Individual differences in novelty-seeking behavior in spontaneously hypertensive rats: Enhanced sensitivity to the reinforcing effect of methylphenidate in the high novelty-preferring subpopulation

Journal of Neuroscience Methods

Volumn 252, Issue , 2015, Pages 48-54

  dela Peña, Ike ^a   Gonzales, Edson Luck ^b   de la Peña, June Bryan ^a   Kim, Bung Nyun ^c   Han, Doug Hyun ^d   Shin, Chan Young ^b   Cheong, Jae Hoon ^a  

^a Sahmyook University   (South Korea)

^b Konkuk University School of Medicine   (South Korea)

^c Seoul National University Hospital   (South Korea)

^d Chung Ang University College of Medicine   (South Korea)

Author keywords

Addiction; ADHD; Methylphenidate; Novelty seeking; SHR

Indexed keywords

METHYLPHENIDATE; CENTRAL STIMULANT AGENT;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ATTENTION DEFICIT DISORDER; CONTROLLED STUDY; DRUG ABUSE; DRUG SELF ADMINISTRATION; EXPLORATORY BEHAVIOR; LOCOMOTION; MALE; NONHUMAN; NOVELTY SEEKING BEHAVIOR; OPEN FIELD TEST; PRIORITY JOURNAL; RAT; SPONTANEOUSLY HYPERTENSIVE RAT; WISTAR KYOTO RAT; ANIMAL; DISEASE MODEL; DRUG EFFECTS; INDIVIDUALITY; INSTRUMENTAL CONDITIONING; MOTOR ACTIVITY; PATHOPHYSIOLOGY; REINFORCEMENT;

ANIMALS; ATTENTION DEFICIT DISORDER WITH HYPERACTIVITY; CENTRAL NERVOUS SYSTEM STIMULANTS; CONDITIONING, OPERANT; DISEASE MODELS, ANIMAL; EXPLORATORY BEHAVIOR; INDIVIDUALITY; MALE; METHYLPHENIDATE; MOTOR ACTIVITY; RATS; RATS, INBRED SHR; RATS, INBRED WKY; REINFORCEMENT (PSYCHOLOGY); SELF ADMINISTRATION;

EID: 84944708864     PISSN: 01650270     EISSN: 1872678X     Source Type: Journal    
DOI: 10.1016/j.jneumeth.2014.08.019     Document Type: Article

References (66)

1. Adriani W., Caprioli A., Granstrem O., Carli M., Laviola G. The spontaneously hypertensive-rat as an animal model of ADHD: evidence for impulsive and non-impulsive subpopulations. Neurosci Biobehav Rev 2003, 27:639-651.
2. Anckarsäter H., Stahlberg O., Larson T., Hakansson C., Jutblad S.B., Niklasson L., et al. The impact of ADHD and autism spectrum disorders on temperament, character, and personality development. Am J Psychiatry 2006, 163(7):1239-1244.
3. Antunes M., Biala G. The novel object recognition memory: neurobiology, test procedure, and its modifications. Cogn Process 2012, 13:93-110.
4. Becker K., Laucht M., El-Faddagh M., Schmidt M. The dopamine D4 receptor gene exon III polymorphism is associated with novelty seeking in 15-year-old males from a high-risk community sample. J Neural Transm 2005, 112:847-858.
5. Belin D., Mar A.C., Dalley J.W., Robbins T.W., Everitt B.J. High impulsivity predicts the switch to compulsive cocaine-taking. Science 2008, 320:1352-1355.
6. Belin D., Berson N., Balado E., Piazza P.V., Deroche-Gamonet V. High-novelty-preference rats are predisposed to compulsive cocaine self-administration. Neuropsychopharmacology 2011, 36:569-579.
7. Bernardi S., Faraone S.V., Cortese S., Kerridge B.T., Pallanti S., Wang S., et al. The lifetime impact of attention deficit hyperactivity disorder: results from the National Epidemiologic Survey on Alcohol and Related Conditions (NESARC). Psychol Med 2012, 42:875-887.
8. Biederman J., Faraone S. Current concepts on the neurobiology of attention-deficit/hyperactivity disorder. J Atten Disord 2001, 6:S7-S16.
9. Biederman J., Wilens T., Mick E., Faraone S.V., Weber W., Curtis S., et al. Is ADHD a risk factor for psychoactive substance use disorders? Findings from a four-year prospective follow-up study. J Am Acad Child Adolesc Psychiatry 1997, 36:21-29.
10. Biederman J., Monuteaux M., Spencer T., Wilens T., MacPherson H., Faraone S. Stimulant therapy and risk for subsequent substance use disorders in male adults with ADHD: a naturalistic controlled 10-year follow-up study. Am J Psychiatry 2008, 165:597-603.
11. Bienkowski P., Koros E., Kostowski W. Novelty-seeking behaviour and operant oral ethanol self-administration in Wistar rats. Alcohol Alcohol 2001, 36(6):525-528.
12. Bizot J.-C., Le Bihan C., Puech A.J., Hamon M., Thiébot M.-H. Serotonin and tolerance to delay of reward in rats. Psychopharmacology 1999, 146:400-412.
13. Blanchard M.M., Mendelsohn D., Stamp J.A. The HR/LR model: further evidence as an animal model of sensation seeking. Neurosci Biobehav Rev 2009, 33:1145-1154.
14. Cain M.E., Saucier D.A., Bardo M.T. Novelty seeking and drug use: contribution of an animal model. Exp Clin Psychopharmacol 2005, 13:367.
15. Chilcoat H.D., Breslau N. Pathways from ADHD to early drug use. J Am Acad Child Adolesc Psychiatry 1999, 38:1347-1354.
16. Cloninger C.R. A unified biosocial theory of personality and its role in the development of anxiety states. Psychiatr Dev 1985, 4:167-226.
17. Crunelle C.L., Veltman D.J., van Emmerik-van Oortmerssen K., Booij J., van den Brink W. Impulsivity in adult ADHD patients with and without cocaine dependence. Drug Alcohol Depend 2013, 129:18-24.
18. Dalley J.W., Mar A.C., Economidou D., Robbins T.W. Neurobehavioral mechanisms of impulsivity: fronto-striatal systems and functional neurochemistry. Pharmacol Biochem Behav 2008, 90:250-260.
19. Dawe S., Loxton N.J. The role of impulsivity in the development of substance use and eating disorders. Neurosci Biobehav Rev 2004, 28:343-351.
20. dela Peña I.C., Ahn H.S., Choi J.Y., Shin C.Y., Ryu J.H., Cheong J.H. Reinforcing effects of methamphetamine in an animal model of attention-deficit/hyperactivity disorder - the spontaneously hypertensive rat. Behav Brain Funct 2010, 9(6):72.
21. dela Peña I.C., Ahn H.S., Choi J.Y., Shin C.Y., Ryu J.H., Cheong J.H. Methylphenidate self-administration and conditioned place preference in an animal model of attention-deficit hyperactivity disorder: the spontaneously hypertensive rat. Behav Pharmacol 2011, 22:31-39.
22. dela Peña I.C., Ahn H.S., Ryu J.H., Shin C.Y., Park I.H., Cheong J.H. Conditioned place preference studies with atomoxetine in an animal model of ADHD: effects of previous atomoxetine treatment. Eur J Pharmacol 2011, 667:238-241.
23. dela Peña I., Yoon S.Y., Lee J.C., dela Peña J.B., Sohn A.R., Ryu J.H., et al. Methylphenidate treatment in the spontaneously hypertensive rat: influence on methylphenidate self-administration and reinstatement in comparison with Wistar rats. Psychopharmacology (Berlin) 2012, 221:217-226.
24. dela Peña I.C., Jeon S.J., Lee E., Ryu J.H., Shin C.Y., Noh M., et al. Neuronal development genes are key elements mediating the reinforcing effects of methamphetamine, amphetamine and methylphenidate. Psychopharmacology (Berlin) 2013, 230(3):399-413.
25. dela Peña I., Kim B.N., Han D.H., Kim Y., Cheong J.H. Abuse and dependence liability analysis of methylphenidate in the spontaneously hypertensive rat model of attention-deficit/hyperactivity disorder (ADHD): what have we learned?. Arch Pharm Res 2013, 36:400-410.
26. Dulawa S.C., Grandy D.K., Low M.J., Paulus M.P., Geyer M.A. Dopamine D4 receptor-knock-out mice exhibit reduced exploration of novel stimuli. J Neurosci 1999, 19:9550-9556.
27. Ebstein R.P., Novick O., Umansky R., Priel B., Osher Y., Blaine D., et al. Dopamine D4 receptor (D4DR) exon III polymorphism associated with the human personality trait of novelty seeking. Nat Genet 1996, 12:78-80.
28. Everitt B.J., Belin D., Economidou D., Pelloux Y., Dalley J.W., Robbins T.W. Neural mechanisms underlying the vulnerability to develop compulsive drug-seeking habits and addiction. Philos Trans R Soc Lond B Biol Sci 2008, 363:3125-3135.
29. Fredericks E.M., Kollins S.H. A pilot study of methylphenidate preference assessment in children diagnosed with attention-deficit/hyperactivity disorder. J Child Adolesc Psychopharmacol 2005, 15:729-741.
30. Gerra G., Avanzini P., Zaimovic A., Sartori R., Bocchi C., Timpano M., et al. Neurotransmitters, neuroendocrine correlates of sensation-seeking temperament in normal humans. Neuropsychobiology 1999, 39:207-213.
31. 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 1997, 133:329-342.
32. Heal D.J., Cheetham S.C., Smith S.L. The neuropharmacology of ADHD drugs in vivo: insights on efficacy and safety. Neuropharmacology 2009, 57:608-618.
33. Jaffe S.L. Intranasal abuse of prescribed methylphenidate by an alcohol and drug abusing adolescent with ADHD. J Am Acad Child Adolesc Psychiatry 1991, 30:773-775.
34. Jama A., Cecchi M., Calvo N., Watson S., Akil H. Inter-individual differences in novelty-seeking behavior in rats predict differential responses to desipramine in the forced swim test. Psychopharmacology 2008, 198:333-340.
35. Katusic S.K., Barbaresi W.J., Colligan R.C., Weaver A.L., Leibson C.L., Jacobsen S.J. Psychostimulant treatment and risk for substance abuse among young adults with a history of attention-deficit/hyperactivity disorder: a population-based, birth cohort study. J Child Adolesc Psychopharmacol 2005, 15:764-776.
36. Klebaur J., Bevins R.A., Segar T., Bardo M. Individual differences in behavioral responses to novelty and amphetamine self-administration in male and female rats. Behav Pharmacol 2001, 12:267-275.
37. Kollins S.H., English J., Robinson R., Hallyburton M., Chrisman A.K. Reinforcing and subjective effects of methylphenidate in adults with and without attention deficit hyperactivity disorder (ADHD). Psychopharmacology 2009, 204:73-83.
38. Lee S.S., Humphreys K.L., Flory K., Liu R., Glass K. Prospective association of childhood attention-deficit/hyperactivity disorder (ADHD) and substance use and abuse/dependence: a meta-analytic review. Clin Psychol Rev 2011, 31:328-341.
39. Marusich J.A., Bardo M.T. Differences in impulsivity on a delay discounting task predict self-administration of a low unit dose of methylphenidate in rats. Behav Pharmacol 2009, 20:447.
40. Matthews I.Z., Morrissey M.D., McCormick C.M. Individual differences in activity predict locomotor activity and conditioned place preference to amphetamine in both adolescent and adult rats. Pharmacol Biochem Behav 2010, 95(1):63-71.
41. Moeller F.G., Barratt E.S., Dougherty D.M., Schmitz J.M., Swann A.C. Psychiatric aspects of impulsivity. Am J Psychiatry 2001, 158:1783-1793.
42. Nair J., Topka M., Abbas K., Isenschmid M., Rainer G. Tree shrews (Tupaia belangeri) exhibit novelty preference in the novel location memory task with 24-h retention periods. Front Psychol 2014, 14(5):303.
43. Nigg J.T., Willcutt E.G., Doyle A.E., Sonuga-Barke E.J.S. Causal heterogeneity in attention-deficit/hyperactivity disorder: do we need neuropsychologically impaired subtypes?. Biol Psychiatry 2005, 57:1224-1230.
44. Parran T.V., Jasinski D.R. Intravenous methylphenidate abuse: prototype for prescription drug abuse. Arch Intern Med 1991, 151:781-783.
45. Perry J.L., Carroll M.E. The role of impulsive behavior in drug abuse. Psychopharmacology 2008, 200:1-26.
46. Piazza P.V., Deminière J.-M., Le Moal M., Simon H. Factors that predict individual vulnerability to amphetamine self-administration. Science 1989, 245(4925):1511-1513.
47. Piazza P.V., Deminière J.M., Maccari S., Mormede P., Le Moal M., Simon H. Individual reactivity to novelty predicts probability of amphetamine self-administration. Behav Pharmacol 1990, 1:339-345.
48. Piazza P.V., Deroche-Gamonent V., Rouge-Pont F., Le Moal M. Vertical shifts in self-administration dose-response functions predict a drug-vulnerable phenotype predisposed to addiction. J Neurosci 2000, 20:4226-4232.
49. Pogorelov V.M., Rodriguiz R.M., Insco M.L., Caron M.G., Wetsel W.C. Novelty seeking and stereotypic activation of behavior in mice with disruption of the Dat1 gene. Neuropsychopharmacology 2005, 30:1818-1831.
50. Poulin C. From attention-deficit/hyperactivity disorder to medical stimulant use to the diversion of prescribed stimulants to non-medical stimulant use: connecting the dots. Addiction 2007, 102:740-751.
51. Purper-Ouakil D., Cortese S., Wohl M., Aubron V., Orejarena S., Michel G., et al. Temperament and character dimensions associated with clinical characteristics and treatment outcome in attention-deficit/hyperactivity disorder boys. Compr Psychiatry 2010, 51:286-292.
52. Purper-Ouakil D., Ramoz N., Lapagnol-Bestel A., Gorwood P., Simonneau M. Neurobiology of attention deficit/hyperactivity disorder. Pediatr Res 2011, 69:69R-76R.
53. Rebec G.V., Grabner C.P., Johnson M., Pierce R.C., Bardo M.T. Transient increases in catecholaminergic activity in medial prefrontal cortex and nucleus accumbens shell during novelty. Neuroscience 1996, 76:707-714.
54. Rebec G.V., Christensen J.R.C., Guerra C., Bardo M.T. Regional and temporal differences in real-time dopamine efflux in the nucleus accumbens during free-choice novelty. Brain Res 1997, 776:61-67.
55. Robbins T.W. The 5-choice serial reaction time task: behavioral pharmacology and functional neurochemistry. Psychopharmacology 2002, 163:362-380.
56. Russell V.A., Sagvolden T., Johansen E.B. Animal models of attention-deficit hyperactivity disorder. Behav Brain Funct 2005, 1:9.
57. Sagvolden T. Behavioral validation of the spontaneously hypertensive rat (SHR) as an animal model of attention-deficit/hyperactivity disorder (AD/HD). Neurosci Biobehav Rev 2000, 24:31-39.
58. Sagvolden T., Russell V.A., Aase H., Johansen E.B., Farshbaf M. Rodent models of attention-deficit/hyperactivity disorder. Biol Psychiatry 2005, 57:1239-1247.
59. Sara S.J., Dyon-Laurent C., Hervé A. Novelty seeking behavior in the rat is dependent upon the integrity of the noradrenergic system. Brain Res Cogn Brain Res 1995, 2(3):181-187.
60. Thiel C.M., Müller C.P., Huston J.P., Schwarting R.K.W. High versus low reactivity to a novel environment: behavioural, pharmacological and neurochemical assessments. Neuroscience 1999, 93:243-251.
61. Vendruscolo L.F., Izidio G.S., Takahashi R.N. Drug reinforcement in a rat model of attention deficit/hyperactivity disorder - the Spontaneously Hypertensive Rat (SHR). Curr Drug Abuse Rev 2009, 2:177-183.
62. Wilens T.E., Morrison N.R. The intersection of attention-deficit/hyperactivity disorder and substance abuse. Curr Opin Psychiatry 2011, 24(4):280-285.
63. Wilens T.E., Gignac M., Swezey A., Monuteaux M.C., Biederman J. Characteristics of adolescents and young adults with ADHD who divert or misuse their prescribed medications. J Am Acad Child Adolesc Psychiatry 2006, 45:408-414.
64. Wilens T.E., Adler L.A., Adams J., Sgambati S., Rotrosen J., Sawtelle R., et al. Misuse and diversion of stimulants prescribed for ADHD: a systematic review of the literature. J Am Acad Child Adolesc Psychiatry 2008, 47:21-31.
65. Wills T.A., Vaccaro D., McNamara G. Novelty seeking, risk taking, and related constructs as predictors of adolescent substance use: an application of Cloninger's theory. J Subst Abuse 1994, 6:1-20.
66. Zhu J., Bardo M.T., Bruntz R.C., Stairs D.J., Dwoskin L.P. Individual differences in response to novelty predict prefrontal cortex dopamine transporter function and cell surface expression. Eur J Neurosci 2007, 26:717-728.