Stress-induced cross-sensitization to amphetamine is related to changes in the dopaminergic system
Abstract
Repeated stress engenders behavioral sensitization. The mesolimbic dopamine system is critically involved in drug-induced behavioral sensitization. In the present study we examined the differences between adolescent and adult rats in stress-induced behavioral sensitization to amphetamine and changes in dopamine (DA) and its metabolite levels in the mesolimbic system. Adolescent or adult rats were restrained for 2 h, once a day, for 7 days. Three days after the last exposure to stress, the animals were challenged with saline or amphetamine (1.0 mg/kg i.p.) and amphetamine-induced locomotion was recorded for 40 min. Immediately after the behavioral tests, rats were decapitated and the nucleus accumbens (NAcc), ventral tegmental area (VTA) and amygdala (AM) were removed to measure tissue levels of DA and its metabolites by HPLC. Exposure to repeated restraint stress promoted behavioral sensitization to amphetamine in both adult and adolescent rats. In adult rats, amphetamine administration increased DA levels in both the stress and control groups in the NAcc and VTA. In adolescent rats, amphetamine increased DA levels in the NAcc in rats exposed to stress. Furthermore, in the AM of adolescent rats in the control group, amphetamine increased the DA levels; however, amphetamine reduced this neurotransmitter in the rats that were exposed to stress. No alteration was observed in the dopamine metabolite levels. Therefore, stress promoted behavioral sensitization to amphetamine and this may be related to changes in DA levels in the mesolimbic system. These changes appear to be dependent on ontogeny.
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Cross-sensitization and the resulting hyper-responsivity of dopaminergic systems also occurs between drugs of abuse and stress at both behavioral and physiological levels.
“and drugs of abuse and stress (at both behavioral and physiological levels) (Cruz, Marin, Leão, & Planeta, 2011; Garcia-Keller et al., 2013; Piazza et al., 1990).”
From Cued for Risk: Evidence for an Incentive Sensitization Framework to Explain the Interplay between Stress and Anxiety, Substance Abuse, and Reward Uncertainty in Disordered Gambling Behavior (2019) · cites this paper as Cruz, Marin, Leão, & Planeta, 2011
Cites
The neural basis of drug craving: An incentive-sensitization theory of addiction
Robinson, T. (1993) · Brain Research Reviews · doi:10.1016/0165-0173(93)90013-p · Cited by 7,346 · see citing works
The adolescent brain and age-related behavioral manifestations
Spear, L. P. (2000) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(00)00014-2 · Cited by 5,433 · see citing works
Chronic stress, drug use, and vulnerability to addiction
Sinha, R. (2008) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1441.030 · Cited by 1,904 · see citing works
A circuitry model of the expression of behavioral sensitization to amphetamine-like psychostimulants
Pierce, R. C., & Kalivas, P. W. (1997) · Brain Research Reviews · doi:10.1016/s0165-0173(97)00021-0 · Cited by 1,239 · see citing works
Stress dysregulation of drug reward pathways, and the transition to drug dependence
Koob, & Kreek, M. J. (2007) · American Journal of Psychiatry · doi:10.1176/appi.ajp.2007.05030503 · Cited by 868 · see citing works
Interchangeability of Stress and Amphetamine in Sensitization
Antelman, S. M., Eichler, A. J., Black, C. A., & Kocan, D. J. (1980) · Science · doi:10.1126/science.7188649 · Cited by 562 · see citing works
Interaction between glucocorticoid hormones, stress and psychostimulant drugs*
Marinelli, M., & Piazza, P. V. (2002) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2002.02089.x · Cited by 426 · see citing works
Brain stress systems in the amygdala and addiction
Koob, G. F. (2009) · Brain Research · doi:10.1016/j.brainres.2009.03.038 · Cited by 388 · see citing works
Social stress, therapeutics and drug abuse: Preclinical models of escalated and depressed intake
MICZEK, K., YAP, J., & COVINGTONIII, H. (2008) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2008.07.006 · Cited by 338 · see citing works
Repeated social-defeat stress, cocaine or morphine
Covington, H. E., & Miczek, K. A. (2001) · Psychopharmacology · doi:10.1007/s002130100858 · Cited by 326 · see citing works
Huang, B., Dawson, D. A., Stinson, F. S., Hasin, D. S., Ruan, W. J., Saha, T. D., Smith, S. M. R., Goldstein, R. B., & Grant, B. F. (2006) · The Journal of Clinical Psychiatry · doi:10.4088/jcp.v67n0708 · Cited by 306 · see citing works
Are adolescents more vulnerable to drug addiction than adults? Evidence from animal models
Schramm-Sapyta, N. L., Walker, Q. D., Caster, J. M., Levin, E. D., & Kuhn, C. M. (2009) · Psychopharmacology · doi:10.1007/s00213-009-1585-5 · Cited by 215 · see citing works
Regulation of the mesocorticolimbic dopamine system by glutamic acid receptor subtypes.
Kalivas, P. W., Duffy, P., & Barrow, J. (1989) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1016/s0022-3565(25)20732-7 · Cited by 215 · see citing works
Imperato, A., Puglisi-Allegra, S., Casolini, P., Zocchi, A., & Angelucci, L. (1989) · European Journal of Pharmacology · doi:10.1016/0014-2999(89)90735-8 · Cited by 203 · see citing works
Subsensitivity to dopaminergic drugs in periadolescent rats: a behavioral and neurochemical analysis
Bolaños, C. A., Glatt, S. J., & Jackson, D. (1998) · Developmental Brain Research · doi:10.1016/s0165-3806(98)00116-3 · Cited by 199 · see citing works
Covington, H. E., & Miczek, K. A. (2005) · Psychopharmacology · doi:10.1007/s00213-005-0190-5 · Cited by 169 · see citing works
Nikulina, E. M., Covington, H. E., Ganschow, L., Hammer, R. P., & Miczek, K. A. (2004) · Neuroscience · doi:10.1016/j.neuroscience.2003.10.029 · Cited by 158 · see citing works
Repeated stress increases locomotor response to amphetamine
Herman, J., Stinus, L., & Moal, M. L. (1984) · Psychopharmacology · doi:10.1007/bf00555227 · Cited by 156 · see citing works
Elliott, B. M., Faraday, M. M., Phillips, J. M., & Grunberg, N. E. (2004) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2003.09.016 · Cited by 148 · see citing works
Perugini, M., & Vezina, P. (1994) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1016/s0022-3565(25)22426-0 · Cited by 148 · see citing works
Kabbaj, M., Norton, C., Kollack‐Walker, S., Watson, S. J., Robinson, T. E., & Akil, H. (2001) · Psychopharmacology · doi:10.1007/s002130100918 · Cited by 141 · see citing works
Adriani, W., & Giovanni Laviola, A. (2000) · Neuropharmacology · doi:10.1016/s0028-3908(99)00115-x · Cited by 137 · see citing works
Haile, C. N., GrandPré, T., & Kosten, T. A. (2001) · Psychopharmacology · doi:10.1007/s002130000650 · Cited by 130 · see citing works
Repeated corticosterone administration sensitizes the locomotor response to amphetamine
Deroche‐Gamonet, V., Piazza, P. V., Maccari, S., Moal, M. L., & Simon, H. (1992) · Brain Research · doi:10.1016/0006-8993(92)90911-r · Cited by 127 · see citing works
SPEAR, L. P., & Isaacson, R. L. (1977) · Brain Research · doi:10.1016/0006-8993(77)90610-2 · Cited by 109 · see citing works
Vidal, J., de Bie, J., Granneman, R. A., Wallinga, A. E., Koolhaas, J. M., & Buwalda, B. (2007) · Physiology & Behavior · doi:10.1016/j.physbeh.2007.06.004 · Cited by 108 · see citing works
Cadoni, C., Solinas, M., Valentini, V., & Chiara, G. D. (2003) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2003.02941.x · Cited by 97 · see citing works
Deroche‐Gamonet, V., Piazza, P. V., Moal, M. L., & Simon, H. (1994) · Brain Research · doi:10.1016/0006-8993(94)91867-8 · Cited by 90 · see citing works
Dopamine-Induced Behavioral Changes and Oxidative Stress in Methamphetamine-Induced Neurotoxicity
Kita, T., Miyazaki, I., Asanuma, M., Takeshima, M., & Wagner, G. C. (2009) · International review of neurobiology · doi:10.1016/s0074-7742(09)88003-3 · Cited by 77 · see citing works
The role of monoamine oxidase and catechol O-methyltransferase in dopaminergic neurotransmission.
Napolitano, A., Cesura, A. M., & Prada, M. D. (1995) · PubMed · Cited by 75 · see citing works
Pacchioni, A. M., Gioino, G., ASSIS, A., & Cancela, L. M. (2002) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2002.tb04165.x · Cited by 74 · see citing works
Age- and sex-dependent amphetamine self-administration in rats
Shahbazi, M., Moffett, A. M., Williams, B. F., & Frantz, K. J. (2007) · Psychopharmacology · doi:10.1007/s00213-007-0933-6 · Cited by 74 · see citing works
Lepsch, L. B., Gonzalo, L., Magro, F., DeLucia, R., Scavone, C., & Planeta, C. S. (2005) · Addiction Biology · doi:10.1080/13556210500269366 · Cited by 74 · see citing works
Self-citationSensitization to Stress and Psychostimulants
Prasad, B. M., Sorg, B. A., Ulibarri, C., & Kalivas, P. W. (1995) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1995.tb44714.x · Cited by 71 · see citing works
Colussi‐Mas, J., Geisler, S., Zimmer, L., Zahm, D. S., & Bérod, A. (2007) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2007.05738.x · Cited by 68 · see citing works
Zovkic, I. B., & McCormick, C. M. (2007) · Behavioural Pharmacology · doi:10.1097/fbp.0b013e3282effbf5 · Cited by 64 · see citing works
Giorgi, O., Piras, G., Lecca, D., & Corda, M. G. (2005) · Neuroscience · doi:10.1016/j.neuroscience.2005.06.075 · Cited by 57 · see citing works
Nikulina, E. M., Miczek, K. A., & Hammer, R. P. (2005) · Neuropsychopharmacology · doi:10.1038/sj.npp.1300658 · Cited by 57 · see citing works
Social defeat stress, sensitization, and intravenous cocaine self-administration in mice
Yap, J. J., & Miczek, K. A. (2007) · Psychopharmacology · doi:10.1007/s00213-007-0712-4 · Cited by 56 · see citing works
Long-lasting sensitization of reward-directed behavior by amphetamine
Mendez, I. A., Williams, M. T., Bhavsar, A., Lu, A. P., Bizon, J. L., & Setlow, B. (2009) · Behavioural Brain Research · doi:10.1016/j.bbr.2009.01.034 · Cited by 50 · see citing works
Díaz–otañez, C. S., Capriles, N., & Cancela, L. M. (1997) · Pharmacology Biochemistry and Behavior · doi:10.1016/s0091-3057(96)00344-9 · Cited by 48 · see citing works
Araújo, A. P. N., DeLucia, R., Scavone, C., & Planeta, C. S. (2003) · Behavioural Brain Research · doi:10.1016/s0166-4328(02)00088-8 · Cited by 45 · see citing works
Self-citationNelson, A. M., Larson, G. A., & Zahniser, N. R. (2009) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.109.159897 · Cited by 43 · see citing works
A single social defeat induces short-lasting behavioral sensitization to amphetamine
DEJONG, J., Wasilewski, M., VANDERVEGT, B., Buwalda, B., & KOOLHAAS, J. (2004) · Physiology & Behavior · doi:10.1016/j.physbeh.2004.10.002 · Cited by 41 · see citing works
Pacchioni, A. M., Cador, M., Bregonzio, C., & Cancela, L. M. (2006) · Neuropsychopharmacology · doi:10.1038/sj.npp.1301080 · Cited by 41 · see citing works
Zovkic, I. B., Waters, P., & McCormick, C. M. (2009) · Developmental Psychobiology · doi:10.1002/dev.20381 · Cited by 40 · see citing works
dos Santos, G. C., Marin, M. T., Cruz, F. C., DeLucia, R., & Planeta, C. S. (2009) · Addiction Biology · doi:10.1111/j.1369-1600.2009.00153.x · Cited by 35 · see citing works
Self-citationCruz, F. C., Marin, M. T., & Planeta, C. S. (2007) · Neuroscience · doi:10.1016/j.neuroscience.2007.10.019 · Cited by 34 · see citing works
Self-citationIzenwasser, S., & French, D. (2002) · Pharmacology Biochemistry and Behavior · doi:10.1016/s0091-3057(02)00942-5 · Cited by 34 · see citing works
Der‐Avakian, A., Bland, S. T., Schmid, M. J., Watkins, L. R., Spencer, R. L., & Maier, S. F. (2006) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2006.02.004 · Cited by 34 · see citing works
Marin, M. T., Cruz, F., & Planeta, C. S. (2008) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2008.06.018 · Cited by 32 · see citing works
Self-citationTirelli, E., Tambour, S., & Michel, A. (2003) · European Neuropsychopharmacology · doi:10.1016/s0924-977x(03)00037-3 · Cited by 28 · see citing works
Giorgi, O., Piras, G., Lecca, D., & Corda, M. G. (2005) · Psychopharmacology · doi:10.1007/s00213-005-2177-7 · Cited by 26 · see citing works
Selective reduction of monoamine oxidase A and B in the frontal cortex of subordinate rats
Dhingra, N. K., Raju, T. R., & Meti, B. L. (1997) · Brain Research · doi:10.1016/s0006-8993(96)01477-1 · Cited by 19 · see citing works
Ziegels, J. (1979) · Journal of Neural Transmission · doi:10.1007/bf01243879 · Cited by 16 · see citing works
Armando, I., Lemoine, A. P., Segura, E. T., et al. (1993) · Cellular and Molecular Neurobiology · doi:10.1007/bf00711559 · Cited by 15 · see citing works
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Burke, A. R., McCormick, C. M., Pellis, S. M., & Lukkes, J. L. (2017) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2017.01.018 · Cited by 225 · see citing works
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- Authors
- Cruz, F. C., Marin, M. T., Leão, R. M., & Planeta, C. S.
- Affiliations
- Universidade Estadual Paulista (Unesp) (BR)
- Universidade Federal de São Carlos (BR)
- Corresponding author
- Planeta, Cleopatra S.
- Venue
- Journal of Neural Transmission
- Published
- 2011-10-18
- Volume
- 119
- Issue
- 4
- Pages
- 415-424
- ISSN
- 0300-9564 (ISSN-L)
- 1435-1463
- OpenAlex
- W2076184516
- Cited by
- 31
- References
- 56
- Citations by year
- 2025: 2 · 2024: 1 · 2023: 1 · 2022: 1 · 2021: 1 · 2019: 5 · 2018: 5 · 2017: 2 · 2016: 2 · 2015: 4 · 2014: 3 · 2013: 2 · 2012: 1
- FWCI
- 0.92
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Journal of Neural Transmission (publishedVersion)
- PubMed (publishedVersion)
- Acervo Digital da Universidade Estadual Paulista (Universidade Estadual Paulista) (submittedVersion)
- UNESP Institutional Repository (São Paulo State University) (submittedVersion)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Keywords
- amphetamine, cross-sensitization, mesolimbic dopamine system, dopamine levels, restraint stress, adolescent rats, ontogeny, nucleus accumbens, ventral tegmental area, amygdala, dopamine metabolites, locomotor activity
- MeSH terms
- Age Factors, Amphetamines, Central Nervous System Stimulants, Analysis of Variance, Animals, Animals, Newborn, Brain, Disease Models, Animal, Dopamine, Homovanillic Acid, Male, Stress, Psychological, 3,4-Dihydroxyphenylacetic Acid, Rats, Wistar, Microdialysis, Rats
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