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Current Reviews in Clinical and Experimental Pharmacology

Editor-in-Chief

ISSN (Print): 2772-4328
ISSN (Online): 2772-4336

Review Article

The Neuroanatomical Basis of the 5-HT Syndrome and Harmalineinduced Tremor

Author(s): Robert Lalonde* and Catherine Strazielle

Volume 19, Issue 2, 2024

Published on: 19 July, 2023

Page: [163 - 172] Pages: 10

DOI: 10.2174/2772432819666230703095203

Price: $65

Abstract

The 5-HT syndrome in rats is composed of head weaving, body shaking, forepaw treading, flat body posture, hindlimb abduction, and Straub tail. The importance of the brainstem and spinal cord for the syndrome is underlined by findings of 5,7-dihydroxytryptamine (5,7-DHT)-induced denervation supersensitivity in response to 5-HT-stimulant drugs. For head weaving and Straub tail, supersensitivity occurred when the neurotoxin was injected into the cisterna magna or spinal cord, for forepaw treading in cisterna magna, and for hindlimb abduction in the spinal cord. Although 5,7- DHT-related body shaking increased in the spinal cord, the sign decreased when injected into the striatum, indicating the modulatory influence of the basal ganglia. Further details on body shaking are provided by its reduced response to harmaline after 5-HT depletion caused by intraventricular 5,7-DHT, electrolytic lesions of the medial or dorsal raphe, and lesions of the inferior olive caused by systemic injection of 3-acetylpyridine along with those found in Agtpbp1pcd or nr cerebellar mouse mutants. Yet the influence of the climbing fiber pathway on other signs of the 5-HT syndrome remains to be determined.

Graphical Abstract

[1]
Bijl D. The serotonin syndrome. Neth J Med 2004; 62(9): 309-13.
[PMID: 15635814]
[2]
Boyer EW, Shannon M. The serotonin syndrome. N Engl J Med 2005; 352(11): 1112-20.
[http://dx.doi.org/10.1056/NEJMra041867] [PMID: 15784664]
[3]
Buckley NA, Dawson AH, Isbister GK. Serotonin syndrome. BMJ 2014; 348: g1626.
[http://dx.doi.org/10.1136/bmj.g1626] [PMID: 24554467]
[4]
Francescangeli J, Karamchandani K, Powell M, Bonavia A. The serotonin syndrome: From molecular mechanisms to clinical practice. Int J Mol Sci 2019; 20(9): 2288.
[http://dx.doi.org/10.3390/ijms20092288] [PMID: 31075831]
[5]
Martin TG. Serotonin syndrome. Ann Emerg Med 1996; 28(5): 520-6.
[http://dx.doi.org/10.1016/S0196-0644(96)70116-6]
[6]
Sporer KA. The serotonin syndrome. Implicated drugs, pathophysiology and management. Drug Saf 1995; 13(2): 94-104.
[http://dx.doi.org/10.2165/00002018-199513020-00004] [PMID: 7576268]
[7]
Sternbach H. The serotonin syndrome. Am J Psychiatry 1991; 148(6): 705-13.
[http://dx.doi.org/10.1176/ajp.148.6.705] [PMID: 2035713]
[8]
Sun-Edelstein C, Tepper SJ, Shapiro RE. Drug-induced serotonin syndrome: A review. Expert Opin Drug Saf 2008; 7(5): 587-96.
[http://dx.doi.org/10.1517/14740338.7.5.587] [PMID: 18759711]
[9]
Haberzettl R, Bert B, Fink H, Fox MA. Animal models of the serotonin syndrome: A systematic review. Behav Brain Res 2013; 256: 328-45.
[http://dx.doi.org/10.1016/j.bbr.2013.08.045] [PMID: 24004848]
[10]
Grahame-Smith DG. Studies in vivo on the relationship between brain tryptophan, brain 5-HT synthesis and hyperactivity in rats treated with a monoamine oxidase inhibitor and L-tryptophan. J Neurochem 1971; 18(6): 1053-66.
[http://dx.doi.org/10.1111/j.1471-4159.1971.tb12034.x] [PMID: 4254940]
[11]
Jacobs BL. An animal behavior model for studying central serotonergic synapses. Life Sci 1976; 19(6): 777-85.
[http://dx.doi.org/10.1016/0024-3205(76)90303-9] [PMID: 823389]
[12]
Jacobs BL. Effect of two dopamine receptor blockers on a serotonin-mediated behavioral syndrome in rats. Eur J Pharmacol 1974; 27(3): 363-6.
[http://dx.doi.org/10.1016/0014-2999(74)90014-4] [PMID: 4472582]
[13]
Jacobs BL. Evidence for the functional interaction of two central neurotransmitters. Psychopharmacology 1974; 39(1): 81-6.
[http://dx.doi.org/10.1007/BF00421461] [PMID: 4153732]
[14]
Trulson ME, Jacobs BL. Behavioral evidence for the rapid release of CNS serotonin by PCA and fenfluramine. Eur J Pharmacol 1976; 36(1): 149-54.
[http://dx.doi.org/10.1016/0014-2999(76)90266-1] [PMID: 131036]
[15]
Young AH, MacDonald LM, St John H, Dick H, Goodwin GM. The effects of corticosterone on 5-HT receptor function in rodents. Neuropharmacology 1992; 31(5): 433-8.
[http://dx.doi.org/10.1016/0028-3908(92)90080-9] [PMID: 1388255]
[16]
Eison AS, Wright RN. 5-HT1A and 5-HT2 receptors mediate discrete behaviors in the Mongolian Gerbil. Pharmacol Biochem Behav 1992; 43(1): 131-7.
[http://dx.doi.org/10.1016/0091-3057(92)90649-Z] [PMID: 1409796]
[17]
Lamarre Y, Mercier LA. Neurophysiological studies of harmaline-induced tremor in the cat. Can J Physiol Pharmacol 1971; 49(12): 1049-58.
[http://dx.doi.org/10.1139/y71-149] [PMID: 5142309]
[18]
Bello EM II, Blumenfeld M, Dao J, Krieg JDS, Wilmerding LK, Johnson MD. Considerations using harmaline for a primate model of tremor. Tremor Other Hyperkinet Mov 2021; 11(1): 35.
[http://dx.doi.org/10.5334/tohm.634] [PMID: 34611499]
[19]
Poirier LJ, Sourkes TL, Bouvier G, Boucher R, Carabin S. Striatal amines, experimental tremor and the effect of harmaline in the monkey. Brain 1966; 89(1): 37-52.
[http://dx.doi.org/10.1093/brain/89.1.37] [PMID: 4956264]
[20]
Costall B, Kelly DM, Naylor RJ. The importance of 5-hydroxytryptamine for the induction of harmine tremor and its antagonism by dopaminergic agonists assessed by lesions of the midbrain raphe nuclei. Eur J Pharmacol 1976; 35(1): 109-19.
[http://dx.doi.org/10.1016/0014-2999(76)90305-8] [PMID: 1253813]
[21]
Jacobs BL, Klemfuss H. Brain stem and spinal cord mediation of a serotonergic behavioral syndrome. Brain Res 1975; 100(2): 450-7.
[http://dx.doi.org/10.1016/0006-8993(75)90500-4] [PMID: 1192191]
[22]
Cheng MM, Tang GM, Kuo SH. Harmaline-induced tremor in mice: Videotape documentation and open questions about the model. Tremor Other Hyperkinet Mov 2013; 3(3): 4668.
[http://dx.doi.org/10.7916/D8H993W3]
[23]
Handforth A. Harmaline tremor: Underlying mechanisms in a potential animal model of essential tremor. Tremor Other Hyperkinet Mov 2012; 2: 02-92-769-1.
[http://dx.doi.org/10.7916/D8TD9W2P]
[24]
Pan MK, Ni CL, Wu YC, Li YS, Kuo SH. Animal models of tremor: Relevance to human tremor disorders. Tremor Other Hyperkinet Mov 2018; 8(0): 587.
[http://dx.doi.org/10.5334/tohm.440] [PMID: 30402338]
[25]
Woodward K, Apps R, Goodfellow M, Cerminara NL. Cerebello-thalamo-cortical network dynamics in the harmaline rodent model of essential tremor. Front Syst Neurosci 2022; 16: 899446.
[http://dx.doi.org/10.3389/fnsys.2022.899446] [PMID: 35965995]
[26]
Jackson HC, Kitchen I. Behavioural profiles of putative 5-hydroxytryptamine receptor agonists and antagonists in developing rats. Neuropharmacology 1989; 28(6): 635-42.
[http://dx.doi.org/10.1016/0028-3908(89)90143-3] [PMID: 2526930]
[27]
Scott PA, Chou JM, Tang H, Frazer A. Differential induction of 5-HT1A-mediated responses in vivo by three chemically dissimilar 5-HT1A agonists. J Pharmacol Exp Ther 1994; 270(1): 198-208.
[PMID: 8035316]
[28]
Peters DAV. Prenatal stress increases the behavioral response to serotonin agonists and alters open field behavior in the rat. Pharmacol Biochem Behav 1986; 25(4): 873-7.
[http://dx.doi.org/10.1016/0091-3057(86)90400-4] [PMID: 3491370]
[29]
Dickinson SL, Kennett GA, Curzon G. Reduced 5-hydroxytryptamine-dependent behaviour in rats following chronic corticosterone treatment. Brain Res 1985; 345(1): 10-8.
[http://dx.doi.org/10.1016/0006-8993(85)90830-3] [PMID: 4063795]
[30]
Sloviter RS, Drust EG, Connor JD. Specificity of a rat behavioral model for serotonin receptor activation. J Pharmacol Exp Ther 1978; 206(2): 339-47.
[PMID: 682117]
[31]
Sloviter RS, Drust EG, Connor JD. Evidence that serotonin mediates some behavioral effects of amphetamine. J Pharmacol Exp Ther 1978; 206(2): 348-52.
[PMID: 308099]
[32]
Lucki I, Nobler MS, Frazer A. Differential actions of serotonin antagonists on two behavioral models of serotonin receptor activation in the rat. J Pharmacol Exp Ther 1984; 228(1): 133-9.
[PMID: 6694097]
[33]
Backus LI, Sharp T, Grahame-Smith DG. Behavioural evidence for a functional interaction between central 5-HT2 and 5-HT1A receptors. Br J Pharmacol 1990; 100(4): 793-9.
[http://dx.doi.org/10.1111/j.1476-5381.1990.tb14094.x] [PMID: 2145051]
[34]
Diaz SL, Maroteaux L. Implication of 5-HT2B receptors in the serotonin syndrome. Neuropharmacology 2011; 61(3): 495-502.
[http://dx.doi.org/10.1016/j.neuropharm.2011.01.025] [PMID: 21277875]
[35]
Smith LM, Peroutka SJ. Differential effects of 5-hydroxytryptamine1A selective drugs on the 5-HT behavioral syndrome. Pharmacol Biochem Behav 1986; 24(6): 1513-9.
[http://dx.doi.org/10.1016/0091-3057(86)90477-6] [PMID: 2942947]
[36]
Skolnick P, Weissman BA, Youdim MBH. Monoaminergic involvement in the pharmacological actions of buspirone. Br J Pharmacol 1985; 86(3): 637-44.
[http://dx.doi.org/10.1111/j.1476-5381.1985.tb08940.x] [PMID: 2933109]
[37]
Ortmann R, Waldmeier PC, Radeke E, Felner A, Delini-Stula A. The effects of 5-HT uptake- and MAO-inhibitors on l-5-HTP-induced excitation in rats. Naunyn Schmiedebergs Arch Pharmacol 1980; 311(2): 185-92.
[http://dx.doi.org/10.1007/BF00510258] [PMID: 6966764]
[38]
Cho HU, Kim S, Sim J, et al. Redefining differential roles of MAO-A in dopamine degradation and MAO-B in tonic GABA synthesis. Exp Mol Med 2021; 53(7): 1148-58.
[http://dx.doi.org/10.1038/s12276-021-00646-3] [PMID: 34244591]
[39]
Gyarmati S, Timar J, Knoll B, Knoll J. Serotonin-mediated behavior in rats chronically treated with (-) deprenyl. Pol J Pharmacol Pharm 1988; 40(6): 667-71.
[PMID: 2479936]
[40]
Adell A, Sarna GS, Hutson PH, Curzon G. An in vivo dialysis and behavioural study of the release of 5-HT by p-chloroamphetamine in reserpine-treated rats. Br J Pharmacol 1989; 97(1): 206-12.
[http://dx.doi.org/10.1111/j.1476-5381.1989.tb11943.x] [PMID: 2720308]
[41]
Tricklebank MD, Forler C, Fozard JR. The involvement of subtypes of the 5-HT1 receptor and of catecholaminergic systems in the behavioural response to 8-hydroxy-2-(di-n-Propylamino) tetralin in the rat. Eur J Pharmacol 1984; 106(2): 271-82.
[http://dx.doi.org/10.1016/0014-2999(84)90714-3] [PMID: 6241568]
[42]
Tricklebank MD, Forler C, Middlemiss DN, Fozard JR. Subtypes of the 5-HT receptor mediating the behavioural responses to 5-methoxy-N,N-dimethyltryptamine in the rat. Eur J Pharmacol 1985; 117(1): 15-24.
[http://dx.doi.org/10.1016/0014-2999(85)90467-4] [PMID: 2935408]
[43]
Andrews CD, Fernando JCR, Curzon G. Differential involvement of dopamine-containing tracts in 5-hydroxytryptamine-dependent behaviours caused by amphetamine in large doses. Neuropharmacology 1982; 21(1): 63-8.
[http://dx.doi.org/10.1016/0028-3908(82)90212-X] [PMID: 6801538]
[44]
Bédard P, Pycock C. ‘Wet-Dog’ shake behaviour in the rat: A possible quantitative model of central 5-hydroxytryptamine activity. Neuropharmacology 1977; 16(10): 663-70.
[http://dx.doi.org/10.1016/0028-3908(77)90117-4] [PMID: 304190]
[45]
Ossowska K, Głowacka U, Kosmowska B, Wardas J. Apomorphine enhances harmaline-induced tremor in rats. Pharmacol Rep 2015; 67(3): 435-41.
[http://dx.doi.org/10.1016/j.pharep.2014.11.008] [PMID: 25933950]
[46]
Dickinson SL, Curzon G. Roles of dopamine and 5-hydroxytryptamine in stereotyped and non-stereotyped behaviour. Neuropharmacology 1983; 22(7): 805-12.
[http://dx.doi.org/10.1016/0028-3908(83)90124-7] [PMID: 6225959]
[47]
Dickinson SL, Jackson A, Curzon G. Effect of apomorphine on behaviour induced by 5-methoxy-N, N-dimethyl tryptamine: Three different scoring methods give three different conclusions. Psychopharmacology 1983; 80(2): 196-7.
[http://dx.doi.org/10.1007/BF00427970] [PMID: 6410451]
[48]
Trulson ME, Eubanks EE, Jacobs BL. Behavioral evidence for supersensitivity following destruction of central serotonergic nerve terminals by 5,7-dihydroxytryptamine. J Pharmacol Exp Ther 1976; 198(1): 23-32.
[PMID: 132525]
[49]
Rényi L. Long lasting supersensitivity to 5-HT mediated behaviour following monoamine depletion in the rat brain. Acta Pharmacol Toxicol 1986; 59(4): 298-302.
[http://dx.doi.org/10.1111/j.1600-0773.1986.tb00172.x] [PMID: 2948371]
[50]
Dickinson SL, Andrews CD, Curzon G. The effects of lesions produced by 5,7-dihydroxytryptamine on 5-hydroxytryptamine-mediated behaviour induced by amphetamine in large doses in the rat. Neuropharmacology 1984; 23(4): 423-9.
[http://dx.doi.org/10.1016/0028-3908(84)90250-8] [PMID: 6728129]
[51]
Nisbet AP, Marsden CA. Increased behavioural response to 5-methoxy-N,N-dimethyltryptamine but not to RU-24969 after intraventricular 5,7-dihydroxytryptamine administration. Eur J Pharmacol 1984; 104(1-2): 177-80.
[http://dx.doi.org/10.1016/0014-2999(84)90387-X] [PMID: 6499914]
[52]
Wieland S, Goodale D, Lucki I. Behavioral effects of 8-OH-DPAT: Studies using the Microtaxic Ventricular Injector. J Neurosci Methods 1989; 30(2): 151-9.
[http://dx.doi.org/10.1016/0165-0270(89)90062-9] [PMID: 2531256]
[53]
Hole K, Fuxe K, Jonsson G. Behavioral effects of 5,7-dihydroxytryptamine lesions of ascending 5-hydroxytryptamine pathways. Brain Res 1976; 107(2): 385-99.
[http://dx.doi.org/10.1016/0006-8993(76)90235-3] [PMID: 944613]
[54]
Kuhn CM, Vogel RA, Mailman RB, Mueller RA, Schanberg SM, Breese GR. Effect of 5,7-dihydroxytryptamine on serotonergic control of prolactin secretion and behavior in rats. Psychopharmacology 1981; 73(2): 188-93.
[http://dx.doi.org/10.1007/BF00429216] [PMID: 6785814]
[55]
Pranzatelli MR, Huang Y, Dollison AM, Stanley M. Brainstem serotonergic hyperinnervation modifies behavioral supersensitivity to 5-hydroxytryptophan in the rat. Brain Res Dev Brain Res 1989; 50(1): 89-99.
[http://dx.doi.org/10.1016/0165-3806(89)90128-4] [PMID: 2582610]
[56]
Deakin JFW, Green AR. The effects of putative 5-hydroxytryptamine antagonists on the behaviour produced by administration of tranylcypromine and L-tryptophan or tranylcypromine and L-DOPA to rats. Br J Pharmacol 1978; 64(2): 201-9.
[http://dx.doi.org/10.1111/j.1476-5381.1978.tb17290.x] [PMID: 708990]
[57]
Fone KCF, Johnson JV, Bennett GW, Marsden CA. Involvement of 5-HT2 receptors in the behaviours produced by intrathecal administration of selected 5-HT agonists and the TRH analogue (CG 3509) to rats. Br J Pharmacol 1989; 96(3): 599-608.
[http://dx.doi.org/10.1111/j.1476-5381.1989.tb11858.x] [PMID: 2470455]
[58]
Vandermaelen CP, Aghajanian GK. Intracellular studies on the effects of systemic administration of serotonin agonists on rat facial motoneurons. Eur J Pharmacol 1982; 78(2): 233-6.
[http://dx.doi.org/10.1016/0014-2999(82)90242-4] [PMID: 7075673]
[59]
Maratta R, Fenrich KK, Zhao E, Neuber-Hess MS, Rose PK. Distribution and density of contacts from noradrenergic and serotonergic boutons on the dendrites of neck flexor motoneurons in the adult cat. J Comp Neurol 2015; 523(11): 1701-16.
[http://dx.doi.org/10.1002/cne.23765] [PMID: 25728799]
[60]
Wieland S, Kreider MS, McGonigle P, Lucki I. Destruction of the nucleus raphe obscurus and potentiation of serotonin-mediated behaviors following administration of the neurotoxin 3-acetylpyridine. Brain Res 1990; 520(1-2): 291-302.
[http://dx.doi.org/10.1016/0006-8993(90)91718-V] [PMID: 1698505]
[61]
Pranzatelli MR, Gantner C, Snodgrass SR. 3-acetylpyridine lesions and four serotonergic behavioral syndromes in the rat. Brain Res Bull 1987; 18(2): 159-63.
[http://dx.doi.org/10.1016/0361-9230(87)90185-7] [PMID: 3567672]
[62]
Abdel-Fattah AFM, Matsumoto K, Murakami Y, El-Hady KAW, Mohamed MF, Watanabe H. Facilitatory and inhibitory effects of harmaline on the tryptophan-induced 5-hydroxytryptamine syndrome and body temperature changes in pargyline-pretreated rats. Jpn J Pharmacol 1996; 72(1): 39-47.
[http://dx.doi.org/10.1254/jjp.72.39] [PMID: 8902598]
[63]
De Arribam AF, Lizcano JM, Balsa MD, Unzeta M. Inhibition of monoamine oxidase from bovine retina by beta-carbolines. J Pharm Pharmacol 2011; 46(10): 809-13.
[http://dx.doi.org/10.1111/j.2042-7158.1994.tb03735.x] [PMID: 7699568]
[64]
Fuentes JA, Neff NH. Selective monoamine oxidase inhibitor drugs as aids in evaluating the role of type A and B enzymes. Neuropharmacology 1975; 14(11): 819-25.
[http://dx.doi.org/10.1016/0028-3908(75)90109-4] [PMID: 1207877]
[65]
Kettler R, Prada MD, Burkard WP. Comparison of monoamine oxidase-A inhibition by moclobemide in vitro and ex vivo in rats. Acta Psychiatr Scand 1990; 82(S360): 101-2.
[http://dx.doi.org/10.1111/j.1600-0447.1990.tb05348.x] [PMID: 2248058]
[66]
Kim H, Sablin SO, Ramsay RR. Inhibition of monoamine oxidase A by beta-carboline derivatives. Arch Biochem Biophys 1997; 337(1): 137-42.
[http://dx.doi.org/10.1006/abbi.1996.9771] [PMID: 8990278]
[67]
Nelson DL, Herbet A, Glowinski J, Hamon M. [3H]Harmaline as a specific ligand of MAO A-II. Measurement of the turnover rates of MAO A during ontogenesis in the rat brain. J Neurochem 1979; 32(6): 1829-36.
[http://dx.doi.org/10.1111/j.1471-4159.1979.tb02297.x] [PMID: 448371]
[68]
Abu GH, Lalies MD, Nutt DJ, Hudson AL. The modulatory action of harmane on serotonergic neurotransmission in rat brain. Brain Res 2015; 1597: 57-64.
[http://dx.doi.org/10.1016/j.brainres.2014.11.056] [PMID: 25498864]
[69]
Headley PM, Lodge D. Could harmaline generate tremor by affecting 5HT release? Br J Pharmacol 1979; 66(1): 116P-7P.
[PMID: 454912]
[70]
Sjölund B, Wiklund L, Björklund A. Functional role of serotonergic innervation of inferior olivary cells. Anatomy & Physiology. Raven Press New York 1980; pp. 163-8.
[71]
Wiklund L, Sjölund B, Björklund A. Morphological and functional studies on the serotoninergic innervation of the inferior olive. J Physiol 1981; 77(2-3): 183-6.
[PMID: 6169826]
[72]
Zhou M, Melin MD, Xu W, Südhof TC. Dysfunction of parvalbumin neurons in the cerebellar nuclei produces an action tremor. J Clin Invest 2020; 130(10): 5142-56.
[http://dx.doi.org/10.1172/JCI135802]
[73]
Wiklund L, Bjo¨rklund A, Sjo¨lund B. The indolaminergic innervation of the inferior olive. 1. Convergence with the direct spinal afferents in the areas projecting to the cerebellar anterior lobe. Brain Res 1977; 131(1): 1-21.
[http://dx.doi.org/10.1016/0006-8993(77)90025-7] [PMID: 884537]
[74]
Weiss M, Pellet J. Raphe — Cerebellum interactions. Exp Brain Res 1982; 48(2): 171-6.
[http://dx.doi.org/10.1007/BF00237212] [PMID: 6293861]
[75]
Czachura JF, Rasmussen K. Effects of acute and chronic administration of fluoxetine on the activity of serotonergic neurons in the dorsal raphe nucleus of the rat. Naunyn Schmiedebergs Arch Pharmacol 2000; 362(3): 266-75.
[http://dx.doi.org/10.1007/s002100000290] [PMID: 10997729]
[76]
Chaput Y, de Montigny C, Blier P. Effects of a selective 5-HT reuptake blocker, citalopram, on the sensitivity of 5-HT autoreceptors: Electrophysiological studies in the rat brain. Naunyn Schmiedebergs Arch Pharmacol 1986; 333(4): 342-8.
[http://dx.doi.org/10.1007/BF00500007] [PMID: 3022157]
[77]
Blier P, De Montigny C. Modification of 5-HT neuron properties by sustained administration of the 5-HT1A agonist gepirone: Electro-physiological studies in the rat brain. Synapse 1987; 1(5): 470-80.
[http://dx.doi.org/10.1002/syn.890010511] [PMID: 2905533]
[78]
Blier P, de Montigny C. Effects of quipazine on pre- and postsynaptic serotonin receptors: Single cell studies in the rat CNS. Neuropharmacology 1983; 22(4): 495-9.
[http://dx.doi.org/10.1016/0028-3908(83)90169-7] [PMID: 6856049]
[79]
Paul V. Involvement of β2-adrenoceptor blockade and 5-hydroxytryptamine mechanism in inhibition of harmaline-induced tremors in rats. Eur J Pharmacol 1986; 122(1): 111-5.
[http://dx.doi.org/10.1016/0014-2999(86)90165-2] [PMID: 2869961]
[80]
Arshaduddin M, Kadasah S, Aldeeb S, Almoutaery K, Tariq M. Exacerbation of harmaline-induced tremor by imipramine. Pharmacol Biochem Behav 2005; 81(1): 9-14.
[http://dx.doi.org/10.1016/j.pbb.2005.01.014] [PMID: 15894058]
[81]
Arshaduddin M, Al Kadasah S, Biary N, Al Deeb S, Al Moutaery K, Tariq M. Citalopram, a selective serotonin reuptake inhibitor augments harmaline-induced tremor in rats. Behav Brain Res 2004; 153(1): 15-20.
[http://dx.doi.org/10.1016/j.bbr.2003.10.035] [PMID: 15219702]
[82]
Mehta H, Saravanan KS, Mohanakumar KP. Serotonin synthesis inhibition in olivo-cerebellar system attenuates harmaline-induced tremor in Swiss albino mice. Behav Brain Res 2003; 145(1-2): 31-6.
[http://dx.doi.org/10.1016/S0166-4328(03)00094-9] [PMID: 14529803]
[83]
Barragan LA, Delhaye-Bouchaud N, Laget P. Drug-induced activation of the inferior olivary nucleus in young rabbits. Neuropharmacology 1985; 24(7): 645-54.
[http://dx.doi.org/10.1016/0028-3908(85)90107-8] [PMID: 3160966]
[84]
Sjo¨lund B, Bjo¨rklund A, Wiklund L. The indolaminergic innervation of the inferior olive. 2. Relation to harmaline induced tremor. Brain Res 1977; 131(1): 23-37.
[http://dx.doi.org/10.1016/0006-8993(77)90026-9] [PMID: 884545]
[85]
Lorden JF, Oltmans GA, McKeon TW, Lutes J, Beales M. Decreased cerebellar 3′,5′-cyclic guanosine monophosphate levels and insen-sitivity to harmaline in the genetically dystonic rat (dt). J Neurosci 1985; 5(10): 2618-25.
[http://dx.doi.org/10.1523/JNEUROSCI.05-10-02618.1985] [PMID: 2995603]
[86]
Michela VL, Stratton SE, Lorden JF. Enhanced sensitivity to quipazine in the genetically dystonic rat (dt). Pharmacol Biochem Behav 1990; 37(1): 129-33.
[http://dx.doi.org/10.1016/0091-3057(90)90053-K] [PMID: 2263655]
[87]
Kolasiewicz W, Kuter K, Nowak P, Pastuszka A, Ossowska K. Lesion of the cerebellar noradrenergic innervation enhances the harmaline-induced tremor in rats. Cerebellum 2011; 10(2): 267-80.
[http://dx.doi.org/10.1007/s12311-011-0250-9] [PMID: 21279489]
[88]
Kolasiewicz W, Kuter K, Berghauzen K, Nowak P, Schulze G, Ossowska K. 6-OHDA injections into A8–A9 dopaminergic neurons modelling early stages of Parkinson’s disease increase the harmaline-induced tremor in rats. Brain Res 2012; 1477: 59-73.
[http://dx.doi.org/10.1016/j.brainres.2012.08.015] [PMID: 22902616]
[89]
Kelly DM, Naylor RJ. An intracerebral injection study on the role of striatal dopamine and 5-hydroxytryptamine in the production of tremor by harmine. Neuropharmacology 1976; 15(5): 303-8.
[http://dx.doi.org/10.1016/0028-3908(76)90133-7] [PMID: 934444]
[90]
Gołembiowska K, Berghauzen-Maciejewska K, Górska A, Kamińska K, Ossowska K. A partial lesion of the substantia nigra pars compacta and retrorubral field decreases the harmaline-induced glutamate release in the rat cerebellum. Brain Res 2013; 1537: 303-11.
[http://dx.doi.org/10.1016/j.brainres.2013.08.059] [PMID: 24012623]
[91]
Kolasiewicz W, Kuter K, Wardas J, Ossowska K. Role of the metabotropic glutamate receptor subtype 1 in the Harmaline-induced tremor in rats. J Neural Transm 2009; 116(9): 1059-63.
[http://dx.doi.org/10.1007/s00702-009-0254-5] [PMID: 19551466]
[92]
Bernard JF, Buisseret-Delmas C, Laplante S. Inferior olivary neurons: 3-acetylpyridine effects on glucose consumption, axonal transport, electrical activity and harmaline-induced tremor. Brain Res 1984; 322(2): 382-7.
[http://dx.doi.org/10.1016/0006-8993(84)90139-2] [PMID: 6210132]
[93]
Guidotti A, Biggio G, Costa E. 3-Acetylpyridine: A tool to inhibit the tremor and the increase of cGMP content in cerebellar cortex elicited by harmaline. Brain Res 1975; 96: pp. (1)201-5.
[http://dx.doi.org/10.1016/0006-8993(75)90598-3]] [PMID: 169960]
[94]
Simantov R, Snyder SH, Oster-Granite ML. Harmaline-induced tremor in the rat: Abolition by 3-acetylpyridine destruction of cerebellar climbing fibers. Brain Res 1976; 114(1): 144-51.
[http://dx.doi.org/10.1016/0006-8993(76)91016-7] [PMID: 134757]
[95]
Balaban C. Central neurotoxic effects of intraperitoneally administered 3-acetylpyridine, harmaline and niacinamide in Sprague-Dawley and Long-Evans rats: A critical review of central 3-acetylpyridine neurotoxicity. Brain Res Brain Res Rev 1985; 9(1): 21-42.
[http://dx.doi.org/10.1016/0165-0173(85)90017-7] [PMID: 3158380]
[96]
Desclin JC, Escubi J. Effects of 3-acetylpyridine on the central nervous system of the rat, as demonstrated by silver methods. Brain Res 1974; 77(3): 349-64.
[http://dx.doi.org/10.1016/0006-8993(74)90627-1] [PMID: 4851791]
[97]
Kelly DM, Naylor RJ. The importance of extrapyramidal function for the induction and antagonism of harmine tremor. Eur J Pharmacol 1975; 32(1): 76-86.
[http://dx.doi.org/10.1016/0014-2999(75)90325-8] [PMID: 1149829]
[98]
Silbergeld EK, Hruska RE. Tremor: Role of striatal cholinergic neurons and the effect of intrastriatal kainic acid. Neurosci Lett 1979; 15(2-3): 235-42.
[http://dx.doi.org/10.1016/0304-3940(79)96119-6] [PMID: 530529]
[99]
Milner TE, Cadoret G, Lessard L, Smith AM. EMG analysis of harmaline-induced tremor in normal and three strains of mutant mice with Purkinje cell degeneration and the role of the inferior olive. J Neurophysiol 1995; 73(6): 2568-77.
[http://dx.doi.org/10.1152/jn.1995.73.6.2568] [PMID: 7666163]
[100]
De Montigny C, Lamarre Y. Rhythmic activity induced by harmaline in the olivo-cerebello-bulbar system of the cat. Brain Res 1973; 53(1): 81-95.
[http://dx.doi.org/10.1016/0006-8993(73)90768-3] [PMID: 4697252]
[101]
Lamarre Y, de Montigny C, Dumont M, Weiss M. Harmaline-induced rhythmic activity of cerebellar and lower brain stem neurons. Brain Res 1971; 32(1): 246-50.
[http://dx.doi.org/10.1016/0006-8993(71)90174-0] [PMID: 5113044]
[102]
Montigny CD, Lamarre Y. Effects produced by local applications of harmaline in the inferior olive. Can J Physiol Pharmacol 1975; 53(5): 845-9.
[http://dx.doi.org/10.1139/y75-116] [PMID: 1201490]
[103]
Llinás R, Volkind RA. The olivo-cerebellar system: Functional properties as revealed by harmaline-induced tremor. Exp Brain Res 1973; 18(1): 69-87.
[http://dx.doi.org/10.1007/BF00236557] [PMID: 4746753]
[104]
Baumel Y, Yamin HG, Cohen D. Cerebellar nuclei neurons display aberrant oscillations during harmaline-induced tremor. Heliyon 2021; 7(10): e08119.
[http://dx.doi.org/10.1016/j.heliyon.2021.e08119] [PMID: 34660929]
[105]
Weiss M, Ptito M, Pellet J. Harmaline-induced rhythmic activities of bulbar reticular cells and antagonistic muscles in the rat: A simultaneous recording study. J Hirnforsch 1983; 24(2): 237-40.
[PMID: 6309952]
[106]
Gogolák G, Jindra R, Stumpf C. Effect of harmaline on the cerebello-rubral system. Experientia 1977; 33(10): 1352-4.
[http://dx.doi.org/10.1007/BF01920176] [PMID: 908412]
[107]
Bekar L, Libionka W, Tian GF, et al. Adenosine is crucial for deep brain stimulation–mediated attenuation of tremor. Nat Med 2008; 14(1): 75-80.
[http://dx.doi.org/10.1038/nm1693] [PMID: 18157140]
[108]
Lee J, Chang S. Altered primary motor cortex neuronal activity in a rat model of harmaline-induced tremor during thalamic deep brain stimulation. Front Cell Neurosci 2019; 13: 448.
[http://dx.doi.org/10.3389/fncel.2019.00448] [PMID: 31680866]
[109]
Kosmowska B, Ossowska K, Konieczny J, Lenda T, Berghauzen-Maciejewska K, Wardas J. Inhibition of excessive glutamatergic transmission in the ventral thalamic nuclei by a selective adenosine A1 receptor agonist, 5′-chloro-5′-deoxy-(±)-ENBA underlies its tremor-olytic effect in the harmaline-induced model of essential tremor. Neuroscience 2020; 429: 106-18.
[http://dx.doi.org/10.1016/j.neuroscience.2019.12.045] [PMID: 31935489]
[110]
Llinás R, Sasaki K. The functional organization of the olivo-cerebellar system as examined by multiple Purkinje cell recordings. Eur J Neurosci 1989; 1(6): 587-602.
[http://dx.doi.org/10.1111/j.1460-9568.1989.tb00365.x] [PMID: 12106117]
[111]
Sugihara I, Lang EJ, Llinás R. Serotonin modulation of inferior olivary oscillations and synchronicity: A multiple-electrode study in the rat cerebellum. Eur J Neurosci 1995; 7(4): 521-34.
[http://dx.doi.org/10.1111/j.1460-9568.1995.tb00657.x] [PMID: 7620604]
[112]
Max Headley P, Lodge D, Duggan AW. Drug-induced rhythmical activity in the inferior olivary complex of the rat. Brain Res 1976; 101(3): 461-78.
[http://dx.doi.org/10.1016/0006-8993(76)90471-6] [PMID: 128400]
[113]
Bardin JM, Batini C, Billard JM, Buisseret-Delmas C, Conrath-Verrier M, Corvaja N. Cerebellar output regulation by the climbing and mossy fibers with and without the inferior olive. J Comp Neurol 1983; 213(4): 464-77.
[http://dx.doi.org/10.1002/cne.902130409] [PMID: 6300201]
[114]
Zhang Y, Forster C, Milner TA, Iadecola C. Attenuation of activity-induced increases in cerebellar blood flow by lesion of the inferior olive. Am J Physiol Heart Circ Physiol 2003; 285(3): H1177-82.
[http://dx.doi.org/10.1152/ajpheart.00240.2003] [PMID: 12750064]
[115]
Blenkinsop TA, Lang EJ. Synaptic action of the olivocerebellar system on cerebellar nuclear spike activity. J Neurosci 2011; 31(41): 14708-20.
[http://dx.doi.org/10.1523/JNEUROSCI.3323-11.2011] [PMID: 21994387]
[116]
Ruigrok TJH, Voogd J. Organization of projections from the inferior olive to the cerebellar nuclei in the rat. J Comp Neurol 2000; 426(2): 209-28.
[http://dx.doi.org/10.1002/1096-9861(20001016)426:2<209:AID-CNE4>3.0.CO;2-0] [PMID: 10982464]
[117]
Wiklund L, Toggenburger G, Cuénod M. Aspartate: Possible neurotransmitter in cerebellar climbing fibers. Science 1982; 216(4541): 78-80.
[http://dx.doi.org/10.1126/science.6121375] [PMID: 6121375]
[118]
Yarden-Rabinowitz Y, Yarom Y. In vivo analysis of synaptic activity in cerebellar nuclei neurons unravels the efficacy of excitatory inputs. J Physiol 2017; 595(17): 5945-63.
[http://dx.doi.org/10.1113/JP274115] [PMID: 28618000]
[119]
Batini C, Buisseret-Delmas C, Conrath-Verrier M. Harmaline-induced tremor. Exp Brain Res 1981; 42(42): 371-82.
[http://dx.doi.org/10.1007/BF00237502] [PMID: 7238677]
[120]
Batini C, Buisseret-Delmas C, Conrath-Verrier M. Olivo-cerebellar activity during harmaline-induced tremor. A 2-[14C] deoxyglucose study. Neurosci Lett 1979; 12(2-3): 241-6.
[http://dx.doi.org/10.1016/0304-3940(79)96069-5] [PMID: 460718]
[121]
Beitz AJ, Saxon D. Harmaline-induced climbing fiber activation causes amino acid and peptide release in the rodent cerebellar cortex and a unique temporal pattern of Fos expression in the olivo-cerebellar pathway. J Neurocytol 2004; 33(1): 49-74.
[http://dx.doi.org/10.1023/B:NEUR.0000029648.81071.20] [PMID: 15173632]
[122]
Miwa H, Nishi K, Fuwa T, Mizuno Y. Differential expression of c-Fos following administration of two tremorgenic agents. Neuroreport 2000; 11(11): 2385-90.
[http://dx.doi.org/10.1097/00001756-200008030-00010] [PMID: 10943690]
[123]
Lee J, Jo HJ, Kim I, et al. Mapping bold activation by pharmacologically evoked tremor in swine. Front Neurosci 2019; 13: 985.
[http://dx.doi.org/10.3389/fnins.2019.00985] [PMID: 31619955]

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