Relationship between impulsivity, hyperactivity and working memory: a differential analysis in the rat

Françoise Dellu-Hagedorn1
1Laboratoire de Neuropsychobiologie des Désadaptations, CNRS UMR 5541, Université Victor Segalen Bordeaux 2 - BP. 31, 146 rue Léo Saignat, 33076, Bordeaux cedex, France

Tóm tắt

Abstract Background Impulsivity is a behavioural trait that comprises several distinct processes. It is a key feature of many psychopathologies such as mania, addictive disorders or attention deficit-hyperactivity disorders. To date, the aspects of impulsiveness involved in these pathologies have not yet been explicitly defined. In these disorders, sensation or drug seeking and cognitive deficits are closely related, but the nature of these relationships remains largely unknown. A new animal model of impulsiveness based on spontaneous inter-individual differences is proposed here to help clarify the relationship between characteristic aspects of impulsive-related pathologies. Methods Rats were divided into sub-groups according to their scores in three operant tasks with varying degrees of behavioural inhibition, timing and motor vs. cognitive impulsivity demands. These tasks included a fixed consecutive number schedule (ability to complete an action to receive a reinforcer), a multiple fixed-interval/extinction schedule of reinforcement (high level of responding), and a delayed reward task (delay discounting). In addition, measurements of locomotor responses to novelty and to amphetamine in a circular corridor, and working memory in an 8-arm radial maze were obtained. Results Substantial behavioural inter-individual differences were observed in each task, whereas few inter-task relationships were found. Impulsive rats, as defined in a task requiring inhibition of premature responses, presented a higher increase in amphetamine-induced locomotion. Reduced working memory performance was only observed in hyperactive rats in an extinction schedule. Conclusion This novel approach shows that distinct aspects of impulsiveness and hyperactivity can be expressed based on large inter-individual differences that vary from poorly to highly adapted behaviours ones in a normal population of rats. Inhibitory deficit was related to a higher response to psychostimulants a characteristic of rats predisposed to amphetamine self-administration and related to higher limbic dopaminergic activity, whereas working memory capacity was only related to hyperactivity. This approach allows for the identification of particular individuals presenting distinct behavioural characteristics of impulsive-related psychopathologies. These individuals may be of great interest in the modelling of these disorders and the exploration of their neurobiological bases.

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Tài liệu tham khảo

Daruna JH, Barnes PA: The impulsive client: theory, research and treatment. A neurodevelopmental view of impulsivity. Edited by: McCown WG, Johnson JL, Shure MB. 1993, Washington DC , American Psychological Association

Evenden J: Impulsivity: a discussion of clinical and experimental findings. J Psychopharmacol. 1999, 13 (2): 180-192.

DSM-IV: American Psychiatric Association, Committee on Nomenclature and Statistics: Diagnostic and Statistical Manual of Mental Disorders. 1994, Washington, DC , American Psychiatric Press, 4th

Moeller FG, Barratt ES, Dougherty DM, Schmitz JM, Swann AC: Psychiatric aspects of impulsivity. Am J Psychiatry. 2001, 158 (11): 1783-1793. 10.1176/appi.ajp.158.11.1783.

Rubia K: The dynamic approach to neurodevelopmental psychiatric disorders: use of fMRI combined with neuropsychology to elucidate the dynamics of psychiatric disorders, exemplified in ADHD and schizophrenia. Behav Brain Res. 2002, 130 (1-2): 47-56. 10.1016/S0166-4328(01)00437-5.

Taylor E: Clinical foundations of hyperactivity research. Behav Brain Res. 1998, 94 (1): 11-24. 10.1016/S0166-4328(97)00165-4.

Volkow ND, Fowler JS: Addiction, a disease of compulsion and drive: involvement of the orbitofrontal cortex. Cereb Cortex. 2000, 10 (3): 318-325. 10.1093/cercor/10.3.318.

Jentsch JD, Taylor JR: Impulsivity resulting from frontostriatal dysfunction in drug abuse: implications for the control of behavior by reward-related stimuli. Psychopharmacology (Berl). 1999, 146 (4): 373-390. 10.1007/PL00005483.

Disney ER, Elkins IJ, McGue M, Iacono WG: Effects of ADHD, conduct disorder, and gender on substance use and abuse in adolescence. Am J Psychiatry. 1999, 156 (10): 1515-1521.

Young SE, Mikulich SK, Goodwin MB, Hardy J, Martin CL, Zoccolillo MS, Crowley TJ: Treated delinquent boys' substance use: onset, pattern, relationship to conduct and mood disorders. Drug Alcohol Depend. 1995, 37 (2): 149-162. 10.1016/0376-8716(94)01069-W.

Wilens TE: Attention-deficit/hyperactivity disorder and the substance use disorders: the nature of the relationship, subtypes at risk, and treatment issues. Psychiatr Clin North Am. 2004, 27 (2): 283-301. 10.1016/S0193-953X(03)00113-8.

Zuckerman M, Neeb M: Sensation seeking and psychopathology. Psychiatry Res. 1979, 1 (3): 255-264. 10.1016/0165-1781(79)90007-6.

Zuckerman M: P-impulsive sensation seeking and its behavioral, psychophysiological and biochemical correlates. Neuropsychobiology. 1993, 28 (1-2): 30-36.

Lesieur HR, Rosenthal RJ: Pathological gambling : a review of the literature. J Gambl Stud. 1991, 7 (1): 5-39. 10.1007/BF01019763.

Pedinielli JL, Rouan G, Bertagne P: Psychopathologie des addictions. 1997, Paris , Nodules PUF

Baddeley AD: Working memory. 1986, Oxford , Oxford University Press

Lenzenweger MF, Clarkin JF, Fertuck EA, Kernberg OF: Executive neurocognitive functioning and neurobehavioral systems indicators in borderline personality disorder: a preliminary study. J Personal Disord. 2004, 18 (5): 421-438. 10.1521/pedi.18.5.421.51323.

Stevens A, Burkhardt M, Hautzinger M, Schwarz J, Unckel C: Borderline personality disorder: impaired visual perception and working memory. Psychiatry Res. 2004, 125 (3): 257-267. 10.1016/j.psychres.2003.12.011.

Dinn WM, Harris CL, Aycicegi A, Greene PB, Kirkley SM, Reilly C: Neurocognitive function in borderline personality disorder. Prog Neuropsychopharmacol Biol Psychiatry. 2004, 28 (2): 329-341. 10.1016/j.pnpbp.2003.10.012.

Barkley RA: Behavioral inhibition, sustained attention, and executive functions: constructing a unifying theory of ADHD. Psychol Bull. 1997, 121 (1): 65-94. 10.1037/0033-2909.121.1.65.

Adler CM, Holland SK, Schmithorst V, Tuchfarber MJ, Strakowski SM: Changes in neuronal activation in patients with bipolar disorder during performance of a working memory task. Bipolar Disord. 2004, 6 (6): 540-549. 10.1111/j.1399-5618.2004.00117.x.

Donaldson S, Goldstein LH, Landau S, Raymont V, Frangou S: The Maudsley Bipolar Disorder Project: the effect of medication, family history, and duration of illness on IQ and memory in bipolar I disorder. J Clin Psychiatry. 2003, 64 (1): 86-93.

Sweeney JA, Kmiec JA, Kupfer DJ: Neuropsychologic impairments in bipolar and unipolar mood disorders on the CANTAB neurocognitive battery. Biol Psychiatry. 2000, 48 (7): 674-684. 10.1016/S0006-3223(00)00910-0.

McGrath J, Chapple B, Wright M: Working memory in schizophrenia and mania: correlation with symptoms during the acute and subacute phases. Acta Psychiatr Scand. 2001, 103 (3): 181-188. 10.1034/j.1600-0447.2001.00114.x.

Peterson JB, Finn PR, Pihl RO: Cognitive dysfunction and the inherited predisposition to alcoholism. J Stud Alcohol. 1992, 53 (2): 154-160.

Finn PR: Motivation, working memory, and decision making: a cognitive-motivational theory of personality vulnerability to alcoholism. Behav Cogn Neurosci Rev. 2002, 1: 183-205. 10.1177/1534582302001003001.

Finn PR, Justus A, Mazas C, Steinmetz JE: Working memory, executive processes and the effects of alcohol on Go/No-Go learning: testing a model of behavioral regulation and impulsivity. Psychopharmacology (Berl). 1999, 146 (4): 465-472. 10.1007/PL00005492.

Deckel AW, Hesselbrock V: Behavioral and cognitive measurements predict scores on the MAST: a 3-year prospective study. Alcohol Clin Exp Res. 1996, 20 (7): 1173-1178. 10.1111/j.1530-0277.1996.tb01107.x.

Aytaclar S, Tarter RE, Kirisci L, Lu S: Association between hyperactivity and executive cognitive functioning in childhood and substance use in early adolescence. J Am Acad Child Adolesc Psychiatry. 1999, 38 (2): 172-178. 10.1097/00004583-199902000-00016.

Evenden JL: Varieties of impulsivity. Psychopharmacology (Berl). 1999, 146 (4): 348-361. 10.1007/PL00005481.

Winstanley CA, Dalley JW, Theobald DE, Robbins TW: Fractionating impulsivity: contrasting effects of central 5-HT depletion on different measures of impulsive behavior. Neuropsychopharmacology. 2004, 29 (7): 1331-1343. 10.1038/sj.npp.1300434.

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 (1): 31-39. 10.1016/S0149-7634(99)00058-5.

Tripp G, Alsop B: Sensitivity to reward delay in children with attention deficit hyperactivity disorder (ADHD). J Child Psychol Psychiatry. 2001, 42 (5): 691-698. 10.1017/S0021963001007430.

McCourt WF, Gurrera RJ, Cutter HS: Sensation seeking and novelty seeking. Are they the same?. J Nerv Ment Dis. 1993, 181 (5): 309-312.

Dellu F, Mayo W, Piazza PV, Le Moal M, Simon H: Individual differences in behavioral responses to novelty in rats. Possible relationship with the sensation-seeking trait in man. Pers Individ Dif. 1993, 14: 411-418. 10.1016/0191-8869(93)90069-F.

Dellu F, Piazza PV, Mayo W, Le Moal M, Simon H: Novelty-seeking in rats - Biobehavioral characteristics and possible relationship with the sensation-seeking trait in man. Neuropsychobiology. 1996, 34 (3): 136-145.

Piazza PV, Deminiere JM, Le Moal M, Simon H: Factors that predict individual vulnerability to amphetamine self-administration. Science. 1989, 245 (4925): 1511-1513.

Dellu-Hagedorn F: Spontaneous individual differences in cognitive performances of young adult rats predict locomotor response to amphetamine. Neurobiol Learn Mem. 2005, 83: 43-47. 10.1016/j.nlm.2004.07.002.

Dellu-Hagedorn F, Trunet S, Simon H: Impulsivity in youth predicts early age-related cognitive deficits in rats. Neurobiol Aging. 2004, 25: 525-537. 10.1016/j.neurobiolaging.2003.06.006.

Evenden JL: The pharmacology of impulsive behaviour in rats II: the effects of amphetamine, haloperidol, imipramine, chlordiazepoxide and other drugs on fixed consecutive number schedules (FCN 8 and FCN 32). Psychopharmacology (Berl). 1998, 138 (3-4): 283-294. 10.1007/s002130050673.

Berger DF, Sagvolden T: Sex differences in operant discrimination behaviour in an animal model of attention-deficit hyperactivity disorder. Behav Brain Res. 1998, 94 (1): 73-82. 10.1016/S0166-4328(97)00171-X.

Sagvolden T, Hendley ED, Knardahl S: Behavior of hypertensive and hyperactive rat strains: hyperactivity is not unitarily determined. Physiol Behav. 1992, 52 (1): 49-57. 10.1016/0031-9384(92)90432-2.

Evenden JL, Ryan CN: The pharmacology of impulsive behaviour in rats: the effects of drugs on response choice with varying delays of reinforcement. Psychopharmacology (Berl). 1996, 128 (2): 161-170. 10.1007/s002130050121.

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. 10.1037/0735-7044.117.4.695.

Olton DS, Samuelson RJ: Remembrance of place passed: spatial memory in rats. J Exp Psychol. 1976, 2: 97-116.

Benjamini Y, Hochberg Y: Controlling the False Discovery Rate: a practical and powerful approach to multiple testing. J R Stat Soc [Ser B]. 1995, 57 (1): 289-300.

Barratt ES, Patton JH: Impulsivity: cognitive, behavioral and psychophysiological correlates. Biological bases of sensation-seeking, impulsivity, and anxiety. Edited by: Zuckerman M. 1983, Hillsdale, NJ , Lawrence Erlbaum Associates, 77-116.

Sagvolden T, Aase H, Zeiner P, Berger D: Altered reinforcement mechanisms in attention-deficit/hyperactivity disorder. Behav Brain Res. 1998, 94 (1): 61-71. 10.1016/S0166-4328(97)00170-8.

Ferster CB, Skinner BF: Schedules of reinforcement. 1957, Englewood Cliffs, NJ , Prentice-Hall

Hata T, Okaichi H: Medial prefrontal cortex and precision of temporal discrimination: a lesion, microinjection, and microdialysis study. Neurosci Res. 2004, 49 (1): 81-89. 10.1016/j.neures.2004.02.005.

Bizot J, Le Bihan C, Puech AJ, Hamon M, Thiebot M: Serotonin and tolerance to delay of reward in rats. Psychopharmacology (Berl). 1999, 146 (4): 400-412. 10.1007/PL00005485.

Evenden JL, Ryan CN: The pharmacology of impulsive behaviour in rats VI: the effects of ethanol and selective serotonergic drugs on response choice with varying delays of reinforcement. Psychopharmacology (Berl). 1999, 146 (4): 413-421. 10.1007/PL00005486.

Thiebot MH, Le Bihan C, Soubrie P, Simon P: Benzodiazepines reduce the tolerance to reward delay in rats. Psychopharmacology. 1985, 86 (1-2): 147-152. 10.1007/BF00431700.

Poulos CX, Le AD, Parker JL: Impulsivity predicts individual susceptibility to high levels of alcohol self-administration. Behav Pharmacol. 1995, 6 (8): 810-814.

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 (7): 639-651. 10.1016/j.neubiorev.2003.08.007.

Cardinal RN, Robbins TW, Everitt BJ: The effects of d-amphetamine, chlordiazepoxide, alpha-flupenthixol and behavioural manipulations on choice of signalled and unsignalled delayed reinforcement in rats. Psychopharmacology (Berl). 2000, 152 (4): 362-375. 10.1007/s002130000536.

Cardinal RN, Pennicott DR, Sugathapala CL, Robbins TW, Everitt BJ: Impulsive choice induced in rats by lesions of the nucleus accumbens core. Science. 2001, 292 (5526): 2499-2501. 10.1126/science.1060818.

McDonald J, Schleifer L, Richards JB, de Wit H: Effects of THC on behavioral measures of impulsivity in humans. Neuropsychopharmacology. 2003, 28 (7): 1356-1365. 10.1038/sj.npp.1300176.

Johansen EB, Sagvolden T: Response disinhibition may be explained as an extinction deficit in an animal model of attention-deficit/hyperactivity disorder (ADHD). Behav Brain Res. 2004, 149 (2): 183-196. 10.1016/S0166-4328(03)00229-8.

Bardo MT, Donohew RL, Harrington NG: Psychobiology of novelty seeking and drug seeking behavior. Behav Brain Res. 1996, 77 (1-2): 23-43. 10.1016/0166-4328(95)00203-0.

Zuckerman M: Sensation seeking: the balance between risk and reward. Self-regulatory behavior and risk-taking: causes and consequences. Edited by: Lipsitt LP, Mitnick LL. 1991, Norwood, NJ , Ablex Publishing Corp., 143-152.

Desrichard O, Denarie V: Sensation seeking and negative affectivity as predictors of risky behaviors: a distinction between occasional versus frequent risk-taking. Addict Behav. 2005, 30 (7): 1449-1453. 10.1016/j.addbeh.2005.01.011.

Villemarette-Pittman NR, Stanford MS, Greve KW: Language and executive function in self-reported impulsive aggression. Pers Individ Dif. 2003, 34: 1533-1544. 10.1016/S0191-8869(02)00136-8.

Whitney P, Jameson T, Hinson JM: Impulsiveness and executive control of working memory. Pers Individ Dif. 2004, 37: 417-428. 10.1016/j.paid.2003.09.013.