Norepinephrine May Oppose Other Neuromodulators to Impact Alzheimer’s Disease
Abstract
:1. Introduction
2. Relationship with GABA and Glutamate
3. Alzheimer’s Disease
4. U-Shaped or Janus-Faced Dose-Response Curves
5. Evaluation of the Hypothesis
6. Consequences of the Hypothesis
Funding
Conflicts of Interest
References
- Maddox, B. The double helix and the “wronged heroine”. Nature 2003, 421, 407–408. [Google Scholar] [CrossRef]
- Watson, J.D.; Crick, F.H.C. Molecular structure of nucleic acids; a structure for deoxyribose nucleic acid. Nature 1953, 171, 737–738. [Google Scholar] [CrossRef] [PubMed]
- Schneider-Poetsch, T.; Yoshida, M. Along the central dogma-controlling gene expression with small molecules. Annu. Rev. Biochem. 2018. [Google Scholar] [CrossRef]
- Weinshenker, D. Long road to ruin: Noradrenergic dysfunction in neurodegenerative disease. Trends Neurosci. 2018, 41, 211–223. [Google Scholar] [CrossRef] [PubMed]
- Gannon, M.; Wang, Q. Complex noradrenergic dysfunction in Alzheimer’s disease: Low norepinephrine input is not always to blame. Brain Res. 2019, 1702, 12–16. [Google Scholar] [CrossRef]
- Toh, S.; García Rodríguez, L.A.; Hernández-Díaz, S. Use of antidepressants and risk of lung cancer. Cancer Causes Control 2007, 18, 1055–1064. [Google Scholar] [CrossRef]
- Strac, D.S.; Pivac, N.; Smolders, I.J.; Fogel, W.A.; de Deurwaerdere, P.D.; di Giovanni, G. Monoaminergic mechanisms in epilepsy may offer innovative therapeutic opportunity for monoaminergic multi-target drugs. Front. Neurosci. 2016, 10, 492. [Google Scholar] [CrossRef]
- Lissoni, P.; Barni, S.; Cattaneo, G.; Tancini, G.; Esposti, G.; Esposti, D.; Fraschini, F. Clinical results with the pineal hormone melatonin in advanced cancer resistant to standard antitumor therapies. Oncology 1991, 48, 448–450. [Google Scholar] [CrossRef] [PubMed]
- Dulawa, S.C.; Janowsky, D.S. Cholinergic regulation of mood: From basic and clinical studies to emerging therapeutics. Mol. Psychiatry 2019, 24, 694–709. [Google Scholar] [CrossRef]
- Åberg, E.; Fandiño-Losada, A.; Sjöholm, L.K.; Forsell, Y.; Lavebratt, C. The functional Val158Met polymorphism in catechol-O- methyltransferase (COMT) is associated with depression and motivation in men from a Swedish population-based study. J. Affect. Disord. 2011, 129, 158–166. [Google Scholar] [CrossRef]
- Fitzgerald, P.J. Is elevated norepinephrine an etiological factor in some cases of Alzheimer’s disease? Curr. Alzheimer Res. 2010, 7, 506–516. [Google Scholar] [CrossRef]
- Mather, M. Noradrenaline in the aging brain: Promoting cognitive reserve or accelerating Alzheimer’s disease? Semin. Cell Dev. Biol. 2021, in press. [Google Scholar] [CrossRef]
- Brown, R.A.M.; Walling, S.G.; Milway, J.S.; Harley, C.W. Locus ceruleus activation suppresses feedforward interneurons and reduces β-γ electroencephalogram frequencies while it enhances θ frequencies in rat dentate gyrus. J. Neurosci. 2005, 25, 1985–1991. [Google Scholar] [CrossRef] [PubMed]
- Xiong, B.; Shi, Q.; Fang, H. Dexmedetomidine alleviates postoperative cognitive dysfunction by inhibiting neuron excitation in aged rats. Am. J. Transl. Res. 2016, 8, 70–80. [Google Scholar]
- Talke, P.; Bickler, P. Effects of dexmedetomidine on hypoxia-evoked glutamate release and glutamate receptor activity in hippocampal slices. Anesthesiology 1996, 85, 551–557. [Google Scholar] [CrossRef] [PubMed]
- Cervantes-Ramírez, V.; Canto-Bustos, M.; Aguilar-Magaña, D.; Pérez-Padilla, E.A.; Góngora-Alfaro, J.L.; Pineda, J.C.; Atzori, M.; Salgado, H. Citalopram reduces glutamatergic synaptic transmission in the auditory cortex via activation of 5-HT1A receptors. Neuroreport 2019, 30, 1316–1322. [Google Scholar] [CrossRef]
- Shen, R.-Y.; Andrade, R. 5-Hydroxytryptamine 2 receptor facilitates GABAergic neurotransmission in rat hippocampus 1. J. Pharmacol. Exp. Ther. 1998, 285, 805–812. [Google Scholar]
- Del Arco, A.; Mora, F. Endogenous dopamine potentiates the effects of glutamate on extracellular GABA in the prefrontal cortex of the freely moving rat. Brain Res. Bull. 2000, 53, 339–345. [Google Scholar] [CrossRef]
- Pralong, E.; Jones, R.S.G. Interactions of dopamine with glutamate-and GABA-mediated synaptic transmission in the rat entorhinal cortex in vitro. Eur. J. Neurosci. 1993, 5, 760–767. [Google Scholar] [CrossRef]
- Abekawa, T.; Ohmori, T.; Ito, K.; Koyama, T. D1 dopamine receptor activation reduces extracellular glutamate and GABA concentrations in the medial prefrontal cortex. Brain Res. 2000, 867, 250–254. [Google Scholar] [CrossRef]
- Harte, M.; O’Connor, W.T. Evidence for a differential medial prefrontal dopamine D1 and D2 receptor regulation of local and ventral tegmental glutamate and GABA release: A dual probe microdialysis study in the awake rat. Brain Res. 2004, 1017, 120–129. [Google Scholar] [CrossRef] [PubMed]
- Kimura, M.; Hayashida, K.; Eisenach, J.C.; Saito, S.; Obata, H. Relief of hypersensitivity after nerve injury from systemic donepezil involves spinal cholinergic and γ-aminobutyric acid mechanisms. Anesthesiology 2013, 118, 173–180. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Trabace, L.; Cassano, T.; Cagiano, R.; Tattoli, M.; Pietra, C.; Steardo, L.; Kendrick, K.M.; Cuomo, V. Effects of ENA713 and CHF2819, two anti-Alzheimer’s disease drugs, on rat amino acid levels. Brain Res. 2001, 910, 182–186. [Google Scholar] [CrossRef]
- Beggiato, S.; Antonelli, T.; Tomasini, M.C.; Tanganelli, S.; Fuxe, K.; Schwarcz, R.; Ferraro, L. Kynurenic acid, by targeting α7 nicotinic acetylcholine receptors, modulates extracellular GABA levels in the rat striatum in vivo. Eur. J. Neurosci. 2013, 37, 1470–1477. [Google Scholar] [CrossRef]
- Dijk, S.N.; Francis, P.T.; Stratmann, G.C.; Bowen, D.M. Cholinomimetics increase glutamate outflow via an action on the corticostriatal pathway: Implications for Alzheimer’s disease. J. Neurochem. 1995, 65, 2165–2169. [Google Scholar] [CrossRef]
- Fitzgerald, P.J.; Hale, P.J.; Ghimire, A.; Watson, B.O. The cholinesterase inhibitor donepezil has antidepressant-like properties in the mouse forced swim test. Transl. Psychiatry 2020, 10. [Google Scholar] [CrossRef]
- Rosenstein, R.E.; Cardinali, D.P. Central gabaergic mechanisms as targets for melatonin activity in brain. Neurochem. Int. 1990, 17, 373–379. [Google Scholar] [CrossRef]
- Xu, F.; Li, J.C.; Ma, K.C.; Wang, M. Effects of melatonin on hypothalamic gamma-aminobutyric acid, aspartic acid, glutamic acid, beta-endorphin and serotonin levels in male mice. Biol. Signals 1995, 4, 225–231. [Google Scholar] [CrossRef]
- Calabresi, P.; Pisani, A.; Mercuri, N.B.; Bernardi, G. The corticostriatal projection: From synaptic plasticity to dysfunctions of the basal ganglia. Trends Neurosci. 1996, 19, 19–24. [Google Scholar] [CrossRef]
- Rorabaugh, B.R. Does prenatal exposure to CNS stimulants increase the risk of cardiovascular disease in adult offspring? Front. Cardiovasc. Med. 2021, 8, 652634. [Google Scholar] [CrossRef]
- Mandel, R.J.; Thal, L.J. Physostigmine improves water maze performance following nucleus basalis magnocellularis lesions in rats. Psychopharmacology 1988, 96, 421–425. [Google Scholar] [CrossRef]
- Grasing, K. A threshold model for opposing actions of acetylcholine on reward behavior: Molecular mechanisms and implications for treatment of substance abuse disorders. Behav. Brain Res. 2016, 312, 148–162. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Fitzgerald, P.J.; Hale, P.J.; Ghimire, A.; Watson, B.O. Repurposing cholinesterase inhibitors as antidepressants? Dose and stress-sensitivity may be critical to opening possibilities. Front. Behav. Neurosci. 2021, 14. [Google Scholar] [CrossRef]
- Schultz, W.; Dickinson, A. Neuronal coding of prediction errors. Annu. Rev. Neurosci. 2000, 23, 473–500. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ranjbar-Slamloo, Y.; Fazlali, Z. Dopamine and noradrenaline in the brain; overlapping or dissociate functions? Front. Mol. Neurosci. 2020, 12, 334. [Google Scholar] [CrossRef] [Green Version]
- Xing, B.; Li, Y.-C.; Gao, W.-J. Norepinephrine versus dopamine and their interaction in modulating synaptic function in the prefrontal cortex. Brain Res. 2015, 2, 147–185. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Arnsten, A.F.T.; Pliszka, S.R. Catecholamine influences on prefrontal cortical function: Relevance to treatment of attention deficit/hyperactivity disorder and related disorders. Pharmacol. Biochem. Behav. 2011, 99, 211–216. [Google Scholar] [CrossRef] [Green Version]
- O’Donnell, J.; Zeppenfeld, D.; Mcconnell, E.; Pena, S. Norepinephrine: A neuromodulator that boosts the function of multiple cell types to optimize CNS performance. Neurochem. Res. 2013, 37, 2496–2512. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Akaike, A.; Ohno, Y.; Sasa, M.; Takaori, S. Excitatory and inhibitory effects of dopamine on neuronal activity of the caudate nucleus neurons in vitro. Brain Res. 1987, 418, 262–272. [Google Scholar] [CrossRef]
- Kelly, J.S.; Dodd, J.; Dingledine, R. Acetylcholine as an excitatory and inhibitory transmitter in the mammalian central nervous system. Prog. Brain Res. 1979, 49, 253–266. [Google Scholar] [CrossRef]
- Root, D.H.; Hoffman, A.F.; Good, C.H.; Zhang, S.; Gigante, E.; Lupica, C.R.; Morales, M. Norepinephrine activates dopamine d4 receptors in the rat lateral habenula. J. Neurosci. 2015, 35, 3460–3469. [Google Scholar] [CrossRef] [Green Version]
- Aslanoglou, D.; Bertera, S.; Sánchez-Soto, M.; Benjamin Free, R.; Lee, J.; Zong, W.; Xue, X.; Shrestha, S.; Brissova, M.; Logan, R.W.; et al. Dopamine regulates pancreatic glucagon and insulin secretion via adrenergic and dopaminergic receptors. Transl. Psychiatry 2021, 11. [Google Scholar] [CrossRef]
- Sánchez-Soto, M.; Casadó-Anguera, V.; Yano, H.; Bender, B.J.; Cai, N.S.; Moreno, E.; Canela, E.I.; Cortés, A.; Meiler, J.; Casadó, V.; et al. α2A- and α2C-adrenoceptors as potential targets for dopamine and dopamine receptor ligands. Mol. Neurobiol. 2018, 55, 8438–8454. [Google Scholar] [CrossRef] [PubMed]
- Sánchez-Soto, M.; Bonifazi, A.; Cai, N.S.; Ellenberger, M.P.; Newman, A.H.; Ferré, S.; Yano, H. Evidence for noncanonical neurotransmitter activation: Norepinephrine as a dopamine D2-like receptor agonist. Mol. Pharmacol. 2016, 89, 457–466. [Google Scholar] [CrossRef] [Green Version]
- Marucci, G.; Buccioni, M.; Ben, D.D.; Lambertucci, C.; Volpini, R.; Amenta, F. Efficacy of acetylcholinesterase inhibitors in Alzheimer’s disease. Neuropharmacology 2020, 108352. [Google Scholar] [CrossRef] [PubMed]
- Liu, A.K.L.; Chang, R.C.C.; Pearce, R.K.B.; Gentleman, S.M. Nucleus basalis of Meynert revisited: Anatomy, history and differential involvement in Alzheimer’s and Parkinson’s disease. Acta Neuropathol. 2015, 129, 527–540. [Google Scholar] [CrossRef]
- Pepeu, G.; Grazia Giovannini, M. The fate of the brain cholinergic neurons in neurodegenerative diseases. Brain Res. 2017, 1670, 173–184. [Google Scholar] [CrossRef] [PubMed]
- James, T.; Kula, B.; Choi, S.; Khan, S.S.; Bekar, L.K.; Smith, N.A. Locus coeruleus in memory formation and Alzheimer’s disease. Eur. J. Neurosci. 2020. [Google Scholar] [CrossRef]
- Zhang, F.; Gannon, M.; Chen, Y.; Zhou, L.; Jiao, K.; Wang, Q. The amyloid precursor protein modulates α2A-adrenergic receptor endocytosis and signaling through disrupting arrestin 3 recruitment. FASEB J. 2017, 31, 4434–4446. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Lee, S.H.; Kang, J.; Ho, A.; Watanabe, H.; Bolshakov, V.Y.; Shen, J. APP family regulates neuronal excitability and synaptic plasticity but not neuronal survival. Neuron 2020. [Google Scholar] [CrossRef]
- Wang, D.; Yuen, E.Y.; Zhou, Y.; Yan, Z.; Xiang, Y.K. Amyloid β peptide-(1–42) induces internalization and degradation of β 2 adrenergic receptors in prefrontal cortical neurons. J. Biol. Chem. 2011, 286, 31852–31863. [Google Scholar] [CrossRef] [Green Version]
- Zhang, F.; Gannon, M.; Chen, Y.; Yan, S.; Zhang, S.; Feng, W.; Tao, J.; Sha, B.; Liu, Z.; Saito, T.; et al. Beta-amyloid redirects norepinephrine signaling to activate the pathogenic GSK3beta/tau cascade. Sci. Transl. Med. 2020, 12, eaay6931. [Google Scholar] [CrossRef]
- Chen, Y.; Peng, Y.; Che, P.; Gannon, M.; Liu, Y.; Li, L.; Bu, G.; van Groen, T.; Jiao, K.; Wang, Q. α2A adrenergic receptor promotes amyloidogenesis through disrupting APP-SorLA interaction. Proc. Natl. Acad. Sci. USA 2014, 111, 17296–17301. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ni, Y.; Zhao, X.; Bao, G.; Zou, L.; Teng, L.; Wang, Z.; Song, M.; Xiong, J.; Bai, Y.; Pei, G. Activation of β2-adrenergic receptor stimulates γ-secretase activity and accelerates amyloid plaque formation. Nat. Med. 2006, 12, 1390–1396. [Google Scholar] [CrossRef]
- Nyth, A.L.; Gottfries, C.G. The clinical efficacy of citalopram in treatment of emotional disturbances in dementia disorders A Nordic multicentre study. Br. J. Psychiatry 1990, 157, 894–901. [Google Scholar] [CrossRef] [PubMed]
- Lyketsos, C.G.; Sheppard, J.M.; Steele, C.D.; Kopunek, S.; Steinberg, M.; Baker, A.S.; Brandt, J.; Rabins, P.V. Randomized, placebo-controlled, double-blind clinical trial of sertraline in the treatment of depression complicating Alzheimer’s disease: Initial results from the depression in Alzheimer’s disease study. Am. J. Psychiatry 2000, 157, 1686–1689. [Google Scholar] [CrossRef]
- Lyketsos, C.G.; Delcampo, L.; Steinberg, M.; Miles, Q.; Steele, C.D.; Munro, C.; Baker, A.S.; Sheppard, J.-M.E.; Frangakis, C.; Brandt, J.; et al. Treating depression in Alzheimer disease efficacy and safety of sertraline therapy, and the benefits of depression reduction: The DIADS. Arch. Gen. Psychiatry 2003, 60, 737–746. [Google Scholar] [CrossRef]
- Mokhber, N.; Abdollahian, E.; Soltanifar, A.; Samadi, R.; Saghebi, A.; Haghighi, M.B.; Azarpazhooh, A. Comparison of sertraline, venlafaxine and desipramine effects on depression, cognition and the daily living activities in Alzheimer patients. Pharmacopsychiatry 2014, 47, 131–140. [Google Scholar] [CrossRef]
- Taragano, F.E.; Lyketsos, C.G.; Mangone, C.A.; Allegri, R.F.; Comesaña-Diaz, E. A double-blind, randomized, fixed-dose trial of fluoxetine vs. amitriptyline in the treatment of major depression complicating Alzheimer’s disease. Psychosomatics 1997, 38, 246–252. [Google Scholar] [CrossRef]
- Mowla, A.; Mosavinasab, M.; Pani, A. Does fluoxetine have any effect on the cognition of patients with mild cognitive impairment? A double-blind, placebo-controlled, clinical trial. J. Clin. Psychopharmacol. 2007, 27, 67–70. [Google Scholar] [CrossRef]
- Petracca, G.; Tesón, A.; Chemerinski, E.; Leiguarda, R.; Starkstein, S.E. A double-blind placebo-controlled study of clomipramine in depressed patients with Alzheimer’s disease. J. Neuropsychiatry Clin. Neurosci. 1996, 8, 270–275. [Google Scholar]
- Herrmann, N.; Rothenburg, L.S.; Black, S.E.; Ryan, M.; Liu, B.A.; Busto, U.E.; Lanctôt, K.L. Methylphenidate for the treatment of apathy in alzheimer disease: Prediction of response using dextroamphetamine challenge. J. Clin. Psychopharmacol. 2008, 28, 296–301. [Google Scholar] [CrossRef]
- Rosenberg, P.B.; Lanctôt, K.L.; Drye, L.T.; Herrmann, N.; Scherer, R.W.; Bachman, D.L.; Mintzer, J.E. Safety and efficacy of methylphenidate for apathy in Alzheimer’s Disease: A randomized, placebo-controlled trial. J. Clin. Psychiatry 2013, 74, 810–816. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Lanctôt, K.L.; Herrmann, N.; Black, S.E.; Ryan, M.; Rothenburg, L.S.; Liu, B.A.; Busto, U.E. Apathy associated with Alzheimer disease: Use of dextroamphetamine challenge. Am. J. Geriatr. Psychiatry 2008, 16, 551–557. [Google Scholar] [CrossRef] [PubMed]
- Padala, P.R.; Padala, K.P.; Lensing, S.Y.; Ramirez, D.; Monga, V.; Bopp, M.M.; Roberson, P.K.; Dennis, R.A.; Petty, F.; Sullivan, D.H.; et al. Methylphenidate for apathy in community-dwelling older veterans with mild Alzheimer’s disease: A double-blind, randomized, placebo-controlled trial. Am. J. Psychiatry 2018, 175, 159–168. [Google Scholar] [CrossRef]
- Wade, A.G.; Farmer, M.; Harari, G.; Fund, N.; Laudon, M.; Nir, T.; Frydman-Marom, A.; Zisapel, N. Add-on prolonged-release melatonin for cognitive function and sleep in mild to moderate Alzheimer’s disease: A 6-month, randomized, placebo-controlled, multicenter trial. Clin. Interv. Aging 2014, 9, 947–961. [Google Scholar] [CrossRef] [PubMed]
- Asayama, K.; Yamadera, H.; Ito, T.; Suzuki, H.; Kudo, Y.; Endo, S. Double blind study of melatonin effects on the sleep-wake rhythm, cognitive and non-cognitive functions in Alzheimer type dementia. J. Nippon Med. Sch. 2003, 70, 334–341. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Cardinali, D.P.; Brusco, L.I.; Liberczuk, C.; Furio, A.M. The use of melatonin in Alzheimer’s disease. Neuro. Endocrinol. Lett. 2002, 23, 20–23. [Google Scholar]
- Shukla, M.; Chinchalongporn, V.; Govitrapong, P. Melatonin prevents neddylation dysfunction in Aβ42-exposed SH-SY5Y neuroblastoma cells by regulating the amyloid precursor protein-binding protein 1 pathway. Curr. Alzheimer Res. 2020, 17, 446–459. [Google Scholar] [CrossRef]
- Paula-Lima, A.C.; Louzada, P.R.; de Mello, F.G.; Ferreira, S.T. Neuroprotection against abeta and glutamate toxicity by melatonin: Are GABA receptors involved? Neurotox. Res. 2003, 5, 323–327. [Google Scholar] [CrossRef]
- Arnsten, A.F.T. Catecholamine and second messenger influences on prefrontal cortical networks of “representational knowledge”: A rational bridge between genetics and the symptoms of mental illness. Cereb. Cortex 2007. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Giustino, T.F.; Fitzgerald, P.J.; Maren, S. Revisiting propranolol and PTSD: Memory erasure or extinction enhancement? Neurobiol. Learn. Mem. 2016, 130, 26–33. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Giustino, T.F.; Maren, S. Noradrenergic modulation of fear conditioning and extinction. Front. Behav. Neurosci. 2018. [Google Scholar] [CrossRef] [PubMed]
- Groft, M.L.; Normann, M.C.; Nicklas, P.R.; Jagielo-Miller, J.E.; McLaughlin, P.J. Biphasic effects of 5-HT1A agonism on impulsive responding are dissociable from effects on anxiety in the variable consecutive number task. Naunyn. Schmiedebergs. Arch. Pharmacol. 2019, 392, 1455–1464. [Google Scholar] [CrossRef]
- Tai, S.H.; Hung, Y.C.; Lee, E.J.; Lee, A.C.; Chen, T.Y.; Shen, C.C.; Chen, H.Y.; Lee, M.Y.; Huang, S.Y.; Wu, T.S. Melatonin protects against transient focal cerebral ischemia in both reproductively active and estrogen-deficient female rats: The impact of circulating estrogen on its hormetic dose-response. J. Pineal Res. 2011, 50, 292–303. [Google Scholar] [CrossRef]
- Vijayraghavan, S.; Wang, M.; Birnbaum, S.G.; Williams, G.V.; Arnsten, A.F.T. Inverted-U dopamine D1 receptor actions on prefrontal neurons engaged in working memory. Nat. Neurosci. 2007, 10, 376–384. [Google Scholar] [CrossRef]
- Fitzgerald, P.J.; Watson, B.O. Gamma oscillations as a biomarker for major depression: An emerging topic. Transl. Psychiatry 2018, 8, 177. [Google Scholar] [CrossRef]
- Fitzgerald, P.J.; Watson, B.O. In vivo electrophysiological recordings of the effects of antidepressant drugs. Exp. Brain Res. 2019, 237, 1593–1614. [Google Scholar] [CrossRef] [Green Version]
- Janowsky, D.S.; Davis, J.M.; El-Yousef, M.K.; Sekerke, H.J. A cholinergic-adrenergic hypothesis of mania and depression. Lancet 1972. [Google Scholar] [CrossRef]
- De la Cruz, F.; Wagner, G.; Schumann, A.; Suttkus, S.; Güllmar, D.; Reichenbach, J.R.; Bär, K.J. Interrelations between dopamine and serotonin producing sites and regions of the default mode network. Hum. Brain Mapp. 2021, 42, 811–823. [Google Scholar] [CrossRef]
- Cooney, R.E.; Eugène, F.; Dennis, E.L. Neural correlates of rumination in depression. Cogn. Affect. Behav. Neurosci. 2015, 10, 470–478. [Google Scholar] [CrossRef] [Green Version]
- Andrade, C. Valproate in pregnancy: Recent research and regulatory responses. J. Clin. Psychiatry 2018, 79. [Google Scholar] [CrossRef]
- Rescorla, R.A.; Wagner, A. A theory of Pavlovian conditioning: Variations in the effectiveness of reinforcement and nonreinforcement. In Classical Conditioning: Current Research and Theory; Appleton-Century-Crofts: New York, NY, USA, 1972. [Google Scholar]
- Conversi, D.; Cruciani, F.; Accoto, A.; Cabib, S. Positive emotional arousal increases duration of memory traces: Different role of dopamine D1 receptor and β-adrenoceptor activation. Pharmacol. Biochem. Behav. 2014, 122, 158–163. [Google Scholar] [CrossRef] [PubMed]
- Hatcher-Martin, J.M.; Armstrong, K.A.; Scorr, L.M.; Factor, S.A. Propranolol therapy for Tardive dyskinesia: A retrospective examination. Park. Relat. Disord. 2016, 32, 124–126. [Google Scholar] [CrossRef] [PubMed]
- Lasaponara, S.; Fortunato, G.; Conversi, D.; Pellegrino, M.; Pinto, M.; Collins, D.L.; Tomaiuolo, F.; Doricchi, F. Pupil dilation during orienting of attention and conscious detection of visual targets in patients with left spatial neglect. Cortex 2021, 134, 265–277. [Google Scholar] [CrossRef] [PubMed]
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2021 by the author. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Fitzgerald, P.J. Norepinephrine May Oppose Other Neuromodulators to Impact Alzheimer’s Disease. Int. J. Mol. Sci. 2021, 22, 7364. https://doi.org/10.3390/ijms22147364
Fitzgerald PJ. Norepinephrine May Oppose Other Neuromodulators to Impact Alzheimer’s Disease. International Journal of Molecular Sciences. 2021; 22(14):7364. https://doi.org/10.3390/ijms22147364
Chicago/Turabian StyleFitzgerald, Paul J. 2021. "Norepinephrine May Oppose Other Neuromodulators to Impact Alzheimer’s Disease" International Journal of Molecular Sciences 22, no. 14: 7364. https://doi.org/10.3390/ijms22147364