Electrophysiological and structural alterations in striatum associated with behavioral sensitization to (±)3,4-methylenedioxymethamphetamine (ecstasy) in rats: Role of drug context

Neuroscience

Volumn 171, Issue 3, 2010, Pages 794-811

  Ball, K T ^a   Wellman, C L ^b   Miller, B R ^b   Rebec, G V ^b  

^a BLOOMSBURG UNIVERSITY   (United States)

^b INDIANA UNIVERSITY   (United States)

Author keywords

Dendritic spines; Electrophysiology; MDMA; Morphology; Sensitization; Striatum

Indexed keywords

3,4 METHYLENEDIOXYMETHAMPHETAMINE;

ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BEHAVIOR CHANGE; BRAIN ELECTROPHYSIOLOGY; CELL STRUCTURE; COGNITIVE DEFECT; CONTROLLED STUDY; CORPUS STRIATUM; LOCOMOTION; MALE; NERVE CELL; NEUROMODULATION; NONHUMAN; PRIORITY JOURNAL; RAT; SENSITIZATION; SYNAPSE;

ADRENERGIC UPTAKE INHIBITORS; ANIMALS; BEHAVIOR, ANIMAL; CELL SHAPE; ELECTROPHYSIOLOGY; MALE; N-METHYL-3,4-METHYLENEDIOXYAMPHETAMINE; NEOSTRIATUM; NEURONS; RATS; RATS, SPRAGUE-DAWLEY; SILVER STAINING;

EID: 78349308325     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2010.09.041     Document Type: Article

References (75)

1. Guidelines for the care and use of mammals in neuroscience and behavioral research 2003, Academies NRCotN, The National Academies Press, Washington, DC.
2. Anagnostaras S.G., Robinson T.E. Sensitization to the psychomotor stimulant effects of amphetamine: modulation by associative learning. Behav Neurosci 1996, 110:1397-1414.
3. Anagnostaras S.G., Schallert T., Robinson T.E. Memory processes governing amphetamine-induced psychomotor sensitization. Neuropsychopharmacology 2002, 26:703-715.
4. Andersen P., Soleng A.F. Long-term potentiation and spatial training are both associated with the generation of new excitatory synapses. Brain Res Rev 1998, 26:353-359.
5. Ball K.T., Budreau D., Rebec G.V. Acute effects of 3,4-methylenedioxymethamphetamine on striatal single-unit activity and behavior in freely moving rats: differential involvement of dopamine D(1) and D(2) receptors. Brain Res 2003, 994:203-215.
6. Ball K.T., Rebec G.V. Role of 5-HT2A and 5-HT2C/B receptors in the acute effects of 3,4-methylenedioxymethamphetamine (MDMA) on striatal single-unit activity and locomotion in freely moving rats. Psychopharmacology (Berl) 2005, 181:676-687.
7. Ball K.T., Budreau D., Rebec G.V. Context-dependent behavioural and neuronal sensitization in striatum to MDMA (ecstasy) administration in rats. Eur J Neurosci 2006, 24:217-228.
8. Ball K.T., Walsh K.M., Rebec G.V. Reinstatement of MDMA (ecstasy) seeking by exposure to discrete drug-conditioned cues. Pharmacol Biochem Behav 2007, 87:420-425.
9. Ball K.T., Wellman C.L., Fortenberry E., Rebec G.V. Sensitizing regimens of MDMA (ecstasy) elicit enduring and differential structural alterations in the brain motive circuit of the rat. Neuroscience 2009, 160:264-274.
10. Bell K., Kalivas P.W. Context-specific cross-sensitization between systemic cocaine and intra-accumbens AMPA infusion in the rat. Psychopharmacology (Berl) 1996, 127:377-383.
11. Bell K., Duffy P., Kalivas P.W. Context-specific enhancement of glutamate transmission by cocaine. Neuropsychopharmacology 2000, 23:335-344.
12. Bradberry C.W., Nobiletti J.B., Elsworth J.D., Murphy B., Jatlow P., Roth R.H. Cocaine and cocaethylene: microdialysis comparison of brain drug levels and effects on dopamine and serotonin. J Neurochem 1993, 60:1429-1435.
13. Brown P., Oliviero A., Mazzone P., Insola A., Tonali P., Di Lazzaro V. Dopamine dependency of oscillations between subthalamic nucleus and pallidum in Parkinson's disease. J Neurosci 2001, 21:1033-1038.
14. Buell S.J. Golgi-cox and rapid Golgi methods as applied to autopsied human brain tissue: widely disparate results. J Neuropathol Exp Neurol 1982, 41:500-507.
15. Caprioli D., Celentano M., Paolone G., Badiani A. Modeling the role of environment in addiction. Prog Neuro-Psychopharmacol Biol Psychiatry 2007, 31:1639-1653.
16. Churchill J.D., Tharp J.A., Wellman C.L., Sengelaub D.R., Garraghty P.E. Morphological correlates of injury-induced reorganization in primate somatosensory cortex. BMC Neurosci 2004, 5:43.
17. Churchill L., Swanson C.J., Urbina M., Kalivas P.W. Repeated cocaine alters glutamate receptor subunit levels in the nucleus accumbens and ventral tegmaental area of rats that develop behavioral sensitization. J Neurochem 1999, 72:2397-2403.
18. Coleman P.D., Flood D.G. Neuron numbers and dendritic extent in normal aging and Alzheimer's disease. Neurobiol Aging 1987, 8:521-545.
19. Comery T.A., Stamoudis C.X., Irwin S.A., Greenough W.T. Increased density of multiple-head dendritic spines on medium-sized spiny neurons of the striatum in rats reared in a complex environment. Neurobiol Learn Mem 1996, 66:93-96.
20. Conrad K.L., Tseng K.Y., Uejima J.L., Reimers J.M., Heng L.-J., Shaham Y., Marinelli M., Wolf M.E. Formation of accumbens GluR2-lacking AMPA receptors mediates incubation of cocaine craving. Nature 2008, 454:118-121.
21. Cook S.C., Wellman C.L. Chronic stress alters dendritic morphology in rat medial prefrontal cortex. J Neurobiol 2004, 60:236-248.
22. Cornish J.L., Kalivas P.W. Glutamate transmission in the nucleus accumbens mediates relapse in cocaine addiction. J Neurosci 2000, 20. RC89:RC89.
23. Courtemanche R., Fujii N., Graybiel A.M. Synchronous, focally modulated beta-band oscillations characterize Local Field potential activity in the striatum of awake behaving monkeys. J Neurosci 2003, 23:11741-11752.
24. Everitt B.J., Robbins T.W. Neural systems of reinforcement for drug addiction: from actions to habits to compulsion. Nat Neurosci 2005, 8:1481-1489.
25. Geinisman Y., Morrell F., deToledo-Morrell L. Perforated synapses on double-headed dendritic spines: a possible structural substrate of synaptic plasticity. Brain Res 1989, 480:326-329.
26. Gerdeman G.L., Partridge J.G., Lupica C.R., Lovinger D.M. It could be habit forming: drugs of abuse and striatal synaptic plasticity. Trends Neurosci 2003, 26:184-192.
27. Glaser E.M., Van der Loos H. Analysis of thick brain sections by obverse-reverse computer microscopy: application of a new, high clarity Golgi-Nissl stain. J Neurosci Methods 1981, 4:117-125.
28. Gudelsky G.A., Yamamoto B.K. Actions of 3,4-methylenedioxymethamphetamine (MDMA) on cerebral dopaminergic, serotonergic and cholinergic neurons. Pharmacol Biochem Behav 2008, 90:198-207.
29. Gulley J.M., Stanis J.J. Adaptations in medial prefrontal cortex function associated with amphetamine-induced behavioral sensitization. Neuroscience 2009, 166(2):615-624. doi: 10.1016/j.neuroscience. (2009).1012.1044.
30. Hammond C., Bergman H., Brown P. Pathological synchronization in Parkinson's disease: networks, models and treatments. Trends Neurosci 2007, 30:357-364.
31. Haracz J.L., Tschanz J.T., Wang Z., White I.M., Rebec G.V. Striatal single-unit responses to amphetamine and neuroleptics in freely moving rats. Neurosci Biobehav Rev 1993, 17:1-12.
32. Haracz J.L., Tschanz J.T., Wang Z., Griffith K.E., Rebec G.V. Amphetamine effects on striatal neurons: implications for models of dopamine function. Neurosci Biobehav Rev 1998, 22:613-622.
33. Harmon K.M., Wellman C.L. Differential effects of cholinergic lesions on dendritic spines in frontal cortex of young adult and aging rats. Brain Res 2003, 992:60-68.
34. Izquierdo A., Wellman C.L., Holmes A. Rapid dendritic retraction in medial prefrontal neurons and impaired fear extinction following exposure to uncontrollable stress. J Neurosci 2006, 26:5733-5738.
35. Jedynak J.P., Uslaner J.M., Esteban J.A., Robinson T.E. Methamphetamine-induced structural plasticity in the dorsal striatum. Eur J Neurosci 2007, 25:847-853.
36. Kalivas P.W., Stewart J. Dopamine transmission in the initiation and expression of drug- and stress-induced sensitization of motor activity. Brain Res Rev 1991, 16:223-244.
37. Lebedev M.A., Nelson R.J. Rhythmically firing neostriatal neurons in monkey: activity patterns during reaction-time hand movements. J Neurophysiol 1999, 82:1832-1842.
38. Leuner B., Falduto J., Shors T.J. Associative memory formation increases the observation of dendritic spines in the hippocampus. J Neurosci 2003, 23:659-665.
39. Li Y., Acerbo M.J., Robinson T.E. The induction of behavioural sensitization is associated with cocaine-induced structural plasticity in the core (but not shell) of the nucleus accumbens. Eur J Neurosci 2004, 20:1647-1654.
40. Miller B.R., Walker A.G., Shah A.S., Barton S.J., Rebec G.V. Dysregulated information processing by medium spiny neurons in striatum of freely behaving mouse models of Huntington's disease. J Neurophysiol 2008, 100:2205-2216.
41. Miller B.R., Walker A.G., Fowler S.C., von Horsten S., Riess O., Johnson M.A., Rebec G.V. Dysregulation of coordinated neuronal firing patterns in striatum of freely behaving transgenic rats that model Huntington's disease. Neurobiol Dis 2010, 37:106-113.
42. Moghaddam B., Homayoun H. Divergent Plasticity of Prefrontal Cortex Networks. Neuropsychopharmacology 2008, 33:42-55.
43. Nelson C.L., Milovanovic M., Wetter J.B., Ford K.A., Wolf M.E. Behavioral sensitization to amphetamine is not accompanied by changes in glutamate receptor surface expression in the rat nucleus accumbens. J Neurochem 2009, 109:35-51.
44. Park W.K., Bari A.A., Jey A.R., Anderson S.M., Spealman R.D., Rowlett J.K., Pierce R.C. Cocaine administered into the medial prefrontal cortex reinstates cocaine-seeking behavior by increasing AMPA receptor-mediated glutamate transmission in the nucleus accumbens. J Neurosci 2002, 22:2916-2925.
45. Paxinos G., Watson C. The rat brain in stereotaxic coordinates 1998, Academic Press, New York, NY. 4th ed.
46. Peters A., Kaiserman-Abramof I.R. The small pyramidal neuron of the rat cerebral cortex. The perikaryon, dendrites and spines. Am J Anat 1970, 127:321-355.
47. Pierce R.C., Bell K., Duffy P., Kalivas P.W. Repeated cocaine augments excitatory amino acid transmission in the nucleus accumbens only in rats having developed behavioral sensitization. J Neurosci 1996, 16:1550-1560.
48. Raz A., Vaadia E., Bergman H. Firing patterns and correlations of spontaneous discharge of pallidal neurons in the normal and the tremulous 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine vervet model of Parkinsonism. J Neurosci 2000, 20:8559-8571.
49. Raz A., Frechter-Mazar V., Feingold A., Abeles M., Vaadia E., Bergman H. Activity of pallidal and striatal tonically active neurons is correlated in MPTP-treated monkeys but not in normal monkeys. J Neurosci 2001, 21:RC128. (1-5).
50. Robbins T.W., Everitt B.J. Drug addiction: bad habits add up. Nature 1999, 398:567-570.
51. Robinson T.E., Berridge K.C. The neural basis of drug craving: an incentive-sensitization theory of addiction. Brain Res Rev 1993, 18:247-291.
52. Robinson T.E., Kolb B. Structural plasticity associated with exposure to drugs of abuse. Neuropharmacology 2004, 47(Suppl 1):33-46.
53. Robinson T.E., Browman K.E., Crombag H.S., Badiani A. Modulation of the induction or expression of psychostimulant sensitization by the circumstances surrounding drug administration. Neurosci Biobehav Rev 1998, 22:347-354.
54. Rosa-Kenig A., Puotz J.K., Rebec G.V. The involvement of D1 and D2 dopamine receptors in amphetamine-induced changes in striatal unit activity in behaving rats. Brain Res 1993, 619:347-351.
55. Sakurai Y. How do cell assemblies encode information in the brain?. Neurosci Biobehav Rev 1999, 23:785-796.
56. Salinas E., Sejnowski T.J. Correlated neuronal activity and the flow of neural information. Nat Rev Neurosci 2001, 2:539-550.
57. Sari Y., Smith K.D., Ali P.K., Rebec G.V. Up-regulation of GLT1 attenuates cue-induced reinstatement of cocaine seeking in rats. J Neurosci 2009, 29:9239-9243.
58. Schneidman E., Berry M.J., Segev R., Bialek W. Weak pairwise correlations imply strongly correlated network states in a neural population. Nature 2006, 440:1007-1012.
59. Segal D.S., Mandell A.J. Long-term administration of d-amphetamine: progressive augmentation of motor activity and stereotypy. Pharmacol Biochem Behav 1974, 2:249-255.
60. Shaham Y., Hope B.T. The role of neuroadaptations in relapse to drug seeking. Nat Neurosci 2005, 8:1437-1439.
61. Sholl D.A. The organization of the cerebral cortex 1956, Methuen, London.
62. Singer B.F., Tanabe L.M., Gorny G., Jake-Matthews C., Li Y., Kolb B., Vezina P. Amphetamine-induced changes in dendritic morphology in rat forebrain correspond to associative drug conditioning rather than nonassociative drug sensitization. Biol Psychiatry 2009, 65:835-840.
63. Soar K., Turner J.J., Parrott A.C. Problematic versus non-problematic ecstasy/MDMA use: the influence of drug usage patterns and pre-existing psychiatric factors. J Psychopharmacol 2006, 20:417-424.
64. Stewart J., Vezina P. Conditioning and behavioral sensitization. Sensitization in the nervous system 1988, 207-224. Telford Press, Caldwell, NJ. P.W. Kalivas, C.D. Barnes (Eds.).
65. Stewart J., Vezina P. Extinction procedures abolish conditioned stimulus control but spare sensitized responding to amphetamine. Behav Pharmacol 1991, 2:65-71.
66. Stewart J., Badiani A. Tolerance and sensitization to the behavioral effects of drugs. Behav Pharmacol 1993, 4:289-312.
67. Teneud L.M., Baptista T., Murzi E., Hoebel B.G., Hernandez L. Systemic and local cocaine increase extracellular serotonin in the nucleus accumbens. Pharmacol Biochem Behav 1996, 53:747-752.
68. Topp L., Hando J., Dillon P., Roche A., Solowij N. Ecstasy use in Australia: patterns of use and associated harm. Drug Alcohol Depend 1999, 55:105-115.
69. Tzschentke T.M., Schmidt W.J. Glutamatergic mechanisms in addiction. Mol Psychiatry 2003, 8:373-382.
70. Uhlhaas P.J., Singer W. Neural synchrony in brain disorders: relevance for cognitive dysfunctions and pathophysiology. Neuron 2006, 52:155-168.
71. Wellman C.L., Izquierdo A., Garrett J.E., Martin K.P., Carroll J., Millstein R., Murphy D.L., Lesch K.-P., Holmes A. Genetic inactivation of the serotonin transporter causes impairment of stress-coping and extinction-recall and medial prefrontal cortex abnormalities. J Neurosci 2007, 27:684-691.
72. Williams D., Tijssen M., Van Bruggen G., Bosch A., Insola A., Di Lazzaro V., Mazzone P., Oliviero A., Quartarone A., Speelman H., Brown P. Dopamine-dependent changes in the functional connectivity between basal ganglia and cerebral cortex in humans. Brain 2002, 125:1558-1569.
73. Williams R.S., Ferrante R.J., Caviness V.S. The golgi rapid method in clinical neuropathology: the morphological consequences of suboptimal fixation. J Neuropathol Exp Neurol 1978, 37:13-33.
74. Wilson C.J., Groves P.M. Fine structure and synaptic connections of the common spiny neuron of the rat neostriatum: a study employing intracellular inject of horseradish peroxidase. J Comp Neurol 1980, 194:599-615.
75. Works S.J., Wilson R.E., Wellman C.L. Age-dependent effect of cholinergic lesion on dendritic morphology in rat frontal cortex. Neurobiol Aging 2004, 25:963-974.