Nicotine Differentially Modulates Emotional-Locomotor Interactions for Adult or Adolescent Rats
La Nicotina Modula Diferencialmente la Interacción Emoción- Locomoción en Ratas Adolescentes o Adultas
DOI:
https://doi.org/10.15446/rcp.v31n1.89822Keywords:
locomotor sensitization, risk-related behaviors, open field, chronic daily nicotine, adolescence (en)adolescencia, campo abierto, comportamientos de riesgo, nicotina crónica diaria, sensibilización locomotriz (es)
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Previous research has shown that exposure to nicotine and other drugs of abuse stimulate dopaminergic neurons in the mesolimbic circuit. Sustained activation of this circuit by prolonged exposure to drugs promotes locomotor sensitization. However, there are inconsistent reports about nicotine-induced locomotor sensitization when assessed among different developmental stages. We evaluated exploratory behavior on specific areas of the open field as an indicator of behavioral disinhibition and general locomotor activity as an indicator of nicotine-induced locomotor sensitization, to further explore the mechanisms underlying behavioral adaptations to nicotine exposure in animals from different developmental stages. We found that while adolescent and adult rats are equally responsive to nicotine-induced locomotor sensitization, nicotine disrupts inhibition of risk-related behavior only in adolescent rats. Together, our results suggest that chronic daily exposure to nicotine promotes potentiation of its stimulant effects on locomotor activity. In adolescents, this effect is accompanied by a decreased capacity to inhibit risk-related behaviors under the acute effect of the drug.
How to cite this article: Novoa, C., Solano, J. L., Ballesteros-Acosta, H., Lamprea, R. M., & Ortega, L. A. (2021). Nicotine Differentially Modulates Emotional-Locomotor Interactions for Adult or Adolescent Rats. Revista Colombiana de Psicología, 31(1), 13-22. https://doi.org/10.15446/rcp.v31n1.89822
Estudios previos han demostrado que exposición a la nicotina y otras drogas de abuso estimula las neuronas dopaminérgicas del circuito mesolímbico. La activación sostenida de este circuito por exposición a las drogas promueve la sensibilización locomotriz. La evaluación de este efecto en diferentes etapas del desarrollo ha mostrado evidencia contradictoria sobre la susceptibilidad de adolescentes. En este trabajo exploramos las adaptaciones conductuales a la exposición crónica a nicotina en ratas adolescentes y adultas; para esto, evaluamos el comportamiento exploratorio en áreas específicas del campo abierto como indicador de desinhibición comportamental y el desplazamiento general como indicador de sensibilización locomotriz. Encontramos que, ambos grupos etarios muestran igual sensibilización locomotriz inducida por la nicotina y que la nicotina altera la inhibición del comportamiento relacionado con el riesgo sólo en adolescentes. Estos resultados sugieren que la exposición crónica diaria a la nicotina promueve la potenciación de sus efectos estimulantes sobre la actividad locomotriz y en los adolescentes, este efecto se acompaña de una disminución de la capacidad para inhibir conductas relacionadas con el riesgo bajo el efecto agudo de la droga.
Cómo citar este artículo: Novoa, C., Solano, J. L., Ballesteros-Acosta, H., Lamprea, R. M., & Ortega, L. A. (2021). Nicotine Differentially Modulates Emotional-Locomotor Interactions for Adult or Adolescent Rats. Revista Colombiana de Psicología, 31(1), 13-22. https://doi.org/10.15446/rcp.v31n1.89822
References
Abreu-Villaça, Y., Seidler, F. J., Tate, C. A., & Slotkin, T. A. (2003). Nicotine is a neurotoxin in the adolescent brain: critical periods, patterns of exposure, regional selectivity, and dose thresholds for macromolecular alterations. Brain Research, 979, 114–128. https://doi.org/10.1016/S0006-8993(03)02885-3 DOI: https://doi.org/10.1016/S0006-8993(03)02885-3
Adermark, L., Morud, J., Lotfi, A., Jonsson, S., Söderpalm, B., & Ericson, M. (2015). Age-contingent influence over accumbal neurotransmission and the locomotor stimulatory response to acute and repeated administration of nicotine in Wistar rats. Neuropharmacology, 97, 104–112. https://doi.org/10.1016/j.neuropharm.2015.06.001 DOI: https://doi.org/10.1016/j.neuropharm.2015.06.001
Benwell, M. E. M., Balfour, D. J. K., & Birrell, C. E. (1995). Desensitization of the nicotine-induced mesolimbic dopamine responses during constant infusion with nicotine. British Journal of Pharmacology, 114, 454–460. https://doi.org/10.1111/j.1476-5381.1995.tb13248.x DOI: https://doi.org/10.1111/j.1476-5381.1995.tb13248.x
Bernardi, R. E., & Spanagel, R. (2014). Basal activity level in mice predicts the initial and sensitized locomotor response to nicotine only in high responders. Behavioural Brain Research, 264, 143–150. https://doi.org/10.1016/j.bbr.2014.01.046 DOI: https://doi.org/10.1016/j.bbr.2014.01.046
Bishnoi, I. R., Ossenkopp, K., & Kavaliers, M. (2020). Sex and age differences in locomotor and anxiety‐like behaviors in rats: From adolescence to adulthood. Developmental Psychobiology, 56, dev.22037. https://doi.org/10.1002/dev.22037 DOI: https://doi.org/10.1002/dev.22037
Cadoni, C., & Di Chiara, G. (2000). Differential changes in accumbens shell and core dopamine in behavioral sensitization to nicotine. European Journal of Pharmacology, 387, R23–R25. https://doi.org/10.1016/S0014-2999(99)00843-2 DOI: https://doi.org/10.1016/S0014-2999(99)00843-2
Camarini, R., & Pautassi, R. M. (2016). Behavioral sensitization to ethanol: Neural basis and factors that influence its acquisition and expression. Brain Research Bulletin, 125, 53–78. https://doi.org/10.1016/j.brainresbull.2016.04.006 DOI: https://doi.org/10.1016/j.brainresbull.2016.04.006
Cao, J., Belluzzi, J. D., Loughlin, S. E., Dao, J. M., Chen, Y., & Leslie, F. M. (2010). Locomotor and stress responses to nicotine differ in adolescent and adult rats. Pharmacology Biochemistry and Behavior, 96, 82–90. https://doi.org/10.1016/j.pbb.2010.04.010 DOI: https://doi.org/10.1016/j.pbb.2010.04.010
Carola, V., D’Olimpio, F., Brunamonti, E., Mangia, F., & Renzi, P. (2002). Evaluation of the elevated plusmaze and open-field tests for the assessment of anxiety-related behaviour in inbred mice. Behavioural Brain Research, 134, 49–57. https://doi.org/10.1016/S0166-4328(01)00452-1 DOI: https://doi.org/10.1016/S0166-4328(01)00452-1
Casey, B. J., & Jones, R. M. (2010). Neurobiology of the adolescent brain and behavior: Implications for substance use disorders. Journal of the American Academy of Child & Adolescent Psychiatry, 49, 1189–1201. https://doi.org/10.1016/j.jaac.2010.08.017 DOI: https://doi.org/10.1016/j.jaac.2010.08.017
Counotte, D. S., Goriounova, N. A., Li, K. W., Loos, M., van der Schors, R. C., Schetters, D., Schoffelmeer, A. N. M., Smit, A. B., Mansvelder, H. D., Pattij, T., & Spijker, S. (2011). Lasting synaptic changes underlie attention deficits caused by nicotine exposure during adolescence. Nature Neuroscience, 14, 417–419. https://doi.org/10.1038/nn.2770 DOI: https://doi.org/10.1038/nn.2770
Counotte, D. S., Spijker, S., Van de Burgwal, L. H., Hogenboom, F., Schoffelmeer, A. N. M., De Vries, T. J., Smit, A. B., & Pattij, T. (2009). Long-lasting cognitive deficits resulting from adolescent nicotine exposure in rats. Neuropsychopharmacology, 34, 299–306. https://doi.org/10.1038/npp.2008.96 DOI: https://doi.org/10.1038/npp.2008.96
Craig, E. L., Zhao, B., Cui, J. Z., Novalen, M., Miksys, S., & Tyndale, R. F. (2014). Nicotine pharmacokinetics in rats is altered as a function of age, impacting the interpretation of animal model data. Drug Metabolism and Disposition, 42, 1447–1455. https://doi.org/10.1124/dmd.114.058719 DOI: https://doi.org/10.1124/dmd.114.058719
DiFranza, J., & Wellman, R. (2007). Sensitization to nicotine: How the animal literature might inform future human research. Nicotine & Tobacco Research, 9, 9–20. https://doi.org/10.1080/14622200601078277 DOI: https://doi.org/10.1080/14622200601078277
Doremus-Fitzwater, T. L., Varlinskaya, E. I., & Spear, L. P. (2010). Motivational systems in adolescence: Possible implications for age differences in substance abuse and other risk-taking behaviors. Brain and Cognition, 72, 114–123. https://doi.org/10.1016/j.bandc.2009.08.008 DOI: https://doi.org/10.1016/j.bandc.2009.08.008
Eiland, L., & Romeo, R. D. (2013). Stress and the developing adolescent brain. Neuroscience, 249, 162–171. https://doi.org/10.1016/j.neuroscience.2012.10.048 DOI: https://doi.org/10.1016/j.neuroscience.2012.10.048
Elliott, B. M., Faraday, M. M., Phillips, J. M., & Grunberg, N. E. (2004). Effects of nicotine on elevated plus maze and locomotor activity in male and female adolescent and adult rats. Pharmacology Biochemistry and Behavior, 77, 21–28. https://doi.org/10.1016/j.pbb.2003.09.016 DOI: https://doi.org/10.1016/j.pbb.2003.09.016
Falco, A. M., & Bevins, R. A. (2015). Individual differences in the behavioral effects of nicotine: A review of the preclinical animal literature. Pharmacology Biochemistry and Behavior, 138, 80–90. https://doi.org/10.1016/j.pbb.2015.09.017 DOI: https://doi.org/10.1016/j.pbb.2015.09.017
Faraday, M. M., Elliott, B. M., & Grunberg, N. E. (2001). Adult vs. adolescent rats differ in biobehavioral responses to chronic nicotine administration. Pharmacology Biochemistry and Behavior, 70, 475–489. https://doi.org/10.1016/S0091-3057(01)00642-6 DOI: https://doi.org/10.1016/S0091-3057(01)00642-6
Fredrickson, P., Boules, M., Yerbury, S., & Richelson, E. (2003). Blockade of nicotine-induced locomotor sensitization by a novel neurotensin analog in rats. European Journal of Pharmacology, 458, 111–118. https://doi.org/10.1016/S0014-2999(02)02689-4 DOI: https://doi.org/10.1016/S0014-2999(02)02689-4
Gabriel, D. B. K., Freels, T. G., Setlow, B., & Simon, N. W. (2019). Risky decision-making is associated with impulsive action and sensitivity to first-time nicotine exposure. Behavioural Brain Research, 359, 579–588. https://doi.org/10.1016/j.bbr.2018.10.008 DOI: https://doi.org/10.1016/j.bbr.2018.10.008
Goriounova, N. A., & Mansvelder, H. D. (2012). Nicotine exposure during adolescence alters the rules for prefrontal cortical synaptic plasticity during adulthood. Frontiers in Synaptic Neuroscience, 4, 1–9. https://doi.org/10.3389/fnsyn.2012.00003 DOI: https://doi.org/10.3389/fnsyn.2012.00003
Goutier, W., O’Connor, J. J., Lowry, J. P., & McCreary, A. C. (2015). The effect of nicotine induced behavioral sensitization on dopamine d1 receptor pharmacology: An in vivo and ex vivo study in the rat. European Neuropsychopharmacology, 25, 933–943. https://doi.org/10.1016/j.euroneuro.2015.02.008 DOI: https://doi.org/10.1016/j.euroneuro.2015.02.008
Kalivas, P. W. (1995). Interactions between dopamine and excitatory amino acids in behavioral sensitization to psychostimulants. Drug and Alcohol Dependence, 37, 95–100. https://doi.org/10.1016/0376-8716(94)01063-Q DOI: https://doi.org/10.1016/0376-8716(94)01063-Q
Kolokotroni, K. Z., Rodgers, R. J., & Harrison, A. A. (2011). Acute nicotine increases both impulsive choice and behavioural disinhibition in rats. Psychopharmacology, 217, 455–473. https://doi.org/10.1007/s00213-011-2296-2 DOI: https://doi.org/10.1007/s00213-011-2296-2
Lamprea, M. R., Cardenas, F. P., Setem, J., & Morato, S. (2008). Thigmotactic responses in an openfield. Brazilian Journal of Medical and Biological Research, 41, 135–140. https://doi.org/10.1590/S0100-879X2008000200010 DOI: https://doi.org/10.1590/S0100-879X2008000200010
Le Foll, B., & Goldberg, S. R. (2005). Nicotine induces conditioned place preferences over a large range of doses in rats. Psychopharmacology, 178, 481–492. https://doi.org/10.1007/s00213-004-2021-5 DOI: https://doi.org/10.1007/s00213-004-2021-5
Levine, A., Huang, Y., Drisaldi, B., Griffin, E. A., Pollak, D. D., Xu, S., Yin, D., Schaffran, C., Kandel, D. B., & Kandel, E. R. (2011). Molecular Mechanism for a Gateway Drug: Epigenetic Changes Initiated by Nicotine Prime Gene Expression by Cocaine. Science Translational Medicine, 3, 107ra109-107ra109. https://doi.org/10.1126/scitranslmed.3003062 DOI: https://doi.org/10.1126/scitranslmed.3003062
Li, Z., DiFranza, J. R., Wellman, R. J., Kulkarni, P., & King, J. A. (2008). Imaging brain activation in nicotinesensitized rats. Brain Research, 1199, 91–99. https://doi.org/10.1016/j.brainres.2008.01.016 DOI: https://doi.org/10.1016/j.brainres.2008.01.016
Matta, S. G., Balfour, D. J., Benowitz, N. L., Boyd, R. T., Buccafusco, J. J., Caggiula, A. R., Craig, C. R., Collins, A. C., Damaj, M. I., Donny, E. C., Gardiner, P. S., Grady, S. R., Heberlein, U., Leonard, S. S., Levin, E. D., Lukas, R. J., Markou, A., Marks, M. J., McCallum, S. E., … Zirger, J. M. (2007). Guidelines on nicotine dose selection for in vivo research. Psychopharmacology, 190, 269–319. https://doi.org/10.1007/s00213-006-0441-0 DOI: https://doi.org/10.1007/s00213-006-0441-0
McCutcheon, J. E., & Marinelli, M. (2009). Age matters. European Journal of Neuroscience, 29(5), 997–1014. https://doi.org/10.1111/j.1460-9568.2009.06648.x DOI: https://doi.org/10.1111/j.1460-9568.2009.06648.x
Meert, T. F. (1986). A comparative study of the effects of ritanserin (R 55 667) and chlordiazepoxide on rat open field behavior. Drug Development Research, 8, 197–204. https://doi.org/10.1002/ddr.430080123 DOI: https://doi.org/10.1002/ddr.430080123
Morud, J., Strandberg, J., Andrén, A., Ericson, M., Söderpalm, B., & Adermark, L. (2018). Progressive modulation of accumbal neurotransmission and anxiety-like behavior following protracted nicotine withdrawal. Neuropharmacology, 128, 86–95. https://doi.org/10.1016/j.neuropharm.2017.10.002 DOI: https://doi.org/10.1016/j.neuropharm.2017.10.002
Nisell, M., Nomikos, G. G., Hertel, P., Panagis, G., & Svensson, T. H. (1996). Condition-independent sensitization of locomotor stimulation and mesocortical dopamine release following chronic nicotine treatment in the rat. Synapse, 22, 369–381. https://doi.org/10.1002/(SICI)1098-2396(199604)22:4<369::AID-SYN8>3.0.CO;2-9 DOI: https://doi.org/10.1002/(SICI)1098-2396(199604)22:4<369::AID-SYN8>3.0.CO;2-9
Ohmura, Y., Tsutsui-Kimura, I., & Yoshioka, M. (2012). Impulsive behavior and nicotinic acetylcholine receptors. Journal of Pharmacological Sciences, 118, 413–422. https://doi.org/10.1254/jphs.11R06CR DOI: https://doi.org/10.1254/jphs.11R06CR
Olausson, P., Ericson, M., Löf, E., Engel, J. A., & Söderpalm, B. (2001). Nicotine-induced behavioral disinhibition and ethanol preference correlate after repeated nicotine treatment. European Journal of Pharmacology, 417, 117–123. https://doi.org/10.1016/S0014-2999(01)00903-7 DOI: https://doi.org/10.1016/S0014-2999(01)00903-7
Picciotto, M. R., & Kenny, P. J. (2020). Mechanisms of nicotine addiction. Cold Spring Harbor Perspectives in Medicine, 3, a039610. https://doi.org/10.1101/cshperspect.a039610 DOI: https://doi.org/10.1101/cshperspect.a039610
Prut, L., & Belzung, C. (2003). The open field as a paradigm to measure the effects of drugs on anxiety-like behaviors: a review. European Journal of Pharmacology, 463, 3–33. https://doi.org/10.1016/S0014-2999(03)01272-X DOI: https://doi.org/10.1016/S0014-2999(03)01272-X
Schochet, T. L., Kelley, A. E., & Landry, C. F. (2004). Differential behavioral effects of nicotine exposure in adolescent and adult rats. Psychopharmacology, 175, 265–273. https://doi.org/10.1007/s00213-004-1831-9 DOI: https://doi.org/10.1007/s00213-004-1831-9
Sharma, S., Arain, Mathur, Rais, Nel, Sandhu, Haque, & Johal. (2013). Maturation of the adolescent brain. Neuropsychiatric Disease and Treatment, 9, 449. https://doi.org/10.2147/NDT.S39776 DOI: https://doi.org/10.2147/NDT.S39776
Stansfield, K. H., & Kirstein, C. L. (2006). Effects of novelty on behavior in the adolescent and adult rat. Developmental Psychobiology, 48, 273–273. https://doi.org/10.1002/dev.20143 DOI: https://doi.org/10.1002/dev.20143
Thorpe, H. H. A., Hamidullah, S., Jenkins, B. W., & Khokhar, J. Y. (2020). Adolescent neurodevelopment and substance use: Receptor expression and behavioral consequences. Pharmacology & Therapeutics, 206, 107431. https://doi.org/10.1016/j.pharmthera.2019.107431 DOI: https://doi.org/10.1016/j.pharmthera.2019.107431
Van Gaalen, M. M., Brueggeman, R. J., Bronius, P. F. C., Schoffelmeer, A. N. M., & Vanderschuren, L. J. M. J. (2006). Behavioral disinhibition requires dopamine receptor activation. Psychopharmacology, 187, 73–85. https://doi.org/10.1007/s00213-006-0396-1 DOI: https://doi.org/10.1007/s00213-006-0396-1
Volkow, N. D. (2011). Epigenetics of Nicotine: Another nail in the coughing. Science Translational Medicine, 3, 107ps43-107ps43. https://doi.org/10.1126/scitranslmed.3003278 DOI: https://doi.org/10.1126/scitranslmed.3003278
Yuan, M., Cross, S. J., Loughlin, S. E., & Leslie, F. M. (2015). Nicotine and the adolescent brain. The Journal of Physiology, 593, 3397–3412. https://doi.org/10.1113/JP270492 DOI: https://doi.org/10.1113/JP270492
Zago, A., Leão, R. M., Carneiro-de-Oliveira, P. E., Marin, M. T., Cruz, F. C., & Planeta, C. S. (2012). Effects of simultaneous exposure to stress and nicotine on nicotine-induced locomotor activation in adolescent and adult rats. Brazilian Journal of Medical and Biological Research, 45, 33–37. https://doi.org/10.1590/S0100-879X2011007500153 DOI: https://doi.org/10.1590/S0100-879X2011007500153
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