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Spontaneous appetence for wheel-running: a model of dependency on physical activity in rat

Published online by Cambridge University Press:  16 April 2020

Anthony Ferreira
Affiliation:
UMR 7593 CNRS, 91, Bvd de l'Hôpital, 75013Paris, France
Stéphanie Lamarque
Affiliation:
UMR 5541 CNRS, Université Victor Segalen, Bordeaux 2, France
Patrice Boyer
Affiliation:
UMR 7593 CNRS, 91, Bvd de l'Hôpital, 75013Paris, France
Fernando Perez-Diaz
Affiliation:
UMR 7593 CNRS, 91, Bvd de l'Hôpital, 75013Paris, France
Roland Jouvent
Affiliation:
UMR 7593 CNRS, 91, Bvd de l'Hôpital, 75013Paris, France
Charles Cohen-Salmon*
Affiliation:
UMR 7593 CNRS, 91, Bvd de l'Hôpital, 75013Paris, France
*
*Corresponding author. Tel.: +33 1 40 77 97 03. E-mail address: [email protected] (C. Cohen-Salmon).
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Abstract

According to human observations of a syndrome of physical activity dependence and its consequences, we tried to examine if running activity in a free activity paradigm, where rats had a free access to activity wheel, may present a valuable animal model for physical activity dependence and most generally to behavioral dependence. The pertinence of reactivity to novelty, a well-known pharmacological dependence predictor was also tested. Given the close linkage observed in human between physical activity and drugs use and abuse, the influence of free activity in activity wheels on reactivity to amphetamine injection and reactivity to novelty were also assessed. It appeared that (1) free access to wheel may be used as a valuable model for physical activity addiction, (2) two populations differing in activity amount also differed in dependence to wheel-running. (3) Reactivity to novelty did not appeared as a predictive factor for physical activity dependence (4) activity modified novelty reactivity and (5) subjects who exhibited a high appetence to wheel-running, presented a strong reactivity to amphetamine. These results propose a model of dependency on physical activity without any pharmacological intervention, and demonstrate the existence of individual differences in the development of this addiction. In addition, these data highlight the development of a likely vulnerability to pharmacological addiction after intense and sustained physical activity, as also described in man. This model could therefore prove pertinent for studying behavioral dependencies and the underlying neurobiological mechanisms. These results may influence the way psychiatrists view behavioral dependencies and phenomena such as doping in sport or addiction to sport itself.

Type
Original article
Copyright
Copyright © Elsevier Masson SAS 2006

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Footnotes

Abbreviations: HPA, Hypothalamo-Pituitary-Adrenal axis; HR, High Reactive (to novelty); HWR, Heavy Wheel Runners; LR, Low Reactive (to novelty); LWR, Light Wheel Runners.

References

Akimoto, K., Hamamura, T., Kazahaya, Y., Akiyama, K., Otsuki, S.Enhanced extracellular dopamine level may be the fundamental neuropharmacological basis of cross-behavioral sensitization between methamphetamine and cocaine—an in vivo dialysis study in freely moving rats Brain Res. 1990; 507:344346.CrossRefGoogle ScholarPubMed
Aquatias, S.D., Leroux, I., Stettinger, M.V., Valette-Vialard, C.Activités sportives, pratiques à risques, usages de substances dopantes et psychoactives : recherche sur la pratique moderne du sport In: Report For the French ministry of youth and sports, 1999 p. 60.Google Scholar
Babbini, M., Davis, W.M.Time-dose relationships for locomotor activity effects of morphine after acute or repeated treatment Br. J. Pharmacol. 1972; 46:213224.CrossRefGoogle ScholarPubMed
Benwell, M.E., Balfour, D.J.The effects of acute and repeated nicotine treatment on nucleus accumbens dopamine and locomotor activity Br. J. Pharmacol. 1992; 105:849856.CrossRefGoogle ScholarPubMed
Borer, K.T., Bestervelt, L.L., Mannheim, M., Brosamer, M.B., Thompson, M., Swamy, U.et al.Stimulation by voluntary exercise of adrenal glucocorticoid secretion in mature female hamsters Physiol. Behav. 1992; 51:713718.CrossRefGoogle ScholarPubMed
Chan, C.S., Grossman, H.Y.Psychological effects of running loss on consistent runners Percept. Mot. Skills 1988; 66:875883.CrossRefGoogle ScholarPubMed
Chapman, C.L., De Castro, J.M.Running addiction: measurement and associated psychological characteristics J. Sports Med. Phys. Fitness 1990; 30:283290.Google ScholarPubMed
Chennaoui, M., Gomez Merino, D., Lesage, J., Drogou, C., Guezennec, C.Y.Effects of moderate and intensive training on the Hypothalamo-Pituitary-Adrenal axis in rats Acta Physiol. Scand. 2002; 175:113121.CrossRefGoogle ScholarPubMed
Christie, M.J., Chesher, G.B.Physical dependence on physiologically released endogenous opiates Life Sci. 1982; 30:11731177.CrossRefGoogle ScholarPubMed
Dellu, F., Mayo, W., Vallee, M., Maccari, S., Piazza, P.V., Le Moal, M.et al.Behavioral reactivity to novelty during youth as a predictive factor of stress-induced corticosterone secretion in the elderly—a life-span study in rats Psychoneuroendocrinology 1996; 21:441453.CrossRefGoogle ScholarPubMed
Dellu, F., Piazza, P.V., 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; 34:136145.CrossRefGoogle ScholarPubMed
Dellu, F., Mayo, W., Piazza, P.V., Le Moal, M., Simon, H.Individual differences in behavioural responses to novelty in rats. Possible relationship with the sensation seeking trait in man Person. Indiv. Diff. 1993; 13:411418.CrossRefGoogle Scholar
Di Chiara, G., Imperato, A.Drugs abused by humans preferentially increase synaptic dopamine concentrations in the mesolimbic system of freely moving rats Proc. Natl. Acad. Sci. USA 1988; 85:52745278.CrossRefGoogle ScholarPubMed
Girard, I., Garland, T. Jr.Plasma corticosterone response to acute and chronic voluntary exercise in female house mice J. Appl. Physiol. 2002; 92:15531561.CrossRefGoogle ScholarPubMed
Gorriti, M.A., Rodriguez de Fonseca, F., Navarro, M., Palomo, T.Chronic (–)-delta9-tetrahydrocannabinol treatment induces sensitization to the psychomotor effects of amphetamine in rats Eur. J. Pharmacol. 1999; 365:133142.CrossRefGoogle ScholarPubMed
Hailey, B.J.A.B.L.A.Negative addiction in runners: a quantitative approach J. Sports Behav. 1982; 5:151154.Google Scholar
Holden, C.‘Behavioral' addictions: do they exist? Science 2001; 294:980982.CrossRefGoogle ScholarPubMed
Horger, B.A., Giles, M.K., Schenk, S.Preexposure to amphetamine and nicotine predisposes rats to self-administer a low dose of cocaine Psychopharmacology (Berlin) 1992; 107:271276.CrossRefGoogle ScholarPubMed
Horger, B.A., Shelton, K., Schenk, S.Preexposure sensitizes rats to the rewarding effects of cocaine Pharmacol. Biochem. Behav. 1990; 37:707711.CrossRefGoogle ScholarPubMed
Hunt, W.A., Barnett, L.W., Branch, L.G.Relapse rates in addiction programs J. Clin. Psychol. 1971; 27:455456.3.0.CO;2-R>CrossRefGoogle ScholarPubMed
Kagan, D.M.Addictive personality factors J. Psychol. 1987; 121:533538.CrossRefGoogle ScholarPubMed
Kagan, D.M., Squires, R.L.Addictive aspects of physical exercise J. Sports Med. Phys. Fitness 1985; 25:227237.Google ScholarPubMed
Kalivas, P.W., Duffy, P.Effect of acute and daily cocaine treatment on extracellular dopamine in the nucleus accumbens Synapse 1990; 5:4858.CrossRefGoogle ScholarPubMed
Kalivas, P.W., Weber, B.Amphetamine injection into the ventral mesencephalon sensitizes rats to peripheral amphetamine and cocaine J. Pharmacol. Exp. Ther. 1988; 245:10951102.Google ScholarPubMed
Ksir, C., Hakan, R., Hall, D.P. Jr., Kellar, K.J.Exposure to nicotine enhances the behavioral stimulant effect of nicotine and increases binding of [3H]acetylcholine to nicotinic receptors Neuropharmacology 1985; 24:527531.CrossRefGoogle Scholar
Lamarque, S., Taghzouti, K., Simon, H.Chronic treatment with Delta(9)-tetrahydrocannabinol enhances the locomotor response to amphetamine and heroin. Implications for vulnerability to drug addiction Neuropharmacology 2001; 41:118129.CrossRefGoogle ScholarPubMed
Le, A., Shaham, Y.Neurobiology of relapse to alcohol in rats Pharmacol. Ther. 2002; 94:137156.CrossRefGoogle ScholarPubMed
Lowenstein, W., Arvers, P., Gourarier, L., Porche, A.S., Cohen, J.M., Nordmann, F.et al.Physical and sports activities in the history of patients treated for addictions. Report 1999 of the study sponsored by the Ministry of Youth and Sports (France) Ann. Med. Interne (Paris) 2000; 151(Suppl A: A18A26.Google Scholar
Maccari, S., Piazza, P.V., Deminiere, J.M., Angelucci, L., Simon, H., Le Moal, M.Hippocampal type I and type II corticosteroid receptor affinities are reduced in rats predisposed to develop amphetamine self-administration Brain Res. 1991; 548:305309.CrossRefGoogle ScholarPubMed
Manley, S.J., Little, H.J.Enhancement of amphetamine- and cocaine-induced locomotor activity after chronic ethanol administration J. Pharmacol. Exp. Ther. 1997; 281:13301339.Google ScholarPubMed
Marinelli, M., Piazza, P.V.Interaction between glucocorticoid hormones, stress and psychostimulant drugs Eur. J. Neurosci. 2002; 16:387394.CrossRefGoogle ScholarPubMed
Marlatt, G.A.Do animal models provide a valid analogue for human drug lapse and relapse? Comment on Leri and Stewart (2002) Exp. Clin. Psychopharmacol. 2002; 10:359360. discussion 364–356].CrossRefGoogle Scholar
Miller, L.Predicting relapse and recovery in alcoholism and addiction: neuropsychology, personality, and cognitive style J. Subst. Abuse Treat. 1991; 8:277291.CrossRefGoogle ScholarPubMed
Mondin, G.W., Morgan, W.P., Piering, P.N., Stegner, A.J., Stotesbery, C.L., Trine, M.R.et al.Psychological consequences of exercise deprivation in habitual exercisers Med. Sci. Sports Exerc. 1996; 28:11991203.CrossRefGoogle ScholarPubMed
Morgan, W.P.Negative addiction in runners Physician Sports Med. 1979; 7:5770.Google ScholarPubMed
Nativ, A.P.J.C., Green, G.A.Lifestyle and health risks of collegiate athletes: a multi-center study Clin. J. Sport. Med. 1997; 7:262272.CrossRefGoogle Scholar
O'Brien, C.P.A range of research-based pharmacotherapies for addiction Science 1997; 278:6670.CrossRefGoogle ScholarPubMed
O'Brien, C.P., Lyons, F.Alcohol and the athlete Sports Med. 2000; 29:295300.CrossRefGoogle ScholarPubMed
Phillips, T.J., Dickinson, S., Burkhart-Kasch, S.Behavioral sensitization to drug stimulant effects in C57BL/6J and DBA/2J inbred mice Behav. Neurosci. 1994; 108:789803.CrossRefGoogle ScholarPubMed
Piazza, P.V., Deminiere, J.M., Le Moal, M., Simon, H.Factors that predict individual vulnerability to amphetamine self-administration Science 1989; 245:15111513.CrossRefGoogle ScholarPubMed
Piazza, P.V., Deminiere, J.M., le Moal, M., Simon, H.Stress- and pharmacologically-induced behavioral sensitization increases vulnerability to acquisition of amphetamine self-administration Brain Res. 1990; 514:2226.CrossRefGoogle ScholarPubMed
Piazza, P.V., Deroche, V., Deminiere, J.M., Maccari, S., Le Moal, M., Simon, H.Corticosterone in the range of stress-induced levels possesses reinforcing properties: implications for sensation-seeking behaviors Proc. Natl. Acad. Sci. USA 1993; 90:1173811742.CrossRefGoogle ScholarPubMed
Pierce, E.F.Exercise dependence syndrome in runners Sports Med. 1994; 18:149155.CrossRefGoogle ScholarPubMed
Pierce, E.F., Daleng, M.L., McGowan, R.W.Scores on exercise dependence among dancers Percept. Mot. Skills 1993; 76:531535.CrossRefGoogle ScholarPubMed
Pierce, E.F., Eastman, N.W., Tripathi, H.L., Olson, K.G., Dewey, W.L.Beta-endorphin response to endurance exercise: relationship to exercise dependence Percept. Mot. Skills 1993; 77:767770.CrossRefGoogle ScholarPubMed
Rainey, C.J., McKeown, R.E., Sargent, R.G., Valois, R.F.Patterns of tobacco and alcohol use among sedentary, exercising, non-athletic, and athletic youth J. Sch. Health 1996; 66:2732.CrossRefGoogle Scholar
Robinson, T.E., Berridge, K.C.The neural basis of drug craving: an incentive-sensitization theory of addiction Brain Res. Brain Res. Rev. 1993; 18:247291.CrossRefGoogle Scholar
Rossetti, Z.L., Melis, F., Carboni, S., Diana, M., Gessa, G.L.Alcohol withdrawal in rats is associated with a marked fall in extraneuronal dopamine Alcohol. Clin. Exp. Res. 1992; 16:529532.CrossRefGoogle ScholarPubMed
Schenk, S., Snow, S., Horger, B.A.Pre-exposure to amphetamine but not nicotine sensitizes rats to the motor activating effect of cocaine Psychopharmacology (Berlin) 1991; 103:6266.CrossRefGoogle Scholar
Schwenk, T.L.Alcohol use in adolescents: The scope of the problem and strategies for intervention Physician Sport Med. 2000; 28:7176.CrossRefGoogle ScholarPubMed
Scully, D.K.J., Meade, M.M., Graham, R., Dudgeon, K.Physical exercise and psychological well being: a critical review Br. J. Sports Med. 1998; 32:11120.CrossRefGoogle ScholarPubMed
Segal, D.S., Mandell, A.J.Long-term administration of d-amphetamine: progressive augmentation of motor activity and stereotypy Pharmacol. Biochem. Behav. 1974; 2:249255.CrossRefGoogle ScholarPubMed
Shalev, U., Grimm, J.W., Shaham, Y.Neurobiology of relapse to heroin and cocaine seeking: a review Pharmacol. Rev. 2002; 54:142.CrossRefGoogle ScholarPubMed
Tate, A.K., Petruzzello, S.J.Varying the intensity of acute exercise: implications for changes in affect J. Sports Med. Phys. Fitness 1995; 35:295302.Google ScholarPubMed
Thombs, D.L.A test of the perceived norms model to explain drinking patterns among university student athletes J. Am. Coll. Health 2000; 49:7583.CrossRefGoogle ScholarPubMed
Tricker, R.Painkilling drugs in collegiate athletics: knowledge, attitudes, and use of student athletes J. Drug Educ. 2000; 30:313324.CrossRefGoogle ScholarPubMed
Valadez, A., Schenk, S.Persistence of the ability of amphetamine preexposure to facilitate acquisition of cocaine self-administration Pharmacol. Biochem. Behav. 1994; 47:203205.CrossRefGoogle ScholarPubMed
Woolverton, W.L., Cervo, L., Johanson, C.E.Effects of repeated methamphetamine administration on methamphetamine self-administration in rhesus monkeys Pharmacol. Biochem. Behav. 1984; 21:737741.CrossRefGoogle ScholarPubMed
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