Cocaine Increases Stimulated Dopamine Release more in Periadolescent than Adult Rats (2008)

Neurotoxicol Teratol. Author manuscript; available in PMC 2009 September 1.
Published in final edited form as:
Published online 2008 April 22. doi:  10.1016/j.ntt.2008.04.002

Abstract

The neural mechanisms responsible for the enhanced adolescent vulnerability for initiating drug abuse are unclear. We investigated whether age differences in dopamine neurotransmission could explain cocaine’s enhanced psychomotor effects in the periadolescent rat. Electrical stimulation the medial forebrain bundle of anesthetized post-natal age 28 days (PN28) and PN65 rats elicited dopamine release in caudate nucleus and nucleus accumbens core before and after 15 mg/kg cocaine i.p. Extracellular dopamine concentrations were greater in PN65 than PN28 caudate following 20 and 60Hz stimulations and in the PN65 nucleus accumbens following 60Hz stimulations. Cocaine increased dopamine concentrations elicited by 20 Hz stimulations 3-fold in the adult, but almost 9-fold in periadolescent caudate. Dopamine release rate was lower in the periadolescent caudate although total dopamine clearance was similar to that of adults. The periadolescent caudate achieved adult levels of clearance by compensating for a lower Vmax with higher uptake affinity. Tighter regulation of extracellular dopamine by the higher uptake/release ratio in periadolescents led to greater increases after cocaine. In nucleus accumbens, dopamine release and Vmax were lower in periadolescents than adults, but uptake affinity and cocaine effects were similar. Immaturity of dopamine neurotransmission in dorsal striatum may underlie enhanced acute responses to psychostimulants in adolescent rats and suggests a mechanism for the greater vulnerability of adolescent humans to drug addiction.

Keywords: Development, addiction, voltammetry, dopamine neurotransmission, cocaine, adolescence


Acknowledgments

This work was supported by grant #DA09079

Abbreviations

PN
post-natal (age)
[DA]p
concentration of dopamine released per stimulus pulse
[DA]max
maximal evoked dopamine concentration

Footnotes

Publisher’s Disclaimer: This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final citable form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.

References

1. Adriani W, Chiarotti F, Laviola G. Elevated novelty seeking and peculiar d-amphetamine sensitization in periadolescent mice compared with adult mice. Behav.Neurosci. 1998;112:1152–1166. [PubMed]
2. Andersen SL, Gazzara RA. The ontogeny of apomorphine-induced alterations of neostriatal dopamine release: effects on spontaneous release. J.Neurochem. 1993;61:2247–2255. [PubMed]
3. Andersen SL, Thompson AP, Krenzel E, Teicher MH. Pubertal changes in gonadal hormones do not underlie adolescent dopamine receptor overproduction. Psychoneuroendocrinology. 2002;27:683–691. [PubMed]
4. Belluzzi JD, Lee AG, Oliff HS, Leslie FM. Age-dependent effects of nicotine on locomotor activity and conditioned place preference in rats. Psychopharmacology (Berl) 2004;174:389–395. [PubMed]
5. Belluzzi JD, Wang RH, Leslie FM. Acetaldehyde enhances acquisition of nicotine self-administration in adolescent rats. Neuropsychopharmacology. 2005;30:705–712. [PubMed]
6. Bergstrom BP, Garris PA. ‘Passive stabilization’ of striatal extracellular dopamine across the lesion spectrum encompassing the presymptomatic phase of Parkinson’s disease: a voltammetric study in the 6-OHDA-lesioned rat. J.Neurochem. 2003;87:1224–1236. [PubMed]
7. Bjork JM, Knutson B, Fong GW, Caggiano DM, Bennett SM, Hommer DW. Incentive-elicited brain activation in adolescents: Similarities and differences from young adults. J.Neurosci. 2004;24:1793–1802. [PubMed]
8. Bolanos CA, Glatt SJ, Jackson D. Subsensitivity to dopaminergic drugs in periadolescent rats: a behavioral and neurochemical analysis. Brain Res Dev.Brain Res. 1998;111:25–33. [PubMed]
9. Cahill PS, Walker QD, Finnegan JM, Mickelson GE, Travis ER, Wightman RM. Microelectrodes for the measurement of catecholamines in biological systems. Anal.Chem. 1996;68:3180–3186. [PubMed]
10. Caster JM, Walker QD, Kuhn CM. Enhanced behavioral response to repeated-dose cocaine in adolescent rats. Psychopharmacology (Berl) 2005;183:218–225. [PubMed]
11. Caster JM, Walker QD, Kuhn CM. Enhanced behavioral response to repeated-dose cocaine in adolescent rats. Psychopharmacology. 2005;183:218–225. [PubMed]
12. Catlow BJ, Kirstein CL. Heightened cocaine-induced locomotor activity in adolescent compared to adult female rats. J.Psychopharmacol. 2005;19:443–447. [PMC free article] [PubMed]
13. Chambers RA, Taylor JR, Potenza MN. Developmental neurocircuitry of motivation in adolescence: A critical period of addiction vulnerability. Am.J.Psychiatry. 2003;160:1041–1052. [PMC free article] [PubMed]
14. Chen K, Kandel DB, Davies M. Relationships between frequency and quantity of marijuana use and last year proxy dependence among adolescents and adults in the United States. Drug Alcohol Depend. 1997;46:53–67. [PubMed]
15. Clark DB, Kirisci L, Tarter RE. Adolescent versus adult onset and the development of substance use disorders in males. Drug Alcohol Depend. 1998;49:115–121. [PubMed]
16. Collins SL, Izenwasser S. Chronic nicotine differentially alters cocaine-induced locomotor activity in adolescent vs. adult male and female rats. Neuropharmacology. 2004;46:349–362. [PubMed]
17. Costall B, Naylor RJ. A comparison of the abilities of typical neuroleptic agents and of thioridazine, clozapine, sulpiride and metoclopramide to antagonise the hyperactivity induced by dopamine applied intracerebrally to areas of the extrapyramidal and mesolimbic systems. Eur.J.Pharmacol. 1976;40:9–19. [PubMed]
18. Creese I, Iverson SD. Blockage of amphetamine induced motor stimulation and stereotypy in the adult rat following neonatal treatment with 6-hydroxydopamine. Brain Res. 1973;55:369–382. [PubMed]
19. Cunningham MG, Bhattacharyya S, Benes FM. Amygdalo-cortical sprouting continues into early adulthood: Implications for the development of normal and abnormal function during adolescence. J.Comp.Neurol. 2002;453:116–130. [PubMed]
20. Estroff TW, Schwartz RH, Hoffmann NG. Adolescent Cocaine Abuse – Addictive Potential, Behavioral and Psychiatric Effects. Clinical Pediatrics. 1989;28:550–555. [PubMed]
21. Everitt BJ, Dickinson A, Robbins TW. The neuropsychological basis of addictive behaviour. Brain Res Brain Res Rev. 2001;36:129–138. [PubMed]
22. Frantz KJ, O’Dell LE, Parsons LH. Behavioral and neurochemical responses to cocaine in periadolescent and adult rats. Neuropsychopharmacology. 2007;32:625–637. [PubMed]
23. Garris PA, Walker QD, Wightman RM. Dopamine release and uptake rates both decrease in the partially denervated striatum in proportion to the loss of dopamine terminals. Brain Res. 1997;753:225–234. [PubMed]
24. Giedd JN, Blumenthal J, Jeffries NO, Castellanos FX, Liu H, Zijdenbos A, Paus T, Evans AC, Rapoport JL. Brain development during childhood and adolescence: a longitudinal MRI study. Nature Neurosci. 1999;2:861–863. [PubMed]
25. Haycock W, Becker L, Ang L, Furukawa Y, Hornykiewicz O, Kish SJ. Marked disparity between age-related changes in dopamine and other presynaptic dopaminergic markers in human striatum. J.Neurochem. 2003;87:574–585. [PubMed]
26. Hyman SE, Malenka RC, Nestler EJ. Neural mechanisms of addiction: The role of reward-related learning and memory. Annual Review of Neuroscience. 2006;29:565–598. [PubMed]
27. Ito R, Robbins TW, Everitt BJ. Differential control over cocaine-seeking behavior by nucleus accumbens core and shell. Nature Neuroscience. 2004;7:389–397. [PubMed]
28. Jones SR, Garris PA, Wightman RM. Different effects of cocaine and nomifensine on dopamine uptake in the caudate-putamen and nucleus accumbens. J.Pharmacol.Exp.Ther. 1995;274:396–403. [PubMed]
29. Kantak KM, Goodrich CM, Uribe V. Influence of sex, estrous cycle, and drug-onset age on cocaine self-administration in rats (Rattus norvegicus) Exp.Clin.Psychopharmacol. 2007;15:37–47. [PubMed]
30. Kelley AE, Schochet T, Landry CF. Risk taking and novelty seeking in adolescence – Introduction to Part I. Adolescent Brain Development: Vulnerabilities and Opportunities. 2004;1021:27–32. [PubMed]
31. Kelly PH. Drug-induced motor behaviour. In: Iverson LL, Iversen SD, Snyder SH, editors. Handbook in Psychopharmacology. New York: Plenum Press; 1977. pp. 295–332.
32. Kelly PH, Seviour PW, Iverson SD. Amphetamine and apomorphine responses in the rat following 6-OHDA lesions of the nucleus accumbens septi and corpus striatum. Brain Res. 1975;94:507–522. [PubMed]
33. Kerstetter KA, Kantak KM. Differential effects of self-administered cocaine in adolescent and adult rats on stimulus-reward learning. Psychopharmacology. 2007;194:403–411. [PubMed]
34. Lanier LP, Isaacson RL. Early developmental changes in the locomotor response to amphetamine and their relation to hippocampal function. Brain Res. 1977;126:567–575. [PubMed]
35. Laviola G, Dellomo G, Alleva E, Bignami G. Ontogeny of Cocaine Hyperactivity and Conditioned Place Preference in Mice. Psychopharmacology. 1992;107:221–228. [PubMed]
36. Laviola G, Pascucci T, Pieretti S. Striatal dopamine sensitization to D-amphetamine in periadolescent but not in adult rats. Pharmacol.Biochem.Behav. 2001;68:115–124. [PubMed]
37. Le Moal M, Simon H. Mesocorticolimbic Dopaminergic Network – Functional and Regulatory Roles. Physiological Reviews. 1991;71:155–234. [PubMed]
38. Leslie FM, Loughlin SE, Wang RH, Perez L, Lotfipour S, Belluzzi JD. Adolescent development of forebrain stimulant responsiveness – Insights from animal studies. Adolescent Brain Development: Vulnerabilities and Opportunities. 2004;1021:148–159. [PubMed]
39. Lew R, Patel A, Vaughan RA, Wilson A, Kuhar MJ. Microheterogeneity of Dopamine Transporters in Rat Striatum and Nucleus-Accumbens. Brain Res. 1992;584:266–271. [PubMed]
40. Li LB, Chen N, Ramamoorthy S, Chi L, Cui XN, Wang LC, Reith ME. The role of N-glycosylation in function and surface trafficking of the human dopamine transporter. J.Biol.Chem. 2004;279:21012–21020. [PubMed]
41. Maldonado AM, Kirstein CL. Cocaine-induced locomotor activity is increased by prior handling in adolescent but not adult female rats. Physiol.Behav. 2005;86:568–572. [PubMed]
42. Masse LC, Tremblay RE. Behavior of boys in kindergarten and the onset of substance use during adolescence. Arch.Gen.Psychiatry. 1997;54:62–68. [PubMed]
43. May LJ, Kuhr WG, Wightman RM. Differentiation of dopamine overflow and uptake processes in the extracellular fluid of the rat caudate nucleus with fast-scan in vivo voltammetry. J Neurochem. 1988;51:1060–1069. [PubMed]
44. Meng SZ, Ozawa Y, Itoh M, Takashima S. Developmental and age-related changes of dopamine transporter, and dopamine D1 and D2 receptors in human basal ganglia. Brain Res. 1999;843:136–144. [PubMed]
45. Michael J, Joseph JD, Kilpatrick MR, Travis ER, Wightman RM. Improving data acquisition for fast-scan cyclic voltammetry. Anal.Chem. 1999;71:3941–3947. [PubMed]
46. Millar J, Stamford JA, Kruk ZL, Wightman RM. Electrochemical, pharmacological and electrophysiological evidence of rapid dopamine release and removal in the rat caudate nucleus following electrical stimulation of the median forebrain bundle. Eur J Pharmacol. 1985;109:341–348. [PubMed]
47. Montague DM, Lawler CP, Mailman RB, Gilmore JH. Developmental regulation of the dopamine D-1 receptor in human caudate and putamen. Neuropsychopharmacology. 1999;21:641–649. [PubMed]
48. Palacios JM, Camps M, Cortes R, Probst A. Mapping dopamine receptors in the human brain. J.Neural Transm. 1988 Suppl, 27:227–235. [PubMed]
49. Patel AP, Cerruti C, Vaughan RA, Kuhar MJ. Developmentally regulated glycosylation of dopamine transporter. Brain Res., Developmental Brain. 1994:53–58. [PubMed]
50. Paus T, Zijdenbos A, Worsley K, Collins DL, Blumenthal J, Giedd JN, Rapoport JL, Evans AC. Structural maturation of neural pathways in children and adolescents: In vivo study. Science. 1999;283:1908–1911. [PubMed]
51. Paxinos G, Watson C. The Rat Brain in Stereotaxic Coordinates. New York: Academic Press; 1986.
52. Pijnenburg AJJ, Honig WMM, Van Rossum JM. Antagonism of apomorphine- and d-amphetamine-induced stereotyped behaviour by injection of low doses of haloperidol into the caudate nucleus and the nucleus accumbens. Psychopharmacologia. 1975;45:65–71.
53. Pijnenburg AJJ, Honig WMM, Van Rossum JM. Inhibition of d-amphetamine-induced locomotor activity by injection of haloperidol into the nucleus accumbens of the rat. Psychopharmacologia. 1975;41:87–95. [PubMed]
54. Robbins TW, Everitt BJ. Drug addiction: bad habits add up. Nature. 1999;398:567–570. [PubMed]
55. Robins LN, Przybeck TR. Age of onset of drug use as a factor in drug and other disorders. Nida Res Monogr. 1995;56:178–192. [PubMed]
56. Robinson TE, Berridge KC. The psychology and neurobiology of addiction: an incentive- sensitization view. Addiction. 2000;95 Suppl 2:S91–S117. [PubMed]
57. Seeman P. Images in neuroscience. Brain development, X: pruning during development. Am.J.Psychiatry. 1999;156:168. [PubMed]
58. Seeman P, Bzowej NH, Guan HC, Bergeron C, Becker LE, Reynolds GP, Bird ED, Riederer P, Jellinger K, Watanabe S. Human brain dopamine receptors in children and aging adults. Synapse. 1987;1:399–404. [PubMed]
59. Sharp T, Zetterstrom T, Ljungberg T, Ungerstedt U. A direct comparison of amphetamine-induced behaviours and regional brain dopamine release in the rat using intracerebral dialysis. Brain Res. 1987;401:322–330. [PubMed]
60. Sowell ER, Thompson PM, Holmes CJ, Jernigan TL, Toga AW. In vivo evidence for post-adolescent brain maturation in frontal and striatal regions. Nature Neurosci. 1999;2:859–861. [PubMed]
61. Spanagel R, Weiss F. The dopamine hypothesis of reward: past and current status. Trends Neurosci. 1999;22:521–527. [PubMed]
62. Spear LP. The adolescent brain and age-related behavioral manifestations. Neurosci Biobehav Rev. 2000;24:417–463. [PubMed]
63. Spear LP, Brick J. Cocaine-induced behavior in the developing rat. Behav.Neural Biol. 1979;26:401–415. [PubMed]
64. Stamford JA. Development and Aging of the Rat Nigrostriatal Dopamine System Studied with Fast Cyclic Voltammetry. J.Neurochem. 1989;52:1582–1589. [PubMed]
65. Tarazi FI, Tomasini EC, Baldessarini RJ. Postnatal development of dopamine D4-like receptors in rat forebrain regions: comparison with D2-like receptors. Brain Res Dev.Brain Res. 1998;110:227–233. [PubMed]
66. Tarazi FI, Tomasini EC, Baldessarini RJ. Postnatal development of dopamine D1-like receptors in rat cortical and striatolimbic brain regions: An autoradiographic study. Dev.Neurosci. 1999;21:43–49. [PubMed]
67. Teicher MH, Andersen SL, Hostetter JC. Evidence for Dopamine-Receptor Pruning Between Adolescence and Adulthood in Striatum But Not Nucleus-Accumbens. Dev.Brain Res. 1995;89:167–172. [PubMed]
68. Thompson PM, Giedd JN, Woods RP, MacDonald D, Evans AC, Toga AW. Growth patterns in the developing brain detected by using continuum mechanical tensor maps. Nature. 2000;404:190–193. [PubMed]
69. Vanderschuren LJ, Di Ciano P, Everitt BJ. Involvement of the dorsal striatum in cue-controlled cocaine seeking. J.Neurosci. 2005;25:8665–8670. [PubMed]
70. Vasilev V, Veskov R, Janac B, Rakic L, Stojiljkovic M. Age-related differences in MK-801- and amphetamine-induced locomotor and stereotypic activities of rats. Neurobiol.Aging. 2003;24:715–723. [PubMed]
71. Walker QD, Morris S, Caster JM, Nagel J, Kuhn CM. Exaggerated behavioral responses to stimulants in adolescents. Soc.Neurosci.Abst. 2005:1026.4.
72. Walker QD, Ray R, Kuhn CM. Sex differences in neurochemical effects of dopaminergic drugs in rat striatum. Neuropsychopharmacology. 2006;31:1193–1202. [PubMed]
73. Walker QD, Rooney MB, Wightman RM, Kuhn CM. Dopamine release and uptake are greater in female than male rat striatum as measured by fast cyclic voltammetry. Neuroscience. 2000;95:1061–1070. [PubMed]
74. Wightman RM, Amatore C, Engstrom RC, Hale PD, Kristensen EW, Kuhr WG, May LJ. Real-time characterization of dopamine overflow and uptake in the rat striatum. Neuroscience. 1988;25:513–523. [PubMed]
75. Wightman RM, Zimmerman JB. Control of Dopamine Extracellular Concentration in Rat Striatum by Impulse Flow and Uptake. Brain Res.Rev. 1990;15:135–144. [PubMed]
76. Wills TA, Vaccaro D, McNamara G. Novelty seeking, risk taking, and related constructs as predictors of adolescent substance use: an application of Cloninger’s theory. J.Substance Abuse. 1994;6:1–20. [PubMed]
77. Wu Q, Reith ME, Wightman RM, Kawagoe KT, Garris PA. Determination of release and uptake parameters from electrically evoked dopamine dynamics measured by real-time voltammetry. J.Neurosci.Methods. 2001;112:119–133. [PubMed]
78. Zuckerman M. Sensation-seeking and the endogenous deficit theory of drug abuse. NIDA.Res.Monogr. 1986;74:59–70. [PubMed]