Effects of treadmill exercise and chronic stress on anxiety-like behavior, neuronal activity, and oxidative stress in basolateral amygdala in morphine-treated rats.
addiction
basolateral amygdala
morphine
stress
treadmill running
Journal
Synapse (New York, N.Y.)
ISSN: 1098-2396
Titre abrégé: Synapse
Pays: United States
ID NLM: 8806914
Informations de publication
Date de publication:
01 2023
01 2023
Historique:
revised:
20
09
2022
received:
06
04
2022
accepted:
22
09
2022
pubmed:
7
10
2022
medline:
23
11
2022
entrez:
6
10
2022
Statut:
ppublish
Résumé
The basolateral amygdala (BLA), which is sensitive to stress, is necessary for reward-seeking behavior and addiction. Regular exercise can produce various positive effects by affecting the BLA. Therefore, we aimed to investigate the effects of chronic stress and treadmill running (TR) on anxiety-like behavior, neuronal activity, lipid peroxidation (measured by malondialdehyde (MDA) levels, a marker for oxidative stress), and total thiol in BLA, in morphine-treated rats. Male Wistar rats were restricted in restraint stress and/or ran on the treadmill and treated with morphine (5 mg/kg) for 21 days. Anxiety-like behavior was evaluated using an elevated plus maze (EPM) and open field tests (OFTs), on day 22. On day 23, neuronal activity in BLA was assessed via single-unit recording. Finally, MDA and total thiol were assessed in BLA. Our results showed that chronic administration of morphine (5 mg/kg) did not affect anxiety-like behavior. However, the morphine-treated rats, subjected to chronic stress and exercise, showed fewer anxiety-like behaviors. Morphine increased BLA's MDA levels but it was prevented by TR. Glutamatergic and GABAergic basal neuronal activities were low in morphine-treated rats but after acute morphine application, there was a significant decrease in GABAergic neuronal activities in the morphine-exercise-stress (Mor-Exe-St) group. The results of this study showed that in morphine-treated rats, stress and exercise or their combination could have either co-directional or opposite effects to the chronic effects of morphine. These results indicate the existence of common pathways similar to endogenous opioids.
Substances chimiques
Morphine
76I7G6D29C
Sulfhydryl Compounds
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
e22256Informations de copyright
© 2022 Wiley Periodicals LLC.
Références
Amohashemi, E., Reisi, P., & Alaei, H. (2021). Lateral habenula electrical stimulation with different intensities in combination with GABAB receptor antagonist reduces acquisition and expression phases of morphine-induced CPP. Neuroscience Letters, 759, 135996. https://doi.org/10.1016/j.neulet.2021.135996
Asan, E. (1997). Ultrastructural features of tyrosine-hydroxylase-immunoreactive afferents and their targets in the rat amygdala. Cell and Tissue Research, 288(3), 449-469.
Azadbakht, A. A., Radahmadi, M., Javanmard, S. H., & Reisi, P. (2015). The effects of doxepin on stress-induced learning, memory impairments, and TNF-α level in the rat hippocampus. Research in Pharmaceutical Sciences, 10(5), 460-465.
Babri, S. H., Raeisi, P., Alaei, H. A., Sharifi, M. R., & Mohades, G. (2008). Effect of forced treadmill exercise on long-term potentiation (LTP) in the dentate gyrus of hippocampus in male rats. Physiology and Pharmacology, 12(1), 39-45.
Bajo, M., Crawford, E. F., Roberto, M., Madamba, S. G., & Siggins, G. R. (2006). Chronic morphine treatment alters expression of N-methyl-D-aspartate receptor subunits in the extended amygdala. Journal of Neuroscience Research, 83(4), 532-537.
Bajo, M., Madamba, S. G., Roberto, M., & Siggins, G. R. (2014). Acute morphine alters GABAergic transmission in the central amygdala during naloxone-precipitated morphine withdrawal: Role of cyclic AMP. Frontiers in Integrative Neuroscience, 8, .https://doi.org/10.3389/fnint.2014.00045
Befort, K., Filliol, D., Ghate, A., Darcq, E., Matifas, A., Muller, J., Lardenois, A., Thibault, C., Dembele, D., Le Merrer, J., Becker, J. A., Poch, O., & Kieffer, B. L. (2008). Mu-opioid receptor activation induces transcriptional plasticity in the central extended amygdala. The European Journal of Neuroscience, 27(11), 2973-2984. https://doi.org/10.1111/j.1460-9568.2008.06273.x
Bisagno, V., González, B., & Urbano, F. J. (2016). Cognitive enhancers versus addictive psychostimulants: The good and bad side of dopamine on prefrontal cortical circuits. Pharmacological Research, 109, 108-118.
Carlsen, J., Záborszky, L., & Heimer, L. (1985). Cholinergic projections from the basal forebrain to the basolateral amygdaloid complex: A combined retrograde fluorescent and immunohistochemical study. Journal of Comparative Neurology, 234(2), 155-167.
Charmchi, E., Faramarzi, G., Rashvand, M., Zendehdel, M., & Haghparast, A. (2021). Restraint stress potentiated morphine sensitization: Involvement of dopamine receptors within the nucleus accumbens. Neurochemical Research, 46(3), 648-659.
de Souza Balk, R., Bridi, J. C., de Lima Portella, R., Carvalho, N. R., Dobrachinski, F., Da Silva, M. H., Amaral, G. P., Dias, G. R., Barbosa, N., & Soares, F. A. (2010). Clomipramine treatment and repeated restraint stress alter parameters of oxidative stress in brain regions of male rats. Neurochemical Research, 35(11), 1761-1770.
Dos Santos, T. M., Kolling, J., Siebert, C., Biasibetti, H., Bertó, C. G., Grun, L. K., Dalmaz, C., Barbé-Tuana, F. M., & Wyse, A. T. (2017). Effects of previous physical exercise to chronic stress on long-term aversive memory and oxidative stress in amygdala and hippocampus of rats. International Journal of Developmental Neuroscience, 56, 58-67. https://doi.org/10.1016/j.ijdevneu.2016.12.003
Eidson, L. N., & Murphy, A. Z. (2019). Inflammatory mediators of opioid tolerance: Implications for dependency and addiction. Peptides, 115, 51-58.
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), 173-181. https://doi.org/10.4103/1735-5362.310524
Fatahi, Z., Zibaii, M. I., & Haghparast, A. (2017). Effect of acute and subchronic stress on electrical activity of basolateral amygdala neurons in conditioned place preference paradigm: An electrophysiological study. Behavioural Brain Research, 335, 19-25. https://doi.org/10.1016/j.bbr.2017.08.008
Ferguson, A. R., Patton, B. C., Bopp, A. C., Meagher, M. W., & Grau, J. W. (2004). Brief exposure to a mild stressor enhances morphine-conditioned place preference in male rats. Psychopharmacology, 175(1), 47-52.
Gil-Lievana, E., Balderas, I., Moreno-Castilla, P., Luis-Islas, J., McDevitt, R. A., Tecuapetla, F., Gutierrez, R., Bonci, A., & Bermúdez-Rattoni, F. (2020). Glutamatergic basolateral amygdala to anterior insular cortex circuitry maintains rewarding contextual memory. Communications Biology, 3(1), 1-11.
Greenwood, B. N., Foley, T. E., Le, T. V., Strong, P. V., Loughridge, A. B., Day, H. E., & Fleshner, M. (2011). Long-term voluntary wheel running is rewarding and produces plasticity in the mesolimbic reward pathway. Behavioural Brain Research, 217(2), 354-362. https://doi.org/10.1016/j.bbr.2010.11.005
Gregus, A., Wintink, A. J., Davis, A. C., & Kalynchuk, L. E. (2005). Effect of repeated corticosterone injections and restraint stress on anxiety and depression-like behavior in male rats. Behavioural Brain Research, 156(1), 105-114.
Guitart, X., Kogan, J. H., Berhow, M., Terwilliger, R. Z., Aghajanian, G. K., & Nestler, E. J. (1993). Lewis and Fischer rat strains display differences in biochemical, electrophysiological and behavioral parameters: Studies in the nucleus accumbens and locus coeruleus of drug naive and morphine-treated animals. Brain Research, 611(1), 7-17.
Hayashi, T., & Su, T.-P. (2008). An update on the development of drugs for neuropsychiatric disorders: Focusing on the σ1 receptor ligand. Expert Opinion on Therapeutic Targets, 12(1), 45-58.
Hayes, R. J., & Gardner, E. L. (2004). The basolateral complex of the amygdala mediates the modulation of intracranial self-stimulation threshold by drug-associated cues. European Journal of Neuroscience, 20(1), 273-280.
Isoardi, N. A., Bertotto, M. E., Martijena, I. D., Molina, V. A., & Carrer, H. F. (2007). Lack of feedback inhibition on rat basolateral amygdala following stress or withdrawal from sedative-hypnotic drugs. European Journal of Neuroscience, 26(4), 1036-1044.
Jokar, Z., Khatamsaz, S., Alaei, H., & Shariati, M. (2022). Effect of electrical stimulation of central nucleus of the amygdala on morphine conditioned place preference in male rats. Iranian Journal of Basic Medical Sciences, 25(5), 604-610.
Jones, J. L., Day, J. J., Wheeler, R. A., & Carelli, R. M. (2010). The basolateral amygdala differentially regulates conditioned neural responses within the nucleus accumbens core and shell. Neuroscience, 169(3), 1186-1198.
Kalivas, P. W., & Stewart, J. (1991). Dopamine transmission in the initiation and expression of drug-and stress-induced sensitization of motor activity. Brain Research Reviews, 16(3), 223-244.
Kelle, A. E., Stinus, L., & Iversen, S. D. (1980). Interactions between D-ala-met-enkephalin, A10 dopaminergic neurons, and spontaneous behaviour in the rat. Behavioural Brain Research, 1(1), 3-24.
Kelley, A. E., Domesick, V. B., & Nauta, W. J. H. (1992). The Amygdalostriatal Projection in the Rat-An Anatomical Study by Anterograde and Retrograde Tracing Methods. In Nauta, W. J. H. (Ed.), Neuroanatomy (pp. 495-509). Boston, MA: Birkhäuser Boston.
Koob, G. F. (2009). Brain stress systems in the amygdala and addiction. Brain Research, 1293, 61-75. https://doi.org/10.1016/j.brainres.2009.03.038
Lee, B., Yun, H. Y., Shim, I., Lee, H., & Hahm, D. H. (2012). Bupleurum falcatum prevents depression and anxiety-like behaviors in rats exposed to repeated restraint stress. Journal of Microbiology and Biotechnology, 22(3), 422-430. https://doi.org/10.4014/jmb.1110.10077
Leem, Y.-H., Jang, J.-H., Park, J.-S., & Kim, H.-S. (2019). Exercise exerts an anxiolytic effect against repeated restraint stress through 5-HT2A-mediated suppression of the adenosine A2A receptor in the basolateral amygdala. Psychoneuroendocrinology, 108, 182-189.
Leuner, B., & Gould, E. (2010). Structural plasticity and hippocampal function. Annual Review of Psychology, 61, 111-140.
Li, C.-Q., Zhang, J.-W., Dai, R.-P., Wang, J., Luo, X.-G., & Zhou, X.-F. (2010). Surgical incision induces anxiety-like behavior and amygdala sensitization: Effects of morphine and gabapentin. Pain Research and Treatment, 2010, .
Lovallo, W. R. (2006). Cortisol secretion patterns in addiction and addiction risk. International Journal of Psychophysiology, 59(3), 195-202.
Ma, Q., Yin, G., Ai, M., & Han, J. (1991). Serotonergic projections from the nucleus raphe dorsalis to the amygdala in the rat. Neuroscience Letters, 134(1), 21-24.
Madden, J. t., Akil, H., Patrick, R. L., & Barchas, J. D. (1977). Stress-induced parallel changes in central opioid levels and pain responsiveness in the rat. Nature, 265(5592), 358-360. https://doi.org/10.1038/265358a0
Martini, L., & Whistler, J. L. (2007). The role of mu opioid receptor desensitization and endocytosis in morphine tolerance and dependence. Current Opinion in Neurobiology, 17(5), 556-564.
McDonald, A. J. (1992). Cell types and intrinsic connections of the amygdala. In: The amygdala: neurobiological aspects of emotion, memory, and mental dysfunction, Aggleton JP(ed) (pp. 67-96, New York, Wiley-Liss, Inc.
Miladi-Gorji, H., Rashidy-Pour, A., & Fathollahi, Y. (2012). Anxiety profile in morphine-dependent and withdrawn rats: Effect of voluntary exercise. Physiology & Behavior, 105(2), 195-202.
Moghaddasi, M., Javanmard, S. H., Reisi, P., Tajadini, M., & Taati, M. (2014). The effect of regular exercise on antioxidant enzyme activities and lipid peroxidation levels in both hippocampi after occluding one carotid in rat. Journal of Physiological Sciences, 64(5), 325-332. https://doi.org/10.1007/s12576-014-0322-y
Mohammadian, J., & Miladi-Gorji, H. (2019). Age-and sex-related changes in the severity of physical and psychological dependence in morphine-dependent rats. Pharmacology Biochemistry and Behavior, 187, 172793.
Mohseni Far, S., Mostashari, G., & Vazirian, M. (2008). Opiate dependence treatment protocol with agonist drugs. Tehran: Department of Substance Abuse Prevention and Treatment Department of Health and Medical Education.
Moreno-Martínez, S., Tendilla-Beltrán, H., Sandoval, V., Flores, G., & Terrón, J. A. (2022). Chronic restraint stress induces anxiety-like behavior and remodeling of dendritic spines in the central nucleus of the amygdala. Behavioural Brain Research, 416, 113523. https://doi.org/10.1016/j.bbr.2021.113523
Motta, V., & Brandão, M. L. (1993). Aversive and antiaversive effects of morphine in the dorsal periaqueductal gray of rats submitted to the elevated plus-maze test. Pharmacology Biochemistry and Behavior, 44(1), 119-125. https://doi.org/10.1016/0091-3057(93)90288-5
Paxinos, G., & Watson, C. (2007). The rat brain in stereotaxic coordinates in stereotaxic coordinates. Elsevier.
Pitkanen, A. (2000). Connectivity of the rat amygdaloid complex. The Amygdala, a Functional Analysis, 2, .
Powell, K. J., Abul-Husn, N. S., Jhamandas, A., Olmstead, M. C., Beninger, R. J., & Jhamandas, K. (2002). Paradoxical effects of the opioid antagonist naltrexone on morphine analgesia, tolerance, and reward in rats. Journal of Pharmacology and Experimental Therapeutics, 300(2), 588-596.
Raghav, R., Jain, R., Jacob, T. G., Dhawan, A., & Roy, T. S. (2021). Co-administration of nalbuphine attenuates the morphine-induced anxiety and dopaminergic alterations in morphine-withdrawn rats. Psychopharmacology, 238(4), 1193-1211. https://doi.org/10.1007/s00213-021-05765-3
Ranjbar, H., Radahmadi, M., Reisi, P., & Alaei, H. (2017). Effects of electrical lesion of basolateral amygdala nucleus on rat anxiety-like behaviour under acute, sub-chronic, and chronic stresses. Clinical and Experimental Pharmacology and Physiology, 44(4), 470-479.
Rezaei, Z., Alaei, H., & Reisi, P. (2022). Effects of electrical stimulation and temporary inactivation of basolateral amygdala on morphine-induced conditioned place preference in rats. Neuroscience Letters, 774, 136519. https://doi.org/10.1016/j.neulet.2022.136519
Reznikov, L. R., Reagan, L. P., & Fadel, J. R. (2009). Effects of acute and repeated restraint stress on GABA efflux in the rat basolateral and central amygdala. Brain Research, 1256, 61-68. https://doi.org/10.1016/j.brainres.2008.12.022
Rizi, A. A., Reisi, P., & Naghsh, N. (2016). Effect of forced treadmill exercise and blocking of opioid receptors with naloxone on memory in male rats. Advanced Biomedical Research, 5.
Rosenkranz, J. A., & Grace, A. A. (1999). Modulation of basolateral amygdala neuronal firing and afferent drive by dopamine receptor activation in vivo. Journal of Neuroscience, 19(24), 11027-11039.
Rybak, L., Somani, S., & Ravi, R. (1995). Effect of exercise training on antioxidant system in brain regions of rat. Pharmacology Biochemistry and Behavior, 50(4), 635-639.
Sadat-Shirazi, M.-S., Zarrindast, M.-R., & Ashabi, G. (2020). Oxidative stress enzymes are changed in opioid abusers and multidrug abusers. Journal of Clinical Neuroscience, 72, 365-369.
Salam, J. N., Fox, J. H., Detroy, E. M., Guignon, M. H., Wohl, D. F., & Falls, W. A. (2009). Voluntary exercise in C57 mice is anxiolytic across several measures of anxiety. Behavioural Brain Research, 197(1), 31-40. https://doi.org/10.1016/j.bbr.2008.07.036
Sapolsky, R. M. (1996). Stress, glucocorticoids, and damage to the nervous system: The current state of confusion. Stress, 1(1), 1-19.
Sevgi, S., Ozek, M., & Eroglu, L. (2006). L-NAME prevents anxiety-like and depression-like behavior in rats exposed to restraint stress. Methods and Findings in Experimental and Clinical Pharmacology, 28(2), 95-100.
Sinha, R. (2001). How does stress increase risk of drug abuse and relapse? Psychopharmacology, 158(4), 343-359. https://doi.org/10.1007/s002130100917
Sinha, R. (2007). The role of stress in addiction relapse. Current Psychiatry Reports, 9(5), 388-395.
Skrabalova, J., Drastichova, Z., & Novotny, J. (2013). Morphine as a potential oxidative stress-causing agent. Mini-Reviews in Organic Chemistry, 10(4), 367-372.
Smith, M. A., & Lyle, M. A. (2006). Chronic exercise decreases sensitivity to mu opioids in female rats: Correlation with exercise output. Pharmacology Biochemistry and Behavior, 85(1), 12-22. https://doi.org/10.1016/j.pbb.2006.06.020
Stagg, N. J., Mata, H. P., Ibrahim, M. M., Henriksen, E. J., Porreca, F., Vanderah, T. W., & Philip Malan, T. (2011). Regular exercise reverses sensory hypersensitivity in a rat neuropathic pain model: Role of endogenous opioids. The Journal of the American Society of Anesthesiologists, 114(4), 940-948.
Steffensen, S. C., Svingos, A. L., Pickel, V. M., & Henriksen, S. J. (1998). Electrophysiological characterization of GABAergic neurons in the ventral tegmental area. Journal of Neuroscience, 18(19), 8003-8015.
Sutoo, D., & Akiyama, K. (2003). Regulation of brain function by exercise. Neurobiology of Disease, 13(1), 1-14.
Thorsell, A., Carlsson, K., Ekman, R., & Heilig, M. (1999). Behavioral and endocrine adaptation, and up-regulation of NPY expression in rat amygdala following repeated restraint stress. Neuroreport, 10(14), 3003-3007.
Trejo, J. L., Llorens-Martín, M. V., & Torres-Alemán, I. (2008). The effects of exercise on spatial learning and anxiety-like behavior are mediated by an IGF-I-dependent mechanism related to hippocampal neurogenesis. Molecular and Cellular Neuroscience, 37(2), 402-411. https://doi.org/10.1016/j.mcn.2007.10.016
Um, H. S., Kang, E. B., Leem, Y. H., Cho, I. H., Yang, C. H., Chae, K. R., Hwang, D. Y., & Cho, J. Y. (2008). Exercise training acts as a therapeutic strategy for reduction of the pathogenic phenotypes for Alzheimer's disease in an NSE/APPsw-transgenic model. International Journal of Molecular Medicine, 22(4), 529-539.
Vyas, A., Mitra, R., Rao, B. S., & Chattarji, S. (2002). Chronic stress induces contrasting patterns of dendritic remodeling in hippocampal and amygdaloid neurons. Journal of Neuroscience, 22(15), 6810-6818.
Wang, X., Geng, X., Li, M., Xie, J., Chen, D., Han, H., Meng, X., Yao, X., Zhang, H., Gao, Y., Chang, H., Zhang, X., Wang, Y., & Wang, M. (2019). Electrophysiological and neurochemical considerations of distinct neuronal populations in the rat pedunculopontine nucleus and their responsiveness following 6-hydroxydopamine lesions. Frontiers in Neuroscience, 13, 1034.
Xi, Z.-X., & Stein, E. A. (2000). Increased mesolimbic GABA concentration blocks heroin self-administration in the rat. Journal of Pharmacology and Experimental Therapeutics, 294(2), 613-619.
Yamada, K., & Nabeshima, T. (1995). Stress-induced behavioral responses and multiple opioid systems in the brain. Behavioural Brain Research, 67(2), 133-145.
Yim, A., Moraes, C., Ferreira, T., & Oliveira, M. G. M. d. (2006). Protein synthesis inhibition in the basolateral amygdala following retrieval does not impair expression of morphine-associated conditioned place preference. Behavioural Brain Research, 171(1), 162-169.
Zarrindast, M.-R., Ahmadi, S., Haeri-Rohani, A., Rezayof, A., Jafari, M.-R., & Jafari-Sabet, M. (2004). GABAA receptors in the basolateral amygdala are involved in mediating morphine reward. Brain Research, 1006(1), 49-58.
Zarrindast, M. R., Babapoor-Farrokhran, S., Babapoor-Farrokhran, S., & Rezayof, A. (2008). Involvement of opioidergic system of the ventral hippocampus, the nucleus accumbens or the central amygdala in anxiety-related behavior. Life Sciences, 82(23-24), 1175-1181. https://doi.org/10.1016/j.lfs.2008.03.020
Zarrinkalam, E., Heidarianpour, A., Salehi, I., Ranjbar, K., & Komaki, A. (2016). Effects of endurance, resistance, and concurrent exercise on learning and memory after morphine withdrawal in rats. Life Sciences, 157, 19-24.