Beneficial effects of early environmental enrichment on motor development and spinal cord plasticity in a rat model of cerebral palsy

Behavioural Brain Research

Volumn 263, Issue , 2014, Pages 149-157

  Marques, Marília Rossato ^a   Stigger, Felipe ^a   Segabinazi, Ethiane ^a   Augustin, Otávio Américo ^a   Barbosa, Sílvia ^a   Piazza, Francele Valente ^a   Achaval, Matilde ^a   Marcuzzo, Simone ^a  

^a FEDERAL UNIVERSITY OF RIO GRANDE DO SUL   (Brazil)

Author keywords

Cerebral palsy; Environmental enrichment; Motor impairment; Rat model

Indexed keywords

SYNAPTOPHYSIN; SYP PROTEIN, RAT;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BODY WEIGHT; CEREBRAL PALSY; CONTROLLED STUDY; ENVIRONMENTAL ENRICHMENT; EXPERIMENTAL LOCOMOTOR ACTIVITY TEST; GAIT; HISTOPATHOLOGY; HORIZONTAL LADDER TEST; MOTONEURON; MOTOR DEVELOPMENT; MOTOR DYSFUNCTION; MOTOR PERFORMANCE; MUSCLE ATROPHY; NARROW SUSPENDED BAR TEST; NERVE CELL PLASTICITY; NONHUMAN; OPEN FIELD TEST; OPTICAL DENSITY; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; ROTAROD TEST; SOLEUS MUSCLE; SPINAL CORD PLASTICITY; SPINAL CORD VENTRAL HORN; WALKING; ANIMAL; ANIMAL HOUSING; ANTERIOR HORN CELL; COMPLICATION; DISEASE MODEL; ENVIRONMENT; METABOLISM; MUSCULAR ATROPHY; ORGAN SIZE; PATHOLOGY; PATHOPHYSIOLOGY; SECONDARY PREVENTION; SKELETAL MUSCLE; SPINAL CORD; TREATMENT OUTCOME; WISTAR RAT;

ANIMALS; ANTERIOR HORN CELLS; BODY WEIGHT; CEREBRAL PALSY; DISEASE MODELS, ANIMAL; ENVIRONMENT; HOUSING, ANIMAL; MOTOR NEURONS; MOTOR SKILLS; MUSCLE, SKELETAL; MUSCULAR ATROPHY; ORGAN SIZE; RATS; RATS, WISTAR; SECONDARY PREVENTION; SPINAL CORD; SYNAPTOPHYSIN; TREATMENT OUTCOME;

EID: 84896721222     PISSN: 01664328     EISSN: 18727549     Source Type: Journal    
DOI: 10.1016/j.bbr.2014.01.007     Document Type: Article

References (53)

1. Bax M., Goldstein M., Rosenbaum P., Leviton A., Paneth N. Proposed definition and classification of cerebral palsy, April 2005. Developmental Medicine & Child Neurology 2005, 47:571-576.
2. Zarrinkalam R., Russo R.N., Gibson C.S., van Essen P., Peek A.K., Haan E.A. CP or not CP?. A review of diagnoses in a cerebral palsy register. Pediatric Neurology 2010, 42:177-180.
3. Johnson A. Prevalence and characteristics of children with cerebral palsy in Europe. Developmental Medicine & Child Neurology 2002, 44:633-640.
4. Krigger K.W. Cerebral palsy: an overview. American Family Physician 2006, 73:91-100.
5. Damiano D.L., Alter K.E., Chambers H. New clinical and research trends in lower extremity management for ambulatory children with cerebral palsy. Physical Medicine & Rehabilitation Clinics of North America 2009, 20:469-491.
6. Brændvík S.M., Elvrum A.-K.G., Vereijken B., Roeleveld K. Involuntary and voluntary muscle activation in children with unilateral cerebral palsy-relationship to upper limb activity. European Journal of Paediatric Neurology 2013, 17:274-279.
7. Goldstein M. The treatment of cerebral palsy: what we know, what we don't know. Journal of Pediatrics 2004, 145:S42-S46.
8. Kesar T.M., Sawaki L., Burdette J.H., Cabrera M.N., Kolaski K., Smith B.P., O'Shea T.M., Koman L.A., Wittenberg G.F. Motor cortical functional geometry in cerebral palsy and its relationship to disability. Clinical Neurophysiology 2012, 123:1383-1390.
9. Abel M.F., Damiano D.L. Strategies for increasing walking speed in diplegic cerebral palsy. Journal of Pediatric Orthopaedics 1996, 16:753-758.
10. Maltais D.B., Pierrynowski M.R., Galea V.A., Bar-Or O. Habitual physical activity levels are associated with biomechanical walking economy in children with cerebral palsy. American Journal of Physical Medicine & Rehabilitation 2005, 83:36-45.
11. 2 cost of walking in cerebral palsy. Medicine & Science in Sports & Exercise 2005, 37:347-353.
12. Piccinini L., Cimolin V., Galli M., Berti M., Crivellini M., Turconi A.C. Quantification of energy expenditure during gait in children affected by cerebral palsy. Europa Medicophysica 2007, 43:7-12.
13. Kurz M.J., Stuberg W.A., DeJong S.L. Mechanical work performed by the legs of children with spastic diplegic cerebral palsy. Gait Posture 2010, 31:347-350.
14. Wrotniak B.H., Epstein L.H., Dorn J.M., Jones K.E., Kondilis V.A. The relationship between motor proficiency and physical activity in children. Pediatrics 2006, 118:e1758-e1765.
15. Jahnsen R., Villien L., Aamodt G., Stanghelle J., Holm I. Musculoskeletal pain in adults with cerebral palsy compared with the general population. Journal of Rehabilitation Medicine 2004, 36:78-84.
16. Damiano D.L. Activity, activity, activity: rethinking our physical therapy approach to cerebral palsy. Physical Therapy 2006, 86:1534-1540.
17. Koman L.A., Smith B.P., Shilt J.S. Cerebral palsy. Lancet 2004, 363:1619-1631.
18. Berker A.N., Yalçin M.S. Cerebral palsy: orthopedic aspects and rehabilitation. Pediatric Clinics of North America 2008, 55:1209-1225.
19. Nithianantharajah J., Hannan A.J. Enriched environments, experience-dependent plasticity and disorders of the nervous system. Nature Reviews Neuroscience 2006, 7:697-709.
20. 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. The Journal Neuroscience 2004, 24:2270-2276.
21. 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. Behavioural Brain Research 2005, 163:78-90.
22. Schneider T., Turczak J., Przewlocki R. Environmental enrichment reverses behavioral alterations in rats prenatally exposed to valproic acid: issues for a therapeutic approach in autism. Neuropsychopharmacology 2006, 31:36-46.
23. Pang T.Y.C., Hannan A.J. Environmental enrichment: a cure for cancer? It's all in the mind. Journal of Molecular Cell Biology 2010, 2:302-304.
24. Fairhurst G.D., Frey M.D., Reichert J.F., Szelest I., Kelly D.M., Bortolotti G.R. Does environmental enrichment reduce stress? An integrated measure of corticosterone from feathers provides a novel perspective. PLoS One 2011, 6:e17663.
25. Rojas J.J., Deniz B.F., Miguel P.M., Diaz R., Hermel E.S-S., Achaval M., Netto C.A., Pereira L.O. Effects of daily environmental enrichment on behavior and dendritic spine density in hippocampus following neonatal hypoxia-ischemia in the rat. Experimental Neurology 2013, 241:25-33.
26. Beauquis J., Pavía P., Pomilio C., Vinuesa A., Podlutskaya N., Galvan V., Saravia F. Environmental enrichment prevents astroglial pathological changes in the hippocampus of APP transgenic mice, model of Alzheimer's disease. Experimental Neurology 2013, 239:28-37.
27. Stigger F., Felizzola A.L.S., Kronbauer G.A., Couto G.K., Achaval M., Marcuzzo S. Effects of fetal exposure to lipopolysaccharide, perinatal anoxia and sensorimotor restriction on motor skills and musculoskeletal tissue: implications for an animal model of cerebral palsy. Experimental Neurology 2011, 228:183-191.
28. Kline A.E., McAloon R.L., Henderson K.A., Bansal U.K., Ganti B.M., Ahmed R.H., Gibbs R.B., Sozda C.N. Evaluation of a combined therapeutic regimen of 8-OH-DPAT and environmental enrichment after experimental traumatic brain injury. Journal of Neurotrauma 2010, 12:289-298.
29. Marcuzzo S., Dutra M.F., Stigger F., Nascimento P.S., Ilha J., Kalil-Gaspar P.I., Achaval M. Beneficial effects of treadmill training in a cerebral palsy-like rodent model: walking pattern and soleus quantitative histology. Brain Research 2008, 1222:129-140.
30. Xavier L.L., Viola G.G., Ferraz A.C., Cunha C.D., Deonizio J.M.D., Netto C.A., Achaval M. A simple and fast densitometric method for the analysis of tyrosine hydroxylase immunoreactivity in the substancia nigra pars compacta and in the ventral tegmental area. Brain Research Protocols 2005, 16:59-64.
31. Samson-Fang L., Fung E., Stallings V.A., Conaway M., Worley G., Rosembaum P., Calvert R., O'Donnell M., Henderson R.C., Chumlea W.C., Liptak G.S., Stevenson R.D. Relationship of nutritional status to health and societal participation in children with cerebral palsy. Journal of Pediatrics 2002, 141:637-643.
32. Strata F., Coq J-Q., Byl N., Merzenich M.M. Effects of sensorimotor restriction and anoxia of gait and motor cortex organization: implications for a rodent model of cerebral palsy. Neuroscience 2004, 129:141-156.
33. Westerga J., Gramsbergen A. Structural changes of the soleus and the tibialis anterior motoneuron pool during development in the rat. Journal of Comparative Neurology 1992, 319:406-416.
34. Wilson S.J., Ross J.J., Harris A.J. A critical period for formation of secondary myotubes defined by prenatal undernourishment in rats. Development 1988, 102:815-821.
35. Marcuzzo S., Dutra M.F., Stigger F., Nascimento P.S., Ilha J., Kalil-Gaspar P.I., Achaval M. Different effects of anoxia and hind-limb immobilization on sensorimotor development and cell numbers in the somatosensory cortex in rats. Brain & Development 2010, 32:323-331.
36. Zaias J., Kelley J.B., Zakharova E.S., Izenwasser S. Social and physical environmental enrichment differentially affect growth and activity of preadolescent and adolescent male rats. Journal of the American Association of Laboratory Animal Science 2008, 47:30-34.
37. Campanozzi A., Capano G., Miele E., Romano A., Scuccimarra G., del Giudice E., Strisciuglio C., Militerni R., Staiano A. Impact of malnutrition on gastrointestinal disorders and gross motor abilities in children with cerebral palsy. Brain & Development 2007, 29:26-29.
38. Risedal A., Mattsson B., Dahlqvist P., Nordborg C., Olsson T., Johansson B.B. Environmental influences on functional outcome after a cortical infarct in the rat. Brain Research Bulletin 2002, 58:315-321.
39. Jadavji N.M., Kolb B., Metz G.A. Enriched environment improves motor function in intact and unilateral dopamine-depleted rats. Neuroscience 2006, 140:1127-1138.
40. Hoffman A.N., Malena R.R., Westergom B.P., Luthra P., Cheng J.P., Aslam H.A., Zafonte R.S., Kline A.E. Environmental enrichment-mediated functional improvement after experimental traumatic brain injury is contingent on task-specific neurobehavioral experience. Neuroscience Letters 2008, 431:226-230.
41. Schrijver N.C.A., Bahr N.I., Weiss I.C., Würbel H. Dissociable effects of isolation rearing and environmental enrichment on exploration, spatial learning and HPA activity in adult rats. Pharmacology Biochemistry and Behavior 2002, 73:209-224.
42. Beranoya-Milshtein N., Hollander N., Apter A., Kukulansky T., Raz N., Yaniv I., Pick C.G. Environmental enrichment in mice decreases anxiety, attenuates stress response and enhances natural killer cell activity. European Journal of Neuroscience 2004, 20:1341-1347.
43. Brenes J.C., Padilla M., Fornaguera J. A detailed analysis of open-field habituation and behavioral and neurochemical antidepressant-like effects in postweaning enriched rats. Behavioural Brain Research 2009, 197:125-137.
44. Nilsson L., Mohammed A.K., Henriksson B.G., Folkesson R., Winblad B., Bergström L. Environmental influence on somatostatin levels and gene expression in the rat brain. Brain Research 1993, 628:93-98.
45. Brown J., Cooper-Kuhn C.M., Kempermann G., Van Praag H., Winkler J., Gage F.H., Kuhn H.G. Enriched environment and physical activity stimulate hippocampal but not olfactory bulb neurogenesis. European Journal of Neuroscience 2003, 17:2042-2046.
46. Thomason D.B., Booth F.W. Atrophy of the soleus muscle by hindlimb unweighting. Journal of Applied Physiology 1990, 68:1-12.
47. Altman J., Sudarshan K. Postnatal development of locomotion in the laboratory rat. Animal Behaviour 1975, 23:896-920.
48. Stigger F., Nascimento P.S., Dutra M.F., Couto G.K., Ilha J., Achaval M., Marcuzzo S. Treadmill training induces plasticity in spinal motoneurons and sciatic nerve after sensorimotor restriction during early postnatal period: new insights into the clinic approach for children with cerebral palsy. International Journal of Developmental Neuroscience 2011, 29:833-838.
49. Kerai B., Greensmith L., Vrbová G., Navarrete R. Effect of transient neonatal muscle paralysis on the growth of soleus motoneurones in the rat. Developmental Brain Research 1995, 85:89-95.
50. Greensmith L., Vrbová G. Alterations of nerve-muscle interaction during postnatal development influence motoneurone survival in rats. Developmental Brain Research 1992, 69:125-131.
51. Walaas S.I., Browning M.D., Greengard P. Synapsin Ia, synapsin Ib, protein IIIa, and protein IIIb, four related synaptic vesicle-associated phosphoproteins, share regional and cellular localization in rat brain. Journal of Neurochemistry 1988, 51:1214-1220.
52. Alder J., Kanki H., Valtorta F., Greengard P., Poo M.M. Overexpression of synaptophysin enhances neurotransmitter secretion at xenopus neuromuscular synapses. The Journal of Neuroscience 1995, 15:511-519.
53. Chou A.K., Muhammad R., Huang S.M., Chen J.T., Wu C.L., Lin C.R., Lee T.H., Lin S.H., Lu C.Y., Yang L.C. Altered synaptophysin expression in the rat spinal cord after chronic constriction injury of sciatic nerve. Neuroscience Letters 2002, 333:155-158.