Effects of selective orexin receptor-2 and cannabinoid receptor-1 antagonists on the response of medial prefrontal cortex neurons to tramadol.


Journal

Synapse (New York, N.Y.)
ISSN: 1098-2396
Titre abrégé: Synapse
Pays: United States
ID NLM: 8806914

Informations de publication

Date de publication:
06 2022
Historique:
revised: 19 02 2022
received: 02 09 2021
accepted: 14 03 2022
pubmed: 22 3 2022
medline: 22 6 2022
entrez: 21 3 2022
Statut: ppublish

Résumé

Tramadol is widely used to control pain in various diseases, but the relevant mechanisms are less known despite the severe risks of abuse. The medial prefrontal cortex (mPFC) is one of the critical centers of the reward system. Studies have shown that orexins and endocannabinoids are likely to play an important role in addiction. In this study, the effect of orexin receptor-2 (OX2R) and endocannabinoid receptor-1 (CB1R) blockade on the neuronal activity of mPFC was investigated in response to tramadol in male rats. Tramadol was injected intraperitoneally, and its effects on the firing of mPFC pyramidal neurons were investigated using in vivo extracellular single-unit recording. Tramadol affected the pyramidal neuronal activity of the mPFC. AM251 (18 nmol/4 μl), as a selective CB1R antagonist, and TCS-OX2-29 (50 nmol/4 μl), as a selective OX2R antagonist, individually or simultaneously were microinjected into the lateral ventricle of the brain (intracerebroventricular, ICV). The results showed that the ratio of neurons with the excitatory/inhibitory or no responses was significantly changed by tramadol (p < .05). These changes were prevented by blockade of CB1Rs alone or blockade of OX2Rs and CB1Rs simultaneously (p < .05). However, blockade of these receptors in the vehicle group had no significant effect on neuronal activity. The findings of this study indicate the potential role of orexin and endocannabinoid systems in mediating the effects of tramadol in mPFC and the possible interaction between the two systems via OX2 and CB1 receptors. However, further studies are needed to identify these effects by examining intracellular signaling.

Identifiants

pubmed: 35313383
doi: 10.1002/syn.22232
doi:

Substances chimiques

Cannabinoid Receptor Antagonists 0
Endocannabinoids 0
Orexin Receptor Antagonists 0
Orexin Receptors 0
Receptor, Cannabinoid, CB1 0
Receptors, Cannabinoid 0
Tramadol 39J1LGJ30J

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

e22232

Informations de copyright

© 2022 Wiley Periodicals LLC.

Références

Adekomi, D. A., Adegoke, A. A., Olaniyan, O. O., Ogunrinde, A. E., & Ijomone, O. K. (2019). Effects of alcohol and tramadol co-treatment on cognitive functions and neuro-inflammatory responses in the medial prefrontal cortex of juvenile male rats. Anatomy, 13(1), 1-12.
Ahmad, T., Lauzon, N. M., de Jaeger, X., & Laviolette, S. R. (2013). Cannabinoid transmission in the prelimbic cortex bidirectionally controls opiate reward and aversion signaling through dissociable kappa versus μ-opiate receptor dependent mechanisms. Journal of Neuroscience, 33(39), 15642-15651. https://doi.org/10.1523/JNEUROSCI.1686-13.2013
Aston-Jones, G., Smith, R. J., Moorman, D. E., & Richardson, K. A. (2009). Role of lateral hypothalamic orexin neurons in reward processing and addiction. Neuropharmacology, 56, 112-121. https://doi.org/10.1016/j.neuropharm.2008.06.060
Aston-Jones, G., Smith, R. J., Sartor, G. C., Moorman, D. E., Massi, L., Tahsili-Fahadan, P., & Richardson, K. A. (2010). Lateral hypothalamic orexin/hypocretin neurons: A role in reward-seeking and addiction. Brain Research, 1314, 74-90. https://doi.org/10.1016/j.brainres.2009.09.106
Auclair, N., Otani, S., Soubrie, P., & Crepel, F. (2000). Cannabinoids modulate synaptic strength and plasticity at glutamatergic synapses of rat prefrontal cortex pyramidal neurons. Journal of Neurophysiology, 83(6), 3287-3293. https://doi.org/10.1152/jn.2000.83.6.3287
Azizi, F., Fartootzadeh, R., Alaei, H., & Reisi, P. (2018). Effects of concurrent blockade of OX2 and CB1 receptors in the ventral tegmental area on nicotine-induced place preference in rats. Neuroscience Letters, 684, 121-126. https://doi.org/10.1016/j.neulet.2018.07.017
Azizi, F., Fartootzadeh, R., Alaei, H., & Reisi, P. (2019). Electrophysiological study of the response of ventral tegmental area non-dopaminergic neurons to nicotine after concurrent blockade of orexin receptor-2 and cannabinoid receptors-1. Brain Research, 1719, 176-182. https://doi.org/10.1016/j.brainres.2019.05.042
Baimel, C., & Borgland, S. L. (2012). Hypocretin modulation of drug-induced synaptic plasticity. Progress in Brain Research, 198, 123-131. https://doi.org/10.1016/B978-0-444-59489-1.00008-2
Baldo, B. A., Daniel, R. A., Berridge, C. W., & Kelley, A. E. (2003). Overlapping distributions of orexin/hypocretin-and dopamine-β-hydroxylase immunoreactive fibers in rat brain regions mediating arousal, motivation, and stress. Journal of Comparative Neurology, 464(2), 220-237. https://doi.org/10.1002/cne.10783
Balleine, B. W., & O'doherty, J. P. (2010). Human and rodent homologies in action control: Corticostriatal determinants of goal-directed and habitual action. Neuropsychopharmacology, 35(1), 48-69. https://doi.org/10.1038/npp.2009.131
Berrendero, F., Flores, Á., & Robledo, P. (2018). When orexins meet cannabinoids: Bidirectional functional interactions. Biochemical Pharmacology, 157, 43-50. https://doi.org/10.1016/j.bcp.2018.08.040
Borgland, S., Storm, E., & Bonci, A. (2008). Orexin B/hypocretin 2 increases glutamatergic transmission to ventral tegmental area neurons. European Journal of Neuroscience, 28(8), 1545-1556. https://doi.org/10.1111/j.1460-9568.2008.06397.x
Cannon, C. Z., Kissling, G. E., Hoenerhoff, M. J., King-Herbert, A. P., & Blankenship-Paris, T. (2010). Evaluation of dosages and routes of administration of tramadol analgesia in rats using hot-plate and tail-flick tests. Laboratory Animals, 39(11), 342-351. https://doi.org/10.1038/laban1110-342
de Fonseca, F. R., Gorriti, M. A., Bilbao, A., Escuredo, L., García-segura, L. M., Piomelli, D., & Navarro, M. (2001). Role of the endogenous cannabinoid system as a modulator of dopamine transmission: Implications for Parkinson's disease and schizophrenia. Neurotoxicity Research, 3(1), 23-35. https://doi.org/10.1007/BF03033228
Delfs, J. M., Zhu, Y., Druhan, J. P., & Aston-Jones, G. S. (1998). Origin of noradrenergic afferents to the shell subregion of the nucleus accumbens: Anterograde and retrograde tract-tracing studies in the rat. Brain Research, 806(2), 127-140. https://doi.org/10.1016/S0006-8993(98)00672-6
Fartootzadeh, R., Alaei, H., & Reisi, P. (2021). Mutual assistance of nucleus accumbens cannabinoid receptor-1 and orexin receptor-2 in response to nicotine: A single-unit study. Research in Pharmaceutical Sciences, 16(2), 173.
Fartootzadeh, R., Azizi, F., Alaei, H., & Reisi, P. (2019). Functional crosstalk of nucleus accumbens CB1 and OX2 receptors in response to nicotine-induced place preference. Neuroscience Letters, 698, 160-164. https://doi.org/10.1016/j.neulet.2019.01.027
Fattore, L., Deiana, S., Spano, S. M., Cossu, G., Fadda, P., Scherma, M., & Fratta, W. (2005). Endocannabinoid system and opioid addiction: Behavioural aspects. Pharmacology Biochemistry and Behavior, 81(2), 343-359. https://doi.org/10.1016/j.pbb.2005.01.031
Fattore, L., Viganò, D., Fadda, P., Rubino, T., Fratta, W., & Parolaro, D. (2007). Bidirectional regulation of mu-opioid and CB1-cannabinoid receptor in rats self-administering heroin or WIN 55,212-2. European Journal of Neuroscience, 25(7), 2191-2200. https://doi.org/10.1111/j.1460-9568.2007.05470.x
Flores, Á., Maldonado, R., & Berrendero, F. (2013). Cannabinoid-hypocretin cross-talk in the central nervous system: What we know so far. Frontiers in Neuroscience, 7, 256. https://doi.org/10.3389/fnins.2013.00256
Fogaça, M. V., Sonego, A. B., Rioli, V., Gozzo, F. C., Dale, C. S., Ferro, E. S., & Guimarães, F. S. (2015). Anxiogenic-like effects induced by hemopressin in rats. Pharmacology Biochemistry and Behavior, 129, 7-13. https://doi.org/10.1016/j.pbb.2014.11.013
Geisler, S., Derst, C., Veh, R. W., & Zahm, D. S. (2007). Glutamatergic afferents of the ventral tegmental area in the rat. Journal of Neuroscience, 27(21), 5730-5743. https://doi.org/10.1523/JNEUROSCI.0012-07.2007
Heidbreder, C. A., & Groenewegen, H. J. (2003). The medial prefrontal cortex in the rat: Evidence for a dorso-ventral distinction based upon functional and anatomical characteristics. Neuroscience & Biobehavioral Reviews, 27(6), 555-579.
Howell, L. L., & Cunningham, K. A. (2015). Serotonin 5-HT2 receptor interactions with dopamine function: Implications for therapeutics in cocaine use disorder. Pharmacological Reviews, 67(1), 176-197. https://doi.org/10.1124/pr.114.009514
Ji, G., & Neugebauer, V. (2011). Pain-related deactivation of medial prefrontal cortical neurons involves mGluR1 and GABA(A) receptors. Journal of Neurophysiology, 106(5), 2642-2652. 10.1152/jn.00461.2011
Ji, G., & Neugebauer, V. (2012). Modulation of medial prefrontal cortical activity using in vivo recordings and optogenetics. Molecular Brain, 5(1), 1-10. https://doi.org/10.1186/1756-6606-5-36
Ji, G., Sun, H., Fu, Y., Li, Z., Pais-Vieira, M., Galhardo, V., & Neugebauer, V. (2010). Cognitive impairment in pain through amygdala-driven prefrontal cortical deactivation. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience, 30(15), 5451-5464. 10.1523/JNEUROSCI.0225-10.2010
Jin, J., Chen, Q., Qiao, Q., Yang, L., Xiong, J., Xia, J., Hu, Z., & Chen, F. (2016). Orexin neurons in the lateral hypothalamus project to the medial prefrontal cortex with a rostro-caudal gradient. Neuroscience Letters, 621, 9-14. https://doi.org/10.1016/j.neulet.2016.04.002
Khodayari, S., Pakdel, F. G., Shahabi, P., & Naderi, S. (2019). Acute tramadol-induced cellular tolerance and dependence of ventral tegmental area dopaminergic neurons: An in vivo electrophysiological study. Basic and Clinical Neuroscience, 10(3), 209.
Kimura, M., Obata, H., & Saito, S. (2012). Antihypersensitivity effects of tramadol hydrochloride in a rat model of postoperative pain. Anesthesia & Analgesia, 115(2), 443-449.
Lafourcade, M., Elezgarai, I., Mato, S., Bakiri, Y., Grandes, P., & Manzoni, O. J. (2007). Molecular components and functions of the endocannabinoid system in mouse prefrontal cortex. Plos One, 2(8), e709. https://doi.org/10.1371/journal.pone.0000709
Li, B., Chen, F., Ye, J., Chen, X., Yan, J., Li, Y., Xiong, Y., Zhou, Z., Xia, J., & Hu, Z. (2010). The modulation of orexin A on HCN currents of pyramidal neurons in mouse prelimbic cortex. Cerebral Cortex, 20(7), 1756-1767. https://doi.org/10.1093/cercor/bhp241
Lisboa, S. F., Borges, A. A., Nejo, P., Fassini, A., Guimarães, F. S., & Resstel, L. B. (2015). Cannabinoid CB1 receptors in the dorsal hippocampus and prelimbic medial prefrontal cortex modulate anxiety-like behavior in rats: Additional evidence. Progress in Neuro-Psychopharmacology and Biological Psychiatry, 59, 76-83. https://doi.org/10.1016/j.pnpbp.2015.01.005
Lisboa, S. F., Reis, D. G., da Silva, A. L., Corrêa, F. M., Guimaraes, F. S., & Resstel, L. B. (2010). Cannabinoid CB1 receptors in the medial prefrontal cortex modulate the expression of contextual fear conditioning. International Journal of Neuropsychopharmacology, 13(9), 1163-1173. https://doi.org/10.1017/S1461145710000684
Mahler, S. V., Smith, R. J., Moorman, D. E., Sartor, G. C., & Aston-Jones, G. (2012). Multiple roles for orexin/hypocretin in addiction. Progress in Brain Research, 198, 79-121. https://doi.org/10.1016/B978-0-444-59489-1.00007-0
Maldonado, R. (2010). The endogenous opioid system and drug addiction. Paper presented at the Annales pharmaceutiques francaises.
Marcus, J. N., Aschkenasi, C. J., Lee, C. E., Chemelli, R. M., Saper, C. B., Yanagisawa, M., & Elmquist, J. K. (2001). Differential expression of orexin receptors 1 and 2 in the rat brain. Journal of Comparative Neurology, 435(1), 6-25. https://doi.org/10.1002/cne.1190
Miller, E. K., & Cohen, J. D. (2001). An integrative theory of prefrontal cortex function. Annual Review of Neuroscience, 24(1), 167-202. https://doi.org/10.1146/annurev.neuro.24.1.167
Miotto, K., Cho, A. K., Khalil, M. A., Blanco, K., Sasaki, J. D., & Rawson, R. (2017). Trends in tramadol: Pharmacology, metabolism, and misuse. Anesthesia & Analgesia, 124(1), 44-51.
Mohamed, H. M., & Mahmoud, A. M. (2019). Chronic exposure to the opioid tramadol induces oxidative damage, inflammation and apoptosis, and alters cerebral monoamine neurotransmitters in rats. Biomedicine & Pharmacotherapy, 110, 239-247.
Munro, G., Erichsen, H. K., Nielsen, A. N., Nielsen, E. Ø., Scheel-Kruger, J., Weikop, P., & Peters, D. (2008). The novel compound (±)-1-[10-((E)-3-Phenyl-allyl)-3, 10-diaza-bicyclo [4.3. 1] dec-3-yl]-propan-1-one (NS7051) attenuates nociceptive transmission in animal models of experimental pain; a pharmacological comparison with the combined μ-opioid receptor agonist and monoamine reuptake inhibitor tramadol. Neuropharmacology, 54(2), 331-343.
Parolaro, D., Vigano, D., Realini, N., & Rubino, T. (2007). Role of endocannabinoids in regulating drug dependence. Neuropsychiatric Disease and Treatment, 3(6), 711.
Parsons, L. H., & Hurd, Y. L. (2015). Endocannabinoid signalling in reward and addiction. Nature Reviews Neuroscience, 16(10), 579-594. https://doi.org/10.1038/nrn4004
Paxinos, G., & Watson, C. (2006). The rat brain in stereotaxic coordinates: Hard cover edition. Elsevier.
Pfarr, S. (2018). The role of the medial prefrontal cortex in reward seeking: Functional evidence on cellular and molecular mechanisms underlying drug and natural reward seeking. Dissertation, heiDok, Heidelberg University.
Pfarr, S., Meinhardt, M. W., Klee, M. L., Hansson, A. C., Vengeliene, V., Schönig, K., Bartsch, D., Hope, B. T., Spanagel, R., & Sommer, W. H. (2015). Losing control: Excessive alcohol seeking after selective inactivation of cue-responsive neurons in the infralimbic cortex. Journal of Neuroscience, 35(30), 10750-10761. https://doi.org/10.1523/JNEUROSCI.0684-15.2015
Piomelli, D. (2011). Erratum: The endocannabinoid system in brain reward processes (British Journal of Pharmacology (2008) 154: 2 (369-383)). British Journal of Pharmacology, 163(6), 1326.
Pistis, M., Ferraro, L., Pira, L., Flore, G., Tanganelli, S., Gessa, G. L., & Devoto, P. (2002). Δ9-Tetrahydrocannabinol decreases extracellular GABA and increases extracellular glutamate and dopamine levels in the rat prefrontal cortex: An in vivo microdialysis study. Brain Research, 948(1-2), 155-158. https://doi.org/10.1016/S0006-8993(02)03055-X
Preston, K. L., Jasinski, D. R., & Testa, M. (1991). Abuse potential and pharmacological comparison of tramadol and morphine. Drug and Alcohol Dependence, 27(1), 7-17. https://doi.org/10.1016/0376-8716(91)90081-9
Sadat-Shirazi, M.-S., Babhadi-Ashar, N., Khalifeh, S., Mahboubi, S., Ahmadian-Moghaddam, H., & Zarrindast, M.-R. (2019). Tramadol induces changes in Δ-FosB, μ-opioid receptor, and p-CREB level in the nucleus accumbens and prefrontal cortex of male Wistar rat. The American Journal of Drug and Alcohol Abuse, 45(1), 84-89. https://doi.org/10.1080/00952990.2018.1529182
Scott, L. J., & Perry, C. M. (2000). Tramadol. Drugs, 60(1), 139-176. https://doi.org/10.2165/00003495-200060010-00008
Sharf, R., Sarhan, M., & DiLeone, R. J. (2010). Role of orexin/hypocretin in dependence and addiction. Brain Research, 1314, 130-138. https://doi.org/10.1016/j.brainres.2009.08.028
Siegel, J. M. (2004). Hypocretin (orexin): Role in normal behavior and neuropathology. Annual Review of Psychology, 55, 125-148. https://doi.org/10.1146/annurev.psych.55.090902.141545
Solinas, M., Goldberg, S. R., & Piomelli, D. (2008). The endocannabinoid system in brain reward processes. British Journal of Pharmacology, 154(2), 369-383. https://doi.org/10.1038/bjp.2008.130
Taslimi, Z., Haghparast, A., Hassanpour-Ezatti, M., & Safari, M.-S. (2011). Chemical stimulation of the lateral hypothalamus induces conditioned place preference in rats: Involvement of OX1 and CB1 receptors in the ventral tegmental area. Behavioural Brain Research, 217(1), 41-46. https://doi.org/10.1016/j.bbr.2010.10.007
Tong, Z. Y., Overton, P., & Clark, D. (1996). Stimulation of the prefrontal cortex in the rat induces patterns of activity in midbrain dopaminergic neurons which resemble natural burst events. Synapse, 22(3), 195-208. https://doi.org/10.1002/(SICI)1098-2396(199603)22:3%3c195::AID-SYN1%3e3.0.CO;2-7
Tsou, K., Brown, S., Sanudo-Pena, M., Mackie, K., & Walker, J. (1998). Immunohistochemical distribution of cannabinoid CB1 receptors in the rat central nervous system. Neuroscience, 83(2), 393-411. https://doi.org/10.1016/S0306-4522(97)00436-3
Tzschentke, T. (2000). The medial prefrontal cortex as a part of the brain reward system. Amino Acids, 19(1), 211-219. https://doi.org/10.1007/s007260070051
Tzschentke, T. M., & Schmidt, W. J. (1998). Discrete quinolinic acid lesions of the rat prelimbic medial prefrontal cortex affect cocaine-and MK-801-, but not morphine-and amphetamine-induced reward and psychomotor activation as measured with the place preference conditioning paradigm. Behavioural Brain Research, 97(1-2), 115-127. https://doi.org/10.1016/S0166-4328(98)00034-5
Xu, P., Chen, A., Li, Y., Xing, X., & Lu, H. (2019). Medial prefrontal cortex in neurological diseases. Physiological Genomics, 51(9), 432-442. https://doi.org/10.1152/physiolgenomics.00006.2019
Yaeger, J. D., Krupp, K. T., Gale, J. J., & Summers, C. H. (2020). Counterbalanced microcircuits for Orx1 and Orx2 regulation of stress reactivity. Medicine in Drug Discovery, 8, 100059. https://doi.org/10.1016/j.medidd.2020.100059
Yang, W., He, H., Pan, Y., Duan, F., Zhao, D., Hu, B., Zhou, Q., & Liu, W. (2017). Cocaine withdrawal reduces gamma-aminobutyric acid-ergic transmission and gephyrin expression at medial prefrontal cortex in cocaine-conditioned place-preference rats, which shows increased cocaine seeking. European Addiction Research, 23(1), 28-36. https://doi.org/10.1159/000452657

Auteurs

Neda Hasanpour Razmanjani (N)

Department of Physiology, School of Medicine, Isfahan University of Medical Sciences, Isfahan, Iran.

Parham Reisi (P)

Department of Physiology, School of Medicine, Isfahan University of Medical Sciences, Isfahan, Iran.

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