Caracterización conductual y neuroinmune de la resiliencia al estrés social: Efectos reforzantes de la cocaína

  1. Francisco Ródenas-González
  2. María del Carmen Blanco-Gandía
  3. José Miñarro López
  4. Marta Rodríguez-Arias
Revista:
Adicciones: Revista de socidrogalcohol

ISSN: 0214-4840

Año de publicación: 2021

Volumen: 33

Número: 4

Páginas: 319-331

Tipo: Artículo

DIALNET GOOGLE SCHOLAR lock_openAcceso abierto editor

Otras publicaciones en: Adicciones: Revista de socidrogalcohol

Resumen

Numerosos estudios preclínicos han demostrado que el estrés social incrementa la vulnerabilidad a los efectos reforzantes de la cocaína. Sin embargo, los resultados obtenidos no son homogéneos, observándose siempre una subpoblación que no muestra dicho incremento. Utilizando el modelo de derrota social (DS) repetida en ratones, en este trabajo hemos querido caracterizar conductualmente a los ratones resilientes al incremento de los efectos reforzantes de la cocaína inducido por el estrés social. Utilizamos ratones adultos macho de la cepa C57/BL6 a los que sometimos al protocolo de DS repetida y tres semanas más tarde, realizamos el Condicionamiento de Preferencia de Lugar (CPL) inducido por una dosis no efectiva de cocaína (1mg/ kg). Una vez finalizado este procedimiento se midieron los niveles estriatales de interleucina 6, ya que el estrés social produce una respuesta de neuroinflamación. No se observó CPL en los ratones controles, pero los animales derrotados tomados en conjunto desarrollaron preferencia. Sin embargo, esta muestra se pudo dividir en ratones resilientes (no desarrollaron preferencia) y susceptibles (presentaron CPL). Durante las derrotas sociales, los animales resilientes pasaron menos tiempo en las conductas de huida y sumisión que los catalogados como susceptible y presentaron conductas de ataque hacia el ratón residente, manifestando por tanto resistencia a ser derrotados. No se observaron diferencias en la respuesta de neuroinflamación, probablemente debido al largo periodo de tiempo trascurrido desde la última derrota social. Nuestros resultados sugieren que un estilo de afrontamiento activo al estrés social va a ser determinante en la protección del sujeto a desarrollar un trastorno por uso de drogas

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Información de financiación

Ministerio de Ciencia, Innovaci?n y Universidades (MICINN), PSI2017-83023. Instituto de Salud Carlos III, Red de Trastornos Adictivos (RD16/0017/0007) and European Union, ERDF Funds ?a way to build Europe?.

Financiadores

Referencias bibliográficas

  • Aguilar, M. A., Rodríguez-Arias, M. & Miñarro, J. (2009). Neurobiological mechanisms of the reinstatement of drug-conditioned place preference. Brain Research Reviews, 59, 253-277. doi:10.1016/j.brainresrev.2008.08.002.
  • Alfonso-Loeches, S., Pascual-Lucas, M., Blanco, A. M., Sanchez-Vera, I. & Guerri, C. (2010). Pivotal role of TLR4 receptors in alcohol-induced neuroinflammation and brain damage. Journal of Neuroscience, 30, 8285-8295. doi:10.1523/JNEUROSCI.0976-10.2010.
  • Araos, P., Pedraz, M., Serrano, A., Lucena, M., Barrios, V., García-Marchena, N.,... Rodríguez de Fonseca, F. (2015). Plasma profile of pro-inflammatory cytokines and chemokines in cocaine users under outpatient treatment: Influence of cocaine symptom severity and psychiatric co-morbidity. Addiction Biology, 20, 756-772. doi:10.1111/adb.12156.
  • Arena, D. T., Covington, 3., Herbert, E., DeBold, J. F. & Miczek, K. A. (2019). Persistent increase of I.V. cocaine self-administration in a subgroup of C57BL/6J male mice after social defeat stress. Psychopharmacology, 236, 1-11. doi:10.1007/s00213-019-05191-6.
  • Arenas, M. C., Aguilar, M. A., Montagud-Romero, S., Mateos-García, A., Navarro-Francés, C. I., Miñarro, J. & Rodríguez-Arias, M. (2016). Influence of the novelty-seeking endophenotype on the rewarding effects of psychostimulant drugs in animal models. Current Neuropharmacology, 14, 87-100. doi:10.2174/1570159X13666150921112841.
  • Arenas, M. C., Daza-Losada, M., Vidal-Infer, A., Aguilar, M. A., Miñarro, J. & Rodríguez-Arias, M. (2014). Capacity of novelty-induced locomotor activity and the hole-board test to predict sensitivity to the conditioned rewarding effects of cocaine. Physiology & Behavior, 133, 152-160. doi:10.1016/j.physbeh.2014.05.028.
  • Bardo, M. T. & Bevins, R. A. (2000). Conditioned place preference: What does it add to our preclinical understanding of drug reward? Psychopharmacology, 153, 31-43. doi:10.1007/s002130000569.
  • Blanco-Gandía, M. C., Cantacorps, L., Aracil-Fernández, A., Montagud-Romero, S., Aguilar, M. A., Manzanares, J.,... Rodríguez-Arias, M. (2017). Effects of bingeing on fat during adolescence on the reinforcing effects of cocaine in adult male mice. Neuropharmacology, 113, 31-44. doi:10.1016/j.neuropharm.2016.09.020.
  • Blanco-Gandía, M. C., Montagud-Romero, S., Aguilar, M. A., Miñarro, J. & Rodríguez-Arias, M. (2018). Housing conditions modulate the reinforcing properties of cocaine in adolescent mice that binge on fat. Physiology & Behavior, 183, 18-26. doi:10.1016/j.physbeh.2017.10.014.
  • Boyson, C. O., Holly, E. N., Shimamoto, A., Albrechet-Souza, L., Weiner, L. A., DeBold, J. F. & Miczek, K. A. (2014). Social stress and CRF-dopamine interactions in the VTA: Role in long-term escalation of cocaine self-administration. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience, 34, 6659-6667. doi:10.1523/JNEUROSCI.3942-13.2014.
  • Boyson, C., Miguel, T., Quadros, I., DeBold, J. & Miczek, K. (2011). Prevention of social stress-escalated cocaine self-administration by CRF-R1 antagonist in the rat VTA. Psychopharmacology, 218, 257-269. doi:10.1007/s00213-011-2266-8.
  • Brodnik, Z. D., Double, M., España, R. A. & Jaskiw, G. E. (2017). L-tyrosine availability affects basal and stimulated catecholamine indices in prefrontal cortex and striatum of the rat. Neuropharmacology, 123, 159-174. doi:10.1016/j.neuropharm.2017.05.030.
  • Brody, G. H., Yu, T., Chen, Y., Kogan, S. M., Evans, G. W., Windle, M.,... Philibert, R. A. (2013). Supportive family environments, genes that confer sensitivity, and allostatic load among rural African American emerging adults: A prospective analysis. Journal of Family Psychology, 27, 22-29. doi:10.1037/a0027829.
  • Burke, A. & Miczek, K. (2014). Stress in adolescence and drugs of abuse in rodent models: Role of dopamine, CRF, and HPA axis. Psychopharmacology, 231, 1557-1580. doi:10.1007/s00213-013-3369-1.
  • Chaouloff, F. (2013). Social stress models in depression research: What do they tell us? Cell and Tissue Research, 354, 179-190. doi:10.1007/s00441-013-1606-x.
  • Charney, D. S. (2004). Psychobiological mechanisms of resilience and vulnerability: Implications for successful adaptation to extreme stress. American Journal of Psychiatry, 161, 195-216. doi:10.1176/appi.ajp.161.2.195.
  • Chen, R., Kelly, G., Sengupta, A., Heydendael, W., Nicholas, B., Beltrami, S.,... Bhatnagar, S. (2015). MicroRNAs as biomarkers of resilience or vulnerability to stress. Neuroscience, 305, 36-48. doi:10.1016/j.neuroscience.2015.07.045.
  • Chmitorz, A., Kunzler, A., Helmreich, I., Tüscher, O., Kalisch, R., Kubiak, T.,... Lieb, K. (2018). Intervention studies to foster resilience – A systematic review and proposal for a resilience framework in future intervention studies.Clinical Psychology Review, 59, 78-100. doi:10.1016/j.cpr.2017.11.002.
  • Clark, K., Wiley, C. & Bradberry, C. (2013). Psychostimulant abuse and neuroinflammation: Emerging evidence of their interconnection. Neurotoxicity Research, 23, 174-188. doi:10.1007/s12640-012-9334-7.
  • Covington III, H., Kikusui, T., Goodhue, J., Nikulina, E. M., Hammer, R. P. & Miczek, K. A. (2005). Brief social defeat stress: Long lasting effects on cocaine taking during a binge and Zif268 mRNA expression in the amygdala and prefrontal cortex. Neuropsychopharmacology, 30, 310-321. doi:10.1038/sj.npp.1300587.
  • Covington III, H. & Miczek, K. (2001). Repeated social-defeat stress, cocaine or morphine. Effects on behavioral sensitization and intravenous cocaine self-administration “binges”. Psychopharmacology, 158, 388-398. doi:10.1007/s002130100858.
  • Covington III, H. & Miczek, K. (2005). Intense cocaine self-administration after episodic social defeat stress, but not after aggressive behavior: Dissociation from corticosterone activation. Psychopharmacology, 183, 331-340. doi:10.1007/s00213-005-0190-5.
  • Cui, C., Shurtleff, D. & Harris, R. A. (2014). Neuroimmune mechanisms of alcohol and drug addiction. International Review of Neurobiology, 118, 1-12. doi:10.1016/B978-0-12-801284-0.00001-4.
  • Delgado-Palacios, R., Campo, A., Henningsen, K., Verhoye, M., Poot, D., Dijkstra, J.,... Van Der Linden, A. (2011). Magnetic resonance imaging and spectroscopy reveal differential hippocampal changes in anhedonic and resilient subtypes of the chronic mild stress rat model. Biological Psychiatry, 70, 449-457. doi:10.1016/j.biopsych.2011.05.014.
  • Duclot, F., Hollis, F., Darcy, M. J. & Kabbaj, M., (2011). Individual differences in novelty-seeking behavior in rats as a model for psychosocial stress-related mood disorders. Physiology & Behavior, 104, 296-305. doi:10.1016/j.physbeh.2010.12.014.
  • Ferrer-Pérez, C., Castro-Zavala, A., Luján, M. Á., Filarowska, J., Ballestín, R., Miñarro, J.,... Rodríguez-Arias, M. (2019). Oxytocin prevents the increase of cocaine-related responses produced by social defeat. Neuropharmacology, 146, 50-64. doi:10.1016/j.neuropharm.2018.11.011.
  • Ferrer-Pérez, C., Martinez, T., Montagud-Romero, S., Ballestín, R., Reguilón, M. D., Miñarro, J. & Rodríguez-Arias, M. (2018a). Indomethacin blocks the increased conditioned rewarding effects of cocaine induced by repeated social defeat. PLoS One, 13, e0209291. doi:10.1371/journal.pone.0209291.
  • Ferrer-Pérez, C., Reguilón, M. D., Manzanedo, C., Aguilar, M. A., Miñarro, J. & Rodríguez-Arias, M. (2018b). Antagonism of corticotropin-releasing factor CRF 1 receptors blocks the enhanced response to cocaine after social stress. European Journal of Pharmacology, 823, 87-95. doi:10.1016/j.ejphar.2018.01.052.
  • Finnell, J. E., Lombard, C. M., Padi, A. R., Moffitt, C. M., Wilson, L. B., Wood, C. S. & Wood, S. K. (2017). Physical versus psychological social stress in male rats reveals distinct cardiovascular, inflammatory and behavioral consequences. PLoS One, 12, e0172868. doi:10.1371/journal.pone.0172868.
  • Finnell, J. E. & Wood, S. K. (2016). Neuroinflammation at the interface of depression and cardiovascular disease: Evidence from rodent models of social stress. Neurobiology of Stress, 4, 1-14. doi:10.1016/j.ynstr.2016.04.001.
  • García-Pardo, M. P., Rodríguez-Arias, M., Miñarro, J. & Aguilar, M. A. (2016). Effects of social stress on ethanol responsivity in adult mice. Neuropsychiatry, 6. doi:10.4172/Neuropsychiatry.1000146.
  • Gold, P. W., Machado-Vieira, R. & Pavlatou, M. G. (2015). Clinical and biochemical manifestations of depression: Relation to the neurobiology of stress. Neural Plasticity, 2015, 581976-11. doi:10.1155/2015/581976.
  • Golden, S. A., Covington, H. E., Berton, O. & Russo, S. J. (2011). A standardized protocol for repeated social defeat stress in mice. Nature Protocols, 6, 1183-1191. doi:10.1038/nprot.2011.361.
  • Gómez-Lázaro, E., Arregi, A., Beitia, G., Vegas, O., Azpiroz, A. & Garmendia, L. (2011). Individual differences in chronically defeated male mice: Behavioral, endocrine, immune, and neurotrophic changes as markers of vulnerability to the effects of stress. Stress, 14, 537-548. doi:10.3109/10253890.2011.562939.
  • Hawley, D. F., Bardi, M., Everette, A. M., Higgins, T. J., Tu, K. M., Kinsley, C. H. & Lambert, K. G. (2010). Neurobiological constituents of active, passive, and variable coping strategies in rats: Integration of regional brain neuropeptide Y levels and cardiovascular responses. Stress, 13, 172-183. doi:10.3109/10253890903144621.
  • Heffner, T. G., Hartman, J. A. & Seiden, L. S. (1980). A rapid method for the regional dissection of the rat brain. Pharmacology Biochemistry and Behavior, 13, 453-456. doi:10.1016/0091-3057(80)90254-3.
  • Henriques-Alves, A. M. & Queiroz, C. M. (2015). Ethological evaluation of the effects of social defeat stress in mice: Beyond the social interaction ratio. Frontiers in Behavioral Neuroscience, 9, 364. doi:10.3389/fnbeh.2015.00364.
  • Hjemdal, O., Friborg, O. & Stiles, T.C. (2012). Resilience is a good predictor of hopelessness even after accounting for stressful life events, mood and personality (NEO-PI-R). Scandinavian Journal of Psychology, 53, 174-180. doi:10.1111/j.1467-9450.2011.00928.x.
  • Hodes, G. E., Ménard, C. & Russo, S. J. (2016). Integrating interleukin-6 into depression diagnosis and treatment. Neurobiology of Stress, 4, 15-22. doi:10.1016/j.ynstr.2016.03.003.
  • Hollis, F., Duclot, F., Gunjan, A. & Kabbaj, M. (2011). Individual differences in the effect of social defeat on anhedonia and histone acetylation in the rat hippocampus. Hormones and Behavior, 59, 331-337. doi:10.1016/j.yhbeh.2010.09.005.
  • Holly, E. N., Boyson, C. O., Montagud-Romero, S., Stein, D. J., Gobrogge, K. L., DeBold, J. F. & Miczek, K. A. (2016). Episodic social stress-escalated cocaine self-administration: Role of phasic and tonic corticotropin releasing factor in the anterior and posterior ventral tegmental area. The Journal of Neuroscience, 36, 4093-4105. doi:10.1523/JNEUROSCI.2232-15.2016.
  • Koolhaas, J., Bartolomucci, A., Buwalda, B., de Boer, F., Flugge, G., Korte, M. & Fuchs, E. (2011). Neuroendocrinology of coping styles: Towards understanding the biology of individual variation. Frontiers in Neuroendocrinology, 31, 307-321. doi:10.1016/j.yfrne.2010.04.001.
  • Krishnan, V. (2014). Defeating the fear: New insights into the neurobiology of stress susceptibility. Experimental Neurology, 261, 412-416. doi:10.1016/j.expneurol.2014.
  • Krishnan, V., Han, M., Graham, A., Graham, D. L., Berton, O., Renthal, W.,... Nestler, E. J. (2007). Molecular adaptations underlying susceptibility and resistance to social defeat in brain reward regions. Cell, 131, 391-404. doi:10.1016/j.cell.2007.09.018.
  • Kumar, S., Hultman, R., Hughes, D., Michel, N., Katz, B. M. & Dzirasa, K. (2014). Prefrontal cortex reactivity underlies trait vulnerability to chronic social defeat stress. Nature Communications, 5, 4537. doi:10.1038/ncomms5537.
  • Laird, K. T., Krause, B., Funes, C. & Lavretsky, H. (2019). Psychobiological factors of resilience and depression in late life. Translational Psychiatry, 9, 88-18. doi:10.1038/s41398-019-0424-7.
  • Lambert, K. G., Hyer, M. M., Rzucidlo, A. A., Bergeron, T., Landis, T. & Bardi, M. (2014). Contingency-based emotional resilience: Effort-based reward training and flexible coping lead to adaptive responses to uncertainty in male rats. Frontiers in Behavioral Neuroscience, 8, 124. doi:10.3389/fnbeh.2014.00124.
  • Lüthi, A. & Lüscher, C. (2014). Pathological circuit function underlying addiction and anxiety disorders. Nature Neuroscience, 17, 1635-1643. doi:10.1038/nn.3849.
  • Lutter, M., Krishnan, V., Russo, S. J., Jung, S., McClung, C. A. & Nestler, E. J. (2008). Orexin signaling mediates the antidepressant-like effect of calorie restriction. Journal of Neuroscience, 28, 3071-3075. doi:10.1523/JNEUROSCI.5584-07.2008.
  • Maes, M., Yirmyia, R., Noraberg, J., Brene, S., Hibbeln, J., Perini, G.,... Maj, M. (2009). The inflammatory & neurodegenerative (I&ND) hypothesis of depression: Leads for future research and new drug developments in depression. Metabolic Brain Disease, 24, 27-53. doi:10.1007/s11011-008-9118-1.
  • Maldonado, C., Rodríguez-Arias, M., Castillo, A., Aguilar, M. & Miñarro, J. (2006). Gamma-hydroxybutyric acid affects the acquisition and reinstatement of cocaine-induced conditioned place preference in mice. Behavioural Pharmacology, 17, 119-131. doi:10.1097/01.fbp.0000190685.84984.ec.
  • Manzanedo, C., Aguilar, M. A., Rodríguez-Arias, M. & Miñarro, J. (2001). Effects of dopamine antagonists with different receptor blockade profiles on morphine-induced place preference in male mice. Behavioural Brain Research, 121, 189-197. doi:10.1016/S0166-4328(01)00164-4.
  • Martínez, M., Miñarro, J. & Simón, V. M. (1991). Análisis etoexperimental de la conducta agonística en ratones. Psicológica, 12, 1-22.
  • McGloin, J. & Widom, C.S. (2001). Resilience among abused and neglected children grown up. Development and Psychopathology, 13, 1021-1038. doi:10.1017/S095457940100414X.
  • Menard, C., Pfau, M. L., Hodes, G. E. & Russo, S. J. (2017). Immune and neuroendocrine mechanisms of stress vulnerability and resilience. Neuropsychopharmacology, 42, 62-80. doi:10.1038/npp.2016.90.
  • Miczek, K. A., Yap, J. J. & Covington, H. E. (2008). Social stress, therapeutics and drug abuse: Preclinical models of escalated and depressed intake. Pharmacology and Therapeutics, 120, 102-128. doi:10.1016/j.pharmthera.2008.07.006.
  • Montagud-Romero, S., Daza-Losada, M., Vidal-Infer, A., Maldonado, C., Aguilar, M. A. & Miñarro, J. (2014). The novelty-seeking phenotype modulates the long-lasting effects of intermittent ethanol administration during adolescence. PLoS One, 9, e92576. doi:10.1371/journal.pone.0092576.
  • Montagud-Romero, S., Reguilon, M. D., Roger-Sanchez, C., Pascual, M., Aguilar, M. A., Guerri, C.,... Rodríguez-Arias, M. (2016a). Role of dopamine neurotransmission in the long-term effects of repeated social defeat on the conditioned rewarding effects of cocaine. Progress in Neuropsychopharmacology & Biological Psychiatry, 71, 144-154. doi:10.1016/j.pnpbp.2016.07.008.
  • Montagud-Romero, S., Montesinos, J., Pascual, M., Aguilar, M. A., Roger-Sanchez, C., Guerri, C.,... Rodríguez-Arias, M. (2016b). Up-regulation of histone acetylation induced by social defeat mediates the conditioned rewarding effects of cocaine. Progress in Neuropsychopharmacology & Biological Psychiatry, 70, 39-48. doi:10.1016/j.pnpbp.2016.04.016.
  • Moreira, F. P., Medeiros, J. R. C., Lhullier, A. C., de Mattos Souza, L. D., Jansen, K., Portela, L. V.,... Oses, J. P. (2016). Cocaine abuse and effects in the serum levels of cytokines IL-6 and IL-10. Drug and Alcohol Dependence, 158, 181-185. doi:10.1016/j.drugalcdep.2015.11.024.
  • Newman, E. L., Leonard, M. Z., Arena, D. T., de Almeida, R. M. M. & Miczek, K. A. (2018). Social defeat stress and escalation of cocaine and alcohol consumption: Focus on CRF. Neurobiology of Stress, 9, 151-165. doi:10.1016/j.ynstr.2018.09.007.
  • Pearson-Leary, J., Eacret, D., Chen, R., Takano, H., Nicholas, B. & Bhatnagar, S. (2017). Inflammation and vascular remodeling in the ventral hippocampus contributes to vulnerability to stress. Translational Psychiatry, 7, e1160. doi:10.1038/tp.2017.122.
  • Pérez-Tejada, J., Arregi, A., Gómez-Lázaro, E., Vegas, O., Azpiroz, A. & Garmendia, L. (2013). Coping with chronic social stress in mice: Hypothalamic-pituitary-adrenal/ sympathetic-adrenal-medullary axis activity, behavioral changes and effects of antalarmin treatment: Implications for the study of stress-related psychopathologies. Neuroendocrinology, 98, 73-88. doi:10.1159/000353620.
  • Pfau, M. L., & Russo, S. J. (2015). Peripheral and central mechanisms of stress resilience. Neurobiology of Stress, 1, 66-79. doi:10.1016/j.ynstr.2014.09.004.
  • Pfau, M. L. & Russo, S. J. (2016). Neuroinflammation regulates cognitive impairment in socially defeated mice. Trends in Neurosciences, 39, 353-355. doi:10.1016/j.tins.2016.04.004.
  • Polter, A. M. & Kauer, J. A. (2014). Stress and VTA synapses: Implications for addiction and depression. European Journal of Neuroscience, 39, 1179-1188. doi:10.1111/ejn.12490.
  • Réus, G. Z., Fries, G. R., Stertz, L., Badawy, M., Passos, I. C., Barichello, T.,... Quevedo, J. (2015). The role of inflammation and microglial activation in the pathophysiology of psychiatric disorders. Neuroscience, 300, 141-154. doi:10.1016/j.neuroscience.2015.05.018.
  • Rodríguez-Arias, M., Montagud-Romero, S., Carrión, A. M. G., Ferrer-Pérez, C., Pérez-Villalba, A., Marco, E.,... Miñarro, J. (2018). Social stress during adolescence activates long-term microglia inflammation insult in reward processing nuclei. PLoS One, 13, e0206421. doi:10.1371/journal.pone.0206421.
  • Rodríguez-Arias, M., Montagud-Romero, S., Rubio-Araiz, A., Aguilar, M. A., Martín-García, E., Cabrera, R.,... Miñarro, J. (2017). Effects of repeated social defeat on adolescent mice on cocaine-induced CPP and self-administration in adulthood: Integrity of the blood–brain barrier. Addiction Biology, 22, 129-141. doi:10.1111/adb.12301.
  • Rodríguez-Arias, M., Navarrete, F., Blanco-Gandia, M. C., Arenas, M. C., Bartoll-Andrés, A., Aguilar, M. A.,... Manzanares, J. (2016). Social defeat in adolescent mice increases vulnerability to alcohol consumption. Addiction Biology, 21, 87-97. doi:10.1111/adb.12184.
  • Rodríguez-Arias, M., Vaccaro, S., Arenas, M. C., Aguilar, M. A. & Miñarro, J. (2015). The novelty-seeking phenotype modulates the long-lasting effects of adolescent MDMA exposure. Physiology & Behavior, 141, 190-198. doi:10.1016/j.physbeh.2015.01.023.
  • Russo, S. J., Murrough, J. W., Han, M., Charney, D. S. & Nestler, E. J. (2012). Neurobiology of resilience. Nature Neuroscience, 15, 1475-1484. doi:10.1038/nn.3234.
  • Tornatzky, W. & Miczek, K. A. (1993). Long-term impairment of autonomic circadian rhythms after brief intermittent social stress. Physiology & Behavior, 53, 983-993. doi:10.1016/0031-9384(93)90278-N.
  • Tzschentke, T. M. (2007). Measuring reward with the conditioned place preference (CPP) paradigm: Update of the last decade. Addiction Biology, 12, 227-462. doi:10.1111/j.1369-1600.2007.00070.x.
  • Vidal-Infer, A., Aguilar, M. A., Miñarro, J. & Rodríguez-Arias, M. (2012). Effect of intermittent exposure to ethanol and MDMA during adolescence on learning and memory in adult mice. Behavioral and Brain Functions, 8, 32. doi:10.1186/1744-9081-8-32.
  • Wang, J., Hodes, G. E., Zhang, H., Zhang, S., Zhao, W., Golden, S. A.,... Pasinetti, G. M. (2018). Epigenetic modulation of inflammation and synaptic plasticity promotes resilience against stress in mice. Nature Communications, 9, 477. doi:10.1038/s41467-017-02794-5.
  • Wood, S. K. & Bhatnagar, S. (2015). Resilience to the effects of social stress: Evidence from clinical and preclinical studies on the role of coping strategies. Neurobiology of Stress, 1, 164-173. doi:10.1016/j.ynstr.2014.11.002.
  • Wood, S. K., Walker, H. E., Valentino, R. J. & Bhatnagar, S. (2010). Individual differences in reactivity to social stress predict susceptibility and resilience to a depressive phenotype: Role of corticotropin-releasing factor. Endocrinology, 151, 1795-1805. doi:10.1210/en.2009-1026.
  • Wood, S. K., Wood, C. S., Lombard, C. M., Lee, C. S., Zhang, X., Finnell, J. E. & Valentino, R. J. (2015). Inflammatory factors mediate vulnerability to a social stress-induced depressive-like phenotype in passive coping rats. Biological Psychiatry, 78, 38-48. doi:10.1016/j.biopsych.2014.10.026.
  • Yap, J., Chartoff, E., Holly, E., Potter, D., Carlezon Jr, W. & Miczek, K. (2015). Social defeat stress-induced sensitization and escalated cocaine self-administration: The role of ERK signaling in the rat ventral tegmental area. Psychopharmacology, 232, 1555-1569. doi:10.1007/s00213-014-3796-7.
  • Zhan, G., Huang, N., Li, S., Hua, D., Zhang, J., Fang, X., ... Yang, C. (2018). PGC-1a–FNDC5–BDNF signaling pathway in skeletal muscle confers resilience to stress in mice subjected to chronic social defeat. Psychopharmacology, 235, 3351-3358. doi:10.1007/s00213-018-5041-2.
Fuente de los datos: Dialnet