Behavioral recovery and anatomical plasticity in adult rats after cortical lesion and treatment with monoclonal antibody IN-1

Behavioural Brain Research

Volumn 152, Issue 2, 2004, Pages 315-325

  Emerick, April J ^a,b   Kartje, Gwendolyn L ^a,b  

^a Surgical Services Edward Hines Veterans Affairs Hospital   (United States)

^b LOYOLA UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Behavioral recovery; Cortical injury; Corticospinal tract; Motor cortex; Nogo A; Plasticity

Indexed keywords

MONOCLONAL ANTIBODY; MONOCLONAL ANTIBODY IN 1; NEUTRALIZING ANTIBODY; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; BEHAVIOR; BRAIN CORTEX; BRAIN CORTEX LESION; CONTROLLED STUDY; CONVALESCENCE; DRUG EFFECT; FORELIMB; HAND GRIP; MALE; MOTOR CORTEX; MOTOR PERFORMANCE; NERVE CELL PLASTICITY; NERVE PROJECTION; NEUROANATOMY; NONHUMAN; PRIORITY JOURNAL; PYRAMIDAL TRACT; RAT; SENSORIMOTOR CORTEX; SKILL; SPINAL CORD; TASK PERFORMANCE;

ANALYSIS OF VARIANCE; ANIMALS; ANTIBODIES, MONOCLONAL; BEHAVIOR, ANIMAL; BIOTIN; BRAIN DISEASES; CEREBRAL CORTEX; CEREBRAL DECORTICATION; DEXTRANS; FUNCTIONAL LATERALITY; HYBRIDOMAS; MALE; MOTOR SKILLS; MYELIN PROTEINS; NEURONAL PLASTICITY; RATS; RATS, LONG-EVANS; RECOVERY OF FUNCTION; TIME FACTORS; WALKING;

EID: 2942560970     PISSN: 01664328     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbr.2003.10.010     Document Type: Article

References (49)

1. Bareyre F.M., Haudenschild B., Schwab M.E. Long-lasting sprouting and gene expression changes induced by the monoclonal antibody IN-1 in the adult spinal cord. J. Neurosci. 22:2002;7097-7110
2. Barth T.M., Stanfield B.B. The recovery of forelimb-placing behavior in rats with neonatal unilateral cortical damage involves the remaining hemisphere. J. Neurosci. 10:1990;3449-3458
3. Bregman B.S., Kunkel-Bagden E., Schnell L., Dai H.N., Gao D., Schwab M.E. Recovery from spinal cord injury mediated by antibodies to neurite growth inhibitors. Nature. 378:1995;497-501
4. Brösamle C., Huber A.B., Fiedler M., Skerra A., Schwab M.E. Regeneration of lesioned corticospinal tract fibers in the adult rat induced by a recombinant, humanized IN-1 antibody fragment. J. Neurosci. 20:2000;8061-8068
5. Buffo A., Zagrebelsky M., Huber A.B., Skerra A., Schwab M.E., Strata P., et al. Application of neutralizing antibodies against NI-35/250 myelin-associated neurite outgrowth inhibitory proteins to the adult rat cerebellum induces sprouting of uninjured Purkinje cell axons. J. Neurosci. 20:2000;2275-2286
6. Carmichael S.T., Chesselet M.-F. Synchronous neuronal activity is a signal for axonal sprouting after cortical lesions in the adult. J. Neurosci. 22:2002;6042-6070
7. Castro A.J. The effects of cortical ablations on digital usage in the rat. Brain Res. 37:1972;173-185
8. Castro A.J. Ipsilateral corticospinal projection after large cerebral lesion in neonatal rats. Exp. Neurol. 46:1975;1-8
9. Castro A.J., Mihailoff G.A. Corticopontine remodelling after cortical and/or cerebellar lesions in newborn rats. J. Comp. Neurol. 219:1983;112-123
10. Chen M.S., Huber A.B., van der Haar M.E., Frank M., Schnell L., Spillmann A.A., et al. Nogo-A is a myelin-associated neurite outgrowth inhibitor and an antigen for monoclonal antibody IN-1. Nature. 403:2000;434-439
11. Emerick A.J., Neafsey E.J., Schwab M.E., Kartje G.L. Functional reorganization of the motor cortex in adult rats after cortical lesion and treatment with mAb IN-1. J. Neurosci. 23:2003;4826-4830
12. Fiedler M., Horn C., Bandtlow C., Schwab M.E., Skerra A. An engineered IN-1 F(ab) fragment with improved affinity for the Nogo-A axonal growth inhibitor permits immunochemical detection and shows enhanced neutralizing activity. Protein Eng. 15:2002;931-941
13. Grand Pré T., Nakamura F., Vartanian T., Strittmatter S.M. Identification of Nogo inhibitor of axon regeneration as a reticulon protein. Nature. 403:2000;439-444
14. Grand Pré T., Li S., Strittmatter S.M. Nogo-66 receptor antagonist peptide promotes axonal regeneration. Nature. 417:2002;547-551
15. Herzog A., Brösamle C. "Semi-free-floating" treatment: a simple and fast method to process consecutive sections for histochemistry and neuronal tracing. J. Neurosci. Methods. 72:1997;57-63
16. Hicks S.P., D'Amato J.C. Motor-sensory and visual behavior after hemispherectomy in newborn and mature rats. Exp. Neurol. 29:1970;416-438
17. Huber A.B., Schwab M.E. Nogo-A, a potent inhibitor of neurite outgrowth and regeneration. Biol. Chem. 381:2000;407-419
18. Huber A.B., Weinmann O., Brösamle C., Oertle T., Schwab M.E. Patterns of Nogo mRNA protein expression in the developing and adult rat and after CNS lesions. J. Neurosci. 22:2002;3553-3567
19. Kartje G.L., Schulz M.K., Lopez-Yunez A., Schnell L., Schwab M.E. Corticostriatal plasticity is restricted by myelin-associated neurite growth inhibitors in the adult rat. Ann. Neurol. 45:1999;778-786
20. Kartje-Tillotson G., Neafsey E.J., Castro A.J. Topography of corticopontine remodeling after cortical lesions in newborn rats. J. Comp. Neurol. 250:1986;206-214
21. Kolb B., Whishaw I.Q. Plasticity in the neocortex: mechanisms underlying recovery from early brain damage. Prog. Neurobiol. 32:1989;235-276
22. Kolb B., Gibb R., van der Kooy D. Cortical and striatal structure and connectivity are altered by neonatal hemidecotication in rats. J. Comp. Neurol. 322:1992;311-324
23. Kolb B., Gibb R., van der Kooy D. Neonatal frontal cortical lesions in rats alter cortical structure and connectivity. Brain Res. 645:1994;85-97
24. Kuang R.Z., Kalil K. Specificity of corticospinal axon arbors sprouting into denervated contralateral spinal cord. J. Comp. Neurol. 244:1990;163-173
25. Leong S.K., Lund R.D. Anomalous bilateral corticofugal pathways in albino rats after neonatal lesions. Brain Res. 62:1973;218-221
26. Li S., Strittmatter S.M. Delayed systemic Nogo-66 receptor antagonist promotes recovery from spinal cord injury. J. Neurosci. 23:2003;4219-4227
27. Liang F., Moret V., Wiesendanger M., Rouiller E.M. Corticomotoneuronal connections in the rat: evidence from double-labeling of motoneurons and corticospinal axons arborizations. J. Comp. Neurol. 311:1991;356-366
28. McKenna J.E., Prusky G.T., Whishaw I.Q. Cervical motoneuron topography reflects the proximodistal organization of muscles and movements of the rat forelimb: a retrograde carbocyanine dye analysis. J. Comp. Neurol. 419:2000;286-296
29. Merkler D., Metz G.A.S., Raineteau O., Dietz V., Schwab M.E., Fouad K. Locomotor recovery in spinal cord injured rats treated with an antibody neutralizing the myelin-associated neurite growth inhibitor Nogo-A. J. Neurosci. 21:2001;3665-3673
30. Metz G.A.S., Whishaw I.Q. Skilled reaching an action pattern: stability in rat (Rattus norvegicus) grasping movements as a function of changing food pellet size. Behav. Brain Res. 116:2000;111-122
31. Metz G.A., Whishaw I.Q. 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. 115:2002;169-179
32. Nah S.H., Leong S.K. Bilateral corticofugal projections to the red nucleus after neonatal lesions in the albino rat. Brain Res. 107:1976;433-436
33. Naus C.G., Flumerfelt B.A., Hrycyshyn A.W. Contralateral corticorubral fibers induced by neonatal lesions are not collaterals of the normal ipsilateral projections. Neurosci Lett. 70:1986;52-58
34. Neafsey E.J., Bold E.L., Haas G., Hurley-Gius K.M., Quirk G., Sievert C.F., et al. The organization of the rat motor cortex: a microstimulation mapping study. Brain Res. Rev. 11:1986;77-96
35. Papadopoulos C.M., Tsai S.-Y., Alsbiei T., O'Brien T.E., Schwab M.E., Kartje G.L. Functional recovery and neuroanatomical plasticity following middle cerebral artery occlusion and IN-1 antibody treatment in the adult rat. Ann. Neurol. 51:2002;433-441
36. Paxinos G, Watson C. The rat brain in stereotaxic coordinates. New York: Academic Press; 1998.
37. Prinjha R., Moore S.E., Vinson M., Blake S., Morrow R., Christie G., et al. Inhibitor of neurite outgrowth in humans. Nature. 403:2000;383-384
38. Raineteau O., Fouad K., North P., Thallmair M., Schwab M.E. Functional switch between motor tracts in the presence of the mAb IN-1 in the adult rat. Proc. Natl. Acad. Sci. U.S.A. 98:2001;6929-6934
39. Rouiller E.M., Fengyi L., Moret V., Wiesendanger M. Trajectory of redirected corticospinal axons after unilateral lesion of the sensorimotor cortex in neonatal rat a Phaseolu vulgaris leucoagglutin (PHA-L) tracing study. Exp. Neurol. 114:1991;53-65
40. Schwab M.E. Repairing the injured spinal cord. Science. 295:2002;1029-1031
41. Thallmair M., Metz G.A.S., Z'Graggen W.J., Raineteau O., Kartje G.L., Schwab M.E. Neurite growth inhibitors restrict structural plasticity and functional recovery following corticospinal tract lesions. Nat. Neurosci. 1:1998;124-131
42. Uryu K., MacKenzie L., Chesselet M.-F. Ultrastructural evidence for differential axonal sprouting in the striatum after thermocoagulatory and aspiration lesions of the cerebral cortex in adult rats. Neuroscience. 105:2001;307-316
43. Voorhies A.C., Jones T.A. The behavioral and dendritic growth effects of focal sensorimotor cortical damage depend on the method of lesion induction. Behav. Brain Res. 133:2002;237-246
44. Wenk C.A., Thallmair M., Kartje G.L., Schwab M.E. Increased corticofugal plasticity after unilateral cortical lesions combined with neutralization of the IN-1 antigen in adult rats. J. Comp. Neurol. 410:1999;143-157
45. Whishaw I.Q. Loss of the innate cortical engram for action patterns used in skilled reaching and the development of behavioral compensation following motor cortex lesions in the rat. Neuropharmacy. 39:2000;788-805
46. Whishaw I.Q., Kolb B. Sparing of skilled forelimb reaching and corticospinal projections after neonatal motor cortex removal or hemidecortication in the rat: support for the Kennard doctrine. Brain Res. 451:1988;97-114
47. Wiessner C., Baeyre F.M., Allegrini P.R., Mir A.K., Fretzel S., Zurini M., et al. Anti Nogo-A antibody infusion 24 hours after experimental stroke improved behavioral outcome and corticospinal plasticity in normotensive and spontaneously hypertensive rats. J. Cereb. Blood Flow Metab. 23:2003;154-165
48. Wiessner C, Kartje GL, Hillenbrand R, Mir AK, Schwab ME. Anti-Nogo-A antibody therapy after experimental stroke. In: Krieglstein J, Klumpp S, editors. Pharmacology of cerebral ischemia. Stuttgart: Medpharm Scientific Publishers; 2002. p. 343-54.
49. Z'Graggen W.J., Metz G.A.S., Kartje G.L., Thallmair M., Schwab M.E. Functional recovery and enhanced corticofugal plasticity after unilateral pyramidal tract lesion and blockade of myelin-associated neurite growth inhibitors in adult rats. J. Neurosci. 18:1998;4744-4757