Age and sex differences in impulsive action in rats: The role of dopamine and glutamate

Behavioural Brain Research

Volumn 230, Issue 1, 2012, Pages 21-33

  Burton, Christie L ^a,b   Fletcher, Paul J ^a,b  

^a UNIVERSITY OF TORONTO   (Canada)

^b CENTRE FOR ADDICTION AND MENTAL HEALTH   (Canada)

Author keywords

Adolescence; Dopamine; Glutamate; Impulsivity; Nicotine; Sex differences

Indexed keywords

AMPHETAMINE; DOPAMINE; GLUTAMIC ACID; N METHYL DEXTRO ASPARTIC ACID RECEPTOR BLOCKING AGENT; NEUROTRANSMITTER; NICOTINE;

ADOLESCENT; AGE; ANIMAL EXPERIMENT; ARTICLE; BRAIN DEVELOPMENT; CONTROLLED STUDY; DECISION MAKING; DOPAMINE RELEASE; FEMALE; IMPULSIVENESS; MALE; NONHUMAN; PHOTOSTIMULATION; PRIORITY JOURNAL; RAT; REINFORCEMENT; RESPONSE TIME; SEX DIFFERENCE; STIMULUS RESPONSE;

AGING; AMPHETAMINE; ANALYSIS OF VARIANCE; ANIMALS; ANIMALS, NEWBORN; CHOICE BEHAVIOR; CONDITIONING, OPERANT; DOPAMINE; DOPAMINE AGENTS; DOSE-RESPONSE RELATIONSHIP, DRUG; EXCITATORY AMINO ACID ANTAGONISTS; FEMALE; FOOD DEPRIVATION; GLUTAMIC ACID; IMPULSIVE BEHAVIOR; MALE; PHENOLS; PIPERIDINES; PREGNANCY; RATS; RATS, SPRAGUE-DAWLEY; SEX CHARACTERISTICS; WATER DEPRIVATION;

EID: 84857011632     PISSN: 01664328     EISSN: 18727549     Source Type: Journal    
DOI: 10.1016/j.bbr.2012.01.046     Document Type: Article

References (101)

1. Romer D. Adolescent risk taking, impulsivity, and brain development: implications for prevention. Dev Psychobiol 2010, 52(3):263-276.
2. Spear L.P. The adolescent brain and age-related behavioral manifestations. Neurosci Biobehav Rev 2000, 24(4):417-463.
3. Arnett J. Reckless behavior in adolescence: a developmental perspective. Dev Rev 1992, 54:317-326.
4. Sturman D.A., Moghaddam B. The neurobiology of adolescence: changes in brain architecture, functional dynamics, and behavioral tendencies. Neurosci Biobehav Rev 2011, 35(8):1704-1712.
5. Estroff T.W., Schwartz R.H., Hoffmann N.G. Adolescent cocaine abuse. Addictive potential: behavioral and psychiatric effects. Clin Pediatr (Phila) 1989, 28(12):550-555.
6. Deas D., Riggs P., Lagenbucher J., Goldman M., Brown S. Adolescents are not adults: developmental considerations in alcohol users. Alcohol Clin Exp Res 2000, 24(2):232-237.
7. Schramm-Sapyta N.L., Walker Q.D., Caster J.M., Levin E.D., Kuhn C.M. Are adolescents more vulnerable to drug addiction than adults? Evidence from animal models. Psychopharmacology (Berl) 2009, 206(1):1-21.
8. Laviola G., Adriani W., Terranova M.L., Gerra G. Psychobiological risk factors for vulnerability to psychostimulants in human adolescents and animal models. Neurosci Biobehav Rev 1999, 23(7):993-1010.
9. Chambers R.A., Taylor J.R., Potenza M.N. Developmental neurocircuitry of motivation in adolescence: a critical period of addiction vulnerability. Am J Psychiatry 2003, 160(6):1041-1052.
10. Evenden J.L. Varieties of impulsivity. Psychopharmacology (Berl) 1999, 146(4):348-361.
11. Winstanley C.A., Dalley J.W., Theobald D.E.H., Robbins T.W. Fractionating impulsivity: contrasting effects of central 5-HT depletion on different measures of impulsive behavior. Neuropsychopharmacology 2004, 29(7):1331-1343.
12. Winstanley C.A., Eagle D.M., Robbins T.W. Behavioral models of impulsivity in relation to ADHD: translation between clinical and preclinical studies. Clin Psychol Rev 2006, 26(4):379-395.
13. Dalley J.W., Mar A.C., Economidou E., Robbins T.W. Neurobehavioral mechanisms of impulsivity: fronto-striatal systems and functional neurochemistry. Pharmacol Biochem Behav 2008, 90(2):250-260.
14. APA Diagnostic and statistical manual of mental disorders 2000, American Psychiatric Association, Washington, DC. 4th ed. (text revision - DSM-IV-TR).
15. Rogers R.D., Moeller F.G., Swann A.C., Clark L. Recent research on impulsivity in individuals with drug use and mental health disorders: implications for alcoholism. Alcohol Clin Exp Res 2010, 34(8):1319-1333.
16. Williams B.R., Ponesse J.S., Schachar R.J., Logan G.D., Tannock R. Development of inhibitory control across the life span. Dev Psychol 1999, 35(1):205-213.
17. Sinopoli K.J., Schachar R., Dennis M. Reward improves cancellation and restraint inhibition across childhood and adolescence. Dev Psychol 2011, 47(5):1479-1489.
18. Green L., Fry A.F., Myerson J. Discounting of delayed rewards: a life-span comparison. Psychol Sci 1994, 5(1):33-36.
19. Overman W.H., Frassrand K., Ansel S., Trawalter S., Bies B., Redmond A. Performance on the IOWA card task by adolescents and adults. Neuropsychologia 2004, 42(13):1838-1851.
20. Green L., Myerson J., Ostaszewski P. Discounting of delayed rewards across the life span: age differences in individual discounting functions. Behav Process 1999, 46:89-96.
21. Steinberg L., Graham S., O'Brien L., Woolard J., Cauffman E., Banich M. Age differences in future orientation and delay discounting. Child Dev 2009, 80(1):28-44.
22. Eigsti I.M., Zayas V., Mischel W., Shoda Y., Ayduk O., Dadlani M.B., et al. Predicting cognitive control from preschool to late adolescence and young adulthood. Psychol Sci 2006, 17(6):478-484.
23. Rubia K., Smith A.B., Woolley J., Nosarti C., Heyman I., Taylor E., et al. Progressive increase of frontostriatal brain activation from childhood to adulthood during event-related tasks of cognitive control. Hum Brain Mapp 2006, 27(12):973-993.
24. Ernst M., Grant S.J., London E.D., Contoreggi C.S., Kimes A.S., Spurgeon L. Decision making in adolescents with behavior disorders and adults with substance abuse. Am J Psychiatry 2003, 160(1):33-40.
25. Eshel N., Nelson E.E., Blair R.J., Pine D.S., Ernst M. Neural substrates of choice selection in adults and adolescents: development of the ventrolateral prefrontal and anterior cingulate cortices. Neuropsychologia 2007, 45(6):1270-1279.
26. Stevens M.C., Kiehl K.A., Pearlson G.D., Calhoun V.D. Functional neural networks underlying response inhibition in adolescents and adults. Behav Brain Res 2007, 181(1):12-22.
27. Adriani W., Laviola G. Elevated levels of impulsivity and reduced place conditioning with d-amphetamine: two behavioral features of adolescence in mice. Behav Neurosci 2003, 117(4):695-703.
28. Pinkston J.W., Lamb R.J. Delay discounting in C57BL/6J and DBA/2J mice: adolescent-limited and life-persistent patterns of impulsivity. Behav Neurosci 2011, 125(2):194-201.
29. Andrzejewski M.E., Schochet T.L., Feit E.C., Harris R., McKee B.L., Kelley A.E. A comparison of adult and adolescent rat behavior in operant learning: extinction, and behavioral inhibition paradigms. Behav Neurosci 2011, 125(1):93-105.
30. Jentsch J.D., Taylor J.R. Sex-related differences in spatial divided attention and motor impulsivity in rats. Behav Neurosci 2003, 117(1):76-83.
31. Anker J.J., Gliddon L.A., Carroll M.E. Impulsivity on a Go/No-go task for intravenous cocaine or food in male and female rats selectively bred for high and low saccharin intake. Behav Pharmacol 2008, 19(5-6):615-629.
32. Beatty W.W. Effects of gonadectomy on sex differences in DRL behavior. Physiol Behav 1973, 10(1):177-178.
33. van Hest A., van Haaren F., van de Poll N.E. Behavioral differences between male and female wistar rats on DRL schedules: effect of stimuli promoting collateral activities. Physiol Behav 1987, 39:255-261.
34. Cross C.P., Copping L.T., Campbell A. Sex differences in impulsivity: a meta-analysis. Psychol Bull 2011, 137(1):97-130.
35. Li C.S., Huang C., Constable R.T., Sinha R. Gender differences in the neural correlates of response inhibition during a stop signal task. Neuroimage 2006, 32(4):1918-1929.
36. Perry J.L., Carroll M.E. The role of impulsive behavior in drug abuse. Psychopharmacology (Berl) 2008, 200(1):1-26.
37. Silveri M.M., Rohan M.L., Pimentel P.J., Gruber S.A., Rosso I.M., Yurgelun-Todd D.A. Sex differences in the relationship between white matter microstructure and impulsivity in adolescents. Magn Reson Imaging 2006, 24(7):833-841.
38. Fields S., Collins C., Leraas K., Reynolds B. Dimensions of impulsive behavior in adolescent smokers and nonsmokers. Exp Clin Psychopharmacol 2009, 17(5):302-311.
39. Robbins T.W. The 5-choice serial reaction time task: behavioural pharmacology and functional neurochemistry. Psychopharmacology (Berl) 2002, 163(3-4):362-380.
40. Fletcher P.J., Chambers J.W., Rizos Z., Chintoh A.F. Effects of 5-HT depletion in the frontal cortex or nucleus accumbens on response inhibition measured in the 5-choice serial reaction time test and on a DRL schedule. Behav Brain Res 2009, 201(1):88-98.
41. Pattij T., Janssen M.C., Vanderschuren L.J., Schoffelmeer A.N., van Gaalen M.M. Involvement of dopamine D1 and D2 receptors in the nucleus accumbens core and shell in inhibitory response control. Psychopharmacology (Berl) 2007, 191(3):587-598.
42. Higgins G.A., Ballard T.M., Huwyler J., Kemp J.A., Gill R. Evaluation of the NR2B-selective NMDA receptor antagonist Ro 63-1908 on rodent behaviour: evidence for an involvement of NR2B NMDA receptors in response inhibition. Neuropharmacology 2003, 44(3):324-341.
43. Mirza N.R., Stolerman I.P. Nicotine enhances sustained attention in the rat under specific task conditions. Psychopharmacology (Berl) 1998, 138(3-4):266-274.
44. van Gaalen M.M., van Koten R., Schoffelmeer A.N., Vanderschuren L.J. Behavioral disinhibition requires dopamine receptor activation. Psychopharmacology (Berl) 2006, 187(1):73-85.
45. Azzaro A.J., Rutledge C.O. Selectivity of release of norepinephrine: dopamine and 5-hydroxytryptamine by amphetamine in various regions of rat brain. Biochem Pharmacol 1973, 22(22):2801-2813.
46. Besson M.J., Cheramy A., Glowinski J. Effects of amphetamine and desmethylimipramine on amines synthesis and release in central catecholamine-containing neurons. Eur J Pharmacol 1969, 7(1):111-114.
47. Nielsen J.A., Chapin D.S., Moore K.E. Differential effects of d-amphetamine: beta-phenylethylamine, cocaine and methylphenidate on the rate of dopamine synthesis in terminals of nigrostriatal and mesolimbic neurons and on the efflux of dopamine metabolites into cerebroventricular perfusates of rats. Life Sci 1983, 33(19):1899-1907.
48. Nisell M., Nomikos G.G., Svensson T.H. Infusion of nicotine in the ventral tegmental area or the nucleus accumbens of the rat differentially affects accumbal dopamine release. Pharmacol Toxicol 1994, 75(6):348-352.
49. Gill R., Alanine A., Bourson A., Buttelmann B., Fischer G., Heitz M.P., et al. Pharmacological characterization of Ro 63-1908 (1-[2-(4-hydroxy-phenoxy)-ethyl]-4-(4-methyl-benzyl)-piperidin-4-ol): a novel subtype-selective N-methyl-d-aspartate antagonist. J Pharmacol Exp Ther 2002, 302(3):940-948.
50. Andersen S.L., Thompson A.T., Rutstein M., Hostetter J.C., Teicher M.H. Dopamine receptor pruning in prefrontal cortex during the periadolescent period in rats. Synapse 2000, 37(2):167-169.
51. Kalsbeek A., Voorn P., Buijs R.M., Pool C.W., Uylings H.B. Development of the dopaminergic innervation in the prefrontal cortex of the rat. J Comp Neurol 1988, 269(1):58-72.
52. Lewis D.A. Development of the prefrontal cortex during adolescence: insights into vulnerable neural circuits in schizophrenia. Neuropsychopharmacology 1997, 16(6):385-398.
53. Liu X.B., Murray K.D., Jones E.G. Switching of NMDA receptor 2A and 2B subunits at thalamic and cortical synapses during early postnatal development. J Neurosci 2004, 24(40):8885-8895.
54. Sheng M., Cummings J., Roldan L.A., Jan Y.N., Jan L.Y. Changing subunit composition of heteromeric NMDA receptors during development of rat cortex. Nature 1994, 368(6467):144-147.
55. Miller L.P., Johnson A.E., Gelhard R.E., Insel T.R. The ontogeny of excitatory amino acid receptors in the rat forebrain: I N-methyl-D-aspartate and quisqualate receptors. Neuroscience 1990, 35(1):31-43.
56. Pian J.P., Criado J.R., Milner R., Ehlers C.L. N-methyl-d-aspartate receptor subunit expression in adult and adolescent brain following chronic ethanol exposure. Neuroscience 2010, 170(2):645-654.
57. Robinson T.E., Berridge K.C. The neural basis of drug craving: an incentive-sensitization theory of addiction. Brain Res Brain Res Rev 1993, 18(3):247-291.
58. Kalivas P.W. Interactions between dopamine and excitatory amino acids in behavioral sensitization to psychostimulants. Drug Alcohol Depend 1995, 37(2):95-100.
59. Dalley J.W., Everitt B.J., Robbins T.W. Impulsivity: compulsivity, and top-down cognitive control. Neuron 2011, 69(4):680-694.
60. Volkow N.D., Wang G.J., Telang F., Fowler J.S., Logan J., Childress A.R., et al. Cocaine cues and dopamine in dorsal striatum: mechanism of craving in cocaine addiction. J Neurosci 2006, 26(24):6583-6588.
61. Ramirez R.L., Varlinskaya E.I., Spear L.P. Effect of the selective NMDA NR2B antagonist: ifenprodil, on acute tolerance to ethanol-induced motor impairment in adolescent and adult rats. Alcohol Clin Exp Res 2011, 35(6):1149-1159.
62. Tirelli E., Laviola G., Adriani W. Ontogenesis of behavioral sensitization and conditioned place preference induced by psychostimulants in laboratory rodents. Neurosci Biobehav Rev 2003, 27(1-2):163-178.
63. Cole B.J., Robbins T.W. Effects of 6-hydroxydopamine lesions of the nucleus accumbens septi on performance of a 5-choice serial reaction time task in rats: implications for theories of selective attention and arousal. Behav Brain Res 1989, 33(2):165-179.
64. Lovic V., Saunders B.T., Yager L.M., Robinson T.E. Rats prone to attribute incentive salience to reward cues are also prone to impulsive action. Behav Brain Res 2011, 223(2):255-261.
65. Dillon G.M., Shelton D., McKinney A.P., Caniga M., Marcus J.N., Ferguson M.T., et al. Prefrontal cortex lesions and scopolamine impair attention performance of C57BL/6 mice in a novel 2-choice visual discrimination task. Behav Brain Res 2009, 204(1):67-76.
66. Galvan A., Poldrack R.A., Baker C.M., McGlennen K.M., London E.D. Neural correlates of response inhibition and cigarette smoking in late adolescence. Neuropsychopharmacology 2011, 36(5):970-978.
67. Sturman D.A., Mandell D.R., Moghaddam B. Adolescents exhibit behavioral differences from adults during instrumental learning and extinction. Behav Neurosci 2010, 124(1):16-25.
68. Perry J.L., Joseph J.E., Jiang Y., Zimmerman R.S., Kelly T.H., Darna M., et al. Prefrontal cortex and drug abuse vulnerability: translation to prevention and treatment interventions. Brain Res Rev 2011, 65(2):124-149.
69. Burton C.L., Noble K., Fletcher P.J. Enhanced incentive motivation for sucrose-paired cues in adolescent rats: possible roles for dopamine and opioid systems. Neuropsychopharmacology 2011, 36(8):1631-1643.
70. Lanier L.P., Isaacson R.L. Early developmental changes in the locomotor response to amphetamine and their relation to hippocampal function. Brain Res 1977, 126(3):567-575.
71. Mathews I.Z., McCormick C.M. Female and male rats in late adolescence differ from adults in amphetamine-induced locomotor activity: but not in conditioned place preference for amphetamine. Behav Pharmacol 2007, 18(7):641-650.
72. Becker J.B., Molenda H., Hummer D.L. Gender differences in the behavioral responses to cocaine and amphetamine. Implications for mechanisms mediating gender differences in drug abuse. Ann N Y Acad Sci 2001, 937:172-187.
73. Carroll M.E., Anker J.J. Sex differences and ovarian hormones in animal models of drug dependence. Horm Behav 2010, 58(1):44-56.
74. Belluzzi J.D., Lee A.G., Oliff H.S., Leslie F.M. Age-dependent effects of nicotine on locomotor activity and conditioned place preference in rats. Psychopharmacology (Berl) 2004, 174(3):389-395.
75. Vastola B.J., Douglas L.A., Varlinskaya E.I., Spear L.P. Nicotine-induced conditioned place preference in adolescent and adult rats. Physiol Behav 2002, 77(1):107-114.
76. Shram M.J., Funk D., Li Z., Lê A.D. Nicotine self-administration, extinction responding and reinstatement in adolescent and adult male rats: evidence against a biological vulnerability to nicotine addiction during adolescence. Neuropsychopharmacology 2008, 33(4):739-748.
77. Stolerman I.P., Mirza N.R., Hahn B., Shoaib M. Nicotine in an animal model of attention. Eur J Pharmacol 2000, 393(1-3):147-154.
78. Adriani W., Macrì S., Pacifici R., Laviola G. Peculiar vulnerability to nicotine oral self-administration in mice during early adolescence. Neuropsychopharmacology 2002, 27(2):212-224.
79. Dao J.M., McQuown S.C., Loughlin S.E., Belluzzi J.D., Leslie F.M. Nicotine alters limbic function in adolescent rat by a 5-HT1A receptor mechanism. Neuropsychopharmacology 2011, 36(7):1319-1331.
80. Chudasama Y., Passetti F., Rhodes S.E., Lopian D., Desai A., Robbins T.W. Dissociable aspects of performance on the 5-choice serial reaction time task following lesions of the dorsal anterior cingulate, infralimbic and orbitofrontal cortex in the rat: differential effects on selectivity, impulsivity and compulsivity. Behav Brain Res 2003, 146(1-2):105-119.
81. Murphy E.R., Dalley J.W., Robbins T.W. Local glutamate receptor antagonism in the rat prefrontal cortex disrupts response inhibition in a visuospatial attentional task. Psychopharmacology (Berl) 2005, 179(1):99-107.
82. Giedd J.N., Blumenthal J., Jeffries N.O., Castellanos F.X., Liu H., Zijdenbos A., et al. Brain development during childhood and adolescence: a longitudinal MRI study. Nat Neurosci 1999, 2(10):861-863.
83. van Eden C.G., Kros J.M., Uylings H.B. The development of the rat prefrontal cortex. Its size and development of connections with thalamus, spinal cord and other cortical areas. Prog Brain Res 1990, 85:169-183.
84. Huttenlocher P.R. Synapse elimination and plasticity in developing human cerebral cortex. Am J Ment Defic 1984, 88(5):488-496.
85. Galvan A., Hare T.A., Parra C.E., Penn J., Voss H., Glover G., et al. Earlier development of the accumbens relative to orbitofrontal cortex might underlie risk-taking behavior in adolescents. J Neurosci 2006, 26(25):6885-6892.
86. Ernst M., Pine D.S., Hardin M. Triadic model of the neurobiology of motivated behavior in adolescence. Psychol Med 2006, 36(3):299-312.
87. Steinberg L. A dual systems model of adolescent risk-taking. Dev Psychobiol 2010, 52(3):216-224.
88. Rogers R.D., Baunez C., Everitt B.J., Robbins T.W. Lesions of the medial and lateral striatum in the rat produce differential deficits in attentional performance. Behav Neurosci 2001, 115(4):799-811.
89. Badanich K.A., Adler K.J., Kirstein C.L. Adolescents differ from adults in cocaine conditioned place preference and cocaine-induced dopamine in the nucleus accumbens septi. Eur J Pharmacol 2006, 550(1-3):95-106.
90. Andersen S.L., Rutstein M., Benzo J.M., Hostetter J.C., Teicher M.H. Sex differences in dopamine receptor overproduction and elimination. Neuroreport 1997, 8(6):1495-1498.
91. Silvagni A., Barros V.G., Mura C., Antonelli M.C., Carboni E. Prenatal restraint stress differentially modifies basal and stimulated dopamine and noradrenaline release in the nucleus accumbens shell: an 'in vivo' microdialysis study in adolescent and young adult rats. Eur J Neurosci 2008, 28(4):744-758.
92. Laviola G., Pascucci T., Pieretti S. Striatal dopamine sensitization to d-amphetamine in periadolescent but not in adult rats. Pharmacol Biochem Behav 2001, 68(1):115-124.
93. Becker J.B. Gender differences in dopaminergic function in striatum and nucleus accumbens. Pharmacol Biochem Behav 1999, 64(4):803-812.
94. Thompson T.L., Moss R.L. Estrogen regulation of dopamine release in the nucleus accumbens: genomic- and nongenomic-mediated effects. J Neurochem 1994, 62(5):1750-1756.
95. Laconi M.R., Reggiani P.C., Penissi A., Yunes R., Cabrera R.J. Allopregnanolone modulates striatal dopamingergic activity of rats under different gonadal hormones conditions. Neurol Res 2007, 29(6):622-627.
96. Soubrie P. Serotonergic neurons and behavior. J Pharmacol 1986, 17(2):107-112.
97. Kuczenski R., Segal D. Concomitant characterization of behavioral and striatal neurotransmitter response to amphetamine using in vivo microdialysis. J Neurosci 1989, 9(6):2051-2065.
98. Harrison A.A., Everitt B.J., Robbins T.W. Central 5-HT depletion enhances impulsive responding without affecting the accuracy of attentional performance: interactions with dopaminergic mechanisms. Psychopharmacology (Berl) 1997, 133(4):329-342.
99. Sulzer D. How addictive drugs disrupt presynaptic dopamine neurotransmission. Neuron 2011, 69(4):628-649.
100. Kirshenbaum A.P., Jackson E.R., Brown S.J., Fuchs J.R., Miltner B.C., Doughty A.H. Nicotine-induced impulsive action: sensitization and attenuation by mecamylamine. Behav Pharmacol 2011, 22(3):207-221.
101. Grottick A.J., Higgins G.A. Effect of subtype selective nicotinic compounds on attention as assessed by the five-choice serial reaction time task. Behav Brain Res 2000, 117(1-2):197-208.