Sensorimotor experience influences recovery of forelimb abilities but not tissue loss after focal cortical compression in adult rats

PLoS ONE

Volumn 6, Issue 2, 2011, Pages

  Martinez, Marina ^a   Brezun, Jean Michel ^a   Xerri, Christian ^a  

^a CNRS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN ASYMMETRY; BRAIN CORTEX LESION; BRAIN INJURY; CONTROLLED STUDY; DORSAL RHIZOTOMY; FOREFOOT; FORELIMB; GLIOSIS; LOCOMOTION; MALE; NONHUMAN; RAT; SENSORIMOTOR FUNCTION; SOCIAL INTERACTION; SOMATOSENSORY CORTEX; TACTILE STIMULATION; AGE; ANIMAL; ANIMAL BEHAVIOR; BRAIN CORTEX; COMPRESSION FRACTURE; CONVALESCENCE; CRANIOTOMY; INJURY; LONG EVANS RAT; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; PSYCHOLOGICAL ASPECT; RANDOMIZATION; SPINAL ROOT;

RATTUS;

AGE FACTORS; ANIMALS; BEHAVIOR, ANIMAL; BRAIN INJURIES; CEREBRAL CORTEX; CRANIOTOMY; FORELIMB; FRACTURES, COMPRESSION; MALE; PHYSICAL CONDITIONING, ANIMAL; RANDOM ALLOCATION; RATS; RATS, LONG-EVANS; RECOVERY OF FUNCTION; SOMATOSENSORY CORTEX; SPINAL NERVE ROOTS;

EID: 79951876359     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0016726     Document Type: Article

References (56)

1. Will B, Galani R, Kelche C, Rosenzweig MR, (2004) Recovery from brain injury in animals: relative efficacy of environmental enrichment, physical exercise or formal training (1990-2002). Prog Neurobiol 72: 167-182.
2. Johansson BB, Ohlsson AL, (1996) Environment, social interaction, and physical activity as determinants of functional outcome after cerebral infarction in the rat. Exp Neurol 139: 322-327.
3. Risedal A, Mattsson B, Dahlqvist P, Nordborg C, Olsson T, et al. (2002) Environmental influences on functional outcome after a cortical infarct in the rat. Brain Res Bull 58: 315-321.
4. Marin R, Williams A, Hale S, Burge B, Mense M, et al. (2003) The effect of voluntary exercise exposure on histological and neurobehavioral outcomes after ischemic brain injury in the rat. Physiol Behav 80: 167-175.
5. Kozlowski DA, James DC, Schallert T, (1996) Use-dependent exaggeration of neuronal injury after unilateral sensorimotor cortex lesions. J Neurosci 16: 4776-4786.
6. Humm JL, Kozlowski DA, James DC, Gotts JE, Schallert T, (1998) Use-dependent exacerbation of brain damage occurs during an early post-lesion vulnerable period. Brain Res 783: 286-292.
7. Auriat AM, Grams JD, Yan RH, Colbourne F, (2006) Forced exercise does not improve recovery after hemorrhagic stroke in rats. Brain Res 1109: 183-191.
8. Keiner S, Wurm F, Kunze A, Witte OW, Redecker C, (2008) Rehabilitative therapies differentially alter proliferation and survival of glial cell populations in the perilesional zone of cortical infarcts. Glia 56: 516-527.
9. Lippert-Gruener M, Maegele M, Garbe J, Angelov DN, (2007) Late effects of enriched environment (EE) plus multimodal early onset stimulation (MEOS) after traumatic brain injury in rats: Ongoing improvement of neuromotor function despite sustained volume of the CNS lesion. Exp Neurol 203: 82-94.
10. Grabowski M, Sorensen JC, Mattsson B, Zimmer J, Johansson BB, (1995) Influence of an enriched environment and cortical grafting on functional outcome in brain infarcts of adult rats. Exp Neurol 133: 96-102.
11. Komitova M, Perfilieva E, Mattsson B, Eriksson PS, Johansson BB, (2006) Enriched environment after focal cortical ischemia enhances the generation of astroglia and NG2 positive polydendrocytes in adult rat neocortex. Exp Neurol 199: 113-21.
12. Bland ST, Schallert T, Strong R, Aronowski J, Grotta JC, et al. (2000) Early exclusive use of the affected forelimb after moderate transient focal ischemia in rats: functional and anatomic outcome. Stroke 31: 1144-1152.
13. Kundrotiene J, Wagner A, Liljequist S, (2002) Extradural compression of sensorimotor cortex: a useful model for studies on ischemic brain damage and neuroprotection. J Neurotrauma 19: 69-84.
14. Watanabe S, Hoffman JR, Craik RL, Hand PJ, Croul SE, et al. (2001) A new model of localized ischemia in rat somatosensory cortex produced by cortical compression. Stroke 32: 2615-2623.
15. Chen JR, Wang YJ, Tseng GF, (2003) The effect of epidural compression on cerebral cortex: a rat model. J Neurotrauma 20: 767-80.
16. Coq JO, Xerri C, (1999) Tactile impoverishment and sensorimotor restriction deteriorate the forepaw cutaneous map in the primary somatosensory cortex of adult rats. Exp Brain Res 129: 518-531.
17. Soblosky JS, Colgin LL, Chorney-Lane D, Davidson JF, Carey ME, (1997) Ladder beam and camera video recording system for evaluating forelimb and hindlimb deficits after sensorimotor cortex injury in rats. J Neurosci Methods 78: 75-83.
18. Metz GA, Whishaw IQ, (2002) Cortical and subcortical lesions impair skilled walking in the ladder rung walking test: a new task to evaluate fore- and hindlimb stepping, placing, and co-ordination. J Neurosci Methods 115: 169-179.
19. Schallert T, Fleming SM, Leasure JL, Tillerson JL, Bland ST, (2000) CNS plasticity and assessment of forelimb sensorimotor outcome in unilateral rat models of stroke, cortical ablation, parkinsonism and spinal cord injury. Neuropharmacology 39: 777-787.
20. Hsu JE, Jones TA, (2006) Contralesional neural plasticity and functional changes in the less-affected forelimb after large and small cortical infarcts in rats. Exp Neurol 201: 479-494.
21. Soblosky JS, Matthews MA, Davidson JF, Tabor SL, Carey ME, (1996) Traumatic brain injury of the forelimb and hindlimb sensorimotor areas in the rat: physiological, histological and behavioral correlates. Behav Brain Res 79: 79-92.
22. Schallert T, Upchurch M, Lobaugh N, Farrar SB, Spirduso WW, et al. (1982) Tactile extinction: distinguishing between sensorimotor and motor asymmetries in rats with unilateral nigrostriatal damage. Pharmacol Biochem Behav 16: 455-462.
23. Schallert T, Upchurch M, Wilcox RE, Vaughn DM, (1983) Posture-independent sensorimotor analysis of inter-hemispheric receptor asymmetries in neostriatum. Pharmacol Biochem Behav 18: 753-759.
24. Vessal M, Darian-Smith C, (2010) Adult neurogenesis occurs in primate sensorimotor cortex following cervical dorsal rhizotomy. J Neurosci 23: 8613-23.
25. Coyle DE, (1998) Partial peripheral nerve injury leads to activation of astroglia and microglia which parallels the development of allodynic behavior. Glia 23: 75-83.
26. Liu L, Persson JK, Svensson M, Aldskogius H, (1998) Glial cell responses, complement, and clusterin in the central nervous system following dorsal root transection. Glia 23: 221-238.
27. Castro AJ, (1977) Limb preference after lesions of the cerebral hemisphere in adult and neonatal rats. Physiol Behav 18: 605-608.
28. Napieralski JA, Banks RJ, Chesselet MF, (1998) Motor and somatosensory deficits following uni- and bilateral lesions of the cortex induced by aspiration or thermocoagulation in the adult rat. Exp Neurol 154: 80-88.
29. Goldberger ME, Murray M, (1974) Restitution of function and collateral sprouting in the cat spinal cord: the deafferented animal. J Comp Neurol 158: 37-54.
30. Helgren ME, Goldberger ME, (1993) The recovery of postural reflexes and locomotion following low thoracic hemisection in adult cats involves compensation by undamaged primary afferent pathways. Exp Neurol 123: 17-34.
31. Bouyer LJG, Rossignol S, (2003) Contribution of cutaneous inputs from the hindpaw to the control of locomotion: 1. Intact cats. J Neurophysiol 90: 3625-3639.
32. Bouyer LJG, Rossignol S, (2003) Contribution of cutaneous inputs from the hindpaw to the control of locomotion: 2. Spinal cats. J Neurophysiol 90: 3640-3653.
33. Webb AA, Muir GD, (2003) Unilateral dorsal column and rubrospinal tract injuries affect overground locomotion in the unrestrained rat. Eur J Neurosci 18: 412-422.
34. Frigon A, Rossignol S, (2006) Experiments and models of sensorimotor interactions during locomotion. Biol Cybern 95: 607-627.
35. Maegele M, Lippert-Gruener M, Ester-Bode T, Garbe J, Bouillon B, et al. (2005) Multimodal early onset stimulation combined with enriched environment is associated with reduced CNS lesion volume and enhanced reversal of neuromotor dysfunction after traumatic brain injury in rats. Eur J Neurosci 21: 2406-2418.
36. Barbay S, Plautz EJ, Friel KM, Frost SB, Dancause N, et al. (2006) Behavioral and neurophysiological effects of delayed training following a small ischemic infarct in primary motor cortex of squirrel monkeys. Exp Brain Res 169: 106-16.
37. Zennou-Azogui Y, Xerri C, Harlay F, (1995) Visual experience during a sensitive period plays a critical role in the vestibular compensation. Neuronal substrates within Deiters nucleus in the alert cat. Restorative Neurol and Neurosci 7: 235-246.
38. Zennou-Azogui Y, Xerri C, Leonard J, Tighilet B, (1996) Vestibular compensation: role of visual experience in the recovery of posturo-kinetic functions during a sensitive period. Behavioral Brain Res 74: 65-77.
39. Metz GA, Antonow-Schlorke I, Witte OW, (2005) Motor improvements after focal cortical ischemia in adult rats are mediated by compensatory mechanisms. Behav Brain Res 162: 71-82.
40. Knieling M, Metz GA, Antonow-Schlorke I, Witte OW, (2009) Enriched environment promotes efficiency of compensatory movements after cerebral ischemia in rats. Neuroscience 163: 759-769.
41. Martinez M, Brezun JM, Bonnier L, Xerri C, (2009a) A new rating scale for open-field evaluation of behavioral recovery after cervical spinal cord injury in rats. J Neurotrauma 26: 1043-1053.
42. Martinez M, Brezun JM, Zennou-Azogui Y, Baril N, Xerri C, (2009b) Sensorimotor training promotes functional recovery and somatosensory cortical map reactivation following cervical spinal cord injury. Eur J Neurosci 30: 2356-2367.
43. Martinez M, Delcour M, Russier M, Zennou-Azogui Y, Xerri C, et al. (2010) Differential tactile and motor recovery and cortical map alteration after C4-C5 spinal hemisection. Exp Neurol 221: 186-197.
44. Ibrahim AG, Raisman G, Li Y, (2009) Permanent loss of fore-paw grasping requires complete deprivation of afferent input from a minimum of four dorsal roots of the rat brachial plexus. Exp Neurol 215: 142-145.
45. Pham TM, Winblad B, Granholm AC, Mohammed AH, (2002) Environmental influences on brain neurotrophins in rats. Pharmacol Biochem Behav 73: 167-75.
46. Chen JR, Wang YJ, Tseng GF, (2004) The effects of decompression and exogenous NGF on compressed cerebral cortex. J Neurotrauma 21: 1640-51.
47. Rose FD, Davey MJ, Love S, Dell PA, (1987) Environmental enrichment and recovery from contralateral sensory neglect in rats with large unilateral neocortical lesions. Behav Brain Res 124: 195-202.
48. Jenkins WM, Merzenich MM, (1987) Reorganization of neocortical representations after brain injury: a neurophysiological model of the bases of recovery from stroke. Prog Brain Res 71: 249-66.
49. Doetsch GS, Johnston KW, Hannan CJ Jr, (1990) Physiological changes in the somatosensory forepaw cerebral cortex of adult raccoons following lesions of a single cortical digit representation. Exp Neurol 108: 162-75.
50. Xerri C, Merzenich MM, Peterson BE, Jenkins W, (1998) Plasticity of primary somatosensory cortex paralleling sensorimotor skill recovery from stroke in adult monkeys. J Neurophysiol 79: 2119-2148.
51. Nudo RJ, Wise BM, SiFuentes F, Milliken GW, (1996) Neural substrates for the effects of rehabilitative training on motor recovery after ischemic infarct. Science 272: 1791-1794.
52. Stroemer RP, Kent TA, Hulsebosch CE, (1998) Enhanced neocortical neural sprouting, synaptogenesis, and behavioral recovery with D-amphetamine therapy after neocortical infarction in rats. Stroke 29: 2381-2393.
53. Carmichael ST, Wei L, Rovainen CM, Woolsey TA, (2001) New patterns of intracortical projections after focal cortical stroke. Neurobiol Dis 8: 910-22.
54. Ip EY, Giza CC, Griesbach GS, Hovda DA, (2002) Effects of enriched environment and fluid percussion injury on dendritic arborization within the cerebral cortex of the developing rat. J Neurotrauma 19: 573-585.
55. Passineau MJ, Green EJ, Dietrich WD, (2001) Therapeutic effects of environmental enrichment on cognitive function and tissue integrity following severe traumatic brain injury in rats. Exp Neurol 168: 373-384.
56. Paxinos G, Watson, C, (1997) The rat brain in stereotaxic coordinates. Academic Press.