Intra-periaqueductal Grey Matter Injection of Orexin A Attenuates Nitroglycerin-induced Deficits in Learning and Memory in Male Rats

Iranian Journal of Veterinary Science and Technology

مقاله 5، دوره 15، شماره 2 - شماره پیاپی 31، مهر 2023، صفحه 38-47   

نوع مقاله: Research Articles

شناسه دیجیتال (DOI): 10.22067/ijvst.2023.77798.1171

نویسندگان

Razieh Kooshki^{* 1}؛ Mehdi Abbasnejad²؛ Baharosadat Majdzadeh²

¹Department of Biology, Faculty of Science, Lorestan University, Khorramabad, Iran.

²Department of Biology, Faculty of Sciences, Shahid Bahonar University of Kerman, Kerman, Iran.

چکیده

This study explored the potential contribution of Orx1R within vlPAG to the learning and memory of animals with chronic migraine-like pain. Migraine was induced by repeated i.p. administration of nitroglycerin (5 mg/kg). Passive avoidance adeptness was evaluated in the shuttle box maze. The spatial memory performance was estimated using MWM tests. In the MWM task, NTG-injected rats revealed an imperative increase in escape latency and traveled the distance to catch the stage and a decrease in the time spent to pass into the goal zone in comparison to the control animals. Such NTG-evoked responses were attenuated by the post-treating intra-vlPAG injection of orexin A at 100 but not 25 and 50 pM. Furthermore, in the shuttle box test, NTG-treated rats showed eversion memory retrieval impairment as reflected by decreased phase through latency and longer time spent in the black chambers of the maze. Administration of orexin A at 50 and 100 pM could suppress NTG-related eversion memory deficiency in rats. However, orexin A (100 pM) aptitude to preserve memory performance, in both MWM and shuttle box tasks, was significantly prevented by SB334867 (20 nM) as an Orx1R antagonist. Overall, these data support the role of Orx1R within vlPAG to modulate migraine-related cognition deficits in rats. 

کلیدواژه‌ها

Migraine؛ Nitroglycerin؛ Orexin A؛ Learning and memory؛ Rats

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مراجع

1.    Dodick DW. A phase‐by‐phase review of migraine pathophysiology. Headache: The Journal of Head and Face Pain. 2018;58:4-16. Doi:10.1111/head.13300.
2.    Charles A. The pathophysiology of migraine: implications for clinical management. The Lancet Neurology. 2018;17(2):174-82. Doi: 10.1016/S1474-4422(17)30435-0.
3.    Guglielmetti M, Raggi A, Ornello R, Sacco S, D’Amico D, Leonardi M, et al. The clinical and public health implications and risks of widening the definition of chronic migraine. Cephalalgia. 2020;40(4):407-10. Doi: 10.1177/0333102419895777.
4.    Berg J, Stovner L. Cost of migraine and other headaches in Europe. European Journal of Neurology. 2005;12:59-62. Doi:10.1111/j.1468-1331.2005.01192.x.
 5.    Ong JJY, De Felice M. Migraine treatment: current acute medications and their potential mechanisms of action. Neurotherapeutics. 2018;15(2):274-90. Doi: 10.1007/s13311-017-0592-1.
6.    May A, Schulte LH. Chronic migraine: risk factors, mechanisms and treatment. Nature Reviews Neurology. 2016;12(8):455. Doi: 10.1038/nrneurol.2016.93.
7.    Mainero C, Boshyan J, Hadjikhani N. Altered functional magnetic resonance imaging resting‐state connectivity in periaqueductal gray networks in migraine. Annals of neurology. 2011;70(5):838-45. Doi: 10.1002/ana.22537.
8.    Welch K, Nagesh V, Aurora SK, Gelman N. Periaqueductal gray matter dysfunction in migraine: cause or the burden of illness? Headache: The Journal of Head and Face Pain. 2001;41(7):629-37. Doi:10.1046/j.1526-4610.2001.041007629.x.
9.    Li Y-Q, Shinonaga Y, Takada M, Mizuno N. Demonstration of axon terminals of projection fibers from the periaqueductal gray onto neurons in the nucleus raphe magnus which send their axons to the trigeminal sensory nuclei. Brain research. 1993;608(1):138-40. Doi: 10.1016/0006-8993(93)90784-k.
10.    Knight Y, Goadsby P. The periaqueductal grey matter modulates trigeminovascular input: a role in migraine? Neuroscience. 2001;106(4):793-800. Doi:10.1016/s0306-4522(01)00303-7.
11.    Messlinger K, Fischer MJ, Lennerz JK. Neuropeptide effects in the trigeminal system: pathophysiology and clinical relevance in migraine. The Keio journal of medicine. 2011;60(3):82-9. Doi: 10.2302/kjm.60.82.
12.    Li Y, Zhang Q, Qi D, Zhang L, Yi L, Li Q, et al. Valproate ameliorates nitroglycerin-induced migraine in trigeminal nucleus caudalis in rats through inhibition of NF-кB. The journal of headache and pain. 2016;17(1):49. Doi: 10.1186/s10194-016-0631-z.
13.    Samsam M, Covenas R, Ahangari R, Yajeya J, Narváez J, Tramu G. Simultaneous depletion of neurokinin A, substance P and calcitonin gene-related peptide from the caudal trigeminal nucleus of the rat during electrical stimulation of the trigeminal ganglion. PAIN®. 2000;84(2-3):389-95. Doi: 10.1016/s0304-3959(99)00240-7.
14.    Goadsby PJ. Pathophysiology of migraine. Neurologic clinics. 2009;27(2):335-60. Doi: 10.1016/j.ncl.2008.11.012.
15.    Guo Y, Tian Q, Xu S, Han M, Sun Y, Hong Y, et al. The impact of attack frequency and duration on neurocognitive processing in migraine sufferers: evidence from event-related potentials using a modified oddball paradigm. BMC neurology. 2019;19(1):73. Doi: 10.1186/s12883-019-1305-7.
16.    Gil-Gouveia R, Oliveira AG, Martins IP. Cognitive dysfunction during migraine attacks: a study on migraine without aura. Cephalalgia. 2015;35(8):662-74. Doi: 10.1177/0333102414553823.
17.    Araújo CMd, Barbosa IG, Lemos SMA, Domingues RB, Teixeira AL. Cognitive impairment in migraine: a systematic review. Dementia & neuropsychologia. 2012;6(2):74-9. Doi: 10.1590/S1980-57642012DN06020002.
18.    Jelicic M, Van Boxtel MP, Houx PJ, Jolles J. Does migraine headache affect cognitive function in the elderly? Report from the Maastricht Aging Study (MAAS). Headache: The Journal of Head and Face Pain. 2000;40(9):715-9. Doi: 10.1046/j.1526-4610.2000.00124.x.
19.    Gaist D, Pedersen L, Madsen C, Tsiropoulos I, Bak S, Sindrup S, et al. Long-term effects of migraine on cognitive function: a population-based study of Danish twins. Neurology. 2005;64(4):600-7. Doi:10.1212/01.WNL.0000151858.15482.66.
20.    Dilekoz E, Houben T, Eikermann-Haerter K, Balkaya M, Lenselink AM, Whalen MJ, et al. Migraine mutations impair hippocampal learning despite enhanced long-term potentiation. Journal of Neuroscience. 2015;35(8):3397-402. Doi: 10.1523/JNEUROSCI.2630-14.2015.
21.    Kilduff TS, Peyron C. The hypocretin/orexin ligand–receptor system: implications for sleep and sleep disorders. Trends in neurosciences. 2000;23(8):359-65. Doi:10.1016/s0166-2236(00)01594-0
22.    Nishino S, Sakurai T. The orexin/hypocretin system: physiology and pathophysiology: Springer; 2007.
23.    Taheri S, Mahmoodi M, Opacka-Juffry J, Ghatei MA, Bloom SR. Distribution and quantification of immunoreactive orexin A in rat tissues. FEBS letters. 1999;457(1):157-61. Doi: 10.1016/s0014-5793(99)01030-3.
24.    Chen C-T, Dun S, Kwok E, Dun N, Chang J-K. Orexin A-like immunoreactivity in the rat brain. Neuroscience letters. 1999;260(3):161-4. Doi: 10.1016/s0304-3940(98)00977-x.
25.    Arima Y, Yokota S, Fujitani M. Lateral parabrachial neurons innervate orexin neurons projecting to brainstem arousal areas in the rat. Scientific reports. 2019;9(1):1-10. Doi: 10.1038/s41598-019-39063-y
26.    Holland P, Akerman S, Goadsby P. Modulation of nociceptive dural input to the trigeminal nucleus caudalis via activation of the orexin 1 receptor in the rat. European Journal of Neuroscience. 2006;24(10):2825-33. Doi: 10.1111/j.1460-9568.2006.05168.x.
27.    Schmitt O, Usunoff KG, Lazarov NE, Itzev DE, Eipert P, Rolfs A, et al. Orexinergic innervation of the extended amygdala and basal ganglia in the rat. Brain Structure and Function. 2012;217(2):233-56. Doi: 10.1007/s00429-011-0343-8.
28.    Kooshki R, Abbasnejad M, Esmaeili-Mahani S, Raoof M. The Modulatory Role of Orexin 1 Receptor in CA1 on Orofacial Pain-induced Learning and Memory Deficits in Rats. Basic and clinical neuroscience. 2017;8(3):213. Doi: 10.18869/nirp.bcn.8.3.213
29.    Kooshki R, Abbasnejad M, Esmaeili-Mahani S, Raoof M. The role of trigeminal nucleus caudalis orexin 1 receptors in orofacial pain transmission and in orofacial pain-induced learning and memory impairment in rats. Physiology & behavior. 2016;157:20-7. Doi: 10.1016/j.physbeh.2016.01.031. 
30.    Shahsavari F, Abbasnejad M, Esmaeili‐Mahani S, Raoof M. Orexin‐1 receptors in the rostral ventromedial medulla are involved in the modulation of capsaicin evoked pulpal nociception and impairment of learning and memory. International endodontic journal. 2018;51(12):1398-409. Doi: 10.1111/iej.12958.
31.    Ardeshiri MR, Hosseinmardi N, Akbari E. The effect of orexin 1 and orexin 2 receptors antagonisms in the basolateral amygdala on memory processing in a passive avoidance task. Physiology & behavior. 2017;174:42-8. Doi: 10.1016/j.physbeh.2017.03.004.
32.    Rizvi TA, Ennis M, Behbehani MM, Shipley MT. Connections between the central nucleus of the amygdala and the midbrain periaqueductal gray: topography and reciprocity. Journal of Comparative Neurology. 1991;303(1):121-31. Doi: 10.1002/cne.903030111.
33.    Floyd NS, Price JL, Ferry AT, Keay KA, Bandler R. Orbitomedial prefrontal cortical projections to distinct longitudinal columns of the periaqueductal gray in the rat. Journal of Comparative Neurology. 2000;422(4):556-78. Doi:10.1002/1096-9861(20000710)422:4<556::aid-cne6>3.0.co;2-u.
34.    Krout KE, Loewy AD. Periaqueductal gray matter projections to midline and intralaminar thalamic nuclei of the rat. Journal of Comparative Neurology. 2000;424(1):111-41.
35.    Guo Y, Xu S, Nie S, Han M, Zhang Y, Chen J, et al. Female versus male migraine: an event-related potential study of visual neurocognitive processing. The journal of headache and pain. 2019;20(1):38.
36.    Bekker A, Haile M, Li Y-S, Galoyan S, Garcia E, Quartermain D, et al. Nimodipine prevents memory impairment caused by nitroglycerin-induced hypotension in adult mice. Anesthesia and analgesia. 2009;109(6):1943. Doi: 10.1002/1096-9861(20000814)424:1<111::aid-cne9>3.0.co;2-3.
37.    Dagdeviren M. Role of Nitric Oxide Synthase in Normal Brain Function and Pathophysiology of Neural Diseases. Nitric Oxide Synthase: Simple Enzyme-Complex Roles. 2017:37. Doi:10.1002/1096-9861(20000710)422:4<556::AID-CNE6>3.0.CO;2-U
38.    Džoljić E, Grabatinić I, Kostić V. Why is nitric oxide important for our brain? Functional neurology. 2015;30(3):159.
39.    Hosseini M, Dastghaib SS, Rafatpanah H, Hadjzadeh MA-R, Nahrevanian H, Farrokhi I. Nitric oxide contributes to learning and memory deficits observed in hypothyroid rats during neonatal and juvenile growth. Clinics. 2010;65(11):1175-81.
40.    James BM, Li Q, Luo L, Kendrick KM. Aged neuronal nitric oxide knockout mice show preserved olfactory learning in both social recognition and odor-conditioning tasks. Frontiers in Cellular Neuroscience. 2015;9:105. Doi: 10.11138/FNeur/2015.30.3.159
41.    Ho Y-C, Lee H-J, Tung L-W, Liao Y-Y, Fu S-Y, Teng S-F, et al. Activation of orexin 1 receptors in the periaqueductal gray of male rats leads to antinociception via retrograde endocannabinoid (2-arachidonoylglycerol)-induced disinhibition. Journal of Neuroscience. 2011;31(41):14600-10. Doi: 10.1523/JNEUROSCI.2671-11.2011 
42.    Pourrahimi AM, Abbasnejad M, Esmaeili-Mahani S, Kooshki R, Raoof M. Intra-periaqueductal gray matter administration of orexin-A exaggerates pulpitis-induced anxiogenic responses and c-fos expression mainly through the interaction with orexin 1 and cannabinoid 1 receptors in rats. Neuropeptides. 2019;73:25-33.
43.    Raoof R, Esmaeili-Mahani S, Abbasnejad M, Raoof M, Sheibani V, Kooshki R, et al. Changes in hippocampal orexin 1 receptor expression involved in tooth pain-induced learning and memory impairment in rats. Neuropeptides. 2015;50:9-16. Doi: 10.1016/j.npep.2018.12.001.
44.    Wang C, Wang Q, Ji B, Pan Y, Xu C, Cheng B, et al. The orexin/receptor system: molecular mechanism and therapeutic potential for neurological diseases. Frontiers in molecular neuroscience. 2018;11:220. Doi: 10.3389/fnmol.2018.00220.
45.    Zhao X, xue Zhang R, Tang S, yan Ren Y, xia Yang W, min Liu X, et al. Orexin-A-induced ERK1/2 activation reverses impaired spatial learning and memory in pentylenetetrazol-kindled rats via OX1R-mediated hippocampal neurogenesis. Peptides. 2014;54:140-7. Doi: 10.1016/j.peptides.2013.11.019. 
46.    Dustrude ET, Caliman IF, Bernabe CS, Fitz SD, Grafe LA, Bhatnagar S, et al. Orexin depolarizes central amygdala neurons via orexin receptor 1, phospholipase C and Sodium-Calcium exchanger and modulates conditioned fear. Frontiers in neuroscience. 2018;12:934.Doi:10.3389/fnins.2018.00934.
47.    Liu M-F, Xue Y, Liu C, Liu Y-H, Diao H-L, Wang Y, et al. Orexin-A exerts neuroprotective effects via OX1R in Parkinson’s disease. Frontiers in neuroscience. 2018;12:835. Doi: 10.3389/fnins.2018.00835.
48.    Faull OK, Pattinson KT. The cortical connectivity of the periaqueductal gray and the conditioned response to the threat of breathlessness. Elife. 2017;6:e21749. Doi: 10.7554/eLife.21749.
49.    Parsons R, Gafford GM, Helmstetter FJ. Regulation of extinction-related plasticity by opioid receptors in the ventrolateral periaqueductal gray matter. Frontiers in behavioral neuroscience. 2010;4:44. Doi:10.3389/fnbeh.2010.00044.
50.    Rozeske R, Valerio S, Chaudun F, Herry C. Prefrontal neuronal circuits of contextual fear conditioning. Genes, Brain and Behavior. 2015;14(1):22-36. Doi:10.1111/gbb.12181. Epub 2014 Oct 27.
51.    Rozeske RR, Jercog D, Karalis N, Chaudun F, Khoder S, Girard D, et al. Prefrontal-periaqueductal gray-projecting neurons mediate context fear discrimination. Neuron. 2018;97(4):898-910. e6. Doi: 10.1016/j.neuron.2017.12.044.
52.    Hervieu G, Cluderay J, Harrison D, Roberts J, Leslie R. Gene expression and protein distribution of the orexin-1 receptor in the rat brain and spinal cord. Neuroscience. 2001;103(3):777-97. Doi: 10.1016/S0306-4522(01)00033-1.
53.    Chen Y-H, Lee H-J, Lee MT, Wu Y-T, Lee Y-H, Hwang L-L, et al. Median nerve stimulation induces analgesia via orexin-initiated endocannabinoid disinhibition in the periaqueductal gray. Proceedings of the National Academy of Sciences. 2018;115(45):E10720-E9. Doi: 10.1073/pnas.1807991115.
54.    Samineni VK, Grajales-Reyes JG, Copits BA, O’Brien DE, Trigg SL, Gomez AM, et al. Divergent modulation of nociception by glutamatergic and GABAergic neuronal subpopulations in the periaqueductal gray. eneuro. 2017;4(2). Doi: 10.1523/ENEURO.0129-16.2017.
55.    Reichling DB, Basbaum AI. Contribution of brainstem GABAergic circuitry to descending antinociceptive controls: I. GABA‐immunoreactive projection neurons in the periaqueductal gray and nucleus raphe magnus. Journal of Comparative Neurology. 1990;302(2):370-7. Doi: 10.1002/cne.903020214. 
56.    Esmaeili M-H, Reisi Z, Ezzatpanah S, Haghparast A. Functional interaction between orexin‐1 and CB 1 receptors in the periaqueductal gray matter during antinociception induced by chemical stimulation of the lateral hypothalamus in rats. European journal of pain. 2016;20(10):1753-62. Doi: 10.1002/ejp.899.
57.    Calva CB, Fayyaz H, Fadel JR. Increased acetylcholine and glutamate efflux in the prefrontal cortex following intranasal orexin‐A (hypocretin‐1). Journal of neurochemistry. 2018;145(3):232-44. Doi: 10.1111/jnc.14279. 
58.    Paxinos G, Watson C. The Rat Brain in Stereotaxic Coordinates in Stereotaxic Coordinates: Elsevier; 2007.