The effect of acute and chronic administration of naloxone on spatial memory in male cholestatic rats

Document Type: Research Paper

Authors

1 Department of medical physiology, faculty of medicine, Tehran University of medical sciences, Tehran, Iran.

2 Department of medical physiology, faculty of medicine, Tehran University of medical sciences, Tehran, Iran

Abstract

Background and Objective: A great body of evidences suggested a marked elevation of endogenous opioid levels in plasma of animals with acute cholestasis. Endogenous opioids are implicated in the pathophysiology of cholestasis. Also, many studies have shown that endogenous opioids modulate memory processes. To clarify possible role of endogenous opioid receptors in information processing in acute cholestatic rats, we administered acute (5 mg/kg, i.p.) and chronic (by implanted osmotic mini-pump, s.c.) naloxone as an opioid receptor antagonist to male cholestatic rats.
Materials and Methods: For this purpose, male rats were divided into eight groups. All the rats were assessed for spatial learning and memory (a major cognitive function in rats) by the Morris water maze task about 8 days after the first operation. Rats were subjected to 6 days of training in the Morris water maze (MWM): 4 days with the invisible platform to test spatial learning and on the 5th day, one day after the last trial, retention performance was examined in a single probe trial. On the 6th day, motivation and sensory-motor coordination was tested with the visible platform.
Results: During the four consecutive acquisition trial days of this behavioral test, acute and chronic naloxone-treated bile duct-ligated rats had a significantly longer latency to escape than the bile duct-ligated groups (p Conclusion: The results of this study suggest that blockade of opioid receptors, both acute and chronic, results in spatial memory deficits in cholestatic rats.

Keywords


  1. Zarrindast MR, Hoseindoost S, Nasehi M. Possible interaction between opioidergic and cholinergic systems of CA1 in cholestasis-induced amnesia in mice. Behavioural Brain Research 2012; 28(1):116-24.
  2. Kremer AE, Namer B, Bolier R, Fischer MJ, Oude Elferink RP, Beuers U. Pathogenesis and Management of Pruritus in PBC and PSC. Digestive Diseases 2015;33 Suppl 2:164-75.
  3. Hasanein P, Parviz M. Role of GABAA receptor in modulation of acute thermal pain using a rat model of cholestasis. Pharmacology Biochemistry & Behavior 2014 Sep;124:226-30.
  4. Haj-Mirzaian A, Hamzeh N, Javadi-Paydar M, Abdollahzadeh Estakhri MR, Dehpour AR. Resistance to depression through interference of opioid and nitrergic systems in bile-duct ligated mice. European Journal of Pharmacology 2013;708(1-3):38-43.
  5. Bunchorntavakul C, Reddy KR. Pruritus in chronic cholestatic liver disease. Clinical Liver Disease 2012; 16(2):331-46.
  6. Swain MG. Alterations in hypothalamic mu-opiate receptor-mediated responses but not methionine enkephalin or proenkephalin messenger RNA levels in rats with acute cholestasis. Hepatology 1994; 20(3):700-5.
  7. Inan S, Cowan A. Reduced kappa-opioid activity in a rat model of cholestasis.  European Journal of Pharmacology 2005; 518(2-3):182-6.
  8. Bodnar RJ. Endogenous opiates and behavior: 2015. Peptides. 2017 Feb;88:126-188.
  9. Hawes SL, Salinas AG, Lovinger DM, Blackwell KT. Long-term plasticity of corticostriatal synapses is modulated by pathway-specific co-release of opioids through κ-opioid receptors. Journal of Physiology 2017;595(16):5637-5652.
  10. Wang SY, Duan YL, Zhao B, Wang XR, Zhao Z, Zhang GM. Effect of delta opioid receptor activation on spatial cognition and neurogenesis in cerebral ischemic rats. Neuroscience Letters 2016;620:20-6.
  11. Rizi AA, Reisi P, Naghsh N. Effect of forced treadmill exercise and blocking of opioid receptors with naloxone on memory in male rats. Advanced Biomedical Research 2016;5:20.
  12. Gold A, Rogers A, Cruchley E, Rankin S, Parmar A, Kamath BM, Avitzur Y, Ng VL. Assessment of School Readiness in Chronic Cholestatic Liver Disease: A Pilot Study Examining Children with and without Liver Transplantation. Canadian Journal of Gastroenterology and Hepatology 2017;9873945.
  13. Huang LT, Hsieh CS, Chou MH, Chuang JH, Liou CW, Tiao MM, Lai MC. Obstructive jaundice in rats: cause of spatial memory deficits with recovery after biliary decompression. World Journal of Surgery 2004;28(3):283-7.
  14. Mokhtari Z, Baluchnejadmojarad T, Nikbakht F, Mansouri M, Roghani M. Riluzole ameliorates learning and memory deficits in Aβ25-35-induced rat model of Alzheimer's disease and is independent of cholinoceptor activation. Biomedicine & Pharmacotherapy 2017;87:135-144.
  15. Bergasa NV, Sabol SL, Young WS 3rd, Kleiner DE, Jones EA.  Cholestasis is associated with preproenkephalin mRNA expression in the adult rat liver.  American Journal of Physiology1995;268(2 Pt 1):G346-54.
  16. Owczarek D, Garlicka M, Pierzchała-Koziec K, Skulina D, Szulewski P. Met-enkephalin plasma concentration and content in liver tissue in patients with primary biliary cirrhosis. Przegl Lek 2003;60(7):461-6
  17. Ebrahimkhani MR, Moezi L, Kiani S, Merat S, Dehpour AR. Opioid receptor blockade improves mesenteric responsiveness in biliary cirrhosis. Digestive Diseases and Sciences 2008;53(11):3007-11.
  18. Jones EA, Bergasa NV. The pruritus of cholestasis: from bile acids to opiate agonists. Hepatology 1990;11(5):884-7.
  19. Swain MG, Rothman RB, Xu H, Vergalla J, Bergasa NV, Jones EA. Endogenous opioids accumulate in plasma in a rat model of acute cholestasis. Gastroenterology 1992;103(2):630-5.
  20. Swain MG, MacArthur L, Vergalla J, Jones EA. Adrenal secretion of BAM-22P, a potent opioid peptide, is enhanced in rats with acute cholestasis. American Journal of Physiology 1994;266(2 Pt 1):G201-5.
  21. Ahmadi S, Karami Z, Mohammadian A, Khosrobakhsh F, Rostamzadeh J. Cholestasis induced antinociception and decreased gene expression of MOR1 in rat brain. Neuroscience 2015;284:78-86.
  22. Zamir N, Quirion R, Segal M. Ontogeny and regional distribution of proenkephalin- and prodynorphin-derived peptides and opioid receptors in rat hippocampus. Neuroscience 1985;15(4):1025-34.
  23. Harte-Hargrove LC, Varga-Wesson A, Duffy AM, Milner TA, Scharfman HE. Opioid receptor-dependent sex differences in synaptic plasticity in the hippocampal mossy fiber pathway of the adult rat. Journal of Neuroscience 2015;35(4):1723-38.
  24. Bodnar RJ. Endogenous opiates and behavior: 2012. Peptides 2013;50:55-95.
  25. Derrick BE, Martinez JL Jr. Opioid receptor activation is one factor underlying the frequency dependence of mossy fiber LTP induction. Journal of Neuroscience 1994 ;14(7):4359-67.
  26. Laredo SA, Steinman MQ, Robles CF, Ferrer E, Ragen BJ, Trainor BC. Effects of defeat stress on behavioral flexibility in males and females: modulation by the mu-opioid receptor. European Journal of Neuroscience 2015 Feb;41(4):434-41.
  27. Cao LQ, Wen J, Liu ZQ. Opioid μ receptors mediate the stress-induced spatial reference memory impairment. Sheng Li Xue Bao 2015;67(2):173-80.
  28. Ukai M, Watanabe Y, Kameyama T. Effects of endomorphins-1 and -2, endogenous mu-opioid receptor agonists, on spontaneous alternation performance in mice. European Journal of Pharmacology 2000;395(3):211-5.
  29. Freitas Castro V, Nascimento Alves P, Franco AC, Martins IP, Conceição I. Cognitive impairment in liver transplanted patients with transthyretin-related hereditary amyloid polyneuropathy. Amyloid 2017;24(2):110-114.
  30. Huang LT, Hsieh CS, Chou MH, Chuang JH, Liou CW, Tiao MM, Lai MC. Obstructive jaundice in rats: cause of spatial memory deficits with recovery after biliary decompression. World Journal of Surgery 2004;28(3):283-7.
  31. Ghiassy B, Rahimi N, Javadi-Paydar M, Gharedaghi MH, Norouzi-Javidan A, Dehpour AR. Nitric oxide mediates effects of acute, not chronic, naltrexone on LPS-induced hepatic encephalopathy in cirrhotic rats. Canadian Journal of Physiology and Pharmacology 2017;95(1):16-22.
  32. Chen JJ, Dymshitz J, Vasko MR. Regulation of opioid receptors in rat sensory neurons in culture. Molecular Pharmacology 1997; 51(4):666-73.