Differential change in cortical and hippocampal monoamines, and behavioral patterns in streptozotocin-induced type 1 diabetes rats

Document Type: Original Article

Authors

1 School of Chinese Medicines for Post-Baccal aureate, I-Shou University, Kaohsiung 82445, Taiwan

2 Taichung Hospital, Ministry of Health and Welfare, Taichung 402, Taiwan

3 School of Post-Baccalaureate Chinese Medicine, Tzu Chi University, Hualien 97071, Taiwan

4 Pintung Branch, Kaohsiung Veterans General Hospital, Pintung 91245, Taiwan

5 Department of Chinese Pharmaceutical Sciences and Chinese Medicine Resources, College of Pharmacy, China Medical University, Taichung 402, Taiwan

Abstract

Objective(s): Diabetes mellitus (DM) is a widespread metabolic disorder worldwide. Clinical physicians have found diabetic patients have mild to middle cognitive dysfunction and an alteration of brain monoaminergic function. This study explored the change in various patterns of behavioral models and brain monoamine function under streptozotocin (STZ)-induced type 1 diabetes.
Materials and Methods: We established a type 1 DM model via intravenous injection with STZ (65 mg/kg) in rats. Three weeks after the STZ injection, various behavioral measurements including the inhibitory avoidance test, active avoidance test and Morris water maze were conducted. Finally, all rats were dissected and the concentrations of monoamines and their metabolites in cortex and hippocampus were measured by high performance liquid chromatography with electrochemical detection.
Results: We found that STZ induced type 1 diabetes (hyperglycemia and lack of insulin) in rats. STZ-induced diabetic rats had cognitive impairment in acquisition sessions and long-term retention of the active avoidance test. STZ-induced diabetic rats also had cognitive impairment in spatial learning, reference and working memory of the Morris water maze. STZ significantly reduced concentrations of norepinephrine (NE) in the cortex and dopamine (DA) in the hippocampus, but increased concentrations of DA and serotonin (5-HT) in the cortex 35 days after injection. The concentration of 5-HT in the hippocampus was also significantly increased.
Conclusion: The data suggested that this cognitive impairment after a short-term period of STZ injection might be related to cortical NE dysfunction, differential alteration of cortical and hippocampal DA function, and brain 5-HT hyperfunction.

Keywords

Main Subjects


1. Crawford K. Review of 2017 Diabetes standards of care. Nurs Clin North Am 2017; 52:621-663.
2. Moheet A, Mangia S, Seaquist ER. Impact of diabetes on cognitive function and brain structure. Ann N Y Acad Sci 2015; 1353:60-71.
3. Yoon S, Kim J, Musen G, Renshaw PF, Hwang J, Bolo NR, et al. Prefronto-temporal white matter microstructural alterations 20 years after the diagnosis of type 1 diabetes mellitus. Pediatr Diabetes 2017.
4. Antenor-Dorsey JA, Meyer E, Rutlin J, Perantie DC, White NH, Arbelaez AM, Shimony JS, et al. White matter microstructural integrity in youth with type 1 diabetes. Diabetes 2013; 62: 581-589.
5. Perantie DC, Koller JM, Weaver PM, Lugar HM, Black KJ, White NH, et al. Prospectively determined impact of type 1 diabetes on brain volume during development. Diabetes 2011; 60: 3006-3014.
6. Uzun N, Uluduz D, Mikla S, Aydin A. Evaluation of asymptomatic central neuropathy in type I diabetes mellitus. Electromyogr Clin Neurophysiol 2006; 46:131-137.
7. Guardia-Olmos J, Gallardo-Moreno GB, Gudayol-Ferre E, Pero-Cebollero M, Gonzalez-Garrido AA. Effect of verbal task complexity in a working memory paradigm in patients with type 1 diabetes. A fMRI study. PLoS One 2017; 12:e0178172.
8. Fried PJ, Schilberg L, Brem AK, Saxena S, Wong B, Cypess AM, et al. Humans with type-2 diabetes show abnormal long-term potentiation-like cortical plasticity associated with verbal learning deficits. J Alzheimers Dis 2017; 55:89-100.
9. Jodar L, Kaneto H. Synaptic plasticity: stairway to memory. Jpn J Pharmacol 1995; 68:359-387.
10. Manjarrez G, Vazquez F, Delgado M, Herrera R, Hernandez J. A functional disturbance in the auditory cortex related to a low serotonergic neurotransmission in women with type 2 diabetes. Neuroendocrinology 2007; 86:289-294.
11. Yokoi K, Kazuta T, Torii R, Endo T, Araki A, Terao S. Effectiveness of levodopa treatment for diabetic chorea with reduced striatal accumulation in dopamine transporter SPECT: a case report. Rinsho Shinkeigaku 2017; 57:591-594.
12. Small DM. Dopamine adaptations as a common pathway for neurocognitive impairment in diabetes and obesity: a neuropsychological perspective. Front Neurosci 2017; 11:134.
13. Tsigos C, Reed P, Weinkove C, White A, Young RJ. Plasma norepinephrine in sensory diabetic polyneuropathy. Diabetes Care 1993; 16:722-727.
14. Ganguly PK, Beamish RE, Dhalla KS, Innes IR, Dhalla NS. Norepinephrine storage, distribution, and release in diabetic cardiomyopathy. Am J Physiol 1987; 252:E734-739.
15. King A, Bowe J. Animal models for diabetes: understanding the pathogenesis and finding new treatments. Biochem Pharmacol 2016; 99:1-10.
16. Al-Awar A, Kupai K, Veszelka M, Szucs G, Attieh Z, Murlasits Z, et al. Experimental diabetes mellitus in different animal models. J Diabetes Res 2016; 2016:9051426.
17. Rajashree R, Patil R, Khlokute SD, Goudar SS. Effect of Salacia reticulata W. and Clitoria ternatea L. on the cognitive and behavioral changes in the streptozotocin-induced young diabetic rats. J Basic Clin Physiol Pharmacol 2017; 28:107-114.
18. Palleria C, Leo A, Andreozzi F, Citraro R, Iannone M, Spiga R, et al. Liraglutide prevents cognitive decline in a rat model of streptozotocin-induced diabetes independently from its peripheral metabolic effects. Behav Brain Res 2017; 321:157-169.
19. Noor A, Zahid S. Alterations in adult hippocampal neurogenesis, aberrant protein s-nitrosylation, and associated spatial memory loss in streptozotocin-induced diabetes mellitus type 2 mice. Iran J Basic Med Sci 2017; 20:1159-1165.
20. Fang SC, Xie H, Chen F, Hu M, Long Y, Sun HB, et al. Simvastatin ameliorates memory impairment and neurotoxicity in streptozotocin-induced diabetic mice. Neuroscience 2017; 355:200-211.
21. Jabbarpour Z, Shahidi S, Saidijam M, Sarihi A, Hassanzadeh T, Esmaeili R. Effect of tempol on the passive avoidance and novel object recognition task in diabetic rats. Brain Res Bull 2014; 101:51-56.
22. Popovic M, Biessels GJ, Isaacson RL, Gispen WH. Learning and memory in streptozotocin-induced diabetic rats in a novel spatial/object discrimination task. Behav Brain Res 2001; 122:201-207.
23. Zaraiskaya Yu I, Aleksandrova EA, Lukashev AO, Shvyrkova NA. Features of active avoidance learning in rats with streptozotocin diabetes. Neurosci Behav Physiol 1994; 24:167-169.
24. Lim DK, Lee KM, Ho IK. Changes in the central dopaminergic systems in the streptozotocin-induced diabetic rats. Arch Pharm Res 1994; 17:398-404.
25. Shimomura Y, Shimizu H, Takahashi M, Uehara Y, Kobayashi I, Kobayashi S. Ambulatory activity and dopamine turnover in streptozotocin-induced diabetic rats. Exp Clin Endocrinol 1990; 95:385-388.
26. Trulson ME, Himmel CD. Decreased brain dopamine synthesis rate and increased (3H)spiroperidol binding in streptozotocin-diabetic rats. J Neurochem 1983; 40:1456-1459.
27. Baranov VG, Propp MV, Sokoloverova IM, Savchenko ON, Onegova RF. Dopamine, noradrenaline and serotonin content in various parts of the hypothalamus in alloxan diabetes. Probl Endokrinol (Mosk) 1980; 26:43-48.
28. Myhrer T. Neurotransmitter systems involved in learning and memory in the rat: a meta-analysis based on studies of four behavioral tasks. Brain Res Brain Res Rev 2003; 41:268-287.
29. Phyu HE, Irwin JC, Vella RK, Fenning AS. Resveratrol shows neuronal and vascular-protective effects in older, obese, streptozotocin-induced diabetic rats. Br J Nutr 2016; 115:1911-1918.
30. Hsieh MT, Wu CR, Hsieh CC. Ameliorating effect of p-hydroxybenzyl alcohol on cycloheximide-induced impairment of passive avoidance response in rats: interactions with compounds acting at 5-HT1A and 5-HT2 receptors. Pharmacol Biochem Behav 1998; 60:337-343.
31. Nasir MN, Habsah M, Zamzuri I, Rammes G, Hasnan J, Abdullah J. Effects of asiatic acid on passive and active avoidance task in male Spraque-Dawley rats. J Ethnopharmacol 2011; 134:203-209.
32. Wagner AK, Brayer SW, Hurwitz M, Niyonkuru C, Zou H, Failla M, et al. Non-spatial pre-training in the water maze as a clinically relevant model for evaluating learning and memory in experimental TBI. Neurobiol Learn Mem 2013; 106:71-86.
33. Shiao YJ, Su MH, Lin HC, Wu CR. Echinacoside ameliorates the memory impairment and cholinergic deficit induced by amyloid beta peptides via the inhibition of amyloid deposition and toxicology. Food Funct 2017; 8:2283-2294.
34. Sarihi A, Motamedi F, Naghdi N, Rashidy-Pour A. Lidocaine reversible inactivation of the median raphe nucleus has no effect on reference memory but enhances working memory versions of the Morris water maze task. Behav Brain Res 2000; 114:1-9.
35. Glowinski J, Iversen LL. Regional studies of catecholamines in the rat brain. I. The disposition of (3H)norepinephrine, (3H)dopamine and (3H)dopa in various regions of the brain. J Neurochem 1966; 13:655-669.
36. Baydas G, Nedzvetskii VS, Nerush PA, Kirichenko SV, Yoldas T. Altered expression of NCAM in hippocampus and cortex may underlie memory and learning deficits in rats with streptozotocin-induced diabetes mellitus. Life Sci 2003; 73:1907-1916.
37. Leedom LJ, Meehan WP, Zeidler A. Avoidance responding in mice with diabetes mellitus. Physiol Behav 1987; 40:447-451.
38. Jing XH, Chen SL, Shi H, Cai H, Jin ZG. Electroacupuncture restores learning and memory impairment induced by both diabetes mellitus and cerebral ischemia in rats. Neurosci Lett 2008; 443:193-198.
39. Telli O, Cavlak U. Measuring the pain threshold and tolerance using electrical stimulation in patients with Type II diabetes mellitus. J Diabetes Complications 2006; 20:308-316.
40. Romanovsky D, Hastings SL, Stimers JR, Dobretsov M. Relevance of hyperglycemia to early mechanical hyperalgesia in streptozotocin-induced diabetes. J Peripher Nerv Syst 2004; 9:62-69.
41. Suzuki Y, Sato J, Kawanishi M, Mizumura K. Lowered response threshold and increased responsiveness to mechanical stimulation of cutaneous nociceptive fibers in streptozotocin-diabetic rat skin in vitro--correlates of mechanical allodynia and hyperalgesia observed in the early stage of diabetes. Neurosci Res 2002; 43:171-178.
42. Kucukatay V, Hacioglu G, Ozkaya G, Agar A, Yargicoglu P. The effect of diabetes mellitus on active avoidance learning in rats: the role of nitric oxide. Med Sci Monit 2009; 15:BR88-93.
43. Biessels GJ, Kamal A, Ramakers GM, Urban IJ, Spruijt BM, Erkelens DW, et al. Place learning and hippocampal synaptic plasticity in streptozotocin-induced diabetic rats. Diabetes 1996; 45:1259-1266.
44. Kapadia M, Xu J, Sakic B. The water maze paradigm in experimental studies of chronic cognitive disorders: Theory, protocols, analysis, and inference. Neurosci Biobehav Rev 2016; 68:195-217.
45. Aung MH, Kim MK, Olson DE, Thule PM, Pardue MT. Early visual deficits in streptozotocin-induced diabetic long evans rats. Invest Ophthalmol Vis Sci 2013; 54:1370-1377.
46. Ezzeldin E, Souror WA, El-Nahhas T, Soudi AN, Shahat AA. Biochemical and neurotransmitters changes associated with tramadol in streptozotocin-induced diabetes in rats. Biomed Res Int 2014; 2014:238780.
47. Tully K, Bolshakov VY. Emotional enhancement of memory: how norepinephrine enables synaptic plasticity. Mol Brain 2010; 3:15.
48. Dai JX, Han HL, Tian M, Cao J, Xiu JB, Song NN, et al. Enhanced contextual fear memory in central serotonin-deficient mice. Proc Natl Acad Sci U S A 2008; 105:11981-11986.