The effect of denervation of the locus coeruleus projections with N-(2-chloroethyl)-N-ethyl-2-bromobenzylamine (DSP-4) on cocaine-induced locomotion and place preference in rats

Behavioural Brain Research

Volumn 216, Issue 1, 2011, Pages 172-179

  Kõiv, Kadri ^a   Zobel, Rein ^a   Raudkivi, Karita ^a   Kivastik, Toomas ^a   Harro, Jaanus ^a  

^a UNIVERSITY OF TARTU   (Estonia)

Author keywords

Cocaine; DSP 4; Locomotion; Locus coeruleus; Noradrenaline; Reward

Indexed keywords

2 BROMO N (2 CHLOROETHYL) N ETHYLBENZYLAMINE; COCAINE; MONOAMINE; NEUROTOXIN; NORADRENALIN;

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; DENERVATION; DOSE RESPONSE; LOCOMOTION; LOCUS CERULEUS; MALE; NERVE PROJECTION; NEUROTRANSMISSION; NONHUMAN; PLACE PREFERENCE; PRIORITY JOURNAL; PSYCHOMOTOR ACTIVITY; RAT; REARING; REWARD; TISSUE DISTRIBUTION;

ANALYSIS OF VARIANCE; ANIMALS; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; COCAINE; CONDITIONING, OPERANT; DENERVATION; DOPAMINE; DOPAMINE UPTAKE INHIBITORS; FRONTAL LOBE; HIPPOCAMPUS; LOCUS COERULEUS; MALE; MOTOR ACTIVITY; NEURAL PATHWAYS; NOREPINEPHRINE; RATS; RATS, WISTAR; REWARD;

EID: 78149415476     PISSN: 01664328     EISSN: 18727549     Source Type: Journal    
DOI: 10.1016/j.bbr.2010.07.030     Document Type: Article

References (82)

1. Abercrombie E.D., Zigmond M.J. Partial injury to central noradrenergic neurons: reduction of tissue norepinephrine content is greater than reduction of extracellular norepinephrine measured by microdialysis. J Neurosci 1989, 9:4062-4067.
2. Acheson A.L., Zigmond M.J. Short and long term changes in tyrosine hydroxylase activity in rat brain after subtotal destruction of central noradrenergic neurons. J Neurosci 1981, 1:493-504.
3. Acheson A.L., Zigmond M.J., Stricker E.M. Compensatory increase in tyrosine hydroxylase activity in rat brain after intraventricular injections of 6-hydroxydopamine. Science 1980, 207:537-540.
4. Alttoa A., Eller M., Herm L., Rinken A., Harro J. Amphetamine-induced locomotion, behavioral sensitization to amphetamine, and striatal D2 receptor function in rats with high or low spontaneous exploratory activity: differences in the role of locus coeruleus. Brain Res 2007, 1131:138-148.
5. Alttoa A., Kõiv K., Eller M., Uustare A., Rinken A., Harro J. Effects of low dose N-(2-chloroethyl)-N-ethyl-2-bromobenzylamine administration on exploratory and amphetamine-induced behavior and dopamine D2 receptor function in rats with high or low exploratory activity. Neuroscience 2005, 132:979-990.
6. Archer T., Fredriksson A., Jonsson G., Lewander T., Mohammed A.K., Ross S.B., et al. Central noradrenaline depletion antagonizes aspects of d-amphetamine-induced hyperactivity in the rat. Psychopharmacology (Berl) 1986, 88:141-146.
7. Archer T., Jonsson G., Ross S.B. A parametric study of the effects of the noradrenaline neurotoxin DSP4 on avoidance acquisition and noradrenaline neurones in the CNS of the rat. Br J Pharmacol 1984, 82:249-257.
8. Archer T., Mohammed A.K., Ross S.B., Söderberg U. T-maze learning, spontaneous activity and food intake recovery following systemic administration of the noradrenaline neurotoxin, DSP4. Pharmacol Biochem Behav 1983, 19:121-130.
9. Archer T., Söderberg U., Ross S.B., Jonsson G. Role of olfactory bulbectomy and DSP4 treatment in avoidance learning in the rat. Behav Neurosci 1984, 98:496-505.
10. Archer T., Ögren SO, Johansson G. Ross SB. DSP4-induced two-way active avoidance impairment in rats: involvement of central and not peripheral noradrenaline depletion. Psychopharmacology (Berl) 1982, 76:303-309.
11. Auclair A., Drouin C., Cotecchia S., Glowinski J., Tassin J.P. 5-HT2A and alpha1b-adrenergic receptors entirely mediate dopamine release, locomotor response and behavioural sensitization to opiates and psychostimulants. Eur J Neurosci 2004, 20:3073-3084.
12. Berthold C.W., Gonzales R.A., Moerschbaecher J.M. Prazosin attenuates the effects of cocaine on motor activity but not on schedule-controlled behavior in the rat. Pharmacol Biochem Behav 1992, 43:111-115.
13. Blanc G., Trovero F., Vezina P., Herve D., Godeheu A.M., Glowinski J., et al. Blockade of prefronto-cortical alpha 1-adrenergic receptors prevents locomotor hyperactivity induced by subcortical d-amphetamine injection. Eur J Neurosci 1994, 6:293-298.
14. Cheetham S.C., Viggers J.A., Butler S.A., Prow M.R., Heal D.J. [3H]nisoxetine-a radioligand for noradrenaline reuptake sites: correlation with inhibition of [3H]noradrenaline uptake and effect of DSP-4 lesioning and antidepressant treatments. Neuropharmacol 1996, 35:63-70.
15. Chen N.H., Reith M.E. Effects of locally applied cocaine, lidocaine, and various uptake blockers on monoamine transmission in the ventral tegmental area of freely moving rats: a microdialysis study on monoamine interrelationships. J Neurochem 1994, 63:1701-1713.
16. Darracq L., Blanc G., Glowinski J., Tassin J.P. Importance of the noradrenaline-dopamine coupling in the locomotor activating effects of d-amphetamine. J Neurosci 1998, 18:2729-2739.
17. Devoto P., Flore G., Saba P., Fa M., Gessa G.L. Co-release of noradrenaline and dopamine in the cerebral cortex elicited by single train and repeated train stimulation of the locus coeruleus. BMC Neurosci 2005, 6:31.
18. Devoto P., Flore G., Saba P., Fa M., Gessa G.L. Stimulation of the locus coeruleus elicits noradrenaline and dopamine release in the medial prefrontal and parietal cortex. J Neurochem 2005, 92:368-374.
19. Dickinson S.L., Gadie B., Tulloch I.F. Alpha 1- and alpha 2-adrenoreceptor antagonists differentially influence locomotor and stereotyped behaviour induced by d-amphetamine and apomorphine in the rat. Psychopharmacology (Berl) 1988, 96:521-527.
20. Dooley D.J., Bittiger H., Hauser K.L., Bischoff S.F., Waldmeier P.C. Alteration of central alpha 2- and beta-adrenergic receptors in the rat after DSP-4, a selective noradrenergic neurotoxin. Neuroscience 1983, 9:889-898.
21. Dooley D.J., Mogilnicka E., Delini-Stula A., Waechter F., Truog A., Wood J. Functional supersensitivity to adrenergic agonists in the rat after DSP-4, a selective noradrenergic neurotoxin. Psychopharmacology (Berl) 1983, 81:1-5.
22. Drouin C., Blanc G., Villegier A.S., Glowinski J., Tassin J.P. Critical role of alpha1-adrenergic receptors in acute and sensitized locomotor effects of d-amphetamine, cocaine, and GBR 12783: influence of preexposure conditions and pharmacological characteristics. Synapse 2002, 43:51-61.
23. Drouin C., Darracq L., Trovero F., Blanc G., Glowinski J., Cotecchia S., et al. Alpha1b-adrenergic receptors control locomotor and rewarding effects of psychostimulants and opiates. J Neurosci 2002, 22:2873-2884.
24. Filip M., Nowak E., Papla I. On the role of serotonin2A/2C receptors in the sensitization to cocaine. J Physiol Pharmacol 2001, 52:471-481.
25. Florin S.M., Kuczenski R., Segal D.S. Regional extracellular norepinephrine responses to amphetamine and cocaine and effects of clonidine pretreatment. Brain Res 1994, 654:53-62.
26. Fredriksson A., Archer T. Effects of clonidine and alpha-adrenoceptor antagonists on motor activity in DSP4-treated mice. II: interactions with apomorphine. Neurotox Res 2000, 1:249-259.
27. Fritschy J.M., Grzanna R. Immunohistochemical analysis of the neurotoxic effects of DSP-4 identifies two populations of noradrenergic axon terminals. Neuroscience 1989, 30:181-197.
28. Fritschy J.M., Grzanna R. 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 1992, 321:421-441.
29. Graham-Jones S., Fillenz M., Gray J.A. The effects of footshock and handling on tyrosine hydroxylase activity in synaptosomes and solubilised preparations from rat brain. Neuroscience 1983, 9:679-686.
30. Grenhoff J., Nisell M., Ferre S., Aston-Jones G., Svensson T.H. Noradrenergic modulation of midbrain dopamine cell firing elicited by stimulation of the locus coeruleus in the rat. J Neural Transm Gen Sect 1993, 93:11-25.
31. Grenhoff J., Svensson T.H. Prazosin modulates the firing pattern of dopamine neurons in rat ventral tegmental area. Eur J Pharmacol 1993, 233:79-84.
32. Gresch P.J., Sved A.F., Zigmond M.J., Finlay J.M. Local influence of endogenous norepinephrine on extracellular dopamine in rat medial prefrontal cortex. J Neurochem 1995, 65:111-116.
33. Grzanna R., Berger U., Fritschy J.M., Geffard M. Acute action of DSP-4 on central norepinephrine axons: biochemical and immunohistochemical evidence for differential effects. J Histochem Cytochem 1989, 37:1435-1442.
34. Hallman H., Sundström E., Jonsson G. Effects of the noradrenaline neurotoxin DSP 4 on monoamine neurons and their transmitter turnover in rat CNS. J Neural Trans 1984, 60:89-102.
35. Han D.D., Gu H.H. Comparison of the monoamine transporters from human and mouse in their sensitivities to psychostimulant drugs. BMC Pharmacol 2006, 6:6.
36. Harro J., Meriküla A., Lepiku M., Modiri A.R., Rinken A., Oreland L. Lesioning of locus coeruleus projections by DSP-4 neurotoxin treatment: effect on amphetamine-induced hyperlocomotion and dopamine D2 receptor binding in rats. Pharmacol Toxicol 2000, 86:197-202.
37. Harro J., Oreland L. Depression as a spreading neuronal adjustment disorder. Eur Neuropsychopharmacol 1996, 6:207-223.
38. Harro J., Oreland L., Vasar E., Bradwejn J. Impaired exploratory behaviour after DSP-4 treatment in rats: implications for the increased anxiety after noradrenergic denervation. Eur Neuropsychopharmacol 1995, 5:447-455.
39. Harro J., Pähkla R., Modiri A.R., Harro M., Kask A., Oreland L. Dose-dependent effects of noradrenergic denervation by DSP-4 treatment on forced swimming and beta-adrenoceptor binding in the rat. J Neural Transm 1999, 106:619-629.
40. Harro J., Terasmaa A., Eller M., Rinken A. 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 2003, 976:209-216.
41. Heal D.J., Butler S.A., Prow M.R., Buckett W.R. Quantification of presynaptic alpha 2-adrenoceptors in rat brain after short-term DSP-4 lesioning. Eur J Pharmacol 1993, 249:37-41.
42. Hughes Z.A., Stanford S.C. A partial noradrenergic lesion induced by DSP-4 increases extracellular noradrenaline concentration in rat frontal cortex: a microdialysis study in vivo. Psychopharmacology 1998, 136:299-303.
43. Häidkind R., Kivastik T., Eller M., Kolts I., Oreland L., Harro J. Denervation of the locus coeruleus projections by treatment with the selective neurotoxin DSP-4 [N-(2-chloroethyl)-N-ethyl-2-bromobenzylamine] reduces dopamine release potential in the nucleus accumbens shell in conscious rats. Neurosci Lett 2002, 332:79-82.
44. Jonsson G., Hallman H., Ponzio F., Ross S. DSP4 (N-(2-chloroethyl)-N-ethyl-2-bromobenzylamine)-a useful denervation tool for central and peripheral noradrenaline neurons. Eur J Pharmacol 1981, 72:173-188.
45. Kask A., Harro J., Tuomainen P., Rägo L., Männistö P.T. 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 1997, 355:267-272.
46. Kawahara H., Kawahara Y., Westerink B.H. The role of afferents to the locus coeruleus in the handling stress-induced increase in the release of noradrenaline in the medial prefrontal cortex: a dual-probe microdialysis study in the rat brain. Eur J Pharmacol 2000, 387:279-286.
47. Kivastik T., Vuorikallas K., Piepponen T.P., Zharkovsky A., Ahtee L. Morphine- and cocaine-induced conditioned place preference: effects of quinpirole and preclamol. Pharmacol Biochem Behav 1996, 54:371-375.
48. Lapiz M.D., Bondi C.O., Morilak D.A. Chronic treatment with desipramine improves cognitive performance of rats in an attentional set-shifting test. Neuropsychopharmacology 2007, 32:1000-1010.
49. Lapiz M.D., Morilak D.A. Noradrenergic modulation of cognitive function in rat medial prefrontal cortex as measured by attentional set shifting capability. Neuroscience 2006, 137:1039-1049.
50. Mackey W.B., Van der kooy D. Neuroleptics block the positive reinforcing effects of amphetamine but not of morphine as measured by place conditioning. Pharmacol Biochem Behav 1985, 22:101-105.
51. Mason S.T., Lin D. Dorsal noradrenergic bundle and selective attention in the rat. J Comp Physiol Psychol 1980, 94:819-832.
52. Mogilnicka E., Dooley D.J., Boissard C.G., Delini-Stula A. Facilitation of shock-induced fighting in the rat after DSP-4, a selective noradrenergic neurotoxin. Pharmacol Biochem Behav 1983, 18:625-628.
53. Mohammed A.K., Danysz W., Ögren S.O., Archer T. Central noradrenaline depletion attenuates amphetamine-induced locomotor behavior. Neurosci Lett 1986, 64:139-144.
54. Moore R.Y., Bloom F.E. Central catecholamine neuron systems: anatomy and physiology of the norepinephrine and epinephrine systems. Annu Rev Neurosci 1979, 2:113-168.
55. Ögren S.O., Archer T., Johansson C. Evidence for a selective brain noradrenergic involvement in the locomotor stimulant effects of amphetamine in the rat. Neurosci Lett 1983, 43:327-331.
56. Ögren S.O., Archer T., Ross S.B. Evidence for a role of the locus coeruleus noradrenaline system in learning. Neurosci Lett 1980, 20:351-356.
57. Pum M., Carey R.J., Huston J.P., Muller C.P. Dissociating effects of cocaine and d-amphetamine on dopamine and serotonin in the perirhinal, entorhinal, and prefrontal cortex of freely moving rats. Psychopharmacology (Berl) 2007, 193:375-390.
58. Reith M.E., Li M.Y., Yan Q.S. Extracellular dopamine, norepinephrine, and serotonin in the ventral tegmental area and nucleus accumbens of freely moving rats during intracerebral dialysis following systemic administration of cocaine and other uptake blockers. Psychopharmacology (Berl) 1997, 134:309-317.
59. Robbins T.W., Everitt B.J., Cole B.J., Archer T., Mohammed A. Functional hypotheses of the coeruleocortical noradrenergic projection: a review of recent experimentation and theory. Physiol Psychol 1985, 13:127-150.
60. Rommelfanger K.S., Mitrano D.A., Smith Y., Weinshenker D. Light and electron microscopic localization of alpha-1 adrenergic receptor immunoreactivity in the rat striatum and ventral midbrain. Neuroscience 2009, 158:1530-1540.
61. Ross S.B. Long-term effects of N-2-chlorethyl-N-ethyl-2-bromobenzylamine hydrochloride on noradrenergic neurones in the rat brain and heart. Br J Pharmacol 1976, 58:521-527.
62. Rudissaar R., Pruus K., Skrebuhhova T., Allikmets L., Matto V. Modulatory role of 5-HT3 receptors in mediation of apomorphine-induced aggressive behaviour in male rats. Behav Brain Res 1999, 106:91-96.
63. Schank J.R., Ventura R., Puglisi-Allegra S., Alcaro A., Cole C.D., Liles L.C., et al. Dopamine beta-hydroxylase knockout mice have alterations in dopamine signaling and are hypersensitive to cocaine. Neuropsychopharmacology 2006, 31:2221-2230.
64. Seeman P., Weinshenker D., Quirion R., Srivastava L.K., Bhardwaj S.K., Grandy D.K., et al. Dopamine supersensitivity correlates with D2High states, implying many paths to psychosis. Proc Natl Acad Sci USA 2005, 102:3513-3518.
65. Snoddy A.M., Tessel R.E. Prazosin: effect on psychomotor-stimulant cues and locomotor activity in mice. Eur J Pharmacol 1985, 116:221-228.
66. Spyraki C., Fibiger H.C., Phillips A.G. Cocaine-induced place preference conditioning: lack of effects of neuroleptics and 6-hydroxydopamine lesions. Brain Res 1982, 253:195-203.
67. Spyraki C., Fibiger H.C., Phillips A.G. Dopaminergic substrates of amphetamine-induced place preference conditioning. Brain Res 1982, 253:185-193.
68. Srinivasan J., Schmidt W.J. Functional recovery of locus coeruleus noradrenergic neurons after DSP-4 lesion: effects on dopamine levels and neuroleptic induced-parkinsonian symptoms in rats. J Neural Transm 2004, 111:13-26.
69. Szot P., Miguelez C., White S.S., Franklin A., Sikkema C., Wilkinson C.W., et al. A comprehensive analysis of the effect of DSP4 on the locus coeruleus noradrenergic system in the rat. Neuroscience 2010, 166:279-291.
70. Stanford C., Fillenz M., Ryan E. The effect of repeated mild stress on cerebral cortical adrenoceptors and noradrenaline synthesis in the rat. Neurosci Lett 1984, 45:163-167.
71. Tassin J.P. Uncoupling between noradrenergic and serotonergic neurons as a molecular basis of stable changes in behavior induced by repeated drugs of abuse. Biochem Pharmacol 2008, 75:85-97.
72. Theron C.N., de Villiers A.S., Taljaard J.J. 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 1993, 18:1321-1327.
73. Thiebot M.H., Kloczko J., Chermat R., Puech A.J., Soubrie P., Simon P. Enhancement of cocaine-induced hyperactivity in mice by benzodiazepines: evidence for an interaction of GABAergic processes with catecholaminergic neurons?. Eur J Pharmacol 1981, 76:335-343.
74. Tzschentke T.M. Measuring reward with the conditioned place preference paradigm: a comprehensive review of drug effects, recent progress and new issues. Prog Neurobiol 1998, 56:613-672.
75. Vanderschuren L.J., Beemster P., Schoffelmeer A.N. On the role of noradrenaline in psychostimulant-induced psychomotor activity and sensitization. Psychopharmacology (Berl) 2003, 169:176-185.
76. Weinshenker D., Miller N.S., Blizinsky K., Laughlin M.L., Palmiter R.D. Mice with chronic norepinephrine deficiency resemble amphetamine-sensitized animals. Proc Natl Acad Sci USA 2002, 99:13873-13877.
77. Weinshenker D., Schroeder J.P. There and back again: a tale of norepinephrine and drug addiction. Neuropsychopharmacology 2007, 32:1433-1451.
78. Wellman P., Ho D., Cepeda-Benito A., Bellinger L., Nation J. Cocaine-induced hypophagia and hyperlocomotion in rats are attenuated by prazosin. Eur J Pharmacol 2002, 455:117-126.
79. Ventura R., Cabib S., Alcaro A., Orsini C., Puglisi-Allegra S. Norepinephrine in the prefrontal cortex is critical for amphetamine-induced reward and mesoaccumbens dopamine release. J Neurosci 2003, 23:1879-1885.
80. Ventura R., Morrone C., Puglisi-Allegra S. Prefrontal/accumbal catecholamine system determines motivational salience attribution to both reward- and aversion-related stimuli. Proc Natl Acad Sci 2007, 104:5181-5186.
81. Wolfman C., Abo V., Calvo D., Medina J., Dajas F., Silveira R. Recovery of central noradrenergic neurons one year after the administration of the neurotoxin DSP4. Neurochem Int 1994, 25:395-400.
82. Xu F., Gainetdinov R.R., Wetsel W.C., Jones S.R., Bohn L.M., Miller G.W., et al. Mice lacking the norepinephrine transporter are supersensitive to psychostimulants. Nat Neurosci 2000, 3:465-471.