Norepinephrine depletion facilitates recovery of function after focal ischemia in the rat

European Journal of Neuroscience

Volumn 26, Issue 7, 2007, Pages 1822-1831

  Windle, Victoria ^a   Power, Alexandra ^a   Corbett, Dale ^a  

^a MEMORIAL UNIVERSITY OF NEWFOUNDLAND   (Canada)

Author keywords

Motor function; N (2 chloroethyl) N ethyl 2 bromobenzylamine; Rehabilitation; Stroke

Indexed keywords

2 BROMO N (2 CHLOROETHYL) N ETHYLBENZYLAMINE; BRAIN DERIVED NEUROTROPHIC FACTOR; DOPAMINE BETA MONOOXYGENASE; NEUROTOXIN; NORADRENALIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN INFARCTION SIZE; BRAIN INJURY; BRAIN ISCHEMIA; CONTROLLED STUDY; CONVALESCENCE; FACILITATION; LOCUS CERULEUS; MALE; NONHUMAN; NORADRENALIN BLOOD LEVEL; NORADRENALIN RELEASE; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; RAT; REHABILITATION CARE; SENSORIMOTOR CORTEX; SENSORIMOTOR FUNCTION; SENSORIMOTOR INTEGRATION; STROKE;

ANALYSIS OF VARIANCE; ANIMALS; BEHAVIOR, ANIMAL; BENZYLAMINES; BRAIN INFARCTION; DISEASE MODELS, ANIMAL; DOPAMINE BETA-HYDROXYLASE; ENVIRONMENT; ISCHEMIA; MALE; MOTOR ACTIVITY; NEUROTRANSMITTER UPTAKE INHIBITORS; NOREPINEPHRINE; PHYSICAL CONDITIONING, ANIMAL; RATS; RATS, SPRAGUE-DAWLEY; RECOVERY OF FUNCTION; TIME FACTORS;

EID: 34848816196     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2007.05799.x     Document Type: Article

References (67)

1. Biernaskie, J. Corbett, D. (2001) Enriched rehabilitative training promotes improved forelimb motor function and enhanced dendritic growth after focal ischemic injury. J. Neurosci., 21, 5272 5280.
2. Biernaskie, J., Chernenko, G. Corbett, D. (2004) Efficacy of rehabilitative experience declines with time after focal ischemic brain injury. J. Neurosci., 24, 1245 1254.
3. Blomqvist, P., Lindvall, O. Wieloch, T. (1985) Lesions of the locus coeruleus system aggravate ischemic damage in the rat brain. Neurosci. Lett., 58, 353 358.
4. Boyeson, M.G. Feeney, D.M. (1990) Intraventricular norepinephrine facilitates motor recovery following sensorimotor cortex injury. Pharmacol. Biochem. Behav., 35, 497 501.
5. Boyeson, M.G., Callister, T.R. Cavazos, J.E. (1992) Biochemical and behavioral effects of a sensorimotor cortex injury in rats pretreated with the noradrenergic neurotoxin DSP-4. Behav. Neurosci., 106, 964 973.
6. Boyeson, M.G., Scherer, P.J., Grade, C.M. Krobert, K.A. (1993) Unilateral locus coeruleus lesions facilitate motor recovery from cortical injury through supersensitivity mechanisms. Pharmacol. Biochem. Behav., 44, 297 305.
7. Brenner, E., Mirmiran, M., Uylings, H.B. Van der Gugten, J. (1985) Growth and plasticity of rat cerebral cortex after central noradrenaline depletion. Exp. Neurol., 89, 264 268.
8. Butefisch, C.M., Davis, B.C., Sawaki, L., Waldvogel, D., Classen, J., Kopylev, L. Cohen, L.G. (2002) Modulation of use-dependent plasticity by d-amphetamine. Ann. Neurol., 51, 59 68.
9. Butovas, S., Lukkarinen, J., Virtanen, T., Jolkkonen, J. Sivenius, J. (2001) Differential effect of the alpha2-adrenoceptor antagonist, atipamezole, in limb-placing task and skilled forepaw use following experimental stroke. Restor. Neurol. Neurosci., 18, 143 151.
10. Dooley, D.J., Bittiger, H., Hauser, K.L., Bischoff, S.F. Waldmeier, P.C. (1983) Alteration of central alpha 2- and beta-adrenergic receptors in the rat after DSP-4, a selective noradrenergic neurotoxin. Neuroscience, 9, 889 898.
11. Dunwiddie, T.V., Mueller, A.L., Bickford, P.C. Zahniser, N.R. (1983) Electrophysiological and biochemical sequelae of the destruction of hippocampal noradrenergic afferents by DSP4. Brain Res., 269, 311 317.
12. Falkenberg, T., Mohammed, A.K., Henriksson, B., Persson, H., Winblad, B. Lindefors, N. (1992) Increased expression of brain-derived neurotrophic factor mRNA in rat hippocampus is associated with improved spatial memory and enriched environment. Neurosci. Lett., 138, 153 156.
13. Feeney, D.M., Gonzalez, A. Law, W.A. (1982) Amphetamine, haloperidol, and experience interact to affect rate of recovery after motor cortex injury. Science, 217, 855 857.
14. Fritschy, J.M. Grzanna, R. (1991) Selective effects of DSP-4 on locus coeruleus axons: are there pharmacologically different types of noradrenergic axons in the central nervous system? Prog. Brain Res., 88, 257 268.
15. Fritschy, J.M. Grzanna, R. (1992) Restoration of ascending noradrenergic projections by residual locus coeruleus neurons: compensatory response to neurotoxin-induced cell death in the adult rat brain. J. Comp. Neurol., 321, 421 441.
16. Garcia, C., Chen, M.J., Garza, A.A., Cotman, C.W. Russo-Neustadt, A. (2003) The influence of specific noradrenergic and serotonergic lesions on the expression of hippocampal brain-derived neurotrophic factor transcripts following voluntary physical activity. Neuroscience, 119, 721 732.
17. Gladstone, D.J. Black, S.E. (2000) Enhancing recovery after stroke with noradrenergic pharmacotherapy: a new frontier? Can. J. Neurol. Sci., 27, 97 105.
18. Gobbo, O.L. O'Mara, S.M. (2004) Impact of enriched-environment housing on brain-derived neurotrophic factor and on cognitive performance after a transient global ischemia. Behav. Brain Res., 152, 231 241.
19. Goldstein, L.B. Bullman, S. (1997) Effects of dorsal noradrenergic bundle lesions on recovery after sensorimotor cortex injury. Pharmacol. Biochem. Behav., 58, 1151 1157.
20. Goldstein, L.B. Davis, J.N. (1990) Beam-walking in rats: studies towards developing an animal model of functional recovery after brain injury. J. Neurosci. Meth., 31, 101 107.
21. Goldstein, L.B., Coviello, A., Miller, G.D. Davis, J.N. (1991) Norepinephrine depletion impairs motor recovery following sensorimotor cortex injury in the rat. Restor. Neurol. Neurosci., 3, 41 47.
22. Gomez-Pinilla, F., Ying, Z., Roy, R.R., Molteni, R. Edgerton, V.R. (2002) Voluntary exercise induces a BDNF-mediated mechanism that promotes neuroplasticity. J. Neurophysiol., 88, 2187 2195.
23. Harro, J., Merikula, A., Lepiku, M., Modiri, A.R., Rinken, A. Oreland, L. (2000) Lesioning of locus coeruleus projections by DSP-4 neurotoxin treatment: effect on amphetamine-induced hyperlocomotion and dopamine D2 receptor binding in rats. Pharmacol. Toxicol., 86, 197 202.
24. Harro, J., Terasmaa, A., Eller, M. Rinken, A. (2003) Effect of denervation of the locus coeruleus projections by DSP-4 treatment on [3H]-raclopride binding to dopamine D(2) receptors and D(2) receptor-G protein interaction in the rat striatum. Brain Res., 976, 209 216.
25. Heal, D.J., Butler, S.A., Prow, M.R. Buckett, W.R. (1993) Quantification of presynaptic alpha 2-adrenoceptors in rat brain after short-term DSP-4 lesioning. Eur. J. Pharmacol., 249, 37 41.
26. Hovda, D.A. Fenney, D.M. (1984) Amphetamine with experience promotes recovery of locomotor function after unilateral frontal cortex injury in the cat. Brain Res., 298, 358 361.
27. Hughes, Z.A. Stanford, S.C. (1998) A partial noradrenergic lesion induced by DSP-4 increases extracellular noradrenaline concentration in rat frontal cortex: a microdialysis study in vivo. Psychopharmacology (Berl.), 136, 299 303.
28. Ickes, B.R., Pham, T.M., Sanders, L.A., Albeck, D.S., Mohammed, A.H. Granholm, A.C. (2000) Long-term environmental enrichment leads to regional increases in neurotrophin levels in rat brain. Exp. Neurol., 164, 45 52.
29. Johansson, B.B. Belichenko, P.V. (2002) Neuronal plasticity and dendritic spines: effect of environmental enrichment on intact and postischemic rat brain. J. Cereb. Blood Flow Metab., 22, 89 96.
30. Jolkkonen, J., Puurunen, K., Rantakomi, S., Harkonen, A., Haapalinna, A. Sivenius, J. (2000) Behavioral effects of the alpha(2)-adrenoceptor antagonist, atipamezole, after focal cerebral ischemia in rats. Eur. J. Pharmacol., 400, 211 219.
31. Jones, T.A., Chu, C.J., Grande, L.A. Gregory, A.D. (1999) Motor skills training enhances lesion-induced structural plasticity in the motor cortex of adult rats. J. Neurosci., 19, 10 153 10 163.
32. Jonsson, G., Hallman, H., Ponzio, F. Ross, S. (1981) DSP4 (N-(2-chloroethyl)-N-ethyl-2-bromobenzylamine) - a useful denervation tool for central and peripheral noradrenaline neurons. Eur. J. Pharmacol., 72, 173 188.
33. Kask, A., Harro, J., Tuomaine, P., Rago, L. Mannisto, P.T. (1997) Overflow of noradrenaline and dopamine in frontal cortex after [N-(2-chloroethyl)-N-ethyl-2-bromobenzylamine] (DSP-4) treatment: in vivo microdialysis study in anaesthetized rats. Naunyn Schmiedebergs Arch. Pharmacol., 355, 267 272.
34. Kleim, J.A., Barbay, S., Cooper, N.R., Hogg, T.M., Reidel, C.N., Remple, M.S. Nudo, R.J. (2002) Motor learning-dependent synaptogenesis is localized to functionally reorganized motor cortex. Neurobiol. Learn. Mem., 77, 63 77.
35. Logue, M.P., Growdon, J.H., Coviella, I.L. Wurtman, R.J. (1985) Differential effects of DSP-4 administration on regional brain norepinephrine turnover in rats. Life Sci., 37, 403 409.
36. Malberg, J.E., Eisch, A.J., Nestler, E.J. Duman, R.S. (2000) Chronic antidepressant treatment increases neurogenesis in adult rat hippocampus. J. Neurosci., 20, 9104 9110.
37. Metz, G.A. Whishaw, I.Q. (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. Meth., 115, 169 179.
38. Mogilnicka, E. (1986) Increase in beta- and alpha 1-adrenoceptor binding sites in the rat brain and in the alpha 1-adrenoceptor functional sensitivity after the DSP-4-induced noradrenergic denervation. Pharmacol. Biochem. Behav., 25, 743 746.
39. Mohammed, A.H., Zhu, S.W., Darmopil, S., Hjerling-Leffler, J., Ernfors, P., Winblad, B., Diamond, M.C., Eriksson, P.S. Bogdanovic, N. (2002) Environmental enrichment and the brain. Prog. Brain Res., 138, 109 133.
40. Montoya, C.P., Campbell-Hope, L.J., Pemberton, K.D. Dunnett, S.B. (1991) The 'staircase test': a measure of independent forelimb reaching and grasping abilities in rats. J. Neurosci. Meth., 36, 219 228.
41. Murtha, S., Pappas, B.A. Raman, S. (1990) Neonatal and adult forebrain norepinephrine depletion and the behavioral and cortical thickening effects of enriched/impoverished environment. Behav. Brain Res., 39, 249 261.
42. Naka, F., Shiga, T., Yaguchi, M. Okado, N. (2002) An enriched environment increases noradrenaline concentration in the mouse brain. Brain Res., 924, 124 126.
43. Nakamura, S. Sakaguchi, T. (1990) Development and plasticity of the locus coeruleus: a review of recent physiological and pharmacological experimentation. Prog. Neurobiol., 34, 505 526.
44. Nakamura, S., Sakaguchi, T. Aoki, F. (1989) Electrophysiological evidence for terminal sprouting of locus coeruleus neurons following repeated mild stress. Neurosci. Lett., 100, 147 152.
45. Nakayama, H., Jorgensen, H.S., Raaschou, H.O. Olsen, T.S. (1994) Recovery of upper extremity function in stroke patients: the Copenhagen Stroke Study. Arch. Phys. Med. Rehabil., 75, 394 398.
46. Nellgard, B., Mackensen, G.B., Sarraf-Yazdi, S., Miura, Y., Pearlstein, R. Warner, D.S. (1999a) Pre-ischemic depletion of brain norepinephrine decreases infarct size in normothermic rats exposed to transient focal cerebral ischemia. Neurosci. Lett., 275, 167 170.
47. Nellgard, B.M., Miura, Y., Burkhard Mackensen, G., Pearlstein, R.D. Warner, D.S. (1999b) Effect of intracerebral norepinephrine depletion on outcome from severe forebrain ischemia in the rat. Brain Res., 847, 262 269.
48. Nibuya, M., Morinobu, S. Duman, R.S. (1995) Regulation of BDNF and trkB mRNA in rat brain by chronic electroconvulsive seizure and antidepressant drug treatments. J. Neurosci., 15, 7539 7547.
49. Nishino, K., Lin, C.S., Morse, J.K. Davis, J.N. (1991) DSP4 treatment worsens hippocampal pyramidal cell damage after transient ischemia. Neuroscience, 43, 361 367.
50. Parker, V.M., Wade, D.T. Langton Hewer, R. (1986) Loss of arm function after stroke: measurement, frequency, and recovery. Int. Rehabil. Med., 8, 69 73.
51. Paxinos, G. Watson, C. (1986) The Rat Brain in Stereotaxic Coordinates. Academic Press, Orlando, FL, USA.
52. Pham, T.M., Ickes, B., Albeck, D., Soderstrom, S., Granholm, A.C. Mohammed, A.H. (1999) Changes in brain nerve growth factor levels and nerve growth factor receptors in rats exposed to environmental enrichment for one year. Neuroscience, 94, 279 286.
53. Ploughman, M., Granter-Button, S., Chernenko, G., Tucker, B.A., Mearow, K.M. Corbett, D. (2005) Endurance exercise regimens induce differential effects on brain-derived neurotrophic factor, synapsin-I and insulin-like growth factor I after focal ischemia. Neuroscience, 136, 991 1001.
54. Prieto, M. Giralt, M.T. (2001) Effects of N-(2-chloroethyl)-N-ethyl-2- bromobenzylamine (DSP4) on alpha2-adrenoceptors which regulate the synthesis and release of noradrenaline in the rat brain. Pharmacol. Toxicol., 88, 152 158.
55. Puurunen, K., Jolkkonen, J., Sirvio, J., Haapalinna, A. Sivenius, J. (2001) An alpha(2)-adrenergic antagonist, atipamezole, facilitates behavioral recovery after focal cerebral ischemia in rats. Neuropharmacology, 40, 597 606.
56. Ross, S.B. (1976) Long-term effects of N-2-chlorethyl-N-ethyl-2- bromobenzylamine hydrochloride on noradrenergic neurones in the rat brain and heart. Br. J. Pharmacol., 58, 521 527.
57. Russo-Neustadt, A.A., Beard, R.C., Huang, Y.M. Cotman, C.W. (2000) Physical activity and antidepressant treatment potentiate the expression of specific brain-derived neurotrophic factor transcripts in the rat hippocampus. Neuroscience, 101, 305 312.
58. Russo-Neustadt, A., Ha, T., Ramirez, R. Kesslak, J.P. (2001) Physical activity-antidepressant treatment combination: impact on brain-derived neurotrophic factor and behavior in an animal model. Behav. Brain Res., 120, 87 95.
59. Sawaki, L., Werhahn, K.J., Barco, R., Kopylev, L. Cohen, L.G. (2003) Effect of an alpha(1)-adrenergic blocker on plasticity elicited by motor training. Exp. Brain Res., 148, 504 508.
60. Schallert, T., Kozlowski, D.A., Humm, J.L. Cocke, R.R. (1997) Use-dependent structural events in recovery of function. Adv. Neurol., 73, 229 238.
61. Stroemer, R.P., Kent, T.A. Hulsebosch, C.E. (1998) Enhanced neocortical neural sprouting, synaptogenesis, and behavioral recovery with d-amphetamine therapy after neocortical infarction in rats. Stroke, 29, 2381 2393 discussion 2393 2395.
62. Theron, C.N., de Villiers, A.S. Taljaard, J.J. (1993) Effects of DSP-4 on monoamine and monoamine metabolite levels and on beta adrenoceptor binding kinetics in rat brain at different times after administration. Neurochem. Res., 18, 1321 1327.
63. Vaynman, S., Ying, Z. Gomez-Pinilla, F. (2003) Interplay between brain-derived neurotrophic factor and signal transduction modulators in the regulation of the effects of exercise on synaptic-plasticity. Neuroscience, 122, 647 657.
64. Windle, V. Corbett, D. (2005) Fluoxetine and recovery of motor function after focal ischemia in rats. Brain Res., 1044, 25 32.
65. Windle, V., Szymanska, A., Granter-Button, S., White, C., Buist, R., Peeling, J. Corbett, D. (2006) An analysis of four different methods of producing focal cerebral ischemia with endothelin-1 in the rat. Exp. Neurol., 201, 324 334.
66. Wolfman, C., Abo, V., Calvo, D., Medina, J., Dajas, F. Silveira, R. (1994) Recovery of central noradrenergic neurons one year after the administration of the neurotoxin DSP4. Neurochem. Int., 25, 395 400.
67. Zahniser, N.R., Weiner, G.R., Worth, T., Philpott, K., Yasuda, R.P., Jonsson, G. Dunwiddie, T.V. (1986) DSP4-induced noradrenergic lesions increase beta-adrenergic receptors and hippocampal electrophysiological responsiveness. Pharmacol. Biochem. Behav., 24, 1397 1402.