptic plasticity in striatum during in vivo development. Proc. Natl. Acad. Sci. U. S. A. 2001, 98:1255-1260.
70. Turner A.M., Greenough W.T. Differential rearing effects on rat visual cortex synapses. I. Synaptic and neuronal density and synapses per neuron. Brain Res. 1985, 329:195-203.
71. van Dellen A., Blakemore C., Deacon R., York D., Hannan A.J. Delaying the onset of Huntington's in mice. Nature 2000, 404:721-722.
72. Wiltschko A.B., Pettibone J.R., Berke J.D. Opposite effects of stimulant and antipsychotic drugs on striatal fast-spiking interneurons. Neuropsychopharmacology 2010, 35:1261-1270.
73. Wolf S.A., Kronenberg G., Lehmann K., Blankenship A., Overall R., Staufenbiel M., Kempermann G. Cognitive and physical activity differently modulate disease progression in the amyloid precursor protein (APP)-23 model of Alzheimer's disease. Biol. Psychiatry 2006, 60:1314-1323.
74. Xerri C., Zennou-Azogui Y. Influence of the postlesion environment and chronic piracetam treatment on the organization of the somatotopic map in the rat primary somatosensory cortex after focal cortical injury. Neuroscience 2003, 118:161-177.
75. Xu Z.C., Wilson C.J., Emson P.C. Synaptic potentials evoked in spiny neurons in rat neostriatal grafts by cortical and thalamic stimulation. J. Neurophysiol. 1991, 65:477-493.
76. Yamada S., Takaki T., Yokoo H., Tanaka M. Differential effects of dopamine antagonists on evoked dopamine release from slices of striatum and nucleus accumbens in rats. J. Pharm. Pharmacol. 1995, 47:259-262.
77. Yoshida H., Ohno M., Watanabe S. Roles of dopamine D-1 receptors in striatal Fos protein induction associated with methamphetamine behavioral sensitization in rats. Brain Res. Bull. 1995, 38:393-397.