David Janowsky:Cholinergic muscarinic mechanisms in depression and mania
David Janowsky: Bibliography
The following is a list of references which summarize selected studies focused on the role of acetylcholine in the pathophysiology of the affective disorders and the role of catecholaminergic /cholinergic balance in these disorders. The references primarily cover the second half of the 20th century and the first 19 years of the 21st century. They range from early observational studies of the depressogenic, sleep and neuroendocrine effects of cholinesterase inhibitors and cholinergic agonists in humans to more recent, highly sophisticated studies utilizing animal models in which gene knock-out techniques, imaging techniques and neurotransmitter-neuromodulator manipulations are applied to understand how cholinergic influences might affect mood. The list of references is not altogether comprehensive, but is extensive and illustrative of a number of significant breakthroughs that have occurred over the past nearly seven decades, most suggesting a role for muscarinic and nicotinic influences as these relate to the pathophysiology of mood disorders. The current list is a companion piece to the previously printed piece entitled “Cholinergic Muscarinic Mechanisms in Depression and Mania.”
Addy NA, Nunes EJ, Wickham RJ. Ventral tegmental area cholinergic mechanisms mediate behavioral responses in the forced swim test. Behav Brain Res. 2015;288:54-62.
Altinyazar V, Sirin FB, Sutcu R, Eren I, Omurlu IK., The red blood cell acetylcholinesterase levels of depressive patients with suicidal behavior in an agricultural area. India J Clin Biochem. Indian J. Clin Biochem. 2016;31:473-479.
Andreasen JT, Henningsen K, Bate S. Christiansen S, Wilborg O. Nicotine reverses anhedonic-like response and cognitive impairment in the rat chronic mild stress model of depression: comparison with sertraline. J Psychopharmacol. 2011;25:1134-41.
Andreasen JT, Redrobe JP, Nielsen EO. Combined α7 nicotinic acetylcholine receptor agonism and partial serotonin transporter inhibition produce antidepressant-like effects in the mouse forced swim and tail suspension tests: a comparison of SSR180711 and PNU-282987. Pharmacy Biochem Behav. 2012;100:624-9.
Ban TA. Depression and the Tricyclic Antidepressants, Chapter 4, Depression, Montreal: Ronalds Federated; 1974;45-6.
Ban TA. Cholinergic mechanisms. inhn.org.books. January 10, 2019.
Bajada S. A trial of choline chloride and physostigmine in Alzheimer’s dementia. In Alzheimer’s Disease: a report of progress. Edited by Corkin S, Davis K, Growden J. New York: Raven Press; 1982. pp. 427-43.
Biala G, Pekala K, Boguszewska-Czbara, Michalac A, Kru Slomka M, Budzynska B. Behavioral and biochemical interaction between nicotine and chronic unpredictable mild stress in mice. Mol Neurobiol. 2017;54 904-21.
Berger M, Lund R, Bronisch T, von Zerssen D. REM latency in neurotic and endogenous depression and the cholinergic REM induction test. Psychiatry Res. 1983;10:113-23.
Berger M, Riemann D, Hochli D, Spiegel R. The cholinergic rapid eye movement sleep induction test with RS-86. State or trait marker of depression? Arch Gen Psychiatry. 1989;46:421-8.
Berkowitz A, Sutton L, Janowsky DS, Gillin JC. Pilocarpine , an orally active muscarinic cholinergic agonist induces REM sleep and reduces delta sleep in normal volunteers. Psychiatry Res. 1990;33:113-9.
Bowers MB, Goodman E, Sim VM. Some behavioral changes in man following anticholinesterase administration. J Nerv Ment Dis.1964;138:383-9.
Cannon DM, Carson RE, Nugent AC, Eckelman WC, Kiesewelter DO, Williams J, Rollis D, Drevets M, Gandhi S, Solono G, Drevets WC. Reduced muscarinic type 2 receptor binding in subjects with bipolar disorder. Arch Gen Psychiatry. 2006;63:741-7.
Cannon DM, Klaver JK, Gandhi SK, Solono G, Peck SA , Erickson K, Akula N, Savitz J, Eckelman WC, Furey ML, Sahakian BJ, McMahon FJ, Drevets WC. Genetic variation in cholinergic muscarinic-2 receptor gene modulates M2 receptor binding in vivo and accounts for reduced binding in bipolar disorder. Mol Psychiatry. 2011;16:407-8.
Carlton PL. Cholinergic mechanisms in the control of behavior by the brain. 1963. Psychol Rev. 70:19-39.
Carroll BJ, Frazer A, Schless A, Mendels J. Cholinergic reversal of manic symptoms. Lancet 1973;428.
Casey DE. Mood alterations during deanol therapy. Psychopharmacology. 1979; 62:187-91.
Chau DT, Rada P, Kosloff RA. Nucleus accumbens muscarinic receptors in the control of behavioral depression: antidepressant effect of local M1 antagonist in the porsolt swim test. Neuroscience. 2001;104:791-8.
Chau DT, Rada PV, Kim K, Kosloff RA, Boebel BG. Fluoxetine alleviates behavioral depression while decreasing acetylcholine release in the nucleus accumbent shell. Neuropsychopharmacology. 2011;36:1729-37.
Charles HC, Lazeyras F, Krishnan IR, Boyko OB, Payne M, Moore D. Brain choline in depression: in vivo detection of potential pharmacodynamic effects of antidepressant therapy using hydrogen localized spectroscopy. Prog Neuropsychopharmacol Biol Psychiatry. 1993;18:1121-7.
Chen YW, Rada PV, Butzler BP, Leibowitz SF, Hoebel BG. Corticotropin-releasing factor in the nucleus accumbens shell induces swim depression, anxiety, and anhedonia along with changes in local dopamine/ acetylcholine balance. Neuroscience. 2010;206:155-66.
Comings DE, Wu S, Rostamkhani M, McGue M, Iacono WG, MacMurray JF. Association of the muscarinic cholinergic 2 receptor (CHRM2) gene with major depression in women. Am J Med Genet. 2002;114:527-9.
Dagyte G, Den Boer JA, Trentani A. The cholinergic system and depression. Behav Brain Res. 2010;221:574-82.
Davis KL, Berger PA, Hollister LE, Defraites E. Physostigmine in mania. Arch Gen Psychiatry. 1979; 35:119-22.
Davis BM, Davis KL. Cholinergic mechanisms and anterior pituitary hormone secretion. Biol Psychiatry. 1980;15:303-10.
Davis KL, Hollander E, Davidson M, Davis BM, Mohs RC, Horvath TB. Induction of depression with oxotremorine in patients with Alzheimer’s disease. Am J Psychiatry. 1987;144:468-71.
Day JC, Kohl M, Le Moal M, Maccari S. Corticotropin-releasing factor administered centrally, but not peripherally stimulates hippocampal acetylcholine release. J Neurochem. 1998;71:622-9.
Doerr P, Berger M. Physostigmine-induced escape from dexamethasone suppression in normal adults. Biological Psychiatry. 1983;18:261-8.
Domino EF, Olds ME. Cholinergic inhibition of self-stimulation behavior. J. Pharm. Exp Therapeutics. 1968;164:202-11.
Dong J, Zhou Q, Wei Z, Yan S, Sun F, Cai X. Protein kinase A mediates scopolamine-induced mTOR activation and an antidepressant response. J Affect Disor. 2018; 227: 633-42.
Drevets WC, Furey ML. Replication of scopolamine’s antidepressant efficacy in major depressive disorder: a randomized placebo-controlled clinical trial. Biological Psychiatry. 2010; 67:432-8.
Drevets WC, Zarate CA Jr., Furey ML. Antidepressant effects of the muscarinic cholinergic receptor antagonist scopolamine: a review. Biological Psychiatry. 2013;73;1156-63.
Dulawa SC, Janowsky DS. Cholinergic regulation of mood: from basic and clinical studies to emerging therapeutics. Mol. Psychiatry, 2019;24:694-709.
El Yousef M, Janowsky DS, Davis JM, Rosenblatt J. Induction of severe depression in marijuana intoxicated individuals. Br J Addict. 1973;68:321-5.
Fernandes SS, Koth AP, Parfitt GM, Condeiro MF, Pelxoto CS, Soubhia A, Moreira FP, Wiener CD, Uses JP, Kozzobowski E, Barros D. Enhanced cholinergic tone during stress induces a depressive like state in mice. Behav Brain Res. 2018;347:17-25.
Fibiger HC, Lynch GS, Cooper HP. A biphasic action of central cholinergic stimulation on behavioral arousal in the rat. Psychopharmacologia (Berl). 1971;20:366-82.
Furey ML, Drevets WC. Antidepressant efficacy of the antimuscarinic drug scopolamine. Arch Gen Psychiatry. 2006;63:1121-9.
Furey ML, Nugent AC, Speer AM, Luckenbaugh DA, Hoffman EM, Frankel E, Drevets WC, Zarate CA Jr. Baseline mood-state measures as predictors of antidepressant response to scopolamine. Psychiatry Res. 2012;196:62-7.
Furey ML, Drevets WC, Szczepanik J, Khanna A, Nugent A, Zarate CA Jr. Pretreatment Differences in BOLD Response to Emotional Faces Correlate with Antidepressant Response to Scopolamine. Int J Neuropsychopharmacol. 2015;18.
Furey ML, Drevets WC, Hoffman EM, Frankel E, Speer AM, Zarate CA. Potential of pretreatment neural activity in the visual cortex during emotional processing to predict treatment response to scopolamine in major depressive disorder. JAMA Psychiatry. 2013;70:280-90.
Gershon S, Shaw FH. Psychiatric sequelae of chronic exposure to organophosphorus insecticides. Lancet. 1961;1:1371-4.
Ghosal S, Bange, Yue W, Hare BD, Lepack AE, Gigente MJ, Dumar RS. Activity-Dependent Brain-Derived Neurotrophic Factor Release Is Required for the Rapid Antidepressant Actions of Scopolamine. Biol psychiatry. 2018;83:29-37.
Gibbons AS, Scarr E, McLean C, Sundram S, Dean B. Decreased muscarinic receptor binding in the frontal cortex of bipolar disorder and major depressive disorder subjects. J Affect Disord. 2009;116:184-91.
Gibbons AS, Jeon WJ, Scarr E, Dean B. Changes in muscarinic M2 receptor levels in the cortex of subjects with bipolar disorder and major depressive disorder and in rats after treatment with mood stabilizers and antidepressants. Int J Neuropsychopharmacology. 2016;20:19;118.
Gillin JC, Sutton L, Ruiz C, Darko D, Golsham S, Risch SC, Janowsky D. The effects of scopolamine on sleep and mood in depressed patients with a history of alcoholism and a normal comparison group. Biol Psychiatry. 1991;30:157-69.
Gillin JC, Sutton L, Ruiz C, Kelsoe J, Dupont RM, Darko D, Risch, Janowsky DS. The cholinergic rapid eye movement induction test with arecoline in depression. Arch Gen Psychiatry. 1991;48:264-70.
Gollan JK, Hongxin D, Bruno D, Nierenberg J, Nobrega JN, Grotte J, Pollock BG, Marmar CR, Teipel S, Csernansky JG, Pomara N. Basal forebrain mediated increase in brain CRF is associated with increased cholinergic tone and depression. Psychiatric Research. 2017;264:76-81.
Growdon JH, Hirsch MJ, Wurtman RJ, Wiener W. Oral choline administration to patients with tardive dyskinesia. N Engl J Med. 1977; 297:524-7.
Hannestad JO, Cosgraove KP, DellaGloia NF, Perkins E, Bois F, Bhagwagar Z, Seibyl JP, McClure-Begley TD, Picciotto MR, Esterlis I. Changes in the cholinergic system between bipolar depression and euthymia as measured with 51A single photon emission computed tomography. Biol. Psychiatry. 2013;74:768-76.
He LL, Zhang QF, Wang LC, Dai JX, Wang CH, Zheng LH, Zhou Z. Muscarinic inhibition of nicotinic transmission in rat sympathetic neurons and adrenal chromaffin cells. Philos Trans R Soc Lnd B Biol Sci. 2015;5:370.
Ikarashi Y, Takahashi A, Ishimaru H, Arai T, Maruyama Y. Suppression of cholinergic activity via dopamine D2 receptor in the rat striatum. Neurochem Int. 1997;30:191-7.
Janowsky DS, El-Yousef MK, Davis JM, Sekerke J. A cholinergic-adrenergic hypothesis of mania and depression. Lancet. 1972;2:63-5.
Janowsky DS, El-Yousef MK, Davis JM, Sekerke J. Parasympathetic suppression of manic symptoms by physostigmine. Arch Gen Psychiatry. 1973;28:542-7.
Janowsky DS, El-Yousef MK, Davis JM. Antagonistic effects of physostigmine and methylphenidate in man. American Journal of Psychiatry. 1973;130:1370-6.
Janowsky DS, El-Yousef MK, Davis JM. Acetylcholine and depression. Psychosom Med. 1974;36:248-57.
Janowsky DS, El-Yousef MK, Davis JM. Cholinergic antagonism of methylphenidate-induced stereotyped behavior. Psychopharmacology 1979;60:237-40.
Janowsky DS, Risch C, Parker D. Huey L, Judd L. Increased vulnerability to cholinergic stimulation in affective-disorder patients (proceedings). Psychopharmacol Bull. 1980;16:29-31.
Janowsky DS, Risch SC. Cholinomimetic and anticholinergic drugs used to investigate an acetylcholine hypothesis of affective disorder and stress. Drug Dev Res. 1984;4:125-42.
Janowsky DS, Risch SC, Kennedy B, Ziegler M, Huey L. Central muscarinic effects of physostigmine on mood, cardiovascular function, pituitary and adrenal neuroendocrine release. Psychopharmacology. 1986;89:150-4.
Janowsky DS, El-Yousef MK, Davis JM, Sekerke J. A cholinergic-adrenergic hypothesis of mania and depression. Lancet. 1972;2:632-5.
Janowsky DS, Overstreet DH, Nurnberger JL Jr. Is cholinergic sensitivity a genetic marker for the affective disorders? Amer J. Med Genet. 1994;54:335-44.
Janowsky DS, Risch SC, Judd LL, Huey L. Cholinergic supersensitivity in affect disorder patients: behavioral and neuroendocrine observations. Psychopharmacol Bull. 1980;17:129-32.
Janowsky DS, Risch SC, Gillin JC. Adrenergic-cholinergic balance and the treatment of affective disorders. Prog Neuropsychopharmacol Biol Psychiatry. 1983;7:297-307.
Janowsky DS., Overstreet DH., Nurnberger JL Jr. Is cholinergic sensitivity a genetic markerfor the affective disorders? Am J Med Genet. 1994;54:335-44.
Jeon WJ, Gibbons AS, Dean B. The use of a modified (3H) 4-DAMP radioligand binding assay with increased selectivity for muscarinic M3 receptor shows that cortical CHRM3 levels are not altered in mood disorders. Prog Neuropsychopharmacol Biol Psychiatry. 2013;47:7-12.
Jeon WJ, Dean B, Scarr E, Gibbons A. The role of muscarinic receptors in the pathophysiology of mood disorders: a potential novel treatment. Current Neuropharmacology. 2015;13:739-749.
Khajavi D, Farokhnia M, Modabbernia A, Ashrafi M, Abbasi Sh, Tabrizi M, Akhondzaeh S. Oral scopolamine augmentation in moderate to severe major depressive disorder: a randomized double-blind, placebo-controlled study. J Clin Psychiatry. 2012;73:1428-33.
Krieg JC, Berger M. Treatment of mania with the cholinomimetic agent RS-86. Br J Psychiatry. 1986;148:613-5.
Laurer CJ, Modell S, Schreiber W, Krieg JC, Holsboer F. Prediction of the development of a first major depressive episode with a rapid eye movement sleep induction test using the cholinergic agonist RS 86. J Clin Psychopharmacol. 2004;24:356-7.
Lauriello J, Kenny WM, Sutton L, Golshan S, Ruiz C, Kelso J, Rapaport M, Gillin JC. The cholinergic REM sleep induction test with pilocarpine in mildly depressed patients and normal controls. Biol Psychiatry 1993,1;33:33-9.
Liu RJ, Banasr M, Li N, Terwilliger R, Sanacora G, Eid T, Aghajanian G, Duman RS. Scopolamine rapidly increases mammalian target of rapamycin complex 1 signaling, synaptogenesis, and antidepressant behavioral responses. Biol Psychiatry. 2013;74:742-9.
Luo X, Kranzler HR, Zuo L, Wang S, Bluberg HP, Gelenter J. CHRM2 gene predisposes to alcohol dependence, drug dependence and affective disorders: results from an extended case-control structured association study. Hum Mol Genet. 2005;14:2421-34.
MacMaster FP, Kusumakar V. Choline in pediatric depression. McGill J Med. 2006;9:24-7.
Martin AE, Schober DA, Nikolayev A, Tolstikov VV, Anderson WH, Higgs RE, Kuo MS, Laksmanan A, Catlow JT, Li X, Felder CC, Witkin JM. Further Evaluation of Mechanisms Associated with the Antidepressantlike Signature of Scopolamine in Mice. CNS Neurol Disord Drug Targets. 2017;16:492-500.
Mineur YS, Cahuzac EL, Mose TN, Bentham MP, Plantenga ME, Thompson DC, Picciotto MR. Interaction between noradrenrgic and cholinergic signaling in amygdala regulates anxiety and depression related behaviors in mice. Neuropsychopharmacology. 2018;43:2118-25.
Modell S, Lauer CJ. Rapid eye movement (REM) sleep: an endophenotype for depression. Curr Psychiatry Rep. 2007;9:480-5.
Laksmanan P, Catlow JT, Li X, Felder CC, Witkin JM. Further evaluation of mechanisms associated with the antidepressant like signature of scopolamine in mice. CNS Neurol Disord Drug Targets. 2017;16:492-500.
Mineur YS, Picciotto MR. Nicotine receptors and depression: revisiting and revising the cholinergic hypothesis. Trends Pharmacol Sci. 2010;31:580-6.
Mineur YS, Obayemi A, Wigestrand MB, Fote GM, Calarco CA, Li AM, Picciotto MR. Cholinergic signaling in the hippocampus regulates social stress resilience and anxiety and depression-like behavior. 2013. Proc Natl Acad Sci USA. 2013;110::3573-8.
Mineur YS, Fote GM, Blakeman S, Cahuza EL, Newbold SA, Picciotto MR. Multiple acetylcholine receptor subtypes in the mouse amygdala regulate affective behaviors and response to social stress. Neuropsychopharmacology. 2016;41:1579-87.
Mineur YS, Cahuzac EL, Mose TN, Bentham NP, Plantessya ME, Thompson DC, Picciotto MR. Interaction between noradrenergic and cholinergic signaling in amygdala regulates anxiety and depression related behaviors in mice. Neuropsychopharmacology. 2018;43:2118-25.
Mineur YS, Mose TN, Blakeman S, Picciotto MR. Hippocampal α7 nicotinic ACh receptors contribute to modulation of depression-like behaviour in C57BL/6J mice. Br J Pharmacol. 2018;175:1903-14.
Navarria A, Wohleb ES, Voleti B, Ota KT, Dutheil S, Lepack AE, Dwyer JM, Fuchikami M, Becker A, Drago F, Duman RS. Rapid antidepressant actions of scopolamine: role of medial prefrontal cortex and M1-subtype muscarinic acetylcholine receptors. Neurobiol Dis. 2015;82:254-61.
Nurnberger JL Jr., Sitraram N, Gershon ES, Gillin JC. A twin study of cholinergic REM induction. Biol Psychiatry. 1983;18:1161-73.
O’Keane V, O’Flinn K, Lucey J, Dinan TG. Pyridostigmine-induced growth hormone responses in healthy and depressed subjects: evidence for cholinergic supersensitivity in depression. Psychol Med. 1992;22:55-60.
Olds ME, Domino EF. Comparison of muscarinic and nicotinic cholinergic agonists on selfstimulating behavior. J Pharm Exp. Therapeutics 1969;166:189-204.
Pádua-Reis M, Aquino NS, Oliveira VEM, Szawka RE, Prado MAM, Prado VF, Pereira GS. Reduced Vesicular Acetylcholine Transporter favors antidepressant behaviors and modulates serotonin and dopamine in female mouse brain. Behav Brain Res. 2017;330:127-32.
Palucha-Poniewiera A, Podkowa K, Lenda T, Pilc A. The involvement of monoaminergic neurotransmission in the antidepressant like effect of scopolamine in the tail suspension test. Prog Neuropsychopharmacol Biol Psychiatry. 2017;79(Pt B):155-61.
Park L, Furey M, Nugent AC, Farmer C, Ellis J, Szczepanik J, Lener MS, Zarate CA Jr. Neurophysiological Changes Associated with Antidepressant Response to Ketamine Not Observed in a Negative Trial of Scopolamine in Major Depressive Disorder. Int J Neuropsychopharmacol. 2019;22:10-18.
Petryshen TL, Lewis MC, Denney KA, Garza JC, Fava M. Antidepressant-like effect of low dose ketamine and scopolamine co-treatment in mice. Neuro. Lett. 2016;4620:70-3.
Picciotto MR, Lewis AS, van Schalkwyk GI, Mineur YS. Mood and anxiety regulation by nicotinic acetylcholine receptors: A potential pathway to modulate aggression and related behavioral states. Neuropharmacology. 2015;96(Pt B):235-43.
Podkowa K, Podkowa A, Salat K, Lenda T, Pilc A, Palucha-Poniewiera A. Antidepressant-like effects of scopolamine in mice are enhanced by the group II mGlu receptor antagonist LY341495. Neuropharmacology. 2016;111:169-79.
Podkowa K, Pochwat B, Branski P, Pilc A. Group II mGlu receptor antagonist LY 341495 enhances the antidepressant-like effects of ketamine in the forced swim test in rats. Psychopharmacology (Berl). 2016;233:2901-14.
Podkowa K, Pilc A, Podkowa A, Sałat K, Marciniak M, Pałucha-Poniewiera A.The potential antidepressant action of adverse effects profiles scopolamine co-adminstered with the mGlu 7 receptor allosteric agonist AMN082 in mice. Neuropharmacology. 2018;141:214-22.
Poland RE, McCracken JT, Lutchmansingh P, Lesser IM, Tondo L, Edwards C, Boone KB, Lin KM. Differential response of rapid eye movement sleep to cholinergic blockade by scopolamine in currently depressed, remitted and normal control subjects. Biological Psychiatry. 1997;41:929-38.
Pytka K, Dziubina A, Mlynniec K, Dziedziczak A, Zmudzka E, Furgala A, Olczyk A, Sapa J, Filipek B. The role of glutamatergic, GABA-ergic, and cholinergic receptors in depression and antidepressant-like effect. Pharmacol Rep. 2016;68:443-50.
Rada P, Colasante C, Skirzewski M, Hernandez L, Hoebel B. Behavioral depression in the swim test causes a biphasic, long-lasting change in accumbens acetylcholine release, with partial compensation by acetylcholinesterase and muscarinic-1 receptors. Neuroscience. 2006;141:67-76.
Rao U, Lutchmansingh P, Poland RE. Age related effects of scopolamine on REM sleep regulation in in normal control subjects: relationship to sleep abnormalities in depression. Neuropsychopharmacology. 1999;21:723-30.
Renshaw PF, Lafer B, Babb SM, Fava M, Still AL, Christensen JD, Yurgelun-Todd DA, Bonello CM, Pillay SS, Rothchild AJ, Nierenburg AA, Rosenbaum F, Cohen BM. Basal Ganglia choline levels in depression and response to fluoxetine treatment: an in vivo proton magnetic resonance spectroscopy study. Biol Psychiatry. 1997;41:837-43.
Reynolds CF, Butters MA, Lopez O, Pollock BG, Dew MA, Mulsant BH, Lenze EJ, Holm M, Rogers JC, Mazumdar S, Houck PR, Begley A, Anderson S, Karp JE, Mller MD, Whyte EM, Stack J. Gildengers A, Szanto K, Bensasi S, Kaufer DI, Kamboh MI, DeKosky ST. Maintenance treatment of depression in old age: a randomized, double-blind, placebo-controlled evaluation of the efficacy and safety of donepezil combined with antidepressant pharmacotherapy. Arch Gen Psychiatry. 2011;68:51-60
Riley CA, Renshaw PF. Brain choline in major depression: A review of the literature. Psychiatry Res Neuroimaging. 2018;271:142-53.
Risch SC, Janowsky DS, Gillin JC. Muscarinic supersensitivity of anterior pituitary ACTH and B-endorphin release in major depressive illness. Peptides. 1983;4:789-92.
Risch SC, Janowsky DS, Mott MA, Gillin JC, Kalir HH, Huey L, Ziegler M, Kennedy B, Turken A. Central and peripheral cholinesterase inhibition: effects on anterior pituitary and sympathomimetic function. Psychoneuroendocrinolgy. 1985;11:221-30.
Rosenblatt JE, Janowsky DS, Davis JM, El-Yousef MK. The augmentation of physostigmine toxicity in the rat by delta 9 tetrahydrocannabinol. Res Com Chem Path Pharm. 1972;3:478-82.
Rowntree DW, Nevin S, Wilson A. The effects of diisopropylfluorophosphonate in schizophrenia and manic depressive psychosis. J Neurol. Neurosurg, Psychiat. 1950;13:47-62.
Rubin RT, Abbasi SA, Rhodes ME, Czambej RK. Growth hormone responses to low dose physostigmine administration: functional sex differences (sexual diergism) between major depressive and matched controls. Psychol Med. 2003;33:655-65.
Rubin RT, Rhodes ME, Miller TH, Jakab RL, Czambel RK. Sequence of pituitary-adrenal cortical hormone responses to low-dose physostigmine administration in young adult women and men. Life Sci. 2006;79:2260-8.
Rubin RT, O’Toole SM, Rhodes ME, Sekula LK, Czambel RK. Hypothalamo-pituitary-adrenal cortical responses to low-dose physostigmine and arginine vasopressin administration: sex differences between major depressives and matched control subjects. Psychiatry Res. 1999;89:1-20.
Salin-Pascual RJ, Rosas M, Jimenez-Genchi A, Rivera-Meza BL, Delgado-Parra V. Antidepressant Effects of transdermal nicotine patches in non-smoking patients with major depression. J Clin Psychiatry. 1996;57:387-9.
Saricicek A, Esterlis I, Maloney KH, Mineur YS, Ruf BM, Muralidharan A, Chen JI, Cosgrove KP, Kerestes R, Ghose S, Tamminga CA, Pittman B, Bois F, Tamagnan G, Seibyl J, PIcciotto MR, Staley JK, Bhagwagar Z. Persistent β2*-nicotinic acetylcholinergic receptor dysfunction in major depressive disorder. Am J Psychiatry. 2012;169:851-9.
Schredl M, Weber B, Leins ML, Heuser I. Donepezil-induced REM sleep augmentation enhances memory performance in elderly, healthy persons. Exp Gerontol. 2001;36:353-61.
Selbach H. Ueber die vegetative Dynamic in der psychiatrischen Pharmakotherapie. Dtsh Med J. 1961;12:511-7.
Shin JH, Adrover MF, Wess J, Alvarez VA. Muscarinic regulation of dopamine and glutamate transmission in the nucleus accumbens. Proc Natl Acad Sci U S A. 2015;112:8124-9.
Singh P, Singh TG. Modulation of muscarinic system of serotonin-norepinephrine reuptake inhibitor antidepressant attenuates depression in mice. Indian J Pharmacol. 2015;47:388-93.
Sitaram N, Nurnberger J, Gershon ES. Faster cholinergic REM sleep induction in euthymic patients with primary affective illness. Science. 1980;208:200-2.
Sitaram N, Jones D, Dube S, Keshavan M, Davies A, Reynal P. The association of supersensitive cholinergic REM-induction and affective illness within pedigrees. J Psychiatr Res. 1987;21:487-97.
Sitaram N, Nurnberger J, Gershon ES, Gillin JC. Cholinergic regulation of mood and REM sleep: a potential model and marker for vulnerability to depression. Am J Psychiatry. 1983;139:571-6.
Sitaram N, Dube S, Keshavan M, Davies A, Reynal P. The association of supersensitive cholinergic REM-induction and affective illness within pedigrees. J Psychiatr Res. 1987;21:487-97.
Small KM, Nunes E, Hughley S, Addy NA. Ventral tegemental area muscarinic receptors modulate depression and anxiety-related behaviors in rats. Neurosci Lett. 2016;616:80-5.
Sokolski KN, DeMet EM. Increased pupillary sensitivity to pilocarpine in depression. Prog Neuropsychopharmacol Biol Psychiatry. 1996;20:253-62.
Sokolski KN, DeMet EM. Cholinergic sensitivity predicts severity of mania. Psychiatry Res. 2000;95:195-200.
Stoll AL, Sachs GS, Cohen BM Lafer B, Christensen JD, Renshaw PF. Choline in the treatment of rapid-cycling bipolar disorder : clinical and neurochemical findings in lithium treated patients. Biol Psychiatry. 1996;40:382-8.
Tamminga C, Smith RC, Change S, Haraszti JS, Davis JM. Depression associated with oral choline. Lancet. 1976;2:905.
van Enkhuizen J, Milienne-Petiot M, Geyer MA, Young JW. Modeling bipolar disorder in mice by increasing acetylcholine or dopamine: chronic lithium treats most but not all features. Psychopharmacology (Berl). 2015;232:3455-67.
van Enkhuizen J, Janowsky DS, Olivier B, Minassian A, Perry W, Young JW, Geyer MA. The catecholaminergic-cholinergic balance hypothesis of bipolar disorder revisited. European Journal of Pharmacology. 2015;753:114-26.
Voleti B, Navarria A, Liu RJ, Banasr M, Li N, Terwilliger R, Sanacora G, Eid T, Aghajanian G, Duman RS. Scopolamine rapidly increases mammalian target of rapamycin complex 1 signaling, synaptogenesis, and antidepressant behavioral responses. Biol Psychiatry. 2013;74:742-9.
Wang JC, Hinrichs AL, Stock H, Budde J, Allen R, Bertelsen S, Kwon JM, Wu W, Dick DM, Rice J, Jones K, Nurnberger JL Jr., Tischfield J, Porjesz B, Edenberg HJ, Hesselbrock V, Crowe R, Schuckit M, Begleiter H, Reich T, Goate AM, Bierut LJ. Evidence of common and specific genetic effects: association of the muscarinic acetylcholine receptor M2 (CHRM2) gene with alcohol dependence and major depressive syndrome. Hum Mol Genet. 2004;13:1903-11.
Willoughby EF. Pilocarpine in Threatening Mania. Lancet. 1889.
Witkin JM, Overshiner C, Li X, Catlow JT, Wishart GN, Schober DA, Heinz BA, Nikolayey A, Tolstikov VV, Anderson WH, Higgs RE, Kuo MS, Felder CC. M1 and m2 muscarinic receptor subtypes regulate antidepressant-like effects of the rapidly acting antidepressant scopolamine. J Pharmacol Exp Ther. 2014;351:448-58.
Wohleb ES, Wu M, Gerhard DM, Taylor SR, Picciotto MR, Duman RS. GABA interneurons mediate the rapid antidepressant like effects of scopolamine. Journal Clinical Investigation 2016:126:1282-94.
Wohleb ES, Gerhard D, Thomas A, Duman RS. Molecular and cellular mechanisms of rapidacting antidepressants ketamine and scopolamine. Curr Neuropharmacol 2017;15:11-26.
Yu H, Li M, Zhou D, Lv D, Liao Q, Lu Z, Shen M, Wang Z, Li M, Xiao X, Zhang Y, Wang C. Vesicular glutamate transporter 1 (VGLUT1)-mediated glutamate release and membrane GluA1 activation is involved in the rapid antidepressant-like effects of scopolamine in mice. Neuropharmacology 2018;131:209-22.
Yu H, Li M, Shen X, Lv D, Sun X, Wang J, Gu X, Hu J, Wang C. The Requirement of L-Type Voltage-Dependent Calcium Channel (L-VDCC) in the Rapid-Acting Antidepressant-Like Effects of Scopolamine in Mice. Int J. Neuropsychopharmacol. 2018;21:174-86.
Yu H, Lv D, Shen M, Zhang Y, Zhou D, Chen Z, Wang C. BDNF mediates the protective effects of scopolamine in reserpine-induced depression-like behaviors via up-regulation of 5-HTT and TPH1. Psychiatry Res. 2019;271:328-34.
Zavitsanou K, Katsifis A, Attner F, Huang XE. Investigation of M1/M4 muscarinic receptors in the anterior cingulate cortex in schizophrenia, bipolar disorder, and major depressive disorder. Neuropsychopharmacology. 2004;29:619-25.
Zavitsanou K, Katsifis A, Yu Y, Huang XE. M2/M4 muscarinic receptor binding in the anterior cingulate cortex in schizophrenia and mood disorders. Brain Res Bull. 2005; 65:397-403.
Zhang C, Liu X, Zhou P. Cholinergic tone in ventral tegmental area: Functional organization and behavioral implications. Neurochem. Int. 2018;114:127-33.
Zhao D, Julian X, Pan L, Zhu W, Fu X, Guo L, Lu Q, Wang J. Pharmacologic activation of cholinergic alpha 7 nicotinic receptors mitigates depressive like behavior in a mouse model of chronic stress. J Neuroinflammation. 2017;14:234.
Zhang X, Feng ZJ, Chergui K. GluN2D-containing NMDA receptors inhibit neurotransmission in the mouse striatum through a cholinergic mechanism: implications for parkinson’s disease. J Neurochem. 2014;129:581-590.
Zhang C, Liu X, Zhou P, Zhang J, He W, Yuan TF. Cholinergic tone in ventral tegmental area: Functional organization and behavioral implications. Neurochem Int. 2018;114:127-33.
Zhao D, Xu X, Pan L, Zhu W, Fu X, Guo L, Lu Q, Wang J. Pharmacologic activation of cholinergic alpha7 nicotinic receptors mitigates depressive-like behavior in a mouse model of chronic stress. J Neuroinflammation. 2017;14:234.
September 19, 2019