Biogenic Amine Neurotransmitter Response to Morphine in the Anterior Cingulate Cortex Predicts Propensity for Acquiring Self-Administration and the Intensity of the Withdrawal Syndrome

DOI: 10.4236/pp.2014.511112   PDF   HTML   XML   3,276 Downloads   3,658 Views   Citations

Abstract

Individual differences in behavioral characteristics or initial responses to abused drugs had been recently demonstrated to have predictive value in the propensity of later abuse. The research described here was initiated to determine the initial response of rats to administration of morphine if the physiological response has predictive value for the propensity of the animals to later self-administration. The initial response of extracellular fluid levels of the biogenic monoamine neurotransmitters in the anterior cingulate cortex (aCC) was assessed in drug rats with in vivo microdialysis following administration of morphine. Rats that did not acquire morphine self-administration (NSA) had higher baseline levels of aCC extracellular fluid levels of dopamine (DA) and 3,4-dihydroxyphenylacetic acid (DOPAC) than animals that developed stable morphine self-administration (SA). However, the response independent administration of morphine resulted in a dramatic increase in (DA) in aCC in the SA group, while the morphine injection in the NSA rats increased extracellular fluid levels of noradrenaline (NA). It is possible that these differences might be related to the development of physical dependence. Therefore, the development of physical dependence was observed in these animals. There was no relationship between the propensity to self-administration morphine and the development of physical dependence. Rats that showed the highest withdrawal scores had lower extracellular fluid levels of serotonin (5-HT) compared to rats showing low withdrawal scores. Thus, monoamine neuronal innervations of the aCC respond to an initial dose of morphine that is predictive of the later propensity to self-administration and the resistance and predisposition to the formation of opiate dependence, but there is no relationship between these two indices in individual animals. These data add to a growing body of evidence for the involvement of neuronal systems in the aCC in the actions of opiates.

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Trigub, M. , Kudrin, V. , Bashkatova, V. , Klodt, P. and Sudakov, S. (2014) Biogenic Amine Neurotransmitter Response to Morphine in the Anterior Cingulate Cortex Predicts Propensity for Acquiring Self-Administration and the Intensity of the Withdrawal Syndrome. Pharmacology & Pharmacy, 5, 1006-1014. doi: 10.4236/pp.2014.511112.

Conflicts of Interest

The authors declare no conflicts of interest.

References

[1] Orsini, C., Buchini, F., Piazza, P.V., Puglisi-Allegra, S. and Cabib, S. (2004) Susceptibility to Amphetamine-Induced Place Preference Is Predicted by Locomotor Response to Novelty and Amphetamine in the Mouse. Psychopharmacology (Berl.), 172, 264-270.
http://dx.doi.org/10.1007/s00213-003-1647-z
[2] Marinelli, M. and Piazza, P.V. (2002) Interaction between Glucocorticoid Hormones, Stress and Psychostimulant Drugs. European Journal of Neuroscience, 16, 387-394.
http://dx.doi.org/10.1046/j.1460-9568.2002.02089.x
[3] Ambrosio, E., Goldberg, S.R. and Elmer, G.I. (1995) Behavior Genetic Investigation of the Relationship between Spontaneous Locomotor Activity and the Acquisition of Morphine Self-Administration Behavior. Behavioural Pharmacology, 6, 229-237.
http://dx.doi.org/10.1097/00008877-199504000-00003
[4] Ballesteros-Yanez, I., Ambrosio, E., Pérez, J., Torres, I., Miguéns, M., García-Lecumberri, C. and DeFelipe, J. (2008) Morphine Self-Administration Effects on the Structure of Cortical Pyramidal Cells in Addiction-Resistant Rats. Brain Research, 16, 61-72.
http://dx.doi.org/10.1016/j.brainres.2008.06.128
[5] Sudakov, S.K., Goldberg, S.R., Borisova, E.V., Surkova, L.A., Turina, I.V., Rusakov, D.Ju. and Elmer, G.I. (1993) Differences in Morphine Reinforcement Property in Two Inbred Rat Strains: Associations with Cortical Receptors, Behavioral Activity, Analgesia and the Cataleptic Effects of Morphine. Psychopharmacology (Berl), 112, 183-188.
http://dx.doi.org/10.1007/BF02244908
[6] Cohen, R.A., Paul, R., Zawacki, T.M., Moser, D.J., Sweet, L. and Wilkinson, H. (2001) Emotional and Personality Changes Following Cingulotomy. Emotion, 1, 38-50.
http://dx.doi.org/10.1037/1528-3542.1.1.38
[7] Alexopoulos, G.S., Gunning-Dixon, F.M., Latoussakis, V., Kanellopoulos, D. and Murphy, C.F. (2008) Anterior Cingulate Dysfunction in Geriatric Depression. International Journal of Geriatric Psychiatry, 23, 347-355.
http://dx.doi.org/10.1002/gps.1939
[8] Risinger, R.C., Salmeron, B.J., Ross, T.J., Amen, S.L., Sanfilipo, M., Hoffmann, R.G., Bloom, A.S., Garavan, H. and Stein, E.A.(2005) Neural Correlates of High and Craving During Cocaine Self-Administration Using BOLD fMRI. Neuroimage, 26, 1097-1108.
http://dx.doi.org/10.1016/j.neuroimage.2005.03.030
[9] Sinha, R., Lacadie, C., Skudlarski, P., Fulbright, R.K., Rounsaville, B.J., Kosten, T.R. and Wexler, B.E. (2005) Neural Activity Associated with Stress-Induced Cocaine Craving: A Functional Magnetic Resonance Imaging Study. Psychopharmacology (Berl), 183, 171-180.
[10] Pockros, L.A., Pentkowski, N.S., Swinford, S.E. and Neisewander, J.L. (2011) Neisewander Blockade of 5-HT2A receptors in the Medial Prefrontal Cortex Attenuates Reinstatement of Cue-Elicited Cocaine-Seeking Behavior in Rats. Psychopharmacology (Berl), Author Manuscript; Available in PMC 2011 April 7.
http://dx.doi.org/10.1007/s00213-005-0147-8
[11] Trafton, C.L. and Marques, P.R. (1971) Effects of Septal Area and Cingulate Cortex Lesions on Opiate Addiction Behavior in Rats. Journal of Comparative and Physiological Psychology, 75, 277-285.
http://dx.doi.org/10.1037/h0030810
[12] Tzschentke, T.M. and Schmidt, W.J. (1999) Functional Heterogeneity of the Rat Medial Prefrontal Cortex: Effects of Discrete Subarea-Specific Lesions on Drug-Induced Conditioned Place Preference and Behavioral Sensitization. European Journal of Neuroscience, 11, 4099-4109.
http://dx.doi.org/10.1046/j.1460-9568.1999.00834.x
[13] Su, Y.L., Huang, J., Wang, N., Wang, J.Y. and Luo, F. (2012) The Effects of Morphine on Basal Neuronal Activities in the Lateral and Medial Pain Pathways. Neuroscience Letters, 525, 173-178.
[14] Volkov, N.D., Fowler, J.S. and Wang, G.J. (2002) Role of Dopamine in Drug Reinforcement and Addiction in Humans: Results from Imaging Studies. Behavioral Pharmacology, 13, 355-366.
http://dx.doi.org/10.1097/00008877-200209000-00008
[15] Jasinska, A.J., Stein, E.A., Kaiser, J., Naumer, M.J. and Yalachkov, Y. (2014) Factors Modulating Neural Reactivity to Drug Cues in Addiction: A Survey of Human Neuroimaging Studies. Neuroscience & Biobehavioral Reviews, 38, 1-16.
http://dx.doi.org/10.1016/j.neubiorev.2013.10.013
[16] Sudakov, S.K., Rusakova, I.V., Trigub, M.N., Shakhmatov, V.Y., Kozel, A.I. and Smith, G.E. (2004) Effect of Destruction of Gyrus Cinguli in Rat Brain on the Development of Tolerance to the Analgesic Effect of Morphine and Physical Dependence on Morphine. Bulletin of Experimental Biology and Medicine, 138, 479-481.
http://dx.doi.org/10.1007/s10517-005-0075-y
[17] Dahlstrom, A. and Fuxe, K. (1964) Localization of Monoamines in the Lower Brain Stem. Experientia, 20, 398-399.
http://dx.doi.org/10.1007/BF02147990
[18] Chandler, D.J., Lamperski, C.S. and Waterhouse, B.D. (2013) Identification and Distribution of Projections from Monoaminergic and Cholinergic Nuclei to Functionally Differentiated Subregions of Prefrontal Cortex. Brain Research, 19, 38-58.
http://dx.doi.org/10.1016/j.brainres.2013.04.057
[19] Paxinos, G. and Watson, C. (1986) The Rat Brain in Stereotaxic Coordinates. Second Edition, Academic Press, Waltham.
[20] Gong, Y.X., Lv, M., Zhu, Y.P., Zhu, Y.Y., Wei, E.Q., Shi, H., Zeng, Q.L. and Chen, Z. (2007) Endogenous Histamine Inhibits the Development of Morphine-Induced Conditioned Place Preference. Acta Pharmacologica Sinica, 28, 10-18.
http://dx.doi.org/10.1111/j.1745-7254.2007.00470.x
[21] Mucha, R.F. and Herz, A. (1985) Motivational Properties of Kappa and Mu Opioid Receptor Agonists Studied with Place and Taste Preference Conditioning. Psychopharmacology, 86, 274-280.
http://dx.doi.org/10.1007/BF00432213
[22] Spyraki, C., Nomikos, G.G., Galanopoulou, P. and DaÏfotis, Z. (1988) Drug-Induced Place Preference in Rats with 5,7-Dihydroxytryptamine Lesions of the Nucleus Accumbens. Behavioural Brain Research, 29, 127-134.
http://dx.doi.org/10.1016/0166-4328(88)90060-5
[23] Koob, G.F. and Le Moal, M. (2001) Drug Addiction, Dysregulation of Reward and Allostasis. Neuropsychopharmacology, 24, 97-129.
http://dx.doi.org/10.1016/S0893-133X(00)00195-0
[24] Maldonado, R., Saiardi, A. and Valverde, O. (1997) Absence of Opiate Rewarding Effects in Mice Lacking Dopamine D2 Receptors. Nature, 388, 586-589. http://dx.doi.org/10.1038/41567
[25] Elmer, G.I., Pieper, J.O., Levy, J., Rubinstein, M., Low, M.L., Grandy, D.K. and Wise, R.A. (2005) Brain Stimulation and Morphine Reward Deficits in Dopamine D2 Receptor-Deficient Mice. Psychopharmacology, 182, 33-44.
http://dx.doi.org/10.1007/s00213-005-0051-2
[26] Wise, R.A., Leone, P., Rivest, A. and Leeb, K. (1995) Elevations of Nucleus Accumbens Dopamine and DOPAC Levels during Intravenous Heroin Self-Administration. Synapse, 21, 140-148.
http://dx.doi.org/10.1002/syn.890210207
[27] Hemby, S.E., Martin, T.J., Co, C., Dworkin, S.I. and Smith, J.E. (1995) The Effects of Intravenous Heroin Administration on Extracellular Nucleus Accumbens Dopamine Concentrations as Determined by in Vivo Microdialysis. Journal of Pharmacology and Experimental Therapeutics, 273, 591-598.
[28] Moleman, P. and Bruinvels, J. (1979) Effect of Morphine on Dopaminergic Neurons in the Rat Basal Forebrain and Striatum. Journal of Neural Transmission, 46, 225-237.
http://dx.doi.org/10.1007/BF01250788
[29] Kim, H.S., Iyengar, S. and Wood, P.L. (1986) Opiate Actions on Mesocortical Dopamine Metabolism in the Rat. Life Sciences, 39, 2033-2036.
http://dx.doi.org/10.1016/0024-3205(86)90327-9
[30] Kim, H.S., Iyengar, S. and Wood, P.L. (1987) Reversal of the Actions of Morphine on Mesocortical Dopamine Metabolism in the Rat by the Kappa Agonist MR-2034: Tentative Mu-2 Opioid Control of Mesocortical Dopaminergic Projections. Life Sciences, 41, 1711-1715.
http://dx.doi.org/10.1016/0024-3205(87)90598-4
[31] Volkov, N.D., Fowler, J.S., Wang, G.J. and Goldstain, R.Z. (2002) Role of Dopamine, the Frontal Cortex and Memory Circuits in Drug Addiction: Insight from Imaging Studies. Neurobiology of Learning and Memory, 78, 610-624.
http://dx.doi.org/10.1006/nlme.2002.4099
[32] Anokhina, I., Veretinskaja, A.G. and Vekshina, N.L. (2003) Functional Peculiarities of Dopamine System of Inbred Mice with High and Low Alcohol and Drug Craving. Questions of Addictions, 6, 62-69.
[33] Volkov, N.D., Fowler, J.S., Wang, G.J. and Swanson, J.M. (2004) Dopamine in Drug Abuse and Addiction: Results from Imaging Studies and Treatment Implications. Molecular Psychiatry, 9, 557-569.
http://dx.doi.org/10.1038/sj.mp.4001507
[34] Watanabe, T., Nakagawa, T., Yamamoto, R., Maeda, A., Minami, M. and Satoh, M. (2003) Involvement of Noradrenergic System within the Central Nucleus of Amygdale in Naloxon-Precipitated Morphine Withdrawal-Induced Conditioned Place Aversion in Rats. Psychopharmacology, 170, 80-88.
http://dx.doi.org/10.1007/s00213-003-1504-0
[35] Devoto, P., Flore, G., Pira, L., Dians, L. and Gessa, G.L. (2002) Co-Release of Noradrenaline and Dopamine in the Prefrontal Cortex after Acute Morphine and during Morphine Withdrawal. Psychopharmacology, 160, 220-224.
http://dx.doi.org/10.1007/s00213-001-0985-y
[36] Ventura, R., Alcaro, A. and Puglisi-Allegra, S. (2005) Prefrontal Cortex Norepinephrine Release Is Critical for Morphine-Induced Reward, Reinstatement and Dopamine Release in the Nucleus Accumbence. Cerebral Cortex, 15, 1877-1886. http://dx.doi.org/10.1093/cercor/bhi066
[37] Olson, V.G., Heusner, C.L., Bland, R.J., During, M.J., Weinshenker, D. and Palmiter, R.D. (2006) Role of Noradrenergic Signaling by Nucleus Tractus Solitarius in Mediating Opiate Reward. Science, 311, 1017-1020.
http://dx.doi.org/10.1126/science.1119311
[38] Sudakov, S.K., Rusakova, I.V., Trigub, M.M., Shahmatov, V.Y., Kozel, A.I. and Smith, J.E. (2005) Changes of Sensitivity to Morphine in Morphin-Dependent Rats after Laser Destruction of Prefrontal Cortex. Bulletin of Experimental Biology and Medicine, 141, 187-190.

  
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