Advertisement

Opposing Short-Term and Long-Term Effects of Amphetamine Sensitization on Operant Responding for a Food Reinforcer

  • Rebecca E. Nordquist
  • Pieter Voorn
  • J. G. de Mooij-van Malsen
  • R. N. J. M. A. Joosten
  • Cyriel M. A. Pennartz
  • Louk J. M. J. Vanderschuren
Conference paper
Part of the Advances in Behavioral Biology book series (ABBI, volume 56)

1. Abstract

Repeated exposure to drugs of abuse causes behavioral sensitization, a progressive and persistent increase in the psychomotor response to drugs. Behavioral sensitization is accompanied by altered responses to motivational stimuli and a wide array of neuroadaptations in limbic corticostriatal systems. Interestingly, both the behavioral and neural changes show markedly different effects when tested during induction of sensitization or after a period of drug abstinence. To directly compare short- and long-term effects of repeated drug administration on motivational behavior, we assessed performance of an operant conditioning task in rats either following a three week period of abstinence from amphetamine treatment or during the induction of amphetamine sensitization. We observed a biphasic response pattern for reward, in which operant responding was persistently potentiated following abstinence but transiently decreased when animals were tested during induction. We propose that drug-induced changes in the function of reward-related cortico-striatal systems underlie this pattern of sensitization-induced changes in motivated behavior.

Keywords

Nucleus Accumbens Ventral Tegmental Area Ventral Striatum Lever Press Behavioral Sensitization 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

6. References

  1. Bamford, N.S., Zhang, H., Schmitz, Y., Wu, N.-P., Cepeda, C., Levine, M.S., Schmauss, C., Zakharenko, S.S., Zablow, L., and Sulzer, D., 2004, Heterosynaptic dopamine neurotransmission selects sets of corticostriatal terminals, Neuron. 42:653–663.PubMedCrossRefGoogle Scholar
  2. Berendse, H.W., Galis-de Graaf, Y., and Groenewegen, H.J., 1992, Topographical organization and relationship with ventral striatal compartments of prefrontal corticostriatal projections in the rat, J. Comp. Neurol. 316:314–347.PubMedCrossRefGoogle Scholar
  3. Berke, J.D., and Hyman, S.E., 2000, Addiction, dopamine, and the molecular mechanisms of memory, Neuron. 25:515–532.PubMedCrossRefGoogle Scholar
  4. Canales, J.J., and Graybiel, A.M., 2000, A measure of striatal function predicts motor stereotypy, Nat. Neurosci. 3:377–383.PubMedCrossRefGoogle Scholar
  5. Cancela, L.M., Basso, A.M., Martijena, I.D., Capriles, N.R., and Molina, V.A., 2001, A dopaminergic mechanism is involved in the “anxiogenic-like” response induced by chronic amphetamine treatment: a behavioral and neurochemical study, Brain Res. 909:197–186.CrossRefGoogle Scholar
  6. Cardinal, R.N., Parkinson, J.A., Hall, J., and Everitt, B.J., 2002, Emotion and motivation: the role of the amygdala, ventral striatum, and prefrontal cortex, Neurosci. Biobehav. Rev. 26:321–352.PubMedCrossRefGoogle Scholar
  7. Crombag, H.S., Gorny, G., Li, Y., Kolb, B., and Robinson, T.E., 2005, Opposite Effects of Amphetamine Self-administration Experience on Dendritic Spines in the Medial and Orbital Prefrontal Cortex, Cereb. Cortex. 15:341–348.PubMedCrossRefGoogle Scholar
  8. Cryan, J.F., Hoyer, D., and Markou, A., 2003, Withdrawal from chronic amphetamine induces depressive-like behavioral effects in rodents, Biol. Psychiatry. 54:49–58.PubMedCrossRefGoogle Scholar
  9. De Vries, T.J., Schoffelmeer, A.N., Tjon, G.H., Nestby, P., Mulder, A.H., and Vanderschuren, L.J., 1996, Mifepristone prevents the expression of long-term behavioural sensitization to amphetamine, Eur. J. Pharmacol. 307:R3–R4.PubMedCrossRefGoogle Scholar
  10. Fiorino, D.F., and Phillips, A.G., 1999, Facilitation of sexual behavior and enhanced dopamine efflux in the nucleus accumbens of male rats after D-amphetamine-induced behavioral sensitization, J. Neurosci. 19:456–463.PubMedGoogle Scholar
  11. Gerfen, C.R., 1989, The neostriatal mosaic: striatal patch-matrix organization is related to cortical lamination, Science 246:385–388.PubMedGoogle Scholar
  12. Gerfen, C.R., 1992, The neostriatal mosaic: multiple levels of compartmental organization, Trends Neurosci. 15:133–139.PubMedCrossRefGoogle Scholar
  13. Graybiel, A.M., 1983, Compartmental organization of the mammalian striatum, Prog. Brain Res 58:247–256.PubMedCrossRefGoogle Scholar
  14. Graybiel, A.M., and Ragsdale, C.W., Jr., 1978, Histochemically distinct compartments in the striatum of human, monkeys, and cat demonstrated by acetylthiocholinesterase staining, Proc. Natl. Acad. Sci. USA 75:5723–5726.PubMedCrossRefGoogle Scholar
  15. Heidbreder, C.A., Thompson, A.C., and Shippenberg, T.S., 1996, Role of extracellular dopamine in the initiation and long-term expression of behavioral sensitization to cocaine, J. Pharmacol. Exp. Ther. 278:490–502.PubMedGoogle Scholar
  16. Hutcheson, D.M., Everitt, B.J., Robbins, T.W., and Dickinson, A., 2001, The role of withdrawal in heroin addiction: enhances reward or promotes avoidance?, Nat. Neurosci. 4:943–947.PubMedCrossRefGoogle Scholar
  17. Jaber, M., Cador, M., Dumartin, B., Normand, E., Stinus, L., and Bloch, B., 1995, Acute and chronic amphetamine treatments differently regulate neuropeptide messenger RNA levels and Fos immunoreactivity in rat striatal neurons, Neuroscience 65:1041–1050.PubMedCrossRefGoogle Scholar
  18. Jongen-Rêlo, A.L., Voorn, P., and Groenewegen, H.J., 1994, Immunohistochemical characterization of the shell and core territories of the nucleus accumbens of the rat, Eur. J. Neurosci. 6:1255–1264.PubMedCrossRefGoogle Scholar
  19. Kalivas, P.W., and Duffy, P., 1993, Time course of extracellular dopamine and behavioral sensitization to cocaine. I. Dopamine axon terminals, J. Neurosci. 13:266–275.PubMedGoogle Scholar
  20. Koob, G.F., Ahmed, S.H., Boutrel, B., Chen, S.A., Kenny, P.J., Markou, A., O’Dell, L.E., Parsons, L.H., and Sanna, P.P., 2004, Neurobiological mechanisms in the transition from drug use to drug dependence, Neurosci. Biobehav. Rev. 27:739–749.PubMedCrossRefGoogle Scholar
  21. Li, Y., Kolb, B., and Robinson, T.E., 2003, The location of persistent amphetamine-induced changes in the density of dendritic spines on medium spiny neurons in the nucleus accumbens and caudate-putamen, Neuropsychopharmacology 28:1082–1085.PubMedCrossRefGoogle Scholar
  22. Lin, D., Koob, G.F., and Markou, A., 2000, Time-dependent alterations in ICSS thresholds associated with repeated amphetamine administrations, Pharmacol. Biochem. Behav. 65:407–417.PubMedCrossRefGoogle Scholar
  23. Nordquist, R.E., Pennartz, C.M.A., Uylings, H.B., Joosten, R.N.J.M.A., Jonker, A.J., Groenewegen, H.J., and Voorn, P., 2003, C-fos activation patterns in rat prefrontal cortex during acquisition of a cued classical conditioning task, Behav. Brain. Res. 146:65–75.PubMedCrossRefGoogle Scholar
  24. Packard, M.G., and Knowlton, B.J., 2002, Learning and memory functions of the basal ganglia, Annual Review of Neuroscience 25:563–593.PubMedCrossRefGoogle Scholar
  25. Paulson, P.E., and Robinson, T.E., 1995, Amphetamine-induced time-dependent sensitization of dopamine neurotransmission in the dorsal and ventral striatum: a microdialysis study in behaving rats, Synapse. 19:56–65.PubMedCrossRefGoogle Scholar
  26. Pierce, R.C., and Kalivas, P.W., 1997, A circuitry model of the expression of behavioral sensitization to amphetamine-like psychostimulants, Brain. Res. Brain. Res. Rev. 25:192–216.PubMedCrossRefGoogle Scholar
  27. Robinson, T.E., and Becker, J.B., 1986, Enduring changes in brain and behavior produced by chronic amphetamine administration: a review and evaluation of animal models of amphetamine psychosis, Brain. Res. 396:157–198.PubMedCrossRefGoogle Scholar
  28. Robinson, T.E., and Berridge, K.C., 1993, The neural basis of drug craving: an incentive-sensitization theory of addiction, Brain. Res. Brain. Res. Rev. 18:247–291.PubMedCrossRefGoogle Scholar
  29. Robinson, T.E., and Berridge, K.C., 2003, Addiction, Annu Rev Psychol 54:25–53.PubMedCrossRefGoogle Scholar
  30. Robinson, T.E., Jurson, P.A., Bennett, J.A., and Bentgen, K.M., 1988, Persistent sensitization of dopamine neurotransmission in ventral striatum (nucleus accumbens) produced by prior experience with (+)-amphetamine: a microdialysis study in freely moving rats, Brain. Res. 462:211–222.PubMedCrossRefGoogle Scholar
  31. Robinson, T.E., and Kolb, B., 1997, Persistent structural modifications in nucleus accumbens and prefrontal cortex neurons produced by previous experience with amphetamine, J. Neurosci. 17:8491–8497.PubMedGoogle Scholar
  32. Robinson, T.E., and Kolb, B., 1999, Alterations in the morphology of dendrites and dendritic spines in the nucleus accumbens and prefrontal cortex following repeated treatment with amphetamine or cocaine, Eur. J. Neurosci. 11:1598–1604.PubMedCrossRefGoogle Scholar
  33. Salamone, J.D., Correa, M., Mingote, S., and Weber, S.M., 2003, Nucleus accumbens dopamine and the regulation of effort in food-seeking behavior: Implications for studies of natural motivation, psychiatry, and drug abuse, J. Pharmacol. Exp. Ther. 305:1–8.PubMedCrossRefGoogle Scholar
  34. Schultz, W., 2002, Getting formal with dopamine and reward, Neuron. 36:241–263.PubMedCrossRefGoogle Scholar
  35. Segal, D.S., and Kuczenski, R., 1992, In vivo microdialysis reveals a diminished amphetamine-induced DA response corresponding to behavioral sensitization produced by repeated amphetamine pretreatment, Brain. Res. 571:330–337.PubMedCrossRefGoogle Scholar
  36. Segal, D.S., and Kuczenski, R., 1992, Repeated cocaine administration induces behavioral sensitization and corresponding decreased extracellular dopamine responses in caudate and accumbens, Brain. Res. 577:351–355.PubMedCrossRefGoogle Scholar
  37. Steiner, H., and Gerfen, C.R., 1998, Role of dynorphin and enkephalin in the regulation of striatal output pathways and behavior, Exp. Brain. Res. 123:60–76.PubMedCrossRefGoogle Scholar
  38. Stewart, J., and Badiani, A., 1993, Tolerance and sensitization to the behavioral effects of drugs, Behav. Pharmacol. 4:289–312.PubMedGoogle Scholar
  39. Taylor, J.R., and Horger, B.A., 1999, Enhanced responding for conditioned reward produced by intraaccumbens amphetamine is potentiated after cocaine sensitization, Psychopharmacology (Berl) 142:31–40.PubMedCrossRefGoogle Scholar
  40. Taylor, J.R., and Jentsch, J.D., 2001, Repeated intermittent administration of psychomotor stimulant drugs alters the acquisition of Pavlovian approach behavior in rats: differential effects of cocaine, damphetamine and 3,4-methylenedioxymethamphetamine (“Ecstasy”), Biol. Psychiatry 50:137–143.PubMedCrossRefGoogle Scholar
  41. Vanderschuren, L.J.M.J., and Kalivas, P.W., 2000, Alterations in dopaminergic and glutamatergic transmission in the induction and expression of behavioral sensitization: a critical review of preclinical studies, Psychopharmacology (Berl) 151:99–120.PubMedCrossRefGoogle Scholar
  42. Vanderschuren, L.J.M.J., Schoffelmeer, A.N., Mulder, A.H., and De Vries, T.J., 1999, Dopaminergic mechanisms mediating the long-term expression of locomotor sensitization following pre-exposure to morphine or amphetamine, Psychopharmacology (Berl) 143:244–253.PubMedCrossRefGoogle Scholar
  43. Vanderschuren, L.J.M.J., Schoffelmeer, A.N, Van Leeuwen, S.D., Hof, L., Jonker, A.J., and Voorn, P., 2002, Compartment-specific changes in striatal neuronal activity during expression of amphetamine sensitization are the result of drug hypersensitivity, Eur. J. Neurosci. 16:2462–2468.PubMedCrossRefGoogle Scholar
  44. Vezina, P., 1996, D1 dopamine receptor activation is necessary for the induction of sensitization by amphetamine in the ventral tegmental area, J. Neurosci. 16:2411–2420.PubMedGoogle Scholar
  45. Vezina, P., 2004, Sensitization of midbrain dopamine neuron reactivity and the self-administration of psychomotor stimulant drugs, Neuroscience & Biobehavioral Reviews 27:827–839.CrossRefGoogle Scholar
  46. Voorn, P., Gerfen, C.R., and Groenewegen, H.J., 1989, Compartmental organization of the ventral striatum of the rat: immunohistochemical distribution of enkephalin, substance P, dopamine, and calcium-binding protein, J. Comp. Neurol. 289:189–201.PubMedCrossRefGoogle Scholar
  47. White, F.J., and Kalivas, P.W., 1998, Neuroadaptations involved in amphetamine and cocaine addiction, Drug Alcohol Depend 51:141–153.PubMedCrossRefGoogle Scholar
  48. White, N.M., 1989, A functional hypothesis concerning the striatal matrix and patches: mediation of S-R memory and reward, Life Sci. 45:1943–1957.PubMedCrossRefGoogle Scholar
  49. White, N.M., and McDonald, R.J., 2002, Multiple parallel memory systems in the brain of the rat, Neurobiol. Learn Mem. 77:125–184.PubMedCrossRefGoogle Scholar
  50. Willuhn, I., Sun, W., and Steiner, H., 2003, Topography of cocaine-induced gene regulation in the rat striatum: relationship to cortical inputs and role of behavioural context, Eur. J. Neurosci. 17:1053–1066.PubMedCrossRefGoogle Scholar
  51. Wolf, M.E., White, F.J., Nassar, R., Brooderson, R.J., and Khansa, M.R., 1993, Differential development of autoreceptor subsensitivity and enhanced dopamine release during amphetamine sensitization, J. Pharmacol. Exp. Ther. 264:249–255.PubMedGoogle Scholar
  52. Wright, C.I., and Groenewegen, H.J., 1995, Patterns of convergence and segregation in the medial nucleus accumbens of the rat: relationships of prefrontal cortical, midline thalamic, and basal amygdaloid afferents, J. Comp. Neurol. 361:383–403.PubMedCrossRefGoogle Scholar
  53. Wyvell, C.L., and Berridge, K.C., 2001, Incentive sensitization by previous amphetamine exposure: increased cue-triggered “wanting” for sucrose reward, J. Neurosci. 21:7831–7840.PubMedGoogle Scholar
  54. Yin, H.H., Knowlton, B.J., and Balleine, B.W., 2004, Lesions of dorsolateral striatum preserve outcome expectancy but disrupt habit formation in instrumental learning, Eur. J. Neurosci. 19:181–189.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, Inc. 2005

Authors and Affiliations

  • Rebecca E. Nordquist
    • 1
    • 2
  • Pieter Voorn
    • 1
  • J. G. de Mooij-van Malsen
    • 2
    • 4
  • R. N. J. M. A. Joosten
    • 2
  • Cyriel M. A. Pennartz
    • 3
  • Louk J. M. J. Vanderschuren
    • 4
  1. 1.Department of AnatomyVrije Universiteit Medical CenterAmsterdam
  2. 2.Netherlands Institute for Brain ResearchNetherlands
  3. 3.Animal Physiology & Cognitive Neuroscience, Swammerdam Institute for Life SciencesUniversity of AmsterdamAmsterdam
  4. 4.Rudolf Magnus Institute of Neuroscience, Dept. of Pharmacology and AnatomyUniversity Medical Center UtrechtUtrecht

Personalised recommendations